vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-25-08vavilov-4477Research ArticleГЕНОМИКА И ТРАНСКРИПТОМИКАPLANT GENETICS AND BREEDINGРазнообразие нута, обусловленноe полиморфизмом вставок транспозоновChickpea diversity driven by transposon insertion polymorpismСтанинB. A.StaninV. A.

Санкт-Петербург

St. Petersburg

https://orcid.org/0000-0003-4634-5656ДукМ. A.DukМ. A.

Санкт-Петербург

St. Petersburg

https://orcid.org/0000-0001-9802-5297КанапинА. A.KanapinА. A.

Санкт-Петербург

St. Petersburg

https://orcid.org/0000-0002-9353-9173СамсоноваА. А.SamsonovaА. A.

Санкт-Петербург

St. Petersburg

СурковаС. Ю.SurkovaS. Yu.

Санкт-Петербург

St. Petersburg

https://orcid.org/0000-0001-8170-1260СамсоноваМ. Г.SamsonovaМ. G.

Санкт-Петербург

St. Petersburg

m.g.samsonova@gmail.comСанкт-Петербургский политехнический университет Петра ВеликогоРоссияPeter the Great St. Petersburg Polytechnic UniversityRussian FederationСанкт-Петербургский политехнический университет Петра Великого; Физико-технический институт им. А.Ф. Иоффе Российской академии наукРоссияPeter the Great St. Petersburg Polytechnic University; Ioffe Institute of the Russian Academy of SciencesRussian Federation2025030320252916171Copyright © Станин B.A., Дук М.A., Канапин А.A., Самсонова А.А., Суркова С.Ю., Самсонова М.Г., 20252025Станин B.A., Дук М.A., Канапин А.A., Самсонова А.А., Суркова С.Ю., Самсонова М.Г.Stanin V.A., Duk М.A., Kanapin А.A., Samsonova А.A., Surkova S.Y., Samsonova М.G.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4477

   Нут – важная зернобобовая культура, которая используется народонаселением разных частей света в пищу в силу высокой ценности. Применение омиксных технологий позволило oхарактеризовать генетическое разнообразие нута, обусловленное однонуклеотидными полиморфизмами, тогда как структурные варианты и инсерции транспозонов выпали из поля зрения исследователей. Поэтому характеристика состава мобилома индивидуальных сортов нута и оценка его влияния на фенотипическую изменчивость и адаптацию актуальны. В фокусе нашего внимания были староместные сорта, собранные до «зеленой революции», поскольку они являются ценным источником видового разнообразия и могут быть использованы для расширения генетической базы современных сортов. Проанализировав 190 геномов нута, мы обнаружили 42 324 сайта инсерции транспозонов 83 семейств. Большинство инсерций (67 %) вызваны мобилизацией ретротранспозонов. Из ДНК-транспозонов наибольшее число инсерций найдено для суперсемейств MuDR, PIF, hAT, CMC и TcMar. Продемонстрирована неравномерность распределения сайтов инсерции вдоль хромосом. Анализ локализации сайтов инсерции транспозонов относительно генов показал, что наибольшее количество вставок у всех суперсемейств транспозонов приходится на интроны, наименьшее – на экзоны. Мы также показали, что сайты встройки транспозонов, которые до недавнего времени находились вне поля зрения популяционной геномики, являются важным фактором, диверсифицирующим фенотипы, что позволяет использовать их в полногеномном поиске ассоциаций в качестве маркеров наряду с однонуклеотидными полиморфизмами. Сравнительный анализ мобиломов сортов из разных географических регионов выявил существенное отличие эфиопских образцов от образцов других групп, собранных в Индии, Узбекистане, Турции, Средиземноморье, на юге России и в Ливане. Совокупность полученных нами данных и результатов – ценный ресурс, который может быть использован в качестве отправной точки для селекции улучшенных сортов нута, адаптированных к различным климатическим условиям.

   Chickpea is the second most important legume crop, which is used as a food by people in different parts of the world due to its high nutritive value. Omics technologies have revolutionized the characterization of chickpea genetic diversity by considering single-nucleotide polymorphisms, while structural variants and transposons have been overlooked. The specific contribution of transposons to the phenotypic diversification of crop species is still poorly documented, therefore its characterization is important. We focused on landraces collected before the “green revolution”, as they are a valuable source of species diversity and can be used to broaden the genetic base of modern cultivars. Analyzing 190 chickpea genomes, we found 42,324 new transposon insertion sites from 83 families and showed that such sites are highly polymorphic. Most insertions were caused by mobilization of retrotransposons (67 % of insertions); among DNA transposons, the highest number of insertions was found for the superfamilies MuDR, PIF, hAT, CMC, and TcMar. We also demonstrated an uneven distribution of insertion sites along chromosomes. Analysis of the localization of transposon insertion sites relative to genes and their structural elements has shown that the largest number of insertions in all transposon superfamilies falls on introns and the smallest, on exons. We also showed that transposon insertion sites, which until recently have been overlooked by population genomics, are an important factor that diversifies phenotypes and can be used in GWAS as markers replacing SNPs. Comparative analysis of landraces collected in different geographic regions showed that the Ethiopian accessions have many unique transposon insertion sites. Our results highlight the unique role of transposon mobilization in chickpea diversification and have important implications for breeding improved chickpea varieties adapted to global climate change.

нуттранспозоныполиморфизмстароместные сортаGWASадаптацияchickpeatransposonspolymorphismlandracesGWASadaptationРабота поддержана грантом РНФ 22-46-02004.This research was funded by Russian Science Foundation, grant number 22-46-02004ReferencesAbbo S., Berger J., Turner N.C. Viewpoint: Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation. Funct Plant Biol. 2003;30(10):1081­1087. doi: 10.1071/fp03084Abbo S., Berger J., Turner N.C. Viewpoint: Evolution of cultivated chickpea: four bottlenecks limit diversity and constrain adaptation. Funct Plant Biol. 2003;30(10):1081­1087. doi: 10.1071/fp03084Aceituno­Valenzuela U., Micol­Ponce R., Ponce M.R. Genome­wide analysis of CCHC­type zinc finger (ZCCHC) proteins in yeast, Arabidopsis, and humans. Cell Mol Life Sci. 2020;77(20):3991-4014. doi: 10.1007/s00018­020­03518­7Aceituno­Valenzuela U., Micol­Ponce R., Ponce M.R. Genome­wide analysis of CCHC­type zinc finger (ZCCHC) proteins in yeast, Arabidopsis, and humans. Cell Mol Life Sci. 2020;77(20):3991-4014. doi: 10.1007/s00018­020­03518­7Akakpo R., Carpentier M., Hsing Y.I., Panaud O. The impact of transposable elements on the structure, evolution and function of the rice genome. New Phytol. 2020;226(1):44­49. doi: 10.1111/nph.16356Akakpo R., Carpentier M., Hsing Y.I., Panaud O. The impact of transposable elements on the structure, evolution and function of the rice genome. New Phytol. 2020;226(1):44­49. doi: 10.1111/nph.16356Alexander D.H., Novembre J., Lange K. Fast model­based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655-1664. doi: 10.1101/gr.094052.109Alexander D.H., Novembre J., Lange K. Fast model­based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655-1664. doi: 10.1101/gr.094052.109Alioto T., Alexiou K.G., Bardil A., Barteri F., Castanera R., Cruz F., Dhingra A., Duval H., Fernández i Martí Á., Frias L., Galán B., García J.L., Howad W., Gómez­Garrido J., Gut M., Julca I., Morata J., Puigdomènech P., Ribeca P., Rubio Cabetas M.J., Vlasova A., Wirthensohn M., Garcia­Mas J., Gabaldón T., Casacuberta J.M., Arús P. Transposons played a major role in the diversification between the closely related almond and peach genomes: results from the almond genome sequence. Plant J. 2020;101(2):455-472. doi: 10.1111/tpj.14538Alioto T., Alexiou K.G., Bardil A., Barteri F., Castanera R., Cruz F., Dhingra A., Duval H., Fernández i Martí Á., Frias L., Galán B., García J.L., Howad W., Gómez­Garrido J., Gut M., Julca I., Morata J., Puigdomènech P., Ribeca P., Rubio Cabetas M.J., Vlasova A., Wirthensohn M., Garcia­Mas J., Gabaldón T., Casacuberta J.M., Arús P. Transposons played a major role in the diversification between the closely related almond and peach genomes: results from the almond genome sequence. Plant J. 2020;101(2):455-472. doi: 10.1111/tpj.14538Binder B.M. Ethylene signaling in plants. J Biol Chem. 2020;295(22): 7710­7725. doi: 10.1074/jbc.rev120.010854Binder B.M. Ethylene signaling in plants. J Biol Chem. 2020;295(22): 7710­7725. doi: 10.1074/jbc.rev120.010854Bourque G., Burns K.H., Gehring M., Gorbunova V., Seluanov A., Hammell M., Imbeault M., Izsvák Z., Levin H.L., Macfarlan T.S., Mager D.L., Feschotte C. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199. doi: 10.1186/s13059-018-1577-zBourque G., Burns K.H., Gehring M., Gorbunova V., Seluanov A., Hammell M., Imbeault M., Izsvák Z., Levin H.L., Macfarlan T.S., Mager D.L., Feschotte C. Ten things you should know about transposable elements. Genome Biol. 2018;19(1):199. doi: 10.1186/s13059-018-1577-zCai X., Lin R., Liang J., King G.J., Wu J., Wang X. Transposable element insertion: a hidden major source of domesticated phenotypic variation in Brassica rapa. Plant Biotechnol J. 2022;20(7):1298-1310. doi: 10.1111/pbi.13807Cai X., Lin R., Liang J., King G.J., Wu J., Wang X. Transposable element insertion: a hidden major source of domesticated phenotypic variation in Brassica rapa. Plant Biotechnol J. 2022;20(7):1298-1310. doi: 10.1111/pbi.13807Catlin N.S., Josephs E.B. The important contribution of transposable elements to phenotypic variation and evolution. Curr Opin Plant Biol. 2022;65:102140. doi: 10.1016/j.pbi.2021.102140Catlin N.S., Josephs E.B. The important contribution of transposable elements to phenotypic variation and evolution. Curr Opin Plant Biol. 2022;65:102140. doi: 10.1016/j.pbi.2021.102140de la Peña T.C., Pueyo J.J. Legumes in the reclamation of marginal soils, from cultivar and inoculant selection to transgenic approaches. Agron Sustain Dev. 2012;32:65­91. doi: 10.1007/s13593­011­0024­2de la Peña T.C., Pueyo J.J. Legumes in the reclamation of marginal soils, from cultivar and inoculant selection to transgenic approaches. Agron Sustain Dev. 2012;32:65­91. doi: 10.1007/s13593­011­0024­2Domínguez M., Dugas E., Benchouaia M., Leduque B., Jiménez­ Gómez J.M., Colot V., Quadrana L. The impact of transposable elements on tomato diversity. Nat Commun. 2020;11(1):4058. doi: 10.1038/s41467­020­17874­2Domínguez M., Dugas E., Benchouaia M., Leduque B., Jiménez­ Gómez J.M., Colot V., Quadrana L. The impact of transposable elements on tomato diversity. Nat Commun. 2020;11(1):4058. doi: 10.1038/s41467­020­17874­2Duk M.A., Kanapin A.A., Bankin M.P., Samsonova M.G. Using the IIIVmrMLM method to confirm and search new genome­wide associations in chickpea. Biofizika = Biophysics. 2024;69(6):1263-1278. doi: 10.31857/S0006302924060126 (in Russian)Duk M.A., Kanapin A.A., Bankin M.P., Samsonova M.G. Using the IIIVmrMLM method to confirm and search new genome­wide associations in chickpea. Biofizika = Biophysics. 2024;69(6):1263-1278. doi: 10.31857/S0006302924060126 (in Russian)Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Clim. 2005;25(15):1965­1978. doi: 10.1002/joc.1276Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Clim. 2005;25(15):1965­1978. doi: 10.1002/joc.1276Igolkina A.A., Noujdina N.V., Vishnyakova M., Longcore T., von Wett berg E., Nuzhdin S.V., Samsonova M.G. Historical routes for diversification of domesticated chickpea inferred from landrace genomics. Mol Biol Evol. 2023;40:msad110. doi: 10.1093/molbev/msad110Igolkina A.A., Noujdina N.V., Vishnyakova M., Longcore T., von Wett berg E., Nuzhdin S.V., Samsonova M.G. Historical routes for diversification of domesticated chickpea inferred from landrace genomics. Mol Biol Evol. 2023;40:msad110. doi: 10.1093/molbev/msad110Jain M., Misra G., Patel R.K., Priya P., Jhanwar S., Khan A.W., Shah N., Singh V.K., Garg R., Jeena G., Yadav M., Kant C., Sharma P., Yadav G., Bhatia S., Tyagi A.K., Chattopadhyay D. A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 2013;74(5):715­729. doi: 10.1111/tpj.12173Jain M., Misra G., Patel R.K., Priya P., Jhanwar S., Khan A.W., Shah N., Singh V.K., Garg R., Jeena G., Yadav M., Kant C., Sharma P., Yadav G., Bhatia S., Tyagi A.K., Chattopadhyay D. A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 2013;74(5):715­729. doi: 10.1111/tpj.12173Jiang Z., Wang M., Nicolas M., Ogé L., Pérez­Garcia M.­D., Crespel L., Li G., Ding Y., Le Gourrierec J., Grappin P., Sakr S. Glucose-6-phosphate dehydrogenases: the hidden players of plant physiology. Int J Mol Sci. 2022;23(24):16128. doi: 10.3390/ijms232416128Jiang Z., Wang M., Nicolas M., Ogé L., Pérez­Garcia M.­D., Crespel L., Li G., Ding Y., Le Gourrierec J., Grappin P., Sakr S. Glucose-6-phosphate dehydrogenases: the hidden players of plant physiology. Int J Mol Sci. 2022;23(24):16128. doi: 10.3390/ijms232416128Kaloki P., Devasirvatham V., Tan D.K.Y. Chickpea abiotic stresses: combating drought, heat and cold. In: Abiotic and Biotic Stress in Plants. IntechOpen, 2019. doi: 10.5772/intechopen.83404Kaloki P., Devasirvatham V., Tan D.K.Y. Chickpea abiotic stresses: combating drought, heat and cold. In: Abiotic and Biotic Stress in Plants. IntechOpen, 2019. doi: 10.5772/intechopen.83404Kang M., Wu H., Liu H., Liu W., Zhu M., Han Y., Liu W., Song C.C.Y., Tan L., Yin K., Zhao Y., Yan Z., Lou S., Zan Y., Liu J. The pan­ genome and local adaptation of Arabidopsis thaliana. Nat Commun. 2023;14(1):6259. doi: 10.1038/s41467­023­42029­4Kang M., Wu H., Liu H., Liu W., Zhu M., Han Y., Liu W., Song C.C.Y., Tan L., Yin K., Zhao Y., Yan Z., Lou S., Zan Y., Liu J. The pan­ genome and local adaptation of Arabidopsis thaliana. Nat Commun. 2023;14(1):6259. doi: 10.1038/s41467­023­42029­4Kofler R., Pandey R.V., Schlotterer C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27(24):3435-3436. doi: 10.1093/bioinformatics/btr589Kofler R., Pandey R.V., Schlotterer C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27(24):3435-3436. doi: 10.1093/bioinformatics/btr589Kofler R., Gómez­Sánchez D., Schlötterer C. PoPoolationTE2: comparative population genomics of transposable elements using Pool-Seq. Mol Biol Evol. 2016;33(10):2759­2764. doi: 10.1093/molbev/msw137Kofler R., Gómez­Sánchez D., Schlötterer C. PoPoolationTE2: comparative population genomics of transposable elements using Pool-Seq. Mol Biol Evol. 2016;33(10):2759­2764. doi: 10.1093/molbev/msw137Li H., Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25(14):1754-1760. doi: 10.1093/bioinformatics/btp324Li H., Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009;25(14):1754-1760. doi: 10.1093/bioinformatics/btp324Li M., Zhang Y.­W., Xiang Y., Liu M.­H., Zhang Y.­M. IIIVmrMLM: the R and C++ tools associated with 3VmrMLM, a comprehensive GWAS method for dissecting quantitative traits. Mol Plant. 2022a; 15(8):1251­1253. doi: 10.1016/j.molp.2022.06.002Li M., Zhang Y.­W., Xiang Y., Liu M.­H., Zhang Y.­M. IIIVmrMLM: the R and C++ tools associated with 3VmrMLM, a comprehensive GWAS method for dissecting quantitative traits. Mol Plant. 2022a; 15(8):1251­1253. doi: 10.1016/j.molp.2022.06.002Li M., Zhang Y.­W., Zhang Z.­C., Xiang Y., Liu M.­H., Zhou Y.­H., Zuo J.­F., Zhang H.­Q., Chen Y., Zhang Y.­M. A compressed variance component mixed model for detecting QTNs and QTN­by­ environment and QTN­by­QTN interactions in genome­wide association studies. Mol Plant. 2022b;15(4):630­650. doi: 10.1016/j.molp.2022.02.012Li M., Zhang Y.­W., Zhang Z.­C., Xiang Y., Liu M.­H., Zhou Y.­H., Zuo J.­F., Zhang H.­Q., Chen Y., Zhang Y.­M. A compressed variance component mixed model for detecting QTNs and QTN­by­ environment and QTN­by­QTN interactions in genome­wide association studies. Mol Plant. 2022b;15(4):630­650. doi: 10.1016/j.molp.2022.02.012Mann H.B., Whitney D.R. On a test of whether one of two random variables is stochastically larger than the other. Ann Math Statistics. 1947;18(1):50­60. doi: 10.1214/aoms/1177730491Mann H.B., Whitney D.R. On a test of whether one of two random variables is stochastically larger than the other. Ann Math Statistics. 1947;18(1):50­60. doi: 10.1214/aoms/1177730491Mhiri C., Borges F., Grandbastien M.­A. Specificities and dynamics of transposable elements in land plants. Biology. 2022;11(4):488. doi: 10.3390/biology11040488Mhiri C., Borges F., Grandbastien M.­A. Specificities and dynamics of transposable elements in land plants. Biology. 2022;11(4):488. doi: 10.3390/biology11040488Mokhtar M.M., Alsamman A.M., Abd-Elhalim H.M., Allali A.E. CicerSpTEdb: a web-based database for high-resolution genome­wide identification of transposable elements in Cicer species. PLoS One. 2021;16(11):e0259540. doi: 10.1371/journal.pone.0259540Mokhtar M.M., Alsamman A.M., Abd-Elhalim H.M., Allali A.E. CicerSpTEdb: a web-based database for high-resolution genome­wide identification of transposable elements in Cicer species. PLoS One. 2021;16(11):e0259540. doi: 10.1371/journal.pone.0259540Niu X.­M., Xu Y.­C., Li Z.­W., Bian Y.­T., Hou X.­H., Chen J.­F., Zou Y.­P., Jiang J., Wu Q., Ge S., Balasubramanian S., Guo Y.­L. Transposable elements drive rapid phenotypic variation in Capsella rubella. Proc Natl Acad Sci USA. 2019;116(14):6908-6913. doi: 10.1073/pnas.1811498116Niu X.­M., Xu Y.­C., Li Z.­W., Bian Y.­T., Hou X.­H., Chen J.­F., Zou Y.­P., Jiang J., Wu Q., Ge S., Balasubramanian S., Guo Y.­L. Transposable elements drive rapid phenotypic variation in Capsella rubella. Proc Natl Acad Sci USA. 2019;116(14):6908-6913. doi: 10.1073/pnas.1811498116Pulido M., Casacuberta J.M. Transposable element evolution in plant genome ecosystems. Curr Opin Plant Biol. 2023;75:102418. doi: 10.1016/j.pbi.2023.102418Pulido M., Casacuberta J.M. Transposable element evolution in plant genome ecosystems. Curr Opin Plant Biol. 2023;75:102418. doi: 10.1016/j.pbi.2023.102418Qiu Y., O’Connor C.H., Della Coletta R., Renk J.S., Monnahan P.J., Noshay J.M., Liang Z., Gilbert A., Anderson S.N., McGaugh S.E., Springer N.M., Hirsch C.N. Whole-genome variation of transposable element insertions in a maize diversity panel. G3 (Bethesda). 2021;11(10):jkab238. doi: 10.1093/g3journal/jkab238Qiu Y., O’Connor C.H., Della Coletta R., Renk J.S., Monnahan P.J., Noshay J.M., Liang Z., Gilbert A., Anderson S.N., McGaugh S.E., Springer N.M., Hirsch C.N. Whole-genome variation of transposable element insertions in a maize diversity panel. G3 (Bethesda). 2021;11(10):jkab238. doi: 10.1093/g3journal/jkab238Quesneville H. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mob DNA. 2020;11:28. doi: 10.1186/s13100-020-00223-xQuesneville H. Twenty years of transposable element analysis in the Arabidopsis thaliana genome. Mob DNA. 2020;11:28. doi: 10.1186/s13100-020-00223-xRadkova M., Revalska M., Kertikova D., Iantcheva A. Zinc finger CCHC-type protein related with seed size in model legume species Medicago truncatula. Biotechnol Biotechnol Equip. 2019;33(1):278-285. doi: 10.1080/13102818.2019.1568914Radkova M., Revalska M., Kertikova D., Iantcheva A. Zinc finger CCHC-type protein related with seed size in model legume species Medicago truncatula. Biotechnol Biotechnol Equip. 2019;33(1):278-285. doi: 10.1080/13102818.2019.1568914Schrader L., Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol. 2019;28(6):1537­1549. doi: 10.1111/mec.14794Schrader L., Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol. 2019;28(6):1537­1549. doi: 10.1111/mec.14794Sokolkova A., Bulyntsev S.V., Chang P.L., Carrasquilla-Garcia N., Igolkina A.A., Noujdina N.V., von Wettberg E., Vishnyakova M.A., Cook D.R., Nuzhdin S.V., Samsonova M.G. Genomic analysis of Vavilov’s historic chickpea landraces reveals footprints of environmental and human selection. Int J Mol Sci. 2020;21(11):3952. doi: 10.3390/ijms21113952Sokolkova A., Bulyntsev S.V., Chang P.L., Carrasquilla-Garcia N., Igolkina A.A., Noujdina N.V., von Wettberg E., Vishnyakova M.A., Cook D.R., Nuzhdin S.V., Samsonova M.G. Genomic analysis of Vavilov’s historic chickpea landraces reveals footprints of environmental and human selection. Int J Mol Sci. 2020;21(11):3952. doi: 10.3390/ijms21113952Sultana T., Zamborlini A., Cristofari G., Lesage P. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet. 2017;18(5):292­308. doi: 10.1038/nrg.2017.7Sultana T., Zamborlini A., Cristofari G., Lesage P. Integration site selection by retroviruses and transposable elements in eukaryotes. Nat Rev Genet. 2017;18(5):292­308. doi: 10.1038/nrg.2017.7Varshney R., Song C., Saxena R., Azam S., Yu S., Sharpe A.G., Cannon S., … Singh K.B., Datta S.K., Jackson S.A., Wang J., Cook D.R. Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol. 2013;31(3):240-246. doi: 10.1038/nbt.2491Varshney R., Song C., Saxena R., Azam S., Yu S., Sharpe A.G., Cannon S., … Singh K.B., Datta S.K., Jackson S.A., Wang J., Cook D.R. Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol. 2013;31(3):240-246. doi: 10.1038/nbt.2491Varshney R., Thudi M., Roorkiwal M., He W., Upadhyaya H.D., Yang W., Bajaj P., … Sutton T., von Wettberg E., Vigouroux Y., Xu X., Liu X. Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet. 2019;51(5):857­864. doi: 10.1038/s41588-019-0401-3Varshney R., Thudi M., Roorkiwal M., He W., Upadhyaya H.D., Yang W., Bajaj P., … Sutton T., von Wettberg E., Vigouroux Y., Xu X., Liu X. Resequencing of 429 chickpea accessions from 45 countries provides insights into genome diversity, domestication and agronomic traits. Nat Genet. 2019;51(5):857­864. doi: 10.1038/s41588-019-0401-3Vourlaki I.-T., Castanera R., Ramos-Onsins S.E., Casacuberta J.M., Pérez­Enciso M. Transposable element polymorphisms improve prediction of complex agronomic traits in rice. Theor Appl Genet. 2022;135(9):3211­3222. doi: 10.1007/s00122­022­04180­2Vourlaki I.-T., Castanera R., Ramos-Onsins S.E., Casacuberta J.M., Pérez­Enciso M. Transposable element polymorphisms improve prediction of complex agronomic traits in rice. Theor Appl Genet. 2022;135(9):3211­3222. doi: 10.1007/s00122­022­04180­2Weiß L., Gaelings L., Reiner T., Mergner J., Kuster B., Fehér A., Hensel G., Gahrtz M., Kumlehn J., Engelhardt S., Hückelhoven R. Posttranslational modification of the RHO of plants protein RACB by phosphorylation and cross-kingdom conserved ubiquitination. PLoS One. 2022;17(3):e0258924. doi: 10.1371/journal.pone.0258924Weiß L., Gaelings L., Reiner T., Mergner J., Kuster B., Fehér A., Hensel G., Gahrtz M., Kumlehn J., Engelhardt S., Hückelhoven R. Posttranslational modification of the RHO of plants protein RACB by phosphorylation and cross-kingdom conserved ubiquitination. PLoS One. 2022;17(3):e0258924. doi: 10.1371/journal.pone.0258924Wuriyanghan H., Zhang B., Cao W.­H., Ma B., Lei G., Liu Y.­F., Wei W., Wu H.­J., Chen L.­J., Chen H.­W., Cao Y.­R., He S.­J., Zhang W.­K., Wang X.­J., Chen S.­Y., Zhang J.­S. The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell. 2009;21(5):1473­1494. doi: 10.1105/tpc.108.065391Wuriyanghan H., Zhang B., Cao W.­H., Ma B., Lei G., Liu Y.­F., Wei W., Wu H.­J., Chen L.­J., Chen H.­W., Cao Y.­R., He S.­J., Zhang W.­K., Wang X.­J., Chen S.­Y., Zhang J.­S. The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell. 2009;21(5):1473­1494. doi: 10.1105/tpc.108.065391Yan H., Haak D.C., Li S., Huang L., Bombarely A. Exploring transposable element-based markers to identify allelic variations underlying agronomic traits in rice. Plant Commun. 2022;3(3):100270. doi: 10.1016/j.xplc.2021.100270Yan H., Haak D.C., Li S., Huang L., Bombarely A. Exploring transposable element-based markers to identify allelic variations underlying agronomic traits in rice. Plant Commun. 2022;3(3):100270. doi: 10.1016/j.xplc.2021.100270Zhao Y., Li X., Xie J., Xu W., Chen S., Zhang X., Liu S., Wu J., El-Kassaby Y.A., Zhang D. Transposable elements: distribution, polymorphism, and climate adaptation in populus. Front Plant Sci. 2022; 13:814718. doi: 10.3389/fpls.2022.814718Zhao Y., Li X., Xie J., Xu W., Chen S., Zhang X., Liu S., Wu J., El-Kassaby Y.A., Zhang D. Transposable elements: distribution, polymorphism, and climate adaptation in populus. Front Plant Sci. 2022; 13:814718. doi: 10.3389/fpls.2022.814718

The authors declare that there are no conflicts of interest present.