The eIF4ET family protein IFET-1 is needed for oocyte development and long-term storage in C. elegans. How IFET-1 plays multiple roles in oocyte biology is unclear. Using pull-downs and mass spectrometry, we identified proteins that interact with IFET-1. We show that three IFET-1-interacting partners—PENR-1, SQD-1, and LSM-4—are essential for producing viable oocytes in C. elegans females.
","acknowledgements":"We thank the Proteomics Core Facility at UT Southwestern.
","authors":[{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["investigation","methodology","writing_originalDraft","writing_reviewEditing","dataCuration","formalAnalysis"],"email":"judith.tafur@utsouthwestern.edu","firstName":"Judith","lastName":"Tafur","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"angelica.moralescueva@UTSouthwestern.edu","firstName":"Angelica","lastName":"Morales Cueva","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"nicole.familiari@utsouthwestern.edu","firstName":"Nicole E.","lastName":"Familiari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"weronika.stachera@utsoutwestern.edu","firstName":"Weronika E.","lastName":"Stachera","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, Texas, United States"],"departments":["Cell Biology"],"credit":["conceptualization","formalAnalysis","project","writing_originalDraft","fundingAcquisition"],"email":"jeffrey.woodruff@utsouthwestern.edu","firstName":"Jeffrey B.","lastName":"Woodruff","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-5590-9620"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Proteomic results from anti-FLAG pull down experiments. N=3 replicates.
","doi":null,"resourceType":"Dataset","name":"Extended_Data_Set_1.xlsx","url":"https://portal.micropublication.org/uploads/47a5259ca2743e0b63d8c942758a4cd3.xlsx"}],"funding":"J.B. Woodruff was supported by supported by the Pew Charitable Trust, the Welch Foundation (V-I-0004-20230731), an R35 grant from the National Institute of General Medical Sciences (5R35GM142522), and the Endowed Scholars program at UT Southwestern.
","image":{"url":"https://portal.micropublication.org/uploads/416906189d7c038e7ef69ed06e4a8687.png"},"imageCaption":"A. Top, confocal image of a day 2 adult feminized worm gonad expressing IFET1::mSCarlet::AID*::3xFlag. Bottom, schematic of IFET-1::3XFlag pulldown assay and mass spectrometry analysis of interacting proteins.
B. Volcano plot of protein abundances in pulldown experiment using ifet-1::mScarlet::AID*::3xFLAG; fem-1(hc17) adult females vs fem-1(hc17) worms as a control. Y-axis represents the –Log transformation of the obtained p-values. X-axis represents fold enrichment in abundance (FLAG-tag vs. control; n = 3 replicates). See Extended Data Set 1 for more information.
C. Log2 transformed fold changes of selected top IFET-1 pulldown hits grouped by gene ontology, molecular function, and biological process categories.
D. Feminized worms were treated with RNAi, then mated with untreated males. Shown is embryo viability post mating (mean ±95% C.I; >25 offspring counted from n=25 mothers (control), n=16 (penr-1), n=9 (sqd-1), n=7 (lsm-4), n=9 (cid-1), n=5 (patr-1), n=4 (edc-3), n=6 (fndc-1), n=7 (sup-26), n=10 (CELE_W01F3.2), n=5 (F26E4.3), n=5 (CELE_F56G4.6), n=5 (CELE_T13H5.8), and n=5 (acly-1)). p-value=0.0007 (control vs. penr-1), p-value<0.0001 (control vs. sqd-1) and p-value<0.0001 (control vs. lsm-4). P values from one-way ANOVA followed with Dunnet's multiple comparisons test.
","imageTitle":"IP-mass spectrometry identifies diverse interacting partners of IFET-1 in C. elegans females
","methods":"Worm husbandry
Worms were grown on Nematode Growth Media (NGM) plates and fed with standard OP50 E. coli. All worms were kept at 16°C for maintenance and 20°C for experiments. fem-1 lines were shifted to 25°C for 2.5 days starting at L1 stage to feminize until adulthood at which point they were moved to 20°C. Experiments involving synchronization were done using 5% sodium hypochlorite and 5 M NaOH to remove all larvae and adult worms. Embryos were then rotated in M9 overnight to hatch.
IFET-1 pull down and mass spectrometry
fem-1(hc17) and fem-1; ifet-1::3XFLAG worms were grown at 16°C on large NGM plates for about a week until they became densely populated. The worms were then washed off with M9 PEG and added to large flasks containing S-Medium Complete as described in Wormbook Maintenance of C. elegans: Chapter 5. The liquid culture was grown in a 16°C shaker for about 4 days. The worms were then washed and synchronized using the same reagents described above. After rotating overnight, new liquid culture flasks were started using the synchronized L1 worms and grown in a 25°C shaker for 2.5 days. They were then transferred to 20°C to grow for a day.
The feminized adult worm samples were collected, pelleted, and flash frozen in PBS containing protease inhibitors. On the day of the pulldown experiment, ChromoTek DYKDDDDK Fab-Trap™ Agarose beads were equilibrated in low salt buffer (165mM KCl, 25 mM HEPES, 1% glycerol and 0.05% Tween 20). They were then blocked for 1 hour at 4°C with 3% milk in low salt buffer and washed 3 times with lysis buffer. While the beads blocked, the feminized worm pellets were thawed at 4°C in lysis buffer (50mM HEPES, 1mM EGTA, 100mM KCL, 1mM MgCl2, 0.05% NP-40 and 1X protease inhibitors added fresh). They were then lysed by dounce homogenization and sonication at 35% amplitude. This lysate was then centrifuged at 17000 g for 25 minutes at 4°C. The lysate supernatant was then incubated on a rotator with the prepared beads for 10 minutes at room temperature and then at 4°C for 1 hour. The beads were sedimented and washed 3 times with low salt buffer. Samples were eluted with SDS and boiled for 5 min. They were then run on an SDS-PAGE gel for a few minutes so they would enter the gel, stained with Instant blue dye and carefully cut out to send to the mass spectrometry core facility.
For mass spectrometry, gel samples were digested overnight with trypsin (Pierce) after reduction and alkylation with DTT and iodoacetamide (Sigma-Aldrich). After solid-phase extraction cleanup with an Oasis HLB μElution plate (Waters), the resulting peptides were reconstituted in 2% (vol/vol) acetonitrile (ACN) and 0.1% trifluoroacetic acid in water. 1 μg of each sample was injected onto an Orbitrap Fusion Lumos mass spectrometer coupled to an UltiMate 3000 RSLCnano liquid chromatography system (Thermo Fisher Scientific). Samples were injected onto a 75 μm i.d., 75-cm-long EasySpray column (Thermo Fisher Scientific), and eluted with a gradient from 0 to 28% buffer B over 90 min. Buffer A contained 2% (vol/vol) ACN and 0.1% formic acid in water, and buffer B contained 80% (vol/vol) ACN, 10% (vol/vol) trifluoroethanol, and 0.1% formic acid in water. The mass spectrometer operated in positive ion mode with a source voltage of 2.5 kV and an ion transfer tube temperature of 300°C. MS scans were acquired at 120,000 resolution in the Orbitrap, and up to 10 MS/MS spectra were obtained in the Orbitrap for each full spectrum acquired using higher energy collisional dissociation (HCD) for ions with charges 2–7. Dynamic exclusion was set for 25 s after an ion was selected for fragmentation.
Raw MS data files were analyzed using Proteome Discoverer v3.0 (Thermo Fisher Scientific), with peptide identification performed using Sequest HT searching against the C. elegans reviewed protein database from UniProt along with the sequence of fluorescent mMaple protein. Fragment and precursor tolerances of 10 ppm and 0.6 D were specified, and three missed cleavages were allowed. Carbamidomethylation of Cys was set as a fixed modification, and oxidation of Met was set as a variable modification. The false discovery rate cutoff was 1% for all peptides.
RNAi Screen and viability assays
RNAi clones were obtained from the Ahringer library or cloned using the pL4440 empty vector plasmid and target DNA sequences of 300 bp ordered from TWIST biosciences. RNAi plates were made by growing the feeding clone containing bacteria on NGM plates containing 1mM IPTG and 100 μg/ml ampicillin. Worms were synchronized and grown on these plates for 2.5 days at 25°C for feminized worms. Feminized worms were put on mating plates at D1 stage at a ratio of 1 female per 3 males for 16 hours at 16°C. The number of embryos laid per mom was tallied and 2 days later the fraction of hatchlings was counted to obtain the viability of the laid eggs. The fraction of hatchlings was counted 2 days later.
Microscopy
The microscope image was taken using a 40X silicone (NA 1.25) objective on a Nikon AX-R confocal microscope.
","reagents":"Plasmid Name | Targeting sequence/tag |
JWB 124 | Empty Vector |
JWB 226 | |
JWB 227 | |
JWB 238 | |
JWB 239 | |
JWB 240 | |
JWB 241 | |
JWB 242 | |
JWB 243 | CELE_W01F3.2 |
JWB 244 | CELE_F56G4.6 |
JWB 245 | CELE_T13H5.8 |
JWB 246 | |
JWB 254 | |
JWB 264 | |
|
|
Strain name | Genotype |
| |
JWW 255 | fem-1 (hc17) IV; ifet-1(dfw16[ifet-1::mScarlet_I::AID*::3xFlag]) III; wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77). |
In C. elegans, RNA-rich biomolecular condensates called P granules are required for germ cell proliferation and sperm/oocyte development (Huggins et al., 2020; Kawasaki et al., 2004; Spike et al., 2008a; Spike et al., 2008b). A key component of P granules is IFET-1, which is a homolog of the eIF4E Transporter (eIF4ET) protein. IFET-1 enables selective repression of certain developmental transcripts, while promoting translation of others encoding cytoskeletal proteins (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). It is likely that IFET-1 acts within a network of proteins to execute these diverse functions. Thus, we reasoned that by identifying interacting partners of IFET-1, we could discover new factors that are essential for oocyte development and storage.
To identify IFET-1 binding partners, we used FLAG-Trap beads (anti-DYKDDDK agarose) to pull down FLAG-tagged IFET-1 (IFET-1::mScarlet::3XFLAG) from adult female worms grown in liquid culture. In this line, IFET-1 localized to cytoplasmic puncta in oocytes and around the nuclei in the syncytial gonad, as expected. This construct was verified to be functional in our prior study (Bhatia et al., 2025). Female worms expressing untagged IFET-1 were used as a control. We analyzed co-purifying proteins by mass spectrometry and defined positive hits as being significantly enriched in the positive sample (enrichment >3-fold, p value <0.05; three replicates).
Top hits included IFET-1 and known IFET-1 interactors such as IFE-3, CAR-1, and CGH-1 (Huggins et al., 2020; Sengupta et al., 2013), validating our approach (Fig. 1B). GO term analysis revealed that IFET-1's top binding partners consisted mostly of proteins involved in translation or mRNA regulation, consistent with reported functions for IFET-1 (Fig. 1C) (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). To find novel proteins that promote oocyte production and viability, we used RNAi to knock down 13 of the top hits not known previously to be IFET-1 interactors (Fig. 1D). Of these, only knockdown of lsm-4, sqd-1, and penr-1 reduced the percentage of viable embryos laid by RNAi-treated female worms mated with untreated males (Fig. 1D). LSM-4 and SQD-1 are both RNA binding proteins that have been characterized in oocyte development (Cornes et al., 2015; Erdmann et al., 2024). PENR-1 was originally identified in a high-throughput screen for genes that affect expression of the transcription factor PHA-4 during C. elegans embryogenesis (Green et al., 2024). The exact role of PENR-1 protein in germline formation remains unknown.
In summary, we identified interacting partners of IFET-1, which could potentially explain how IFET-1 plays multiple roles in germline development and translational control. IFET-1 likely suppresses translation of specific transcripts by binding to IFE-3, the 4E translation initiation factor in C. elegans. Some interactors, such as CAR-1 and CGH-1, likely cooperate with IFET-1 in the P granule to sequester developmentally regulated mRNAs. Most of the other interactors have similar characterized roles in mRNA binding and processing. Interestingly, we identified unexpected interactors that do not have well-defined roles, one of which (PENR-1) also is required for oocyte development. Future studies are needed to clarify how these IFET-1 partners could contribute to germline expansion and promotion of translation during oocyte storage.
","references":[{"reference":"Bhatia P, Tafur J, Amin R, Familiari NE, Yaguchi K, Tran VM, et al., Woodruff JB. 2025. Condensate-forming eIF4ET ensures adequate levels of meiotic proteins to support oocyte storage. Life Sci Alliance 8(8): 10.26508/lsa.202503387.
","pubmedId":"40441896","doi":""},{"reference":"Cornes E, Porta-De-La-Riva M, Aristizábal-Corrales D, Brokate-Llanos AM, García-Rodríguez FJ, Ertl I, et al., Cerón J. 2015. Cytoplasmic LSM-1 protein regulates stress responses through the insulin/IGF-1 signaling pathway in Caenorhabditis elegans. RNA 21(9): 1544-53.
","pubmedId":"26150554","doi":""},{"reference":"Erdmann EA, Forbes M, Becker M, Perez S, Hundley HA. 2024. ADR-2 regulates fertility and oocyte fate in C. elegans. bioRxiv: pii: 2023.11.01.565157. 10.1101/2023.11.01.565157.
","pubmedId":"37961348","doi":""},{"reference":"Green RA, Khaliullin RN, Zhao Z, Ochoa SD, Hendel JM, Chow TL, et al., Oegema K. 2024. Automated profiling of gene function during embryonic development. Cell 187(12): 3141-3160.e23.
","pubmedId":"38759650","doi":""},{"reference":"Huggins HP, Subash JS, Stoffel H, Henderson MA, Hoffman JL, Buckner DS, et al., Keiper BD. 2020. Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans. J Cell Sci 133(6): 10.1242/jcs.237990.
","pubmedId":"32079657","doi":""},{"reference":"Kawasaki I, Amiri A, Fan Y, Meyer N, Dunkelbarger S, Motohashi T, et al., Strome S. 2004. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 167(2): 645-61.
","pubmedId":"15238518","doi":""},{"reference":"Sengupta MS, Low WY, Patterson JR, Kim HM, Traven A, Beilharz TH, et al., Boag PR. 2013. ifet-1 is a broad-scale translational repressor required for normal P granule formation in C. elegans. J Cell Sci 126(Pt 3): 850-9.
","pubmedId":"23264733","doi":""},{"reference":"Spike C, Meyer N, Racen E, Orsborn A, Kirchner J, Kuznicki K, et al., Strome S. 2008. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178(4): 1973-87.
","pubmedId":"18430929","doi":""},{"reference":"Spike CA, Bader J, Reinke V, Strome S. 2008. DEPS-1 promotes P-granule assembly and RNA interference in C. elegans germ cells. Development 135(5): 983-93.
","pubmedId":"18234720","doi":""}],"title":"Identification of eIF4ET binding partners in C. elegans
","reviews":[{"reviewer":{"displayName":"Andrea Putnam"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[{"curator":{"displayName":"KJ Yook"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Gary Craig Schindelman"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Jaehyoung Cho"},"openAcknowledgement":false,"submitted":null}]},{"id":"64c88729-c5a9-44d3-8ebd-78d0a9948c68","decision":"revise","abstract":"The eIF4ET family protein IFET-1 is needed for oocyte development and long-term storage in C. elegans. How IFET-1 plays multiple roles in oocyte biology is unclear. Using pull-downs and mass spectrometry, we identified proteins that interact with IFET-1. We show that three IFET-1-interacting partners—PENR-1, SQD-1, and LSM-4—are essential for producing viable oocytes in C. elegans females.
","acknowledgements":"We thank the Proteomics Core Facility at UT Southwestern.
","authors":[{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["investigation","methodology","writing_originalDraft","writing_reviewEditing","dataCuration","formalAnalysis"],"email":"judith.tafur@utsouthwestern.edu","firstName":"Judith","lastName":"Tafur","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"angelica.moralescueva@UTSouthwestern.edu","firstName":"Angelica","lastName":"Morales Cueva","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"nicole.familiari@utsouthwestern.edu","firstName":"Nicole E.","lastName":"Familiari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"weronika.stachera@utsoutwestern.edu","firstName":"Weronika E.","lastName":"Stachera","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["conceptualization","formalAnalysis","project","writing_originalDraft","fundingAcquisition"],"email":"jeffrey.woodruff@utsouthwestern.edu","firstName":"Jeffrey B.","lastName":"Woodruff","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-5590-9620"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Proteomic results from anti-FLAG pull down experiments. N=3 replicates.
","doi":null,"resourceType":"Dataset","name":"Extended_Data_Set_1.xlsx","url":"https://portal.micropublication.org/uploads/47a5259ca2743e0b63d8c942758a4cd3.xlsx"}],"funding":"J.B. Woodruff was supported by supported by the Pew Charitable Trust, the Welch Foundation (V-I-0004-20230731), an R35 grant from the National Institute of General Medical Sciences (5R35GM142522), and the Endowed Scholars program at UT Southwestern.
","image":{"url":"https://portal.micropublication.org/uploads/cb8786d40ba480c97d52065ee381e246.png"},"imageCaption":"A. Top, confocal image of a day 2 adult feminized worm gonad expressing IFET1::mSCarlet::AID*::3xFlag. Bottom, schematic of IFET-1::3XFlag pulldown assay and mass spectrometry analysis of interacting proteins.
B. Volcano plot of protein abundances in pulldown experiment using ifet-1::mScarlet::AID*::3xFLAG; fem-1(hc17) adult females vs fem-1(hc17) worms as a control. Y-axis represents the –Log transformation of the obtained p-values. X-axis represents fold enrichment in abundance (FLAG-tag vs. control; n = 3 replicates). See Extended Data Set 1 for more information.
C. Log2 transformed fold changes of selected top IFET-1 pulldown hits grouped by gene ontology, molecular function, and biological process categories. Note: LSM-4 was identified in the IFET-1::3xFLAG pull-down and not in the control; thus, a fold-change score could not be determined.
D. Feminized worms were treated with RNAi, then mated with untreated males. Shown is embryo viability post mating (mean ±95% C.I; >25 offspring counted from n=25 mothers (control), n=16 (penr-1), n=9 (sqd-1), n=7 (lsm-4), n=9 (cid-1), n=5 (patr-1), n=4 (edc-3), n=6 (fndc-1), n=7 (sup-26), n=10 (CELE_W01F3.2), n=5 (F26E4.3), n=5 (CELE_F56G4.6), n=5 (CELE_T13H5.8), and n=5 (acly-1)). p-value=0.0007 (control vs. penr-1), p-value<0.0001 (control vs. sqd-1) and p-value<0.0001 (control vs. lsm-4). P values from one-way ANOVA followed with Dunnet's multiple comparisons test.
","imageTitle":"IP-mass spectrometry identifies diverse interacting partners of IFET-1 in C. elegans females
","methods":"Worm husbandry
Worms were grown on Nematode Growth Media (NGM) plates and fed with standard OP50 E. coli. All worms were kept at 16°C for maintenance and 20°C for experiments. fem-1 lines were shifted to 25°C for 2.5 days starting at L1 stage to feminize until adulthood at which point they were moved to 20°C. Experiments involving synchronization were done using 5% sodium hypochlorite and 5 M NaOH to remove all larvae and adult worms. Embryos were then rotated in M9 overnight to hatch.
IFET-1 pull down and mass spectrometry
fem-1(hc17) and fem-1; ifet-1::3XFLAG worms were grown at 16°C on large NGM plates for about a week until they became densely populated. The worms were then washed off with M9 PEG and added to large flasks containing S-Medium Complete as described in Wormbook Maintenance of C. elegans: Chapter 5. The liquid culture was grown in a 16°C shaker for about 4 days. The worms were then washed and synchronized using the same reagents described above. After rotating overnight, new liquid culture flasks were started using the synchronized L1 worms and grown in a 25°C shaker for 2.5 days. They were then transferred to 20°C to grow for a day.
The feminized adult worm samples were collected, pelleted, and flash frozen in PBS containing protease inhibitors. On the day of the pulldown experiment, ChromoTek DYKDDDDK Fab-Trap™ Agarose beads were equilibrated in low salt buffer (165mM KCl, 25 mM HEPES, 1% glycerol and 0.05% Tween 20). They were then blocked for 1 hour at 4°C with 3% milk in low salt buffer and washed 3 times with lysis buffer. While the beads blocked, the feminized worm pellets were thawed at 4°C in lysis buffer (50mM HEPES, 1mM EGTA, 100mM KCL, 1mM MgCl2, 0.05% NP-40 and 1X protease inhibitors added fresh). They were then lysed by dounce homogenization and sonication at 35% amplitude. This lysate was then centrifuged at 17000 g for 25 minutes at 4°C. The lysate supernatant was then incubated on a rotator with the prepared beads for 10 minutes at room temperature and then at 4°C for 1 hour. The beads were sedimented and washed 3 times with low salt buffer. Samples were eluted with SDS and boiled for 5 min. They were then run on an SDS-PAGE gel for a few minutes so they would enter the gel, stained with Instant blue dye and carefully cut out to send to the mass spectrometry core facility.
For mass spectrometry, gel samples were digested overnight with trypsin (Pierce) after reduction and alkylation with DTT and iodoacetamide (Sigma-Aldrich). After solid-phase extraction cleanup with an Oasis HLB μElution plate (Waters), the resulting peptides were reconstituted in 2% (vol/vol) acetonitrile (ACN) and 0.1% trifluoroacetic acid in water. 1 μg of each sample was injected onto an Orbitrap Fusion Lumos mass spectrometer coupled to an UltiMate 3000 RSLCnano liquid chromatography system (Thermo Fisher Scientific). Samples were injected onto a 75 μm i.d., 75-cm-long EasySpray column (Thermo Fisher Scientific), and eluted with a gradient from 0 to 28% buffer B over 90 min. Buffer A contained 2% (vol/vol) ACN and 0.1% formic acid in water, and buffer B contained 80% (vol/vol) ACN, 10% (vol/vol) trifluoroethanol, and 0.1% formic acid in water. The mass spectrometer operated in positive ion mode with a source voltage of 2.5 kV and an ion transfer tube temperature of 300°C. MS scans were acquired at 120,000 resolution in the Orbitrap, and up to 10 MS/MS spectra were obtained in the Orbitrap for each full spectrum acquired using higher energy collisional dissociation (HCD) for ions with charges 2–7. Dynamic exclusion was set for 25 s after an ion was selected for fragmentation.
Raw MS data files were analyzed using Proteome Discoverer v3.0 (Thermo Fisher Scientific), with peptide identification performed using Sequest HT searching against the C. elegans reviewed protein database from UniProt along with the sequence of fluorescent mMaple protein. Fragment and precursor tolerances of 10 ppm and 0.6 D were specified, and three missed cleavages were allowed. Carbamidomethylation of Cys was set as a fixed modification, and oxidation of Met was set as a variable modification. The false discovery rate cutoff was 1% for all peptides.
RNAi Screen and viability assays
RNAi clones were obtained from the Ahringer library or cloned using the pL4440 empty vector plasmid and target DNA sequences of 300 bp ordered from TWIST biosciences. RNAi plates were made by growing the feeding clone containing bacteria on NGM plates containing 1mM IPTG and 100 μg/ml ampicillin. Worms were synchronized and grown on these plates for 2.5 days at 25°C for feminized worms. Feminized worms were put on mating plates at D1 stage at a ratio of 1 female per 3 males for 16 hours at 16°C. The number of embryos laid per mom was tallied and 2 days later the fraction of hatchlings was counted to obtain the viability of the laid eggs.
Microscopy
The microscope image was taken using a 40X silicone (NA 1.25) objective on a Nikon AX-R confocal microscope.
","reagents":"Table S1: Worm Strains
Strain name
| Genotype | Source |
CGC | ||
| CGC | |
wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | CGC | |
JWW 255 | fem-1 (hc17) IV; ifet-1(dfw16[ifet-1::mScarlet_I::AID*::3xFlag]) III; wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | Our lab |
Table S2: Plasmids and RNAi Feeding Clones
Plasmid Name | Parent Plasmid | Targeting Sequence |
JWB 124 | pL4440 | Empty Vector |
JWB 226 | pL4440 | |
JWB 227 | pL4440 | |
JWB 238 | pL4440 | |
JWB 239 | pL4440 | |
JWB 240 | pL4440 | |
JWB 241 | pL4440 | |
JWB 242 | pL4440 | |
JWB 243 | pL4440 | CELE_W01F3.2 |
JWB 244 | pL4440 | CELE_F56G4.6 |
JWB 245 | pL4440 | CELE_T13H5.8 |
JWB 246 | pL4440 | |
JWB 254 | pL4440 | |
JWB 264 | pL4440 |
In C. elegans, RNA-rich biomolecular condensates called germ granules are required for germ cell proliferation and sperm/oocyte development (Huggins et al., 2020; Kawasaki et al., 2004; Spike et al., 2008a; Spike et al., 2008b). Germ granules are multi-phase compartments, which allows for localized concentration of distinct protein pools and specialized functions in RNA processing and export from the nucleus. One important sub-compartment is the P-body, which contains the dead box helicase DDX6 (CGH-1 in C. elegans), the LSM domain-containing protein LSM14 (CAR-1), the translation initiation factor eIF4E (IFE-3), and the eIF4E Transporter (IFET-1)(Huang et al., 2025). IFET-1 enables selective repression of certain developmental transcripts, while promoting translation of others encoding cytoskeletal proteins (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). It is likely that IFET-1 acts together with other P-body proteins to execute these diverse functions. For example, eIF4E Transporter interacts directly with DDX6 and LSM14 (Ozgur et al., 2015; Brandmann et al., 2018), and IFET-1 has been pulled down with IFE-3 (Li et al., 2009). Thus, we reasoned that by identifying interacting partners of IFET-1, we could discover new factors that are essential for translational control during oocyte development and storage.
To identify IFET-1 binding partners, we used FLAG-Trap beads (anti-DYKDDDK agarose) to pull down FLAG-tagged IFET-1 (IFET-1::mScarlet::3XFLAG) from adult female worms grown in liquid culture. In this line, IFET-1 localized to cytoplasmic puncta in oocytes and around the nuclei in the syncytial gonad, as expected (Fig. 1A). This construct was verified to be functional in our prior study (Bhatia et al., 2025). Female worms expressing untagged IFET-1 were used as a control. We analyzed co-purifying proteins by mass spectrometry and defined positive hits as being significantly enriched in the positive sample (enrichment >3-fold, p value <0.05; three replicates).
Top hits included IFET-1 and known IFET-1 interactors such as IFE-3, CAR-1, and CGH-1 (Huggins et al., 2020; Sengupta et al., 2013), validating our approach (Fig. 1B). GO term analysis revealed that IFET-1's top binding partners consisted mostly of proteins involved in translation or mRNA regulation, consistent with reported functions for IFET-1 (Fig. 1C) (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). To find novel proteins that promote oocyte production and viability, we used RNAi to knock down 13 of the top hits not known previously to be IFET-1 interactors (Fig. 1D). Of these, only knockdown of lsm-4, sqd-1, and penr-1 reduced the percentage of viable embryos laid by RNAi-treated female worms mated with untreated males (Fig. 1D). LSM-4 and SQD-1 are both RNA binding proteins that have been characterized in oocyte development (Cornes et al., 2015; Erdmann et al., 2024). PENR-1 was originally identified in a high-throughput screen for genes that affect expression of the transcription factor PHA-4 during C. elegans embryogenesis (Green et al., 2024). The exact role of PENR-1 protein in germline formation remains unknown.
In summary, we identified interacting partners of IFET-1, which could potentially explain how IFET-1 plays multiple roles in germline development and translational control. IFET-1 likely suppresses translation of specific transcripts by binding to IFE-3—the cap-binding eIF4E initiation factor—and blocking its ability form a complex with eIF4G, thus preventing ribosome recruitment (Peter et al., 2015; Huggins et al, 2020). Some interactors, such as CAR-1 and CGH-1, likely cooperate with IFET-1 in the P-body to sequester developmentally regulated mRNAs. Most of the other interactors have similar characterized roles in mRNA binding and processing. Interestingly, we identified unexpected interactors that do not have well-defined roles, one of which (PENR-1) is also required for oocyte development. Future studies are needed to clarify how these IFET-1 partners could contribute to germline expansion and promotion of translation during oocyte storage.
","references":[{"reference":"Bhatia P, Tafur J, Amin R, Familiari NE, Yaguchi K, Tran VM, et al., Woodruff JB. 2025. Condensate-forming eIF4ET ensures adequate levels of meiotic proteins to support oocyte storage. Life Sci Alliance 8(8): 10.26508/lsa.202503387.
","pubmedId":"40441896","doi":""},{"reference":"Brandmann T, Fakim H, Padamsi Z, Youn JY, Gingras AC, Fabian MR, Jinek M. 2018. Molecular architecture of LSM14 interactions involved in the assembly of mRNA silencing complexes. EMBO J 37(7): 10.15252/embj.201797869.
","pubmedId":"29510985","doi":""},{"reference":"Cornes E, Porta-De-La-Riva M, Aristizábal-Corrales D, Brokate-Llanos AM, García-Rodríguez FJ, Ertl I, et al., Cerón J. 2015. Cytoplasmic LSM-1 protein regulates stress responses through the insulin/IGF-1 signaling pathway in Caenorhabditis elegans. RNA 21(9): 1544-53.
","pubmedId":"26150554","doi":""},{"reference":"Erdmann EA, Forbes M, Becker M, Perez S, Hundley HA. 2024. ADR-2 regulates fertility and oocyte fate in C. elegans. bioRxiv: pii: 2023.11.01.565157. 10.1101/2023.11.01.565157.
","pubmedId":"37961348","doi":""},{"reference":"Green RA, Khaliullin RN, Zhao Z, Ochoa SD, Hendel JM, Chow TL, et al., Oegema K. 2024. Automated profiling of gene function during embryonic development. Cell 187(12): 3141-3160.e23.
","pubmedId":"38759650","doi":""},{"reference":"Huang X, Feng X, Yan YH, Xu D, Wang K, Zhu C, et al., Chen X. 2025. Compartmentalized localization of perinuclear proteins within germ granules in C. elegans. Dev Cell 60(8): 1251-1270.e3.
","pubmedId":"39742661","doi":""},{"reference":"Huggins HP, Subash JS, Stoffel H, Henderson MA, Hoffman JL, Buckner DS, et al., Keiper BD. 2020. Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans. J Cell Sci 133(6): 10.1242/jcs.237990.
","pubmedId":"32079657","doi":""},{"reference":"Kawasaki I, Amiri A, Fan Y, Meyer N, Dunkelbarger S, Motohashi T, et al., Strome S. 2004. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 167(2): 645-61.
","pubmedId":"15238518","doi":""},{"reference":"Li W, DeBella LR, Guven-Ozkan T, Lin R, Rose LS. 2009. An eIF4E-binding protein regulates katanin protein levels in C. elegans embryos. J Cell Biol 187(1): 33-42.
","pubmedId":"19786575","doi":""},{"reference":"Ozgur S, Basquin J, Kamenska A, Filipowicz W, Standart N, Conti E. 2015. Structure of a Human 4E-T/DDX6/CNOT1 Complex Reveals the Different Interplay of DDX6-Binding Proteins with the CCR4-NOT Complex. Cell Rep 13(4): 703-711.
","pubmedId":"26489469","doi":""},{"reference":"Peter D, Igreja C, Weber R, Wohlbold L, Weiler C, Ebertsch L, Weichenrieder O, Izaurralde E. 2015. Molecular architecture of 4E-BP translational inhibitors bound to eIF4E. Mol Cell 57(6): 1074-1087.
","pubmedId":"25702871","doi":""},{"reference":"Sengupta MS, Low WY, Patterson JR, Kim HM, Traven A, Beilharz TH, et al., Boag PR. 2013. ifet-1 is a broad-scale translational repressor required for normal P granule formation in C. elegans. J Cell Sci 126(Pt 3): 850-9.
","pubmedId":"23264733","doi":""},{"reference":"Spike C, Meyer N, Racen E, Orsborn A, Kirchner J, Kuznicki K, et al., Strome S. 2008. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178(4): 1973-87.
","pubmedId":"18430929","doi":""},{"reference":"Spike CA, Bader J, Reinke V, Strome S. 2008. DEPS-1 promotes P-granule assembly and RNA interference in C. elegans germ cells. Development 135(5): 983-93.
","pubmedId":"18234720","doi":""}],"title":"Identification of eIF4ET binding partners in C. elegans
","reviews":[{"reviewer":{"displayName":"Andrea Putnam"},"openAcknowledgement":false,"status":{"submitted":true}}],"curatorReviews":[{"curator":{"displayName":"Jaehyoung Cho"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Gary Craig Schindelman"},"openAcknowledgement":false,"submitted":"1784075857239"},{"curator":{"displayName":"KJ Yook"},"openAcknowledgement":false,"submitted":"1784500147404"}]},{"id":"284c1c69-5f68-4f76-b34b-512478258fb7","decision":"accept","abstract":"The eIF4ET family protein IFET-1 is needed for oocyte development and long-term storage in C. elegans. How IFET-1 plays multiple roles in oocyte biology is unclear. Using pull-downs and mass spectrometry, we identified proteins that interact with IFET-1. We show that three IFET-1-interacting partners—PENR-1, SQD-1, and LSM-4—are essential for producing viable oocytes in C. elegans females.
","acknowledgements":"We thank the Proteomics Core Facility at UT Southwestern.
","authors":[{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["investigation","methodology","writing_originalDraft","writing_reviewEditing","dataCuration","formalAnalysis"],"email":"judith.tafur@utsouthwestern.edu","firstName":"Judith","lastName":"Tafur","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"angelica.moralescueva@UTSouthwestern.edu","firstName":"Angelica","lastName":"Morales Cueva","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"nicole.familiari@utsouthwestern.edu","firstName":"Nicole E.","lastName":"Familiari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"weronika.stachera@utsoutwestern.edu","firstName":"Weronika E.","lastName":"Stachera","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["conceptualization","formalAnalysis","project","writing_originalDraft","fundingAcquisition"],"email":"jeffrey.woodruff@utsouthwestern.edu","firstName":"Jeffrey B.","lastName":"Woodruff","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-5590-9620"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Proteomic data and a list of meaningful IFET-1 interactors.
","doi":"10.22002/je5p4-zyb48","resourceType":"Dataset","name":"Extended_Data_Set_1.xlsx","url":"https://portal.micropublication.org/uploads/54cc92983e57a1afa5d7e85df1a495ab.xlsx"}],"funding":"J.B. Woodruff was supported by supported by the Pew Charitable Trust, the Welch Foundation (V-I-0004-20230731), an R35 grant from the National Institute of General Medical Sciences (5R35GM142522), and the Endowed Scholars program at UT Southwestern.
","image":{"url":"https://portal.micropublication.org/uploads/cb8786d40ba480c97d52065ee381e246.png"},"imageCaption":"A. Top, confocal image of a day 2 adult feminized worm gonad expressing IFET1::mSCarlet::AID*::3xFlag. Bottom, schematic of IFET-1::3XFlag pulldown assay and mass spectrometry analysis of interacting proteins.
B. Volcano plot of protein abundances in pulldown experiment using ifet-1::mScarlet::AID*::3xFLAG; fem-1(hc17) adult females vs fem-1(hc17) worms as a control. Y-axis represents the –Log transformation of the obtained p-values. X-axis represents fold enrichment in abundance (FLAG-tag vs. control; n = 3 replicates). See Extended Data Set 1 for more information.
C. Log2 transformed fold changes of selected top IFET-1 pulldown hits grouped by gene ontology, molecular function, and biological process categories. Note: LSM-4 was identified in the IFET-1::3xFLAG pull-down and not in the control; thus, a fold-change score could not be determined.
D. Feminized worms were treated with RNAi, then mated with untreated males. Shown is embryo viability post mating (mean ±95% C.I; >25 offspring counted from n=25 mothers (control), n=16 (penr-1), n=9 (sqd-1), n=7 (lsm-4), n=9 (cid-1), n=5 (patr-1), n=4 (edc-3), n=6 (fndc-1), n=7 (sup-26), n=10 (CELE_W01F3.2), n=5 (F26E4.3), n=5 (CELE_F56G4.6), n=5 (CELE_T13H5.8), and n=5 (acly-1)). p-value=0.0007 (control vs. penr-1), p-value<0.0001 (control vs. sqd-1) and p-value<0.0001 (control vs. lsm-4). P values from one-way ANOVA followed with Dunnet's multiple comparisons test.
","imageTitle":"IP-mass spectrometry identifies diverse interacting partners of IFET-1 in C. elegans females
","methods":"Worm husbandry
Worms were grown on Nematode Growth Media (NGM) plates and fed with standard OP50 E. coli. All worms were kept at 16°C for maintenance and 20°C for experiments. fem-1 lines were shifted to 25°C for 2.5 days starting at L1 stage to feminize until adulthood at which point they were moved to 20°C. Experiments involving synchronization were done using 5% sodium hypochlorite and 5 M NaOH to remove all larvae and adult worms. Embryos were then rotated in M9 overnight to hatch.
IFET-1 pull down and mass spectrometry
fem-1(hc17) and fem-1; ifet-1::3XFLAG worms were grown at 16°C on large NGM plates for about a week until they became densely populated. The worms were then washed off with M9 PEG and added to large flasks containing S-Medium Complete as described in Wormbook Maintenance of C. elegans: Chapter 5. The liquid culture was grown in a 16°C shaker for about 4 days. The worms were then washed and synchronized using the same reagents described above. After rotating overnight, new liquid culture flasks were started using the synchronized L1 worms and grown in a 25°C shaker for 2.5 days. They were then transferred to 20°C to grow for a day.
The feminized adult worm samples were collected, pelleted, and flash frozen in PBS containing protease inhibitors. On the day of the pulldown experiment, ChromoTek DYKDDDDK Fab-Trap™ Agarose beads were equilibrated in low salt buffer (165mM KCl, 25 mM HEPES, 1% glycerol and 0.05% Tween 20). They were then blocked for 1 hour at 4°C with 3% milk in low salt buffer and washed 3 times with lysis buffer. While the beads blocked, the feminized worm pellets were thawed at 4°C in lysis buffer (50mM HEPES, 1mM EGTA, 100mM KCL, 1mM MgCl2, 0.05% NP-40 and 1X protease inhibitors added fresh). They were then lysed by dounce homogenization and sonication at 35% amplitude. This lysate was then centrifuged at 17000 g for 25 minutes at 4°C. The lysate supernatant was then incubated on a rotator with the prepared beads for 10 minutes at room temperature and then at 4°C for 1 hour. The beads were sedimented and washed 3 times with low salt buffer. Samples were eluted with SDS and boiled for 5 min. They were then run on an SDS-PAGE gel for a few minutes so they would enter the gel, stained with Instant blue dye and carefully cut out to send to the mass spectrometry core facility.
For mass spectrometry, gel samples were digested overnight with trypsin (Pierce) after reduction and alkylation with DTT and iodoacetamide (Sigma-Aldrich). After solid-phase extraction cleanup with an Oasis HLB μElution plate (Waters), the resulting peptides were reconstituted in 2% (vol/vol) acetonitrile (ACN) and 0.1% trifluoroacetic acid in water. 1 μg of each sample was injected onto an Orbitrap Fusion Lumos mass spectrometer coupled to an UltiMate 3000 RSLCnano liquid chromatography system (Thermo Fisher Scientific). Samples were injected onto a 75 μm i.d., 75-cm-long EasySpray column (Thermo Fisher Scientific), and eluted with a gradient from 0 to 28% buffer B over 90 min. Buffer A contained 2% (vol/vol) ACN and 0.1% formic acid in water, and buffer B contained 80% (vol/vol) ACN, 10% (vol/vol) trifluoroethanol, and 0.1% formic acid in water. The mass spectrometer operated in positive ion mode with a source voltage of 2.5 kV and an ion transfer tube temperature of 300°C. MS scans were acquired at 120,000 resolution in the Orbitrap, and up to 10 MS/MS spectra were obtained in the Orbitrap for each full spectrum acquired using higher energy collisional dissociation (HCD) for ions with charges 2–7. Dynamic exclusion was set for 25 s after an ion was selected for fragmentation.
Raw MS data files were analyzed using Proteome Discoverer v3.0 (Thermo Fisher Scientific), with peptide identification performed using Sequest HT searching against the C. elegans reviewed protein database from UniProt along with the sequence of fluorescent mMaple protein. Fragment and precursor tolerances of 10 ppm and 0.6 D were specified, and three missed cleavages were allowed. Carbamidomethylation of Cys was set as a fixed modification, and oxidation of Met was set as a variable modification. The false discovery rate cutoff was 1% for all peptides.
RNAi Screen and viability assays
RNAi clones were obtained from the Ahringer library or cloned using the pL4440 empty vector plasmid and target DNA sequences of 300 bp ordered from TWIST biosciences. RNAi plates were made by growing the feeding clone containing bacteria on NGM plates containing 1mM IPTG and 100 μg/ml ampicillin. fem-1(hc17) worms were synchronized at L1 stage, then grown on RNAi plates for 2.5 days at 25°C. Female adult worms were transferred to mating plates at a ratio of 1 female per 3 males, then incubated for 16 hours at 16°C. The number of embryos laid per mom was tallied and 2 days later the fraction of hatchlings was counted to obtain the viability of the laid eggs.
Microscopy
The microscope image was taken using a 40X silicone (NA 1.25) objective on a Nikon AX-R confocal microscope.
","reagents":"Table 1: Worm Strains
Strain name
| Genotype | Source |
CGC | ||
| CGC | |
wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | CGC | |
JWW255 | fem-1 (hc17) IV; ifet-1(dfw16[ifet-1::mScarlet_I::AID*::3xFlag]) III; wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | Our lab |
Table 2: Plasmids and RNAi Feeding Clones
Plasmid Name | Parent Plasmid | Targeting Sequence |
JWB 124 | pL4440 | Empty Vector |
JWB 226 | pL4440 | |
JWB 227 | pL4440 | |
JWB 238 | pL4440 | |
JWB 239 | pL4440 | |
JWB 240 | pL4440 | |
JWB 241 | pL4440 | |
JWB 242 | pL4440 | |
JWB 243 | pL4440 | CELE_W01F3.2 |
JWB 244 | pL4440 | CELE_F56G4.6 |
JWB 245 | pL4440 | CELE_T13H5.8 |
JWB 246 | pL4440 | |
JWB 254 | pL4440 | |
JWB 264 | pL4440 |
In C. elegans, RNA-rich biomolecular condensates called germ granules are required for germ cell proliferation and sperm/oocyte development (Huggins et al., 2020; Kawasaki et al., 2004; Spike et al., 2008a; Spike et al., 2008b). Germ granules are multi-phase compartments, which allows for localized concentration of distinct protein pools and specialized functions in RNA processing and export from the nucleus. One important sub-compartment is the P-body, which contains the dead box helicase DDX6 (CGH-1 in C. elegans), the LSM domain-containing protein LSM14 (CAR-1), the translation initiation factor eIF4E (IFE-3), and the eIF4E Transporter (IFET-1)(Huang et al., 2025). IFET-1 enables selective repression of certain developmental transcripts, while promoting translation of others encoding cytoskeletal proteins (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). It is likely that IFET-1 acts together with other P-body proteins to execute these diverse functions. For example, eIF4E Transporter interacts directly with DDX6 and LSM14 (Ozgur et al., 2015; Brandmann et al., 2018), and IFET-1 has been pulled down with IFE-3 (Li et al., 2009). Thus, we reasoned that by identifying interacting partners of IFET-1, we could discover new factors that are essential for translational control during oocyte development and storage.
To identify IFET-1 binding partners, we used FLAG-Trap beads (anti-DYKDDDK agarose) to pull down FLAG-tagged IFET-1 (IFET-1::mScarlet::3XFLAG) from adult female worms grown in liquid culture. In this line, IFET-1 localized to cytoplasmic puncta in oocytes and around the nuclei in the syncytial gonad, as expected (Fig. 1A). This construct was verified to be functional in our prior study (Bhatia et al., 2025). Female worms expressing untagged IFET-1 were used as a control. We analyzed co-purifying proteins by mass spectrometry and defined positive hits as being significantly enriched in the positive sample (enrichment >3-fold, p value <0.05; three replicates).
Top hits included IFET-1 and known IFET-1 interactors such as IFE-3, CAR-1, and CGH-1 (Huggins et al., 2020; Sengupta et al., 2013), validating our approach (Fig. 1B). GO term analysis revealed that IFET-1's top binding partners consisted mostly of proteins involved in translation or mRNA regulation, consistent with reported functions for IFET-1 (Fig. 1C) (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). To find novel proteins that promote oocyte production and viability, we used RNAi to knock down 13 of the top hits not known previously to be IFET-1 interactors (Fig. 1D). Of these, only knockdown of lsm-4, sqd-1, and penr-1 reduced the percentage of viable embryos laid by RNAi-treated female worms mated with untreated males (Fig. 1D). LSM-4 and SQD-1 are both RNA binding proteins that have been characterized in oocyte development (Cornes et al., 2015; Erdmann et al., 2024). PENR-1 was originally identified in a high-throughput screen for genes that affect expression of the transcription factor PHA-4 during C. elegans embryogenesis (Green et al., 2024). The exact role of PENR-1 protein in germline formation remains unknown.
In summary, we identified interacting partners of IFET-1, which could potentially explain how IFET-1 plays multiple roles in germline development and translational control. IFET-1 likely suppresses translation of specific transcripts by binding to IFE-3—the cap-binding eIF4E initiation factor—and blocking its ability form a complex with eIF4G, thus preventing ribosome recruitment (Peter et al., 2015; Huggins et al, 2020). Some interactors, such as CAR-1 and CGH-1, likely cooperate with IFET-1 in the P-body to sequester developmentally regulated mRNAs. Most of the other interactors have similar characterized roles in mRNA binding and processing. Interestingly, we identified unexpected interactors that do not have well-defined roles, one of which (PENR-1) is also required for oocyte development. Future studies are needed to clarify how these IFET-1 partners could contribute to germline expansion and promotion of translation during oocyte storage.
","references":[{"reference":"Bhatia P, Tafur J, Amin R, Familiari NE, Yaguchi K, Tran VM, et al., Woodruff JB. 2025. Condensate-forming eIF4ET ensures adequate levels of meiotic proteins to support oocyte storage. Life Sci Alliance 8(8): 10.26508/lsa.202503387.
","pubmedId":"40441896","doi":""},{"reference":"Brandmann T, Fakim H, Padamsi Z, Youn JY, Gingras AC, Fabian MR, Jinek M. 2018. Molecular architecture of LSM14 interactions involved in the assembly of mRNA silencing complexes. EMBO J 37(7): 10.15252/embj.201797869.
","pubmedId":"29510985","doi":""},{"reference":"Cornes E, Porta-De-La-Riva M, Aristizábal-Corrales D, Brokate-Llanos AM, García-Rodríguez FJ, Ertl I, et al., Cerón J. 2015. Cytoplasmic LSM-1 protein regulates stress responses through the insulin/IGF-1 signaling pathway in Caenorhabditis elegans. RNA 21(9): 1544-53.
","pubmedId":"26150554","doi":""},{"reference":"Erdmann EA, Forbes M, Becker M, Perez S, Hundley HA. 2024. ADR-2 regulates fertility and oocyte fate in C. elegans. bioRxiv: pii: 2023.11.01.565157. 10.1101/2023.11.01.565157.
","pubmedId":"37961348","doi":""},{"reference":"Green RA, Khaliullin RN, Zhao Z, Ochoa SD, Hendel JM, Chow TL, et al., Oegema K. 2024. Automated profiling of gene function during embryonic development. Cell 187(12): 3141-3160.e23.
","pubmedId":"38759650","doi":""},{"reference":"Huang X, Feng X, Yan YH, Xu D, Wang K, Zhu C, et al., Chen X. 2025. Compartmentalized localization of perinuclear proteins within germ granules in C. elegans. Dev Cell 60(8): 1251-1270.e3.
","pubmedId":"39742661","doi":""},{"reference":"Huggins HP, Subash JS, Stoffel H, Henderson MA, Hoffman JL, Buckner DS, et al., Keiper BD. 2020. Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans. J Cell Sci 133(6): 10.1242/jcs.237990.
","pubmedId":"32079657","doi":""},{"reference":"Kawasaki I, Amiri A, Fan Y, Meyer N, Dunkelbarger S, Motohashi T, et al., Strome S. 2004. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 167(2): 645-61.
","pubmedId":"15238518","doi":""},{"reference":"Li W, DeBella LR, Guven-Ozkan T, Lin R, Rose LS. 2009. An eIF4E-binding protein regulates katanin protein levels in C. elegans embryos. J Cell Biol 187(1): 33-42.
","pubmedId":"19786575","doi":""},{"reference":"Ozgur S, Basquin J, Kamenska A, Filipowicz W, Standart N, Conti E. 2015. Structure of a Human 4E-T/DDX6/CNOT1 Complex Reveals the Different Interplay of DDX6-Binding Proteins with the CCR4-NOT Complex. Cell Rep 13(4): 703-711.
","pubmedId":"26489469","doi":""},{"reference":"Peter D, Igreja C, Weber R, Wohlbold L, Weiler C, Ebertsch L, Weichenrieder O, Izaurralde E. 2015. Molecular architecture of 4E-BP translational inhibitors bound to eIF4E. Mol Cell 57(6): 1074-1087.
","pubmedId":"25702871","doi":""},{"reference":"Sengupta MS, Low WY, Patterson JR, Kim HM, Traven A, Beilharz TH, et al., Boag PR. 2013. ifet-1 is a broad-scale translational repressor required for normal P granule formation in C. elegans. J Cell Sci 126(Pt 3): 850-9.
","pubmedId":"23264733","doi":""},{"reference":"Spike C, Meyer N, Racen E, Orsborn A, Kirchner J, Kuznicki K, et al., Strome S. 2008. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178(4): 1973-87.
","pubmedId":"18430929","doi":""},{"reference":"Spike CA, Bader J, Reinke V, Strome S. 2008. DEPS-1 promotes P-granule assembly and RNA interference in C. elegans germ cells. Development 135(5): 983-93.
","pubmedId":"18234720","doi":""}],"title":"Identification of eIF4ET binding partners in C. elegans
","reviews":[],"curatorReviews":[{"curator":{"displayName":"Jaehyoung Cho"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Gary Craig Schindelman"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"KJ Yook"},"openAcknowledgement":false,"submitted":"1786336664708"}]},{"id":"35220764-11ea-44d6-ba73-0cfa66badbf5","decision":"publish","abstract":"The eIF4ET family protein IFET-1 is needed for oocyte development and long-term storage in C. elegans. How IFET-1 plays multiple roles in oocyte biology is unclear. Using pull-downs and mass spectrometry, we identified proteins that interact with IFET-1. We show that three IFET-1-interacting partners—PENR-1, SQD-1, and LSM-4—are essential for producing viable oocytes in C. elegans females.
","acknowledgements":"We thank the Proteomics Core Facility at UT Southwestern.
","authors":[{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["investigation","methodology","writing_originalDraft","writing_reviewEditing","dataCuration","formalAnalysis"],"email":"judith.tafur@utsouthwestern.edu","firstName":"Judith","lastName":"Tafur","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"angelica.moralescueva@UTSouthwestern.edu","firstName":"Angelica","lastName":"Morales Cueva","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"nicole.familiari@utsouthwestern.edu","firstName":"Nicole E.","lastName":"Familiari","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["methodology"],"email":"weronika.stachera@utsoutwestern.edu","firstName":"Weronika E.","lastName":"Stachera","submittingAuthor":false,"correspondingAuthor":false,"equalContribution":false,"WBId":null,"orcid":null},{"affiliations":["The University of Texas Southwestern Medical Center, Dallas, TX, United States"],"departments":["Cell Biology"],"credit":["conceptualization","formalAnalysis","project","writing_originalDraft","fundingAcquisition"],"email":"jeffrey.woodruff@utsouthwestern.edu","firstName":"Jeffrey B.","lastName":"Woodruff","submittingAuthor":true,"correspondingAuthor":true,"equalContribution":false,"WBId":null,"orcid":"0000-0002-5590-9620"}],"awards":[],"conflictsOfInterest":"The authors declare that there are no conflicts of interest present.
","dataTable":{"url":null},"extendedData":[{"description":"Proteomic data and a list of meaningful IFET-1 interactors.
","doi":"10.22002/je5p4-zyb48","resourceType":"Dataset","name":"Extended_Data_Set_1.xlsx","url":"https://portal.micropublication.org/uploads/54cc92983e57a1afa5d7e85df1a495ab.xlsx"}],"funding":"J.B. Woodruff was supported by supported by the Pew Charitable Trust, the Welch Foundation (V-I-0004-20230731), an R35 grant from the National Institute of General Medical Sciences (5R35GM142522), and the Endowed Scholars program at UT Southwestern.
","image":{"url":"https://portal.micropublication.org/uploads/cb8786d40ba480c97d52065ee381e246.png"},"imageCaption":"A. Top, confocal image of a day 2 adult feminized worm gonad expressing IFET1::mSCarlet::AID*::3xFlag. Bottom, schematic of IFET-1::3XFlag pulldown assay and mass spectrometry analysis of interacting proteins.
B. Volcano plot of protein abundances in pulldown experiment using ifet-1::mScarlet::AID*::3xFLAG; fem-1(hc17) adult females vs fem-1(hc17) worms as a control. Y-axis represents the –Log transformation of the obtained p-values. X-axis represents fold enrichment in abundance (FLAG-tag vs. control; n = 3 replicates). See Extended Data Set 1 for more information.
C. Log2 transformed fold changes of selected top IFET-1 pulldown hits grouped by gene ontology, molecular function, and biological process categories. Note: LSM-4 was identified in the IFET-1::3xFLAG pull-down and not in the control; thus, a fold-change score could not be determined.
D. Feminized worms were treated with RNAi, then mated with untreated males. Shown is embryo viability post mating (mean ±95% C.I; >25 offspring counted from n=25 mothers (control), n=16 (penr-1), n=9 (sqd-1), n=7 (lsm-4), n=9 (cid-1), n=5 (patr-1), n=4 (edc-3), n=6 (fndc-1), n=7 (sup-26), n=10 (CELE_W01F3.2), n=5 (F26E4.3), n=5 (CELE_F56G4.6), n=5 (CELE_T13H5.8), and n=5 (acly-1)). p-value=0.0007 (control vs. penr-1), p-value<0.0001 (control vs. sqd-1) and p-value<0.0001 (control vs. lsm-4). P values from one-way ANOVA followed with Dunnet's multiple comparisons test.
","imageTitle":"IP-mass spectrometry identifies diverse interacting partners of IFET-1 in C. elegans females
","methods":"Worm husbandry
Worms were grown on Nematode Growth Media (NGM) plates and fed with standard OP50 E. coli. All worms were kept at 16°C for maintenance and 20°C for experiments. fem-1 lines were shifted to 25°C for 2.5 days starting at L1 stage to feminize until adulthood at which point they were moved to 20°C. Experiments involving synchronization were done using 5% sodium hypochlorite and 5 M NaOH to remove all larvae and adult worms. Embryos were then rotated in M9 overnight to hatch.
IFET-1 pull down and mass spectrometry
fem-1(hc17) and fem-1; ifet-1::3XFLAG worms were grown at 16°C on large NGM plates for about a week until they became densely populated. The worms were then washed off with M9 PEG and added to large flasks containing S-Medium Complete as described in Wormbook Maintenance of C. elegans: Chapter 5. The liquid culture was grown in a 16°C shaker for about 4 days. The worms were then washed and synchronized using the same reagents described above. After rotating overnight, new liquid culture flasks were started using the synchronized L1 worms and grown in a 25°C shaker for 2.5 days. They were then transferred to 20°C to grow for a day.
The feminized adult worm samples were collected, pelleted, and flash frozen in PBS containing protease inhibitors. On the day of the pulldown experiment, ChromoTek DYKDDDDK Fab-Trap™ Agarose beads were equilibrated in low salt buffer (165mM KCl, 25 mM HEPES, 1% glycerol and 0.05% Tween 20). They were then blocked for 1 hour at 4°C with 3% milk in low salt buffer and washed 3 times with lysis buffer. While the beads blocked, the feminized worm pellets were thawed at 4°C in lysis buffer (50mM HEPES, 1mM EGTA, 100mM KCL, 1mM MgCl2, 0.05% NP-40 and 1X protease inhibitors added fresh). They were then lysed by dounce homogenization and sonication at 35% amplitude. This lysate was then centrifuged at 17000 g for 25 minutes at 4°C. The lysate supernatant was then incubated on a rotator with the prepared beads for 10 minutes at room temperature and then at 4°C for 1 hour. The beads were sedimented and washed 3 times with low salt buffer. Samples were eluted with SDS and boiled for 5 min. They were then run on an SDS-PAGE gel for a few minutes so they would enter the gel, stained with Instant blue dye and carefully cut out to send to the mass spectrometry core facility.
For mass spectrometry, gel samples were digested overnight with trypsin (Pierce) after reduction and alkylation with DTT and iodoacetamide (Sigma-Aldrich). After solid-phase extraction cleanup with an Oasis HLB μElution plate (Waters), the resulting peptides were reconstituted in 2% (vol/vol) acetonitrile (ACN) and 0.1% trifluoroacetic acid in water. 1 μg of each sample was injected onto an Orbitrap Fusion Lumos mass spectrometer coupled to an UltiMate 3000 RSLCnano liquid chromatography system (Thermo Fisher Scientific). Samples were injected onto a 75 μm i.d., 75-cm-long EasySpray column (Thermo Fisher Scientific), and eluted with a gradient from 0 to 28% buffer B over 90 min. Buffer A contained 2% (vol/vol) ACN and 0.1% formic acid in water, and buffer B contained 80% (vol/vol) ACN, 10% (vol/vol) trifluoroethanol, and 0.1% formic acid in water. The mass spectrometer operated in positive ion mode with a source voltage of 2.5 kV and an ion transfer tube temperature of 300°C. MS scans were acquired at 120,000 resolution in the Orbitrap, and up to 10 MS/MS spectra were obtained in the Orbitrap for each full spectrum acquired using higher energy collisional dissociation (HCD) for ions with charges 2–7. Dynamic exclusion was set for 25 s after an ion was selected for fragmentation.
Raw MS data files were analyzed using Proteome Discoverer v3.0 (Thermo Fisher Scientific), with peptide identification performed using Sequest HT searching against the C. elegans reviewed protein database from UniProt along with the sequence of fluorescent mMaple protein. Fragment and precursor tolerances of 10 ppm and 0.6 D were specified, and three missed cleavages were allowed. Carbamidomethylation of Cys was set as a fixed modification, and oxidation of Met was set as a variable modification. The false discovery rate cutoff was 1% for all peptides.
RNAi Screen and viability assays
RNAi clones were obtained from the Ahringer library or cloned using the pL4440 empty vector plasmid and target DNA sequences of 300 bp ordered from TWIST biosciences. RNAi plates were made by growing the feeding clone containing bacteria on NGM plates containing 1mM IPTG and 100 μg/ml ampicillin. fem-1(hc17) worms were synchronized at L1 stage, then grown on RNAi plates for 2.5 days at 25°C. Female adult worms were transferred to mating plates at a ratio of 1 female per 3 males, then incubated for 16 hours at 16°C. The number of embryos laid per mom was tallied and 2 days later the fraction of hatchlings was counted to obtain the viability of the laid eggs.
Microscopy
The microscope image was taken using a 40X silicone (NA 1.25) objective on a Nikon AX-R confocal microscope.
","reagents":"Table 1: Worm Strains
Strain name
| Genotype | Source |
CGC | ||
| CGC | |
wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | CGC | |
fem-1 (hc17) IV; ifet-1(dfw16[ifet-1::mScarlet_I::AID*::3xFlag]) III; wrdSi3 [sun-1p::TIR1::F2A::mTagBFP2::AID*::NLS::tbb-2 3'UTR] (II:0.77) | Our lab |
Table 2: Plasmids and RNAi Feeding Clones
Plasmid Name | Parent Plasmid | Targeting Sequence |
JWB 124 | pL4440 | Empty Vector |
JWB 226 | pL4440 | |
JWB 227 | pL4440 | |
JWB 238 | pL4440 | |
JWB 239 | pL4440 | |
JWB 240 | pL4440 | |
JWB 241 | pL4440 | |
JWB 242 | pL4440 | |
JWB 243 | pL4440 | CELE_W01F3.2 |
JWB 244 | pL4440 | CELE_F56G4.6 |
JWB 245 | pL4440 | CELE_T13H5.8 |
JWB 246 | pL4440 | |
JWB 254 | pL4440 | |
JWB 264 | pL4440 |
In C. elegans, RNA-rich biomolecular condensates called germ granules are required for germ cell proliferation and sperm/oocyte development (Huggins et al., 2020; Kawasaki et al., 2004; Spike et al., 2008a; Spike et al., 2008b). Germ granules are multi-phase compartments, which allows for localized concentration of distinct protein pools and specialized functions in RNA processing and export from the nucleus. One important sub-compartment is the P-body, which contains the dead box helicase DDX6 (CGH-1 in C. elegans), the LSM domain-containing protein LSM14 (CAR-1), the translation initiation factor eIF4E (IFE-3), and the eIF4E Transporter (IFET-1)(Huang et al., 2025). IFET-1 enables selective repression of certain developmental transcripts, while promoting translation of others encoding cytoskeletal proteins (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). It is likely that IFET-1 acts together with other P-body proteins to execute these diverse functions. For example, eIF4E Transporter interacts directly with DDX6 and LSM14 (Ozgur et al., 2015; Brandmann et al., 2018), and IFET-1 has been pulled down with IFE-3 (Li et al., 2009). Thus, we reasoned that by identifying interacting partners of IFET-1, we could discover new factors that are essential for translational control during oocyte development and storage.
To identify IFET-1 binding partners, we used FLAG-Trap beads (anti-DYKDDDK agarose) to pull down FLAG-tagged IFET-1 (IFET-1::mScarlet::3XFLAG) from adult female worms grown in liquid culture. In this line, IFET-1 localized to cytoplasmic puncta in oocytes and around the nuclei in the syncytial gonad, as expected (Fig. 1A). This construct was verified to be functional in our prior study (Bhatia et al., 2025). Female worms expressing untagged IFET-1 were used as a control. We analyzed co-purifying proteins by mass spectrometry and defined positive hits as being significantly enriched in the positive sample (enrichment >3-fold, p value <0.05; three replicates).
Top hits included IFET-1 and known IFET-1 interactors such as IFE-3, CAR-1, and CGH-1 (Huggins et al., 2020; Sengupta et al., 2013), validating our approach (Fig. 1B). GO term analysis revealed that IFET-1's top binding partners consisted mostly of proteins involved in translation or mRNA regulation, consistent with reported functions for IFET-1 (Fig. 1C) (Bhatia et al., 2025; Huggins et al., 2020; Sengupta et al., 2013). To find novel proteins that promote oocyte production and viability, we used RNAi to knock down 13 of the top hits not known previously to be IFET-1 interactors (Fig. 1D). Of these, only knockdown of lsm-4, sqd-1, and penr-1 reduced the percentage of viable embryos laid by RNAi-treated female worms mated with untreated males (Fig. 1D). LSM-4 and SQD-1 are both RNA binding proteins that have been characterized in oocyte development (Cornes et al., 2015; Erdmann et al., 2024). PENR-1 was originally identified in a high-throughput screen for genes that affect expression of the transcription factor PHA-4 during C. elegans embryogenesis (Green et al., 2024). The exact role of PENR-1 protein in germline formation remains unknown.
In summary, we identified interacting partners of IFET-1, which could potentially explain how IFET-1 plays multiple roles in germline development and translational control. IFET-1 likely suppresses translation of specific transcripts by binding to IFE-3—the cap-binding eIF4E initiation factor—and blocking its ability form a complex with eIF4G, thus preventing ribosome recruitment (Peter et al., 2015; Huggins et al, 2020). Some interactors, such as CAR-1 and CGH-1, likely cooperate with IFET-1 in the P-body to sequester developmentally regulated mRNAs. Most of the other interactors have similar characterized roles in mRNA binding and processing. Interestingly, we identified unexpected interactors that do not have well-defined roles, one of which (PENR-1) is also required for oocyte development. Future studies are needed to clarify how these IFET-1 partners could contribute to germline expansion and promotion of translation during oocyte storage.
","references":[{"reference":"Bhatia P, Tafur J, Amin R, Familiari NE, Yaguchi K, Tran VM, et al., Woodruff JB. 2025. Condensate-forming eIF4ET ensures adequate levels of meiotic proteins to support oocyte storage. Life Sci Alliance 8(8): 10.26508/lsa.202503387.
","pubmedId":"40441896","doi":""},{"reference":"Brandmann T, Fakim H, Padamsi Z, Youn JY, Gingras AC, Fabian MR, Jinek M. 2018. Molecular architecture of LSM14 interactions involved in the assembly of mRNA silencing complexes. EMBO J 37(7): 10.15252/embj.201797869.
","pubmedId":"29510985","doi":""},{"reference":"Cornes E, Porta-De-La-Riva M, Aristizábal-Corrales D, Brokate-Llanos AM, García-Rodríguez FJ, Ertl I, et al., Cerón J. 2015. Cytoplasmic LSM-1 protein regulates stress responses through the insulin/IGF-1 signaling pathway in Caenorhabditis elegans. RNA 21(9): 1544-53.
","pubmedId":"26150554","doi":""},{"reference":"Erdmann EA, Forbes M, Becker M, Perez S, Hundley HA. 2024. ADR-2 regulates fertility and oocyte fate in C. elegans. bioRxiv: pii: 2023.11.01.565157. 10.1101/2023.11.01.565157.
","pubmedId":"37961348","doi":""},{"reference":"Green RA, Khaliullin RN, Zhao Z, Ochoa SD, Hendel JM, Chow TL, et al., Oegema K. 2024. Automated profiling of gene function during embryonic development. Cell 187(12): 3141-3160.e23.
","pubmedId":"38759650","doi":""},{"reference":"Huang X, Feng X, Yan YH, Xu D, Wang K, Zhu C, et al., Chen X. 2025. Compartmentalized localization of perinuclear proteins within germ granules in C. elegans. Dev Cell 60(8): 1251-1270.e3.
","pubmedId":"39742661","doi":""},{"reference":"Huggins HP, Subash JS, Stoffel H, Henderson MA, Hoffman JL, Buckner DS, et al., Keiper BD. 2020. Distinct roles of two eIF4E isoforms in the germline of Caenorhabditis elegans. J Cell Sci 133(6): 10.1242/jcs.237990.
","pubmedId":"32079657","doi":""},{"reference":"Kawasaki I, Amiri A, Fan Y, Meyer N, Dunkelbarger S, Motohashi T, et al., Strome S. 2004. The PGL family proteins associate with germ granules and function redundantly in Caenorhabditis elegans germline development. Genetics 167(2): 645-61.
","pubmedId":"15238518","doi":""},{"reference":"Li W, DeBella LR, Guven-Ozkan T, Lin R, Rose LS. 2009. An eIF4E-binding protein regulates katanin protein levels in C. elegans embryos. J Cell Biol 187(1): 33-42.
","pubmedId":"19786575","doi":""},{"reference":"Ozgur S, Basquin J, Kamenska A, Filipowicz W, Standart N, Conti E. 2015. Structure of a Human 4E-T/DDX6/CNOT1 Complex Reveals the Different Interplay of DDX6-Binding Proteins with the CCR4-NOT Complex. Cell Rep 13(4): 703-711.
","pubmedId":"26489469","doi":""},{"reference":"Peter D, Igreja C, Weber R, Wohlbold L, Weiler C, Ebertsch L, Weichenrieder O, Izaurralde E. 2015. Molecular architecture of 4E-BP translational inhibitors bound to eIF4E. Mol Cell 57(6): 1074-1087.
","pubmedId":"25702871","doi":""},{"reference":"Sengupta MS, Low WY, Patterson JR, Kim HM, Traven A, Beilharz TH, et al., Boag PR. 2013. ifet-1 is a broad-scale translational repressor required for normal P granule formation in C. elegans. J Cell Sci 126(Pt 3): 850-9.
","pubmedId":"23264733","doi":""},{"reference":"Spike C, Meyer N, Racen E, Orsborn A, Kirchner J, Kuznicki K, et al., Strome S. 2008. Genetic analysis of the Caenorhabditis elegans GLH family of P-granule proteins. Genetics 178(4): 1973-87.
","pubmedId":"18430929","doi":""},{"reference":"Spike CA, Bader J, Reinke V, Strome S. 2008. DEPS-1 promotes P-granule assembly and RNA interference in C. elegans germ cells. Development 135(5): 983-93.
","pubmedId":"18234720","doi":""}],"title":"Identification of eIF4ET binding partners in C. elegans
","reviews":[],"curatorReviews":[{"curator":{"displayName":"KJ Yook"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Jaehyoung Cho"},"openAcknowledgement":false,"submitted":null},{"curator":{"displayName":"Gary Craig Schindelman"},"openAcknowledgement":false,"submitted":null}]}]}},"species":{"species":[{"value":"acer saccharum","label":"Acer saccharum","imageSrc":"","imageAlt":"","mod":"TreeGenes","modLink":"https://treegenesdb.org","linkVariable":""},{"value":"achillea millefolium","label":"Achillea millefolium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"acinetobacter baylyi","label":"Acinetobacter baylyi","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"actinobacteria bacterium","label":"Actinobacteria bacterium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"adelges tsugae","label":"Adelges tsugae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"adenocaulon chilense","label":"Adenocaulon chilense","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aedes japonicus","label":"Aedes japonicus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aegorhinus vitulus","label":"Aegorhinus vitulus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alaimidae","label":"Alaimidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"allobates femoralis","label":"Allobates femoralis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alnus glutinosa","label":"Alnus glutinosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alosa aestivalis","label":"Alosa aestivalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alosa pseudoharengus","label":"Alosa pseudoharengus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"alternaria alternata","label":"Alternaria alternata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"amynthas agrestis","label":"Amynthas Agrestis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ancylostoma caninum","label":"Ancylostoma caninum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ancylostoma ceylanicum","label":"Ancylostoma ceylanicum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anemone multifida","label":"Anemone multifida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anguilla rostrata","label":"Anguilla rostrata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anisakis simplex","label":"Anisakis simplex","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anomala albopilosa","label":"Anomala albopilosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anthomyiidae sp","label":"Anthomyiidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"anthomyiidae sp","label":"Anthomyiidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arabidopsis","label":"Arabidopsis","imageSrc":"arabidopsis.png","imageAlt":"Arabidopsis graphic by Zoe Zorn CC BY 4.0","mod":"TAIR","modLink":"https://arabidopsis.org","linkVariable":""},{"value":"architeuthis dux","label":"Architeuthis dux","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arion vulgaris","label":"Arion vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"armeria","label":"Armeria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"artemia","label":"Artemia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"arthrobacter sp.","label":"Arthrobacter sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ascaridia","label":"Ascaridia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ascaridia galli","label":"Ascaridia galli","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"asparagopsis taxiformis","label":"Asparagopsis taxiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"astatotilapia burtoni","label":"Astatotilapia burtoni","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"avena sativa","label":"Avena sativa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"aves","label":"Aves","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus","label":"Bacillus (firmicutes)","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus cereus","label":"Bacillus cereus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus mycoides","label":"Bacillus mycoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus subtilis","label":"Bacillus subtilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus thuringiensis","label":"Bacillus thuringiensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus toyonensis","label":"Bacillus toyonensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacillus wiedmannii","label":"Bacillus wiedmannii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacteria","label":"Bacteria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bacteriophage","label":"Bacteriophage","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bactrocera","label":"Bactrocera sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"batrachospermum gelatinosum","label":"Batrachospermum gelatinosum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"betula lenta","label":"Betula lenta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"betula nigra","label":"Betula nigra","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombus dahlbohmii","label":"Bombus dahlbohmii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombus terrestris","label":"Bombus terrestris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bombyx mori","label":"Bombyx mori","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bos taurus","label":"Bos Taurus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brachygobius doriae","label":"Brachygobius doriae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brassica oleracea","label":"Brassica oleracea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brassica rapa","label":"Brassica rapa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"brugia malayi","label":"Brugia malayi","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"burkholderia thailandensis","label":"Burkholderia thailandensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"buttiauxella","label":"Buttiauxella","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caenorhabditis brenneri","label":"Caenorhabditis brenneri","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis briggsae","label":"Caenorhabditis briggsae","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"c. elegans","label":"Caenorhabditis elegans","imageSrc":"c-elegans.jpg","imageAlt":"C. elegans graphic by Zoe Zorn CC BY 4.0","mod":"WormBase","modLink":"https://wormbase.org","linkVariable":""},{"value":"caenorhabditis inopinata","label":"Caenorhabditis inopinata","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis japonica","label":"Caenorhabditis japonica","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis nigoni","label":"Caenorhabditis nigoni","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caenorhabditis remanei","label":"Caenorhabditis remanei","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"caenorhabditis tropicalis","label":"Caenorhabditis tropicalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calidifontibacillus","label":"Calidifontibacillus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calidifontibacillus erzuremensis","label":"Calidifontibacillus erzuremensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"calliphora sp","label":"Calliphora sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caltha sagittata","label":"Caltha sagittata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cambarus latimanus","label":"Cambarus latimanus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"candida albicans","label":"Candida albicans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"canis familiaris","label":"Canis familiaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cannabis sativa","label":"Cannabis sativa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caretta caretta","label":"Caretta caretta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cassiopea xamachana","label":"Cassiopea xamachana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"caulobacter vibrioides","label":"Caulobacter vibrioides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cephalopods","label":"Cephalopoda","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cerastium arvense","label":"Cerastium arvense","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ceriodaphnia","label":"Ceriodaphnia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ceroglossus suturalis","label":"Ceroglossus suturalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chaetoceros","label":"Chaetoceros","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chamaecrista fasciculata","label":"Chamaecrista fasciculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chilicola chalcidiformis","label":"Chilicola chalcidiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chitinimonas","label":"Chitinimonas","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chlamydomonas reinhardtii","label":"Chlamydomonas reinhardtii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chromobacterium","label":"Chromobacterium","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chrysemys picta","label":"Chrysemys picta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"chrysoperla rufilabris","label":"Chrysoperla rufilabris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"citrus","label":"Citrus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"clavibacter sp.","label":"Clavibacter sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"colinus virginianus","label":"Colinus virginianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"crassostrea virginica","label":"Crassostrea virginica","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"crithidia fasciculata","label":"Crithidia fasciculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cutibacterium acnes","label":"Cutibacterium acnes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"cyanobacteria","label":"Cyanobacteria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"daphnia","label":"Daphnia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"daphnia pulex","label":"Daphnia pulex","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dermacoccus nishinomiyaensis","label":"Dermacoccus nishinomiyaensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"diabrotica virgifera","label":"Diabrotica virgifera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"diabrotica virgifera virgifera virus 1","label":"Diabrotica virgifera virgifera virus 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"d. discoideum","label":"Dictyostelium discoideum","imageSrc":"dicty.png","imageAlt":"D. discoideum","mod":"dictyBase","modLink":"http://dictybase.org","linkVariable":""},{"value":"diptera","label":"Diptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dotocryptus bellicosus","label":"Dotocryptus bellicosus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"drechmeria coniospora","label":"Drechmeria coniospora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"drosophila","label":"Drosophila","imageSrc":"drosophila.png","imageAlt":"Drosophila graphic by Zoe Zorn CC BY 4.0","mod":"FlyBase","modLink":"https://flybase.org/doi/","linkVariable":"doi"},{"value":"dryopteris campyloptera","label":"Dryopteris campyloptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dryopteris expansa","label":"Dryopteris expansa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dryopteris intermedia","label":"Dryopteris intermedia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"dugesia dorotocephala","label":"Dugesia dorotocephala","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"elasmobranchii","label":"Elasmobranchii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"embryophyta","label":"Embryophyta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enoploteuthis chunii","label":"Enoploteuthis chunii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enterobacter aerogenes","label":"Enterobacter aerogenes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"enterococcus raffinosus","label":"Enterococcus raffinosus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"epichloë coenophiala","label":"Epichloë coenophiala","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"equus caballus","label":"Equus caballus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erigeron sp","label":"Erigeron sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eristalis","label":"Eristalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eruca vesicaria","label":"Eruca vesicaria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erwinia carotovora","label":"Erwinia carotovora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"erythronium americanum","label":"Erythronium americanum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"escherichia coli","label":"Escherichia coli","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"eukaryota","label":"Eukaryotes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"felis catus","label":"Felis catus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"francisella novicida","label":"Francisella novicida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"francisella tularensis","label":"Francisella tularensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fraxinus americana","label":"Fraxinus americana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fucus distichus","label":"Fucus distichus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"fungi","label":"Fungi","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gasteropelecus sp.","label":"Gasteropelecus sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"geranium sp","label":"Geranium sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"girardia","label":"Girardia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"glaucomys volans","label":"Glaucomys volans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"glycine max","label":"Glycine max","imageSrc":"","imageAlt":"","mod":"Soybase","modLink":"https://soybase.org","linkVariable":""},{"value":"glyptemys insculpta","label":"Glyptemys insculpta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gossypium hirsutum","label":"Gossypium hirsutum","imageSrc":"","imageAlt":"","mod":"CottonGen","modLink":"https://www.cottongen.org/","linkVariable":""},{"value":"gromphadorhina portentosa","label":"Gromphadorhina portentosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"gryllodes sigillatus","label":"Gryllodes sigillatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"haliotis rufescens","label":"Haliotis rufescens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hepacivirus hominis","label":"Hepatitis C Virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"herpes simplex virus type 1","label":"Herpes simplex virus type 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"human","label":"Human","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"human coronavirus oc43","label":"Human coronavirus OC43","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hydra vulgaris","label":"Hydra vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hydropsyche sp","label":"Hydropsyche sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hymenoptera","label":"Hymenoptera","imageSrc":"","imageAlt":"","mod":"Hymenoptera Genome Database","modLink":"https://hymenoptera.elsiklab.missouri.edu/","linkVariable":""},{"value":"hypochaeris radicata","label":"Hypochaeris radicata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"hypodynerus vespiformis","label":"Hypodynerus vespiformis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"iflaviridae","label":"Iflaviridae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"iflavuris","label":"Iflavirus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ipomoea hederacea","label":"Ipomoea hederacea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ischnomera","label":"Ischnomera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ischnomera ruficollis","label":"Ischnomera ruficollis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"julidochromis marlieri","label":"Julidochromis marlieri","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"juniperus virginiana","label":"Juniperus virginiana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"kluyveromyces marxianus","label":"Kluyveromyces marxianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"l. casei","label":"L. casei","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lacticaseibacillus casei","label":"Lacticaseibacillus casei","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"larentiinae sp","label":"Larentiinae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"laurus nobilis","label":"Laurus nobilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lepidoptera","label":"Lepidoptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"leucanthemum vulgare","label":"Leucanthemum vulgare","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"linepithema humile","label":"Linepithema humile","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"liometopum occidentale","label":"Liometopum occidentale","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lolium arundinaceum","label":"Lolium arundinaceum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lontra longicaudis","label":"Lontra longicaudis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lumbriculus variegatus","label":"Lumbriculus variegatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lumbricus terrestris","label":"Lumbricus terrestris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lupinus polyphyllus","label":"Lupinus polyphyllus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lycorma delicatula","label":"Lycorma delicatula","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"lynx rufus","label":"Lynx rufus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"magnaporthe oryzae","label":"Magnaporthe oryzae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mammalia","label":"Mammalia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"manihot esculenta","label":"Manihot esculenta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"medicago lupulina","label":"Medicago lupulina","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"meloidogyne","label":"Meloidogyne","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mimus polyglottos","label":"Mimus polyglottos","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"bryophyta","label":"Mosses","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mouse","label":"Mouse","imageSrc":"","imageAlt":"","mod":"MGI","modLink":"https://informatics.jax.org","linkVariable":""},{"value":"m. minutoides","label":"Mus minutoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"mycobacterium smegmatis","label":"Mycobacterium smegmatis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nakaseomyces glabratus","label":"Nakaseomyces glabratus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nauphoeta cinerea","label":"Nauphoeta cinerea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"neurospora","label":"Neurospora","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"n. benthamiana","label":"Nicotiana benthamiana","imageSrc":"","imageAlt":"","mod":"Solgenomics Network","modLink":"https://solgenomics.net/organism/Nicotiana_benthamiana/genome","linkVariable":""},{"value":"nicotiana tabacum","label":"Nicotiana tabacum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"noctuidae","label":"Noctuidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"noctuidae sp","label":"Noctuidae sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"nothobranchius furzeri","label":"Nothobranchius furzeri","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"onchocerca volvulus","label":"Onchocerca volvulus","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"orconectes virilis","label":"Orconectes virilis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ormia ochracea","label":"Ormia ochracea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"o. sativa","label":"Oryza sativa","imageSrc":"","imageAlt":"","mod":"Gramene","modLink":"https://www.gramene.org/","linkVariable":""},{"value":"other","label":"Other","imageSrc":"","imageAlt":"","mod":null,"modLink":null,"linkVariable":null},{"value":"oxalis enneaphylla","label":"Oxalis enneaphylla","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paenarthrobacter nicotinovorans","label":"Paenarthrobacter nicotinovorans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paenarthrobacter nicotinovorans","label":"Paenarthrobacter nicotinovorans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pantoea","label":"Pantoea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pantoea agglomerans","label":"Pantoea agglomerans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"papaver sp","label":"Papaver sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"paramecium bursaria","label":"Paramecium bursaria","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"partitiviridae","label":"Partitiviridae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pelodiscus sinensis","label":"Pelodiscus sinensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"perezia recurvata","label":"Perezia recurvata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"petromyzon marinus","label":"Petromyzon marinus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis","label":"Photinus pyralis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis associated partiti-like virus","label":"Photinus pyralis associated partiti-like virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"photinus pyralis iflavirus 1","label":"Photinus pyralis iflavirus 1","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"physcomitrium patens","label":"Physcomitrium patens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pinus strobus","label":"Pinus strobus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pinus taeda","label":"Pinus taeda","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"platycheirus","label":"Platycheirus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"plectus sambesii","label":"Plectus sambesii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pogonomyrmex occidentalis","label":"Pogonomyrmex occidentalis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"poncirus trifoliata","label":"Poncirus trifoliata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"populus deltoides","label":"Populus deltoides","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"potato virus y","label":"Potato virus Y","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"primula magellanica","label":"Primula magellanica","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pristionchus pacificus","label":"Pristionchus pacificus","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"prunus persica","label":"Prunus persica","imageSrc":"","imageAlt":"","mod":"Genome Database for Rosaceae","modLink":"https://www.rosaceae.org/","linkVariable":""},{"value":"psalmopoeus iriminia","label":"Psalmopoeus iriminia","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudanabaena sp.","label":"Pseudanabaena sp.","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas","label":"Pseudomonas","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas aeruginosa","label":"Pseudomonas aeruginosa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas glycinae","label":"Pseudomonas glycinae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas putida","label":"Pseudomonas putida","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pseudomonas syringae","label":"Pseudomonas syringae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"pterophyllum scalare","label":"Pterophyllum scalare","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"python regius","label":"Python regius","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"quercus macrocarpa","label":"Quercus macrocarpa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ralstonia solanacearum","label":"Ralstonia solanacearum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ranitomeya imitator","label":"Ranitomeya imitator","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ranunculus peduncularis","label":"Ranunculus peduncularis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"rat","label":"Rat","imageSrc":"","imageAlt":"","mod":"RGD","modLink":"https://rgd.mcw.edu","linkVariable":""},{"value":"rheinheimera","label":"Rheinheimera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ribes rubrum","label":"Ribes rubrum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"sars-cov-2","label":"SARS-CoV-2","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. cerevisiae","label":"Saccharomyces cerevisiae","imageSrc":"yeast.png","imageAlt":"Yeast graphic by Zoe Zorn CC BY 4.0","mod":"SGD","modLink":"https://yeastgenome.org","linkVariable":""},{"value":"saccharomyces paradoxus","label":"Saccharomyces paradoxus ","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. uvarum","label":"Saccharomyces uvarum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"schistosoma","label":"Schistosoma","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"schizosaccharomyces japonicus","label":"Schizosaccharomyces japonicus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. pombe","label":"Schizosaccharomyces pombe","imageSrc":"pombe.png","imageAlt":"Pombe graphic by Zoe Zorn © Caltech","mod":"PomBase","modLink":"https://www.pombase.org/reference/PMID:","linkVariable":"pmId"},{"value":"schmidtea mediterranea","label":"Schmidtea mediterranea","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"senecio sp","label":"Senecio sp","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"simocephalus","label":"Simocephalus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"siraitia grosvenorii","label":"Siraitia grosvenorii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"solanum lycopersicum","label":"Solanum lycopersicum","imageSrc":"","imageAlt":"","mod":"Solgenomics Network","modLink":"https://solgenomics.net/organism/1/view/","linkVariable":""},{"value":"sorghum","label":"Sorghum","imageSrc":"","imageAlt":"","mod":"SorghumBase","modLink":"https://www.sorghumbase.org","linkVariable":""},{"value":"spiroplasma eriocheiris","label":"Spiroplasma eriocheiris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"staphylococcus aureus","label":"Staphylococcus aureus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"staphylococcus epidermidis","label":"Staphylococcus epidermidis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"steinernema carpocapsae","label":"Steinernema carpocapsae","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"https://wormbase.org","linkVariable":""},{"value":"steinernema hermaphroditum","label":"Steinernema hermaphroditum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"stenotrophomonas geniculata","label":"Stenotrophomonas geniculata","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"stewartia floidana","label":"Stewartia floridana","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"streptococcus gordonii ","label":"Streptococcus gordonii ","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"streptococcus mutans","label":"Streptococcus mutans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":" streptococcus pneumoniae","label":"Streptococcus pneumoniae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"s. purpuratus","label":"Strongylocentrotus purpuratus","imageSrc":"","imageAlt":"","mod":"Echinobase","modLink":"https://www.echinobase.org","linkVariable":""},{"value":"strongyloides ratti","label":"Strongyloides ratti","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"sulfolobus","label":"Sulfolobus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"symphoricarpos albus","label":"Symphoricarpos albus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"syncirsodes","label":"Syncirsodes","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"synechococcus elongatus","label":"Synechococcus elongatus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"syrphidae","label":"Syrphidae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tarantobelus jeffdanielsi","label":"Tarantobelus jeffdanielsi","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"taraxacum officinale","label":"Taraxacum officinale","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tatochila theodice","label":"Tatochila theodice","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tetrahymena","label":"Tetrahymena","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tetramorium immigrans","label":"Tetramorium immigrans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tomato brown rugose fruit virus","label":"ToBRFV","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trachemys scripta","label":"Trachemys scripta","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tribolium castaneum","label":"Tribolium castaneum","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trichoptera","label":"Trichoptera","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trichuris muris","label":"Trichuris muris","imageSrc":"","imageAlt":"","mod":"WormBase","modLink":"www.wormbase.org","linkVariable":""},{"value":"trifolium repens","label":"Trifolium repens","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"trypoxylus dichotomus","label":"Trypoxylus dichotomus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"tsuga canadensis","label":"Tsuga canadensis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"ulva expansa","label":"Ulva expansa","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"universal","label":"Universal","imageSrc":"","imageAlt":"","mod":null,"modLink":null,"linkVariable":null},{"value":"vargula hilgendorfii","label":"Vargula hilgendorfii","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"vespula vulgaris","label":"Vespula vulgaris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"virus","label":"Virus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"watasenia scintillans","label":"Watasenia scintillans","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"wolbachia pipientis","label":"Wolbachia pipientis","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"xenopus","label":"Xenopus","imageSrc":"xenopus.png","imageAlt":"Xenopus graphic by Zoe Zorn CC BY 4.0","mod":"XenBase","modLink":"https://xenbase.org","linkVariable":""},{"value":"xenorhabdus griffiniae","label":"Xenorhabdus griffiniae","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"yramea cytheris","label":"Yramea cytheris","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"zaprionus indianus","label":"Zaprionus indianus","imageSrc":"","imageAlt":"","mod":"","modLink":"","linkVariable":""},{"value":"zea mays","label":"Zea mays","imageSrc":"","imageAlt":"","mod":"MaizeGDB","modLink":"https://www.maizegdb.org","linkVariable":""},{"value":"zebrafish","label":"Zebrafish","imageSrc":"zebrafish.png","imageAlt":"Zebrafish graphic by Zoe Zorn CC BY 4.0","mod":"ZFIN","modLink":"https://zfin.org","linkVariable":""}]}},"pageContext":{"id":"19678df5-1946-43bf-bb4d-d86026fb8554","citedBy":[],"parsedCsv":{"csvHeader":[],"csvData":[]}}}, "staticQueryHashes": ["2114697108"]}