Russian Journal of GeneticsRussian Journal of GeneticsГенетика0016-67583034-5103The Russian Academy of Sciences66718010.31857/S0016675824100055wfjmccГЕНЕТИКА РАСТЕНИЙResearch ArticleCysteine-Rich Peptide Genes of Wheatgrass Thinopyrum elongatumГены цистеин-богатых пептидов пырея Thinopyrum elongatumSlezinaM. P.СлезинаМ. П.
Russian Federation
odintsova2005@rambler.ruIstominaE. A.ИстоминаЕ. А.
Russian Federation
odintsova2005@rambler.ruShiyanA. N.ШиянА. Н.
Russian Federation
odintsova2005@rambler.ruOdintsovaT. I.ОдинцоваТ. И.
Russian Federation
odintsova2005@rambler.ruVavilov Institute of General Genetics, Russian Academy of SciencesИнститут общей генетики им. Н.И. Вавилова Российской академии наук161020246010567026022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://transsyst.ru/0016-6758/article/view/667180

Cysteine-rich peptides play an important role in the plant defense system. The aim of the present work was to search in silico for genes encoding antimicrobial and signaling peptides in the genome of Thinopyrum elongatum (Host) D.R. Dewey (2n = 14, EE) − a wild grass species with high resistance to pathogens and abiotic stress. Bioinformatic analysis revealed 154 new genes of antimicrobial and signaling peptide precursors belonging to 9 families in Th. elongatum genome. Introns were detected in a number of cysteine-rich peptide genes. The structure of peptide precursors and localization of peptide genes in wheat chromosomes were determined. The greatest similarity of the sequences of Th. elongatum peptides with homologous peptides of plants of the genera Triticum and Aegilops was shown, which confirms the cytogenetic data on the relatedness of genome E with genome D and similar genomes. The results obtained contribute to the characterization of molecular components of the immune system of Th. elongatum and will serve as a basis for further studies of resistance mechanisms, as well as for scientifically justified practical use of this species as a resistance donor in wheat breeding.

Цистеин-богатые пептиды играют важную роль в защитной системе растений. Цель настоящей работы состояла в поиске in silico генов антимикробных и сигнальных пептидов в геноме пырея удлиненного Thinopyrum elongatum (Host) D.R. Dewey (2n = 14, EE) − дикорастущего злака, обладающего высокой устойчивостью к патогенам и абиотическому стрессу. В результате биоинформатического анализа в геноме пырея было выявлено 154 новых гена предшественников антимикробных и сигнальных пептидов, относящихся к девяти семействам. В ряде генов цистеин-богатых пептидов обнаружены интроны. Были определены структура предшественников пептидов и локализация генов пептидов в хромосомах пырея. Показано наибольшее сходство последовательностей пептидов пырея с гомологичными пептидами растений родов Triticum и Aegilops, что подтверждает цитогенетические данные о родстве генома Е с геномом D и близкими ему геномами. Полученные результаты вносят вклад в характеристику молекулярных компонентов иммунной системы Th. elongatum и послужат базой для дальнейшего исследования механизмов устойчивости, а также для научно обоснованного практического использования этого вида в качестве донора устойчивости в селекции пшеницы.

plant immunityThinopyrum elongatumcysteine-rich peptidesgene biodiversityиммунитет растенийThinopyrum elongatumцистеин-богатые пептидыбиоразнообразие геновРоссийский научный фонд (гранд)Russian Science Foundation (grand)22-16-00010Министерство науки и высшего образования РФ (проект)Ministry of Science and Higher Education of the Russian Federation (project)122022600163-7Dodds P., Rathjen J. Plant immunity: Towards an integrated view of plant–pathogen interactions // Nat. Rev. Genet. 2010. V. 11. P. 539–548. doi: 10.1038/nrg2812.Zou F., Tan C., Shinali T.S. et al. Plant antimicrobial peptides: A comprehensive review of their classification, production, mode of action, functions, applications, and challenges // Food Funct. 2023. V. 14. № 12. P. 5492−5515. doi: 10.1039/d3fo01119dLi J., Hu S., Jian W. et al. Plant antimicrobial peptides: structures, functions, and applications // Bot. Stud. 2021. V. 62. № 1. 5. doi: 10.1186/s40529-021-00312-xTam J.P., Wang S., Wong K.H., Tan W.L. Antimicrobial peptides from plants // Pharmaceuticals. 2015. V. 8. № 4. P. 711–757. doi: 10.3390/ph8040711Bolouri Moghaddam M.R., Vilcinskas A., Rahnamaeian M. Cooperative interaction of antimicrobial peptides with the interrelated immune pathways in plants // Mol. Plant Pathol. 2016. V. 17. № 3. P. 464−471. doi: 10.1111/mpp.12299Campos M.L., de Souza C.M., de Oliveira K.B.S. et al. The role of antimicrobial peptides in plant immunity // J. Exp. Bot. 2018. V. 69. № 21. P. 4997−5011. doi: 10.1093/jxb/ery294Hu Z., Zhang H., Shi K. Plant peptides in plant defense responses // Plant Signal. Behav. 2018. V. 13. № 8. doi: 10.1080/15592324.2018.1475175Xie H., Zhao W., Li W. et al. Small signaling peptides mediate plant adaptions to abiotic environmental stress // Planta. 2022. V. 255. № 4. 72. doi: 10.1007/s00425-022-03859-6Marmiroli N., Maestri E. Plant peptides in defense and signaling // Peptides. 2014. V. 56. P. 30−44. doi: 10.1016/j.peptides.2014.03.013Yamaguchi K., Kawasaki T. Pathogen- and plant-derived peptides trigger plant immunity // Peptides. 2021. V. 144. doi: 10.1016/j.peptides.2021.170611Tavormina P., De Coninck B., Nikonorova N. et al. The plant peptidome: An expanding repertoire of structural features and biological functions // Plant Cell. 2015. V. 27. № 8. P. 2095−2118. doi: 10.1105/tpc.15.00440Silverstein K.A., Graham M.A., Paape T.D. et al. Genome organization of more than 300 defensin-like genes in Arabidopsis // Plant Physiol. 2005. V. 138. № 2. P. 600−610. doi: 10.1104/pp.105.060079Silverstein K.A., Moskal W.A. Jr., et al. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants // Plant J. 2007. V. 51. № 2. P. 262−280. doi: 10.1111/j.1365-313X.2007.03136.xКоростылева Т.В., Шиян А.Н., Одинцова Т.И. Генетический ресурс пырея Thinopyrum elongatum (Host) D.R. Dewey в селекционном улучшении пшеницы // Генетика. 2023. Т. 59. № 10. С. 1112–1119. doi: 10.31857/S0016675823100077Slezina M.P., Istomina E.A., Korostyleva T.V. et al. Molecular insights into the role of cysteine-rich peptides in induced resistance to Fusarium oxysporum infection in tomato based on transcriptome profiling // Int. J. Mol. Sci. 2021. V. 22. № 11. doi: 10.3390/ijms22115741.Teufel F., Almagro Armenteros J.J., Johansen A.R. et al. SignalP 6.0 predicts all five types of signal peptides using protein language models // Nat. Biotechnol. 2022. V. 40. P. 1023−1025. doi: 10.1038/s41587-021-01156-3Gawde U., Chakraborty S., Waghu F.H. et al. CAMPR4: A database of natural and synthetic antimicrobial peptides // Nucl. Acids Res. 2023. V. 51. P. D377–D383. doi: 10.1093/nar/gkac933.Gasteiger E., Hoogland C., Gattiker A. et al. Protein identification and analysis tools on the ExPASy server // The Proteomics Protocols Handbook / Ed. John M. Walker. USA: Humana Press, 2005. P. 571–607.Eisenhaber B., Wildpaner M., Schultz C.J. et al. Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence- and genome-wide studies for Arabidopsis and rice // Plant Physiol. 2003. V. 133. P. 1691−1701. doi: 10.1104/pp.103.023580.Parisi K., Shafee T.M.A., Quimbar P. et al. The evolution, function and mechanisms of action for plant defensins // Semin. Cell Dev. Biol. 2019. V. 88. P. 107–118. doi: 10.1016/j.semcdb.2018.02.004Lay F.T., Anderson M.A. Defensins − components of the innate immune system in plants // Curr. Protein and Pept. Sci. 2005. V. 6. № 1. P. 85–101. doi: 10.2174/1389203053027575.Cools T.L., Struyfs C., Cammue B.P., Thevissen K. Antifungal plant defensins: Increased insight in their mode of action as a basis for their use to combat fungal infections // Future Microbiol. 2017. V. 12. P. 441−454. doi: 10.2217/fmb-2016-0181Sathoff A.E., Samac D.A. Antibacterial activity of plant defensins // Mol. Plant Microbe Interact. 2019. V. 32. № 5. P. 507−514. doi: 10.1094/MPMI-08-18-0229-CRMirouze M., Sels J., Richard O. et al. A putative novel role for plant defensins: A defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance // Plant J. 2006. V. 47. № 3. P. 329−342. doi: 10.1111/j.1365-313X.2006.02788.xSasaki K., Kuwabara C., Umeki N. et al. The cold-induced defensin TAD1 confers resistance against snow mold and Fusarium head blight in transgenic wheat // J. Biotechnol. 2016. V. 228. P. 3−7. doi: 10.1016/j.jbiotec.2016.04.015Stotz H.U., Spence B., Wang Y. A defensin from tomato with dual function in defense and development // Plant Mol. Biol. 2009. V. 71. № 1−2. P. 131−143. doi: 10.1007/s11103-009-9512-zOdintsova T.I., Slezina M.P., Istomina E.A. et al. Defensin-like peptides in wheat analyzed by whole-transcriptome sequencing: A focus on structural diversity and role in induced resistance // PeerJ. 2019. V. 7. doi: 10.7717/peerj.6125Slezina M.P., Istomina E.A., Kulakovskaya E.V. et al. The γ-core motif peptides of AMPs from grasses display inhibitory activity against human and plant pathogens // Int. J. Mol. Sci. 2022. V. 23. № 15. doi: 10.3390/ijms23158383Segura A., Moreno M., Madueño F. et al. Snakin-1, a peptide from potato that is active against plant pathogens // Mol. Plant Microbe Interact. 1999. V. 12. № 1. P. 16−23. doi: 10.1094/MPMI.1999.12.1.16Nahirñak V., Almasia N.I., Fernandez P.V. et al. Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition // Plant Physiol. 2012. V. 158. № 1. P. 252−263. doi: 10.1104/pp.111.186544Zhang S., Yang C., Peng J. et al. GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana // Plant Mol. Biol. 2009. V. 69. P. 745–759. doi: 10.1007/s11103-009-9452-7Oliveira-Lima M., Benko-Iseppon A.M., Neto J.R.C.F. et al. Snakin: Structure, roles and applications of a plant antimicrobial peptide // Curr. Protein Pept. Sci. 2017. V. 18. № 4. P. 368–374. doi: 10.2174/1389203717666160619183140Berrocal-Lobo M., Segura A., Moreno M. et al. Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection // Plant Physiol. 2002. V. 128. № 3. P. 951−961. doi: 10.1104/pp.010685Meiyalaghan S., Thomson S.J., Fiers M.W. et al. Structure and expression of GSL1 and GSL2 genes encoding gibberellin stimulated-like proteins in diploid and highly heterozygous tetraploid potato reveals their highly conserved and essential status // BMC Genomics. 2014. V. 15. 2. doi: 10.1186/1471-2164-15-2Iqbal A., Khan R.S. Snakins: Antimicrobial potential and prospects of genetic engineering for enhanced disease resistance in plants // Mol. Biol. Rep. 2023. V. 50. № 10. P. 8683−8690. doi: 10.1007/s11033-023-08734-5Slavokhotova A.A., Shelenkov A.A., Andreev Y.A., Odintsova T.I. Hevein-like antimicrobial peptides of plants // Biochemistry (Mosc). 2017. V. 82. № 13. P. 1659−1674. doi: 10.1134/S0006297917130065Slavokhotova A.A., Naumann T.A., Price N.P. et al. Novel mode of action of plant defense peptides – hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases // FEBS J. 2014. V. 281. № 20. P. 4754−4764. doi: 10.1111/febs.13015Van den Bergh K.P., Rougé P., Proost P. et al. Synergistic antifungal activity of two chitin-binding proteins from spindle tree (Euonymus europaeus L.) // Planta. 2004. V. 219. № 2. P. 221−232. doi: 10.1007/s00425-004-1238-1Loo S., Tay S.V., Kam A. et al. Anti-fungal hevein-like peptides biosynthesized from quinoa cleavable hololectins // Molecules. 2021. V. 26. № 19. doi: 10.3390/molecules26195909Odintsova T.I., Vassilevski A.A., Slavokhotova A.A. et al. A novel antifungal hevein-type peptide from Triticum kiharae seeds with a unique 10-cysteine motif // FEBS J. 2009. V. 276. № 15. P. 4266−4275. doi: 10.1111/j.1742-4658.2009.07135.xHöng K., Austerlitz T., Bohlmann T., Bohlmann H. The thionin family of antimicrobial peptides // PLoS One. 2021. V. 16. № 7. doi: 10.1371/journal.pone.0254549Oard S., Rush M.C., Oard J.H. Characterization of antimicrobial peptides against a US strain of the rice pathogen Rhizoctonia solani // J. Appl. Microbiol. 2004. V. 97. № 1. P. 169−180. doi: 10.1111/j.1365-2672.2004.02291.xMolina A., Ahl Goy P., Fraile A. et al. Inhibition of bacterial and fungal plant pathogens by thionins of types I and II // Plant Science. 1993. V. 92. № 2. P. 169–177. doi: 10.1016/0168-9452(93)90203-CTerras F., Schoofs H., Thevissen K. et al. Synergistic enhancement of the antifungal activity of wheat and barley thionins by radish and oilseed rape 2S albumins and by barley trypsin inhibitors // Plant Physiol. 1993. V. 103. № 4. P. 1311−1319. doi: 10.1104/pp.103.4.1311Salminen T.A., Blomqvist K., Edqvist J. Lipid transfer proteins: classification, nomenclature, structure, and function // Planta. 2016. V. 244. № 5. P. 971−997. doi: 10.1007/s00425-016-2585-4Kader J.C. Lipid-transfer proteins in plants // Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996. V. 47. P. 627−654. doi: 10.1146/annurev.arplant.47.1.627Santos-Silva C.A.D., Ferreira-Neto J.R.C., Amador V.C. et al. From gene to transcript and peptide: A deep overview on non-specific lipid transfer proteins (nsLTPs) // Antibiotics (Basel). 2023. V. 12. № 5. 939. doi: 10.3390/antibiotics12050939Fahlberg P., Buhot N., Johansson O.N., Andersson M.X. Involvement of lipid transfer proteins in resistance against a non-host powdery mildew in Arabidopsis thaliana // Mol. Plant Pathol. 2019. V. 20. № 1. P. 69−77. doi: 10.1111/mpp.12740Edstam M.M., Blomqvist K., Eklöf A. et al. Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin // Plant Mol. Biol. 2013. V. 83. № 6. P. 625−649. doi: 10.1007/s11103-013-0113-5Yang Y., Li P., Liu C. et al. Systematic analysis of the non-specific lipid transfer protein gene family in Nicotiana tabacum reveal its potential roles in stress responses // Plant Physiol. Biochem. 2022. V. 172. P. 33−47. doi: 10.1016/j.plaphy.2022.01.002Liu F., Zhang X., Lu C. et al. Non-specific lipid transfer proteins in plants: Presenting new advances and an integrated functional analysis // J. Exp. Bot. 2015. V. 66. № 19. P. 5663−5681. doi: 10.1093/jxb/erv313Missaoui K., Gonzalez-Klein Z., Pazos-Castro D. et al. Plant non-specific lipid transfer proteins: An overview // Plant Physiol. Biochem. 2022. V. 171. P. 115−127. doi: 10.1016/j.plaphy.2021.12.026Odintsova T.I., Slezina M.P., Istomina E.A. et al. Non-specific lipid transfer proteins in Triticum kiharae Dorof. et Migush.: Identification, characterization and expression profiling in response to pathogens and resistance inducers // Pathogens. 2019. V. 8. № 4. 221. doi: 10.3390/pathogens8040221Pearce G., Moura D.S., Stratmann J., Ryan C.A. Jr. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development // Proc. Natl Acad. Sci. USA. 2001. V. 98. № 22. P. 12843−12847. doi: 10.1073/pnas.201416998Blackburn M.R., Haruta M., Moura D.S. Twenty years of progress in physiological and biochemical investigation of RALF peptides // Plant Physiol. 2020. V. 182. № 4. P. 1657−1666. doi: 10.1104/pp.19.01310Stegmann M., Monaghan J., Smakowska-Luzan E. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling // Science. 2017. V. 355. № 6322. P. 287−289. doi: 10.1126/science.aal2541Gutiérrez-Marcos J.F., Costa L.M., Biderre-Petit C. et al. Maternally expressed gene1 Is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression // Plant Cell. 2004. V. 16. № 5. P. 1288−1301. doi: 10.1105/tpc.019778Villalba M., Batanero E., López-Otín C. et al. The amino acid sequence of Ole e I, the major allergen from olive tree (Olea europaea) pollen // Eur. J. Biochem. 1993. V. 216. № 3. P. 863−869. doi: 10.1111/j.1432-1033.1993.tb18208.xCastro A.J., de Dios Alché J., Cuevas J. et al. Pollen from different olive tree cultivars contains varying amounts of the major allergen Ole e 1 // Int. Arch. Allergy Immunol. 2003. V. 131. № 3. P. 164−173. doi: 10.1159/000071482De Dios Alché J., M’rani-Alaoui M., Castro A.J., Rodríguez-García M.I. Ole e 1, the major allergen from olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination // Plant Cell. Physiol. 2004. V. 45. № 9. P. 1149−1157. doi: 10.1093/pcp/pch127Han F.P., Fedak G. Molecular characterization of partial amphiploids from Triticum durum × tetraploid Thinopyrum elongatum as novel source of resistance to wheat Fusarium head blight // Proc. 10th Int. Wheat Genet. Symp. Paestum. 2003. P. 1148–1150.Miller S.S., Watson E.M., Lazebnik J. et al. Characterization of an alien source of resistance to Fusarium head blight transferred to Chinese spring wheat // Botany. 2011. V. 89. P. 301–311. doi: 10.1139/b11-017Ceoloni C., Forte P., Kuzmanović L. et al. Cytogenetic mapping of a major locus for resistance to Fusarium head blight and crown rot of wheat on Thinopyrum elongatum 7EL and its pyramiding with valuable genes from a Th. ponticum homoeologous arm onto bread wheat 7DL // Theor. Appl. Genet. 2017. V. 130. P. 2005– 2024. doi: 10.1007/s00122-017-2939-8Konkin D., Hsueh Y.C., Kirzinger M. et al. Genomic sequencing of Thinopyrum elongatum chromosome arm 7EL, carrying fusarium head blight resistance, and characterization of its impact on the transcriptome of the introgressed line CS-7EL // BMC Genomics. 2022. V. 23. № 1. 228. doi: 10.1186/s12864-022-08433-8Wang R.R., Larson S.R., Jensen K.B. et al. Genome evolution of intermediate wheatgrass as revealed by EST-SSR markers developed from its three progenitor diploid species // Genome. 2015. V. 58. № 2. P. 63–70. doi: 10.1139/gen-2014-0186Singh J., Chhabra B., Raza A. et al. Important wheat diseases in the US and their management in the 21st century // Front. Plant Sci. 2023. V. 13. doi: 10.3389/fpls.2022.1010191Liu Z., Li D., Zhang X. Genetic relationships among five basic genomes St, E, A, B and D in Triticeae revealed by genomic southern and in situ hybridization // J. Integr. Plant Biol. 2007. V. 49. № 7. P. 1080–1086. doi: 10.1111/j.1672-9072.2007.00462.xGaál E., Valárik M., Molnár I. et al. Identification of COS markers for Thinopyrum elongatum chromosomes preliminary revealed high level of macrosyntenic relationship between the wheat and Th. elongatum genomes // PLoS One. 2018. V. 13. № 12. doi: 10.1371/journal.pone.0208840.Ke T., Cao H., Huang J. et al. EST-based in silico identification and in vitro test of antimicrobial peptides in Brassica napus // BMC Genomics. 2015. V. 16. № 1. 653. doi: 10.1186/s12864-015-1849-xTian D., Xie Q., Deng Z. et al. Small secreted peptides encoded on the wheat (Triticum aestivum L.) genome and their potential roles in stress responses // Front. Plant Sci. 2022. V. 13. doi: 10.3389/fpls.2022.1000297