Role of peptide hormones in regulation of plant growth and development and their adaptation to environmental factors

  • Halina G. Filiptsova Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

Abstract

Plant peptide hormones are a class of signaling substances involved in the regulation of growth and development processes, as well as the adaptation of plant organisms to stress. Induction of genes, which encode precursors of peptide hormones, occurs in response to a variety of external and internal stimuli. Peptide hormones are perceived by specific receptors of plant cells and trigger a multi-level signaling system that ensures the coordination of cellular processes under changing environmental conditions, the development of protective reactions and the formation of immunity. This work analyses recent studies on the structure, functional activity and signaling mechanisms of the main groups of plant peptide hormones.

Author Biography

Halina G. Filiptsova, Belarusian State University, 4 Niezaliezhnasci Avenue, Minsk 220030, Belarus

PhD (biology), docent; associate professor at the department of plant cell biology and bioengineering, faculty of biology

References

  1. Dorion S, Ouellet JC, Rivoal J. Glutathione metabolism in plants under stress: beyond reactive oxygen species detoxification. Metabolites. 2021;11(9):641–673. DOI: 10.3390/metabo11090641.
  2. Ageitos JM, Sánchez-Pérez A, Calo-Mata P, Villa TG. Antimicrobial peptides (AMPs): ancient compounds that represent novel weapons in the fight against bacteria. Biochemical Pharmacology. 2017;133:117–138. DOI: 10.1016/j.bcp.2016.09.018.
  3. Lima AM, Azevedo MIG, Sousa LM, Oliveira NS, Andrade CR, Freitaset CDT, et al. Plant antimicrobial peptides: an overview about classification, toxicity and clinical applications. International Journal of Biological Macromolecules. 2022;214:10–21. DOI: 10.1016/j.ijbiomac.2022.06.043.
  4. Roy S, Lundquist P, Udvardi M, Scheibleet W-R. Small and mighty: peptide hormones in plant biology. Plant Cell. 2018;30(8): tpc.118.tt0718. DOI: 10.1105/tpc.118.tt0718.
  5. Kondo Y, Hirakawa Y, Fukuda H. Peptide ligands in plants. In: Machida Y, Lin C, Tamanoi F, editors. Signaling pathways in plants. Amsterdam: Academic Press; 2014. p. 85–112 (The enzymes; volume 35). DOI: 10.1016/B978-0-12-801922-1.00004-X.
  6. Lease KA, Walker JC. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiology. 2006;142(3):831–838. DOI: 10.1104/pp.106.086041.
  7. Matsubayashi Y. Posttranslationally modified small-peptide signals in plants. Annual Review of Plant Biology. 2014;65:385–413. DOI: 10.1146/annurev-arplant-050312-120122.
  8. Gancheva MS, Malovichko YV, Poliushkevich LO, Dodueva IE, Lutova LA. Plant peptide hormones. Fiziologiya rastenii. 2019; 66(2):83–103. Russian. DOI: 10.1134/S001533031901007X.
  9. Das D, Jaiswal M, Khan FN, Ahamad S, Kumar S. PlantPepDB: a manually curated plant peptide database. Scientific Reports. 2020;10:2194. DOI: 10.1038/s41598-020-59165-2.
  10. Kim JS, Jeon BW, Kim J. Signaling peptides regulating abiotic stress responses in plants. Frontiers in Plant Science. 2021; 12:704490. DOI: 10.3389/fpls.2021.704490.
  11. Xie H, Zhao W, Li W, Zhang Y, Hajný J, Han H. Small signaling peptides mediate plant adaptions to abiotic environmental stress. Planta. 2022;255(4):72. DOI: 10.1007/s00425-022-03859-6.
  12. Tavormina P, Coninck BD, Nikonorova N, Smet ID, Cammue BPA. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell. 2015;27(8):2095–2118. DOI: 10.1105/tpc.15.00440.
  13. Pearce G, Strydom D, Johnson S, Ryan CA. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science. 1991;253(5022):895–897. DOI: 10.1126/science.253.5022.895.
  14. Ryan CA. The systemin signaling pathway: differential activation of plant defensive genes. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology. 2000;1477(1–2):112–121. DOI: 10.1016/s0167-4838(99)00269-1.
  15. Constabel CP, Yip L, Ryan CA. Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Molecular Biology. 1998;36(1):55–62. DOI: 10.1023/A:1005986004615.
  16. Ryan CA, Pearce G. Systemins: a functionally defined family of peptide signal that regulate defensive genes in Solanaceae species. PNAS. 2003;100(supplement 2):14577–14580. DOI: 10.1073/pnas.1934788100.
  17. Scheer JM, Ryan CA. A 160-kD systemin receptor on the surface of Lycopersicon peruvianum suspension-cultured cells. Plant Cell. 1999;11(8):1525–1535. DOI: 10.2307/3870980.
  18. Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ. Cloning the tomato curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell. 2002; 14(12):3163–3176. DOI: 10.1105/tpc.006379.
  19. Meindl T, Boller T, Felix G. The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell. 1998;10(9):1561–1570. DOI: 10.1105/tpc.10.9.1561.
  20. Scheer JM, Ryan CA. The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. PNAS. 2002;99(14):9585–9590. DOI: 10.1073/pnas.132266499.
  21. Stratmann J, Scheer J, Ryan CA. Suramin inhibits initiation of defense signaling by systemin, chitosan, and a beta-glucan elicitor in suspension-cultured Lycopersicon peruvianum cells. PNAS. 2000;97(16):8862–8867. DOI: 10.1073/pnas.97.16.8862.
  22. Coppola M, Corrado G, Coppola V, Cascone P, Martinelli R, Digilio MC, et al. Prosystemin overexpression in tomato enhances resistance to different biotic stresses by activating genes of multiple signaling pathways. Plant Molecular Biology Reporter. 2015;33: 1270–1285. DOI: 10.1007/s11105-014-0834-x.
  23. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. PNAS. 2005;102(52):19237–19242. DOI: 10.1073/pnas.0509026102.
  24. Corrado G, Sasso R, Pasquariello M, Iodice L, Carretta A, Cascone P, et al. Systemin regulates both systemic and volatile signaling in tomato plants. Journal of Chemical Ecology. 2007;33:669–681. DOI: 10.1007/s10886-007-9254-9.
  25. Molisso D, Coppola M, Buonanno M, Di Lelio I, Aprile AM, Langella E, et al. Not only systemin: prosystemin harbors other active regions able to protect tomato plants. Frontiers in Plant Science. 2022;13:887674. DOI: 10.3389/fpls.2022.887674.
  26. Covarrubias AA, Cuevas-Velazquez CL, Romero-Pérez PS, Rendón-Luna DF, Chater CCC. Structural disorder in plant proteins: where plasticity meets sessility. Cellular and Molecular Life Sciences. 2017;74(17):3119–3147. DOI: 10.1007/s00018-017-2557-2.
  27. Pearce G, Moura DS, Stratmann J, Ryan CA. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. PNAS. 2001;98(22):12843–12847. DOI: 10.1073/pnas.201416998.
  28. Zhang R, Shi P-T, Zhou M, Liu H-Z, Xu X-J, Liu W-T, et al. Rapid alkalinization factor: function, regulation, and potential applications in agriculture. Stress Biology. 2023;3:16. DOI: 10.1007/s44154-023-00093-2.
  29. Olsen AN, Mundy J, Skriver K. Peptomics, identification of novel cationic Arabidopsis peptides with conserved sequence motifs. In Silico Biology. 2002;2(4):441–451. PMID: 12611624.
  30. Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science. 2014;343(6169):408–411. DOI: 10.1126/science.1244454.
  31. Gao Q, Wang C, Xi Y, Shao Q, Hou C, Li L, et al. RALF signaling pathway activates MLO calcium channels to maintain pollen tube integrity. Cell Research. 2023;33:71–79. DOI: 10.1038/s41422-022-00754-3.
  32. Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe. 2014;15(3):329–338. DOI: 10.1016/j.chom.2014.02.009.
  33. AbarcaA, Franck CM, Zipfel C. Family-wide evaluation of rapid alkalinization factor peptides. Plant Physiology. 2021;187(2): 996–1010. DOI: 10.1093/plphys/kiab308.
  34. Srivastava R, Liu J-X, Guo H, Yin Y, Howell SH. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant Journal. 2009;59(6):930–939. DOI: 10.1111/j.1365-313X.2009.03926.x.
  35. Li L, Chen H, Alotaibi SS, Pěnčík A, Adamowski M, Novák O, et al. RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis. PNAS. 2022;119(31):e2121058119. DOI: 10.1073/pnas.2121058119.
  36. Bergonci T, Ribeiro B, Ceciliato PHO, Guerrero-Abad JC, Silva-Filho MC, Moura DS, et al. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. Journal of Experimental Botany. 2014;65(8):2219–2230. DOI: 10.1093/jxb/eru099.
  37. Duan Q, Liu MCJ, Kita D, Jordan SS, Yeh FL, Yvon R, et al. FERONIA controls pectin- and nitric oxide-mediated male – female interaction. Nature. 2020;579(7800):561–566. DOI: 10.1038/s41586-020-2106-2.
  38. Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, et al. The receptor kinase FER is a RALFregulated scaffold controlling plant immune signaling. Science. 2017;355(6322):287–289. DOI: 10.1126/science.aal2541.
  39. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Molecular Cell. 2014;54(1):43–55. DOI: 10.1016/j.molcel.2014.02.021.
  40. Guo H, Nolan TM, Song G, Liu S, Xie Z, Chen J, et al. FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Current Biology. 2018;28(20):3316–3324. DOI: 10.1016/j.cub.2018.07.078.
  41. Haruta M, Monshausen G, Gilroy S, Sussman MR. A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. Biochemistry. 2008;47(24):6311–6321. DOI: 10.1021/bi8001488.
  42. Liu Y, Chen Y, Jiang H, Shui Z, Zhong Y, Shang J, et al. Genome-wide characterization of soybean RALF genes and their expression responses to Fusarium oxysporum. Frontiers in Plant Science. 2022;13:1006028. DOI: 10.3389/fpls.2022.1006028.
  43. He YH, Zhang Z-R, Xu Y-P, Chen S-Y, Cai X-Z. Genome-wide identification of rapid alkalinization factor family in Bassica napus and functional analysis of BnRALF10 in immunity to Sclerotinia sclerotiorum. Frontiers in Plant Science. 2022;13:877404. DOI: 10.3389/fpls.2022.877404.
  44. Duan Z, Liu W, Li K, Duan W, Zhu S, Xing J, et al. Regulation of immune complex formation and signalling by FERONIA, a busy goddess in plant – microbe interactions. Molecular Plant Pathology. 2022;23(11):1695–1700. DOI: 10.1111/mpp.13256.
  45. Dodueva I, Lebedeva M, Lutova L. Dialog between kingdoms: enemies, allies and peptide phytohormones. Plants. 2021;10(11):2243. DOI: 10.3390/plants10112243.
  46. Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Current Biology. 2018;28(5):666–675. DOI: 10.1016/j.cub.2018.01.023.
  47. Zhao C, Jiang W, Zayed O, Liu X, Tang K, Nie W, et al. The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones. National Science Review. 2021;8(1):nwaa149. DOI: 10.1093/nsr/nwaa149.
  48. Xu Y, Magwanga RO, Jin D, Cai X, Hou Y, Juyun Z, et al. Comparative transcriptome analysis reveals evolutionary divergence and shared network of cold and salt stress response in diploid D-genome cotton. BMC Plant Biology. 2020;20:518. DOI: 10.1186/ s12870-020-02726-4.
  49. Opsahl-Ferstad HG, Deunff EL, Dumas C, Rogowsky PM. ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant Journal. 1997;12(1):235–246. DOI: 10.1046/j.1365-313x.1997.12010235.x.
  50. Yamaguchi YL, Ishida T, Sawa S. CLE peptides and their signaling pathways in plant development. Journal of Experimental Botany. 2016;67(16):4813–4826. DOI: 10.1093/jxb/erw208.
  51. Song X-F, Hou X-L, Liu C-M. CLE peptides: critical regulators for stem cell maintenance in plants. Planta. 2021;255:5. DOI: 10.1007/s00425-021-03791-1.
  52. Kang J, Wang X, Ishida T, Grienenberger E, Zheng Q, Wang J, et al. A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana. New Phytologist. 2022;235(6):2300–2312. DOI: 10.1111/nph.18291.
  53. Bashyal S, Gautam CK, Müller LM. CLAVATA signaling in plant – environment interactions. Plant Physiology. 2024;194(3): 1336–1357. DOI: 10.1093/plphys/kiad591.
  54. Cock JM, McCormick S. A large family of genes that share homology with CLAVATA3. Plant Physiology. 2001;126(3):939–942. DOI: 10.1104/pp.126.3.939.
  55. Betsuyaku S, Sawa S, Yamada M. The function of the CLE peptides in plant development and plant – microbe interactions. The Arabidopsis Book. 2011;9:e0149. DOI: 10.1199/tab.0149.
  56. Matsubayashi Y. Small post-translationally modified peptide signals in Arabidopsis. The Arabidopsis Book. 2011;9:e0150. DOI: 10.1199/tab.0150.
  57. Hirakawa Y. CLAVATA3, a plant peptide controlling stem cell fate in the meristem. Peptides. 2021;142:170579. DOI: 10.1016/ j.peptides.2021.170579.
  58. Hu C, Zhu Y, Cui Y, Cheng K, Liang W, Wei Z, et al. A group of receptor kinases are essential for CLAVATA signaling to maintain stem cell homeostasis. Nature Plants. 2018;4:205–211. DOI: 10.1038/s41477-018-0123-z.
  59. Basu U, Parida SK. CLAVATA signaling pathway receptors modulate developmental traits and stress responses in crops. In: Upadhyay SK, Shumayla, editors. Plant receptor-like kinases. Role in development and stress. Amsterdam: Academic Press; 2023. p. 371–392. DOI: 10.1016/B978-0-323-90594-7.00004-1.
  60. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, et al. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science. 2008;322(5901):594–597. DOI: 10.1126/science.1160158.
  61. Wang J, Kucukoglu M, Zhang L, Chen P, Decker D, Nilsson O, et al. The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway. BMC Plant Biology. 2013;13:94. DOI: 10.1186/ 1471-2229-13-94.
  62. Hazak O, Hardtke CS. CLAVATA1-type receptors in plant development. Journal of Experimental Botany. 2016;67(16):4827–4833. DOI: 10.1093/jxb/erw247.
  63. Willoughby AC, Nimchuk ZL. WOX going on: CLE peptides in plant development. Current Opinion in Plant Biology. 2021; 63:102056. DOI: 10.1016/j.pbi.2021.102056.
  64. Jha P, Ochatt SJ, Kumar V. WUSCHEL: a master regulator in plant growth signaling. Plant Cell Reports. 2020;39(4):431–444. DOI: 10.1007/s00299-020-02511-5.
  65. Strabala TJ, O’Donnell PJ, Smit A-M, Ampomah-Dwamena C, Martin EJ, Netzler N, et al. Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiology. 2006;140(4):1331–1344. DOI: 10.1104/pp.105.075515.
  66. Yang S, Bai J, Wang J. TDIF peptides regulate root growth by affecting auxin homeostasis and PINs expression in Arabidopsis thaliana. Planta. 2020;251:109. DOI: 10.1007/s00425-020-03406-1.
  67. Lee H, Chah O-K, Sheen J. Stem-cell-triggered immunity through CLV3p – FLS2 signalling. Nature. 2011;473(7347):376–379. DOI: 10.1038/nature09958.
  68. Endo S, Shinohara H, Matsubayashi Y, Fukuda H. A novel pollen – pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. Current Biology. 2013;23(17):1670–1676. DOI: 10.1016/j.cub.2013.06.060.
  69. Ma D, Endo S, Betsuyaku S, Shimotohno A, Fukuda H. CLE2 regulates light-dependent carbohydrate metabolism in Arabidopsis shoots. Plant Molecular Biology. 2020;104(6):561–574. DOI: 10.1007/s11103-020-01059-y.
  70. Gutiérrez-Alanís D, Yong-Villalobos L, Jiménez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, Mora-Macías J, et al. Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Developmental Cell. 2017;41(5):555–570. DOI: 10.1016/j.devcel.2017.05.009.
  71. Bartels S, Boller T. Quo vadis, Pep? Plant elicitor peptides at the crossroads of immunity, stress, and development. Journal of Experimental Botany. 2015;66(17):5183–5193. DOI: 10.1093/jxb/erv180.
  72. Chen YL, Fan KT, Hung SC, Chen YR. The role of peptides cleaved from protein precursors in eliciting plant stress reactions. New Phytologist. 2020;225(6):2267–2282. DOI: 10.1111/nph.16241.
  73. Zelman AK, Berkowitz GA. Plant elicitor peptide (Pep) signaling and pathogen defense in tomato. Plants. 2023;12(15):2856. DOI: 10.3390/plants12152856.
  74. Jing Y, Zou X, Sun C, Qin X, Zheng X. Danger-associate peptide regulates root immunity in Arabidopsis. Biochemical and Biophysical Research Communications. 2023;663:163–170. DOI: 10.1016/j.bbrc.2023.04.091.
  75. Huffaker A, Pearce G, Ryan CA. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. PNAS. 2006;103(26):10098–10103. DOI: 10.1073/pnas.0603727103.
  76. Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, Hander T, et al. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. Journal of Experimental Botany. 2013;64(17):5309–5321. DOI: 10.1093/jxb/ert330.
  77. Huffaker A, Ryan CA. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. PNAS. 2007;104(25):10732–10736. DOI: 10.1073/pnas.0703343104.
  78. Huffaker A, Dafoe NJ, Schmelz EA. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiology. 2011;155(3):1325–1338. DOI: 10.1104/pp.110.166710.
  79. Wang A, Guo J, Wang S, Zhang Y, Lu F, Duan J, et al. BoPEP4, a C-terminally encoded plant elicitor peptide from Broccoli, plays a role in salinity stress tolerance. International Journal of Molecular Sciences. 2022;23(6):3090. DOI: 10.3390/ijms23063090.
  80. Lori M, van Verk MC, Hander T, Schatowitz H, Klauser D, Flury P, et al. Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: interfamily incompatibility of perception but downstream signaling. Journal of Experimental Botany. 2015;66(17):5315–5325. DOI: 10.1093/jxb/erv236.
  81. Ross A, Yamada K, Hiruma K, Yamashita‐Yamada M, Lu X, Takano Y, et al. The Arabidopsis PEPR pathway couples local and systemic plant immunity. The EMBO Journal. 2013;33:62–75. DOI: 10.1002/embj.201284303.
  82. Uemura T, Hachisu M, Desaki Y, Ito A, Hoshino R, Sano Y, et al. Soy and Arabidopsis receptor-like kinases respond to polysaccharide signals from Spodoptera species and mediate herbivore resistance. Communications Biology. 2020;3:224. DOI: 10.1038/ s42003-020-0959-4.
  83. Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ, Sartor R, et al. Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. PNAS. 2013;110(14):5707–5712. DOI: 10.1073/pnas.1214668110.
  84. Safaeizadeh M. Endogenous peptide signals in Arabidopsis thaliana, their receptors and their role in innate immunity. Journal of Plant Molecular Breeding. 2019;9(1):1–11. DOI: 10.22058/JPMB.2022.548053.1251.
  85. Lee MW, Huffaker A, Crippen D, Robbins RT, Goggin FL. Plant elicitor peptides promote plant defences against nematodes in soybean. Molecular Plant Pathology. 2018;19:858–869. DOI: 10.1111/mpp.12570.
  86. Yamaguchi Y, Pearce G, Ryan CA. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. PNAS. 2006;103(26):10104–10109. DOI: 10.1073/pnas.0603729103.
  87. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell. 2010;22(2):508–522. DOI: 10.1105/tpc.109.068874.
  88. Ma Y, Walker RK, Zhao Y, Berkowitz GA. Linking ligand perception by PEPR pattern recognition receptors to cytosolic Ca2+ elevation and downstream immune signaling in plants. PNAS. 2012;109(48):19852–19857. DOI: 10.1073/pnas.1205448109.
  89. Ma Y, Zhao Y, Walker RK, Berkowitz GA. Molecular steps in the immune signaling pathway evoked by plant elicitor peptides: Ca2+-dependent protein kinases, nitric oxide, and reactive oxygen species are downstream from the early Ca2+ signal. Plant Physiology. 2013;163(3):1459–1471. DOI: 10.1104/pp.113.226068.
  90. Filiptsova HG. The role of endogenous elicitor peptides in plant resistance to biotic stress. Journal of the Belarusian State University. Biology. 2019;2:3–12. Russian. DOI: 10.33581/2521-1722-2019-2-3-12.
  91. Filiptsova HG, Yurin VM. Physiological and biochemical mechanisms of plants resistance to oxidative stress under peptide elicitor AtPep1. Journal of the Belarusian State University. Biology. 2021;3:38–46. Russian. DOI: 10.33581/2521-1722-2021-3-38-46.
  92. Gully K, Hander T, Boller T, Bartels S. Perception of Arabidopsis AtPep peptides, but not bacterial elicitors, accelerates starvation-induced senescence. Frontiers in Plant Science. 2015;6:1–10. DOI: 10.3389/fpls.2015.00014.
  93. Poncini L, Wyrsch I, Dénervaud Tendon V, Vorley T, Boller T, Geldner N, et al. In root of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signaling than flg22 or the chitin heptamer. PLoS ONE. 2017;12(10):e0185808. DOI: 10.1371/journal.pone.0185808.
  94. Okada K, Kubota Y, Hirase T, Otani K, Goh T, Hiruma K, et al. Uncoupling root hair formation and defence activation from growth inhibition in response to damage-associated Pep peptides in Arabidopsis thaliana. New Phytologist. 2021;229(5):2844–2858. DOI: 10.1111/nph.17064.
  95. Ohyama K, Ogawa M, Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant Journal. 2008;55(1):152–160. DOI: 10.1111/j.1365-313X. 2008.03464.x.
  96. Taleski M, Imin N, Djordjevic MA. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. Journal of Experimental Botany. 2018;69(8):1829–1836. DOI: 10.1093/jxb/ery037.
  97. Aggarwal S, Kumar A, Jain M, Sudan J, Singh K, Kumari S, et al. C-terminally encoded peptides (CEPs) are potential mediators of abiotic stress response in plants. Physiology and Molecular Biology of Plants. 2020;26(10):2019–2033. DOI: 10.1007/s12298- 020-00881-4.
  98. Delay C, Imin N, Djordjevic MA. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. Journal of Experimental Botany. 2013;64(17):5383–5394. DOI: 10.1093/jxb/ert332.
  99. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. Perception of root-derived peptides by shoot LRRRKs mediates systemic N-demand signaling. Science. 2014;346(6207):343–346. DOI: 10.1126/science.1257800.
  100. Mohd-Radzman NA, Laffont C, Ivanovici A, Patel N, Reid D, Stougaard J, et al. Different pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development. Plant Physiology. 2016;171(4):2536–2548. DOI: 10.1104/ pp.16.00113.
  101. Chapman K, Ivanovici A, Taleski M, Sturrock CJ, Ng JLP, Mohd-Radzman NA, et al. CEP receptor signalling controls root system architecture in Arabidopsis and Medicago. New Phytologist. 2020;226(6):1809–1821. DOI: 10.1111/nph.16483.
  102. Smith S, Zhu S, Joos L, Roberts I, Nikonorova N, Vu LD, et al. The CEP5 peptide promotes abiotic stress tolerance, as revealed by quantitative proteomics, and attenuates the AUX/IAA equilibrium in Arabidopsis. Molecular & Cellular Proteomics. 2020; 19(8):1248–1262. DOI: 10.1074/mcp.RA119.001826.
  103. Taleski M, Chapman K, Novák O, Schmülling T, Frank M, Djordjevic MA. CEP peptide and cytokinin pathways converge on CEPD glutaredoxins to inhibit root growth. Nature Communications. 2023;14:1683. DOI: 10.1038/s41467-023-37282-6.
  104. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science. 2010;329(5995):1065–1067. DOI: 10.1126/science.1191132.
  105. Kaufmann C, Sauter M. Sulfated plant peptide hormones. Journal of Experimental Botany. 2019;70(16):4267–4277. DOI: 10.1093/jxb/erz292.
  106. Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y. Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. PNAS. 2016;113(14):3897–3902. DOI: 10.1073/pnas.1522639113.
  107. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science. 2002;296(5572):1470–1472. DOI: 10.1126/science.1069607.
  108. Rzemieniewski J, Stegmann M. Regulation of pattern-triggered immunity and growth by phytocytokines. Current Opinion in Plant Biology. 2022;68:102230. DOI: 10.1016/j.pbi.2022.102230.
  109. Matsubayashi Y, Sakagami Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. PNAS. 1996;93(15):7623–7627. DOI: 10.1073/pnas.93.15.7623.
  110. Lorbiecke R, Sauter M. Comparative analysis of PSK peptide growth factor precursor homologs. Plant Science. 2002;1639(2): 321–332. DOI: 10.1016/S0168-9452(02)00101-2.
  111. Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant Journal. 2017;89(4):789–804. DOI: 10.1111/tpj.13415.
  112. Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, et al. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature. 2015;525(7568):265–268. DOI: 10.1038/nature14858.
  113. Ladwig F, Dahlke RI, Stührwohldt N, Hartmann J, Harter K, Sauter M, et al. Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes cyclic nucleotide-gated channel 17, H+-ATPase, and BAK1. Plant Cell. 2015;27(6):1718–1729. DOI: 10.1105/tpc.15.00306.
  114. Kaufmann C, Motzkus M, Sauter M. Phosphorylation of the phytosulfokine peptide receptor PSKR1 controls receptor activity. Journal of Experimental Botany. 2017;68(7):1411–1423. DOI: 10.1093/jxb/erx030.
  115. Hartmann J, Fischer C, Dietrich P, Sauter M. Kinase activity and calmodulin binding are essential for growth signaling by the phytosulfokine receptor PSKR1. Plant Journal. 2014;78(2):192–202. DOI: 10.1111/tpj.12460.
  116. Igasaki T, Akashi N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K. Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant and Cell Physiology. 2003;44(12):1412–1416. DOI: 10.1093/pcp/pcg161.
  117. Yamakawa S, Sakuta C, Matsubayashi Y, Sakagami Y, Kamada H, Satoh S. The promotive effects of a peptidyl plant growth factor, phytosulfokine-α, on the formation of adventitious roots and expression of a gene for a root-specific cystatin in cucumber hypocotyls. Journal of Plant Research. 1998;111:453–458. DOI: 10.1007/BF02507810.
  118. Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y. The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of zinnia. Plant Physiology. 1999;120(4):1043–1048. DOI: 10.1104/pp.120.4.1043.
  119. Zhang H, Hu Z, Lei C, Zheng C, Wang J, Shao S, et al. A plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca2+ signaling in tomato. Plant Cell. 2018;30(3):652–667. DOI: 10.1105/tpc.17.00537.
  120. Wu T, Kamiya T, Yumoto H, Sotta N, Katsushi Y, Shigenobu S, et al. An Arabidopsis thaliana copper-sensitive mutant suggests a role of phytosulfokine in ethylene production. Journal of Experimental Botany. 2015;66(13):3657–3667. DOI: 10.1093/jxb/erv105.
  121. Stührwohldt N, Dahlke RI, Kutschmar A, Peng X, Sun M-X, Sauter M. Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiologia Plantarum. 2015;153(4):643–653. DOI: 10.1111/ ppl.12270.
  122. Loivamäki M, Stührwohldt N, Deeken R, Steffens B, Roitsch T, Hedrich R, et al. A role for PSK signaling in wounding and microbial interactions in Arabidopsis. Physiologia Plantarum. 2010;139(4):348–357. DOI: 10.1111/j.1399-3054.2010.01371.x.
  123. Rodiuc N, Barlet X, Hok S, Perfus-Barbeoch L, Allasia V, Engler G, et al. Evolutionarily distant pathogens require the Arabidopsis phytosulfokine signalling pathway to establish disease. Plant, Cell and Environment. 2016;39(7):1396–1407. DOI: 10.1111/ pce.12627.
  124. Igarashi D, Tsuda K, Katagiri F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant Journal. 2012;71(2):194–204. DOI: 10.1111/j.1365-313X.2012.04950.x.
  125. Stührwohldt N, Bühler E, Sauter M, Schaller A. Phytosulfokine (PSK) precursor processing by subtilase SBT3.8 and PSK signaling improve drought stress tolerance in Arabidopsis. Journal of Experimental Botany. 2021;72(9):3427–3440. DOI: 10.1093/jxb/ erab017.
  126. Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. PNAS. 2007;104(46):18333–18338. DOI: 10.1073/pnas.0706403104.
  127. Fuglsang AT, Kristensen A, Cuin TA, Schulze WX, Persson J, Thuesen KH, et al. Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. Plant Journal. 2014;80(6):951–964. DOI: 10.1111/tpj.12680.
  128. Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA, Dayaratne S, et al. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant Journal. 2013;73(3):469–482. DOI: 10.1111/tpj.12050.
  129. Ou Y, Lu X, Zi Q, Xun Q, Zhang J, Wu Y, et al. RGF1 insensitive 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Research. 2016;26:686–698. DOI: 10.1038/cr.2016.63.
  130. Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T, Madder A, et al. Transcriptional and functional classification of the GOLVEN/root growth factor/CLE-like signaling peptides reveals their role in lateral root and hair formation. Plant Physiology. 2013;161(2):954–970. DOI: 10.1104/pp.112.206029.
  131. Whitford R, Fernandez A, Tejos R, Pérez Amparo C, Kleine-Vehn J, Vanneste S, et al. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Developmental Cell. 2012;22(3):678–685. DOI: 10.1016/j.devcel.2012.02.002.
  132. Jeon BW, Kim JS, Oh E, Kang NY, Kim J. Root meristem growth factor 1 (RGF1) – RGF1 insensitive 1 peptide – receptor pair inhibits lateral root development via the MPK6-PUCHI module in Arabidopsis. Journal of Experimental Botany. 2023;74(5):1475–1488. DOI: 10.1093/jxb/erac495.
  133. Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, et al. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science. 2017;355(6322):280–284. DOI: 10.1126/science.aaj1562.
  134. Fujita S. Casparian strip integrity factor (CIF) family peptides – regulator of plant extracellular barriers. Peptides. 2021;143:170599. DOI: 10.1016/j.peptides.2021.170599.
  135. Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science. 2017;355(6322):284–286. DOI: 10.1126/science.aai9057.
  136. Okuda S, Fujita S, Moretti A, Hohmann U, Doblas VG, Ma Y, et al. Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2. PNAS. 2020;117(5):2693–2703. DOI: 10.1073/pnas.1911553117.
  137. Compaan B, Yang W-C, Bisseling T, Franssen H. ENOD40 expression in the pericycle precedes cortical cell division in Rhizobium – legume interaction and the highly conserved internal region of the gene does not encode a peptide. Plant and Soil. 2001;230(1):1–8. DOI: 10.1023/A:1004687822174.
  138. Röhrig H, Schmidt J, Miklashevichs E, Schell J, John M. Soybean ENOD40 encodes two peptides that bind to sucrose synthase. PNAS. 2002;99(4):1915–1920. DOI: 10.1073/pnas.022664799.
  139. Campalans A, Kondorosi A, Crespi M. Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell. 2004;16(4):1047–1059. DOI: 10.1105/tpc.019406.
  140. Kouchi H, Takane K, So RB, Ladha JK, Reddy PM. Rice ENOD40: isolation and expression analysis in rice and transgenic soybean root nodules. Plant Journal. 1999;18(2):121–129. DOI: 10.1046/j.1365-313x.1999.00432.x.
  141. Gultyaev AP, Roussis A. Identification of conserved secondary structures and expansion segments in enod40 RNAs reveals new enod40 homologues in plants. Nucleic Acids Research. 2007;35(9):3144–3152. DOI: 10.1093/nar/gkm173.
  142. Shafee TMA, Lay FT, Phan TK, Anderson MA, Hulett MD. Convergent evolution of defensin sequence, structure and function. Cellular and Molecular Life Sciences. 2017;74(4):663–682. DOI: 10.1007/s00018-016-2344-5.
  143. Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature. 2011;480(7378):520–524. DOI: 10.1038/nature10625.
  144. Downie JA, Kondorosi E. Why should nodule cysteine-rich (NCR) peptides be absent from nodules of some groups of legumes but essential for symbiotic N-fixation in others? Frontiers in Agronomy. 2021;3:654576. DOI: 10.3389/fagro.2021.654576.
  145. Horvath B, Domonkos Á, Kereszt A, Szűcs A, Ábrahám E, Ayaydin F, et al. Loss of the nodule-specific cysteine-rich peptide, NCR169, abolishes symbiotic nitrogen fixation in the Medicago truncatula dnf 7 mutant. PNAS. 2015;112(49):15232–15237. DOI: 10.1073/pnas.1500777112.
  146. Singh J, Valdés-López O. A nodule peptide confiscates haem to promote iron uptake in rhizobia. Trends in Plant Science. 2023; 28(2):125–127. DOI: 10.1016/j.tplants.2022.11.005.
  147. Rychel AL, Peterson KM, Torii KU. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. Journal of Plant Research. 2010;123:275–280. DOI: 10.1007/s10265-010-0330-9.
  148. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, et al. Epidermal cell density is autoregulated via a secretory peptide, epidermal patterning factor 2 in Arabidopsis leaves. Plant and Cell Physiology. 2009;50(6):1019–1031. DOI: 10.1093/pcp/ pcp068.
  149. Xiong L, Huang Y, Liu Z, Li C, Yu H, Shahid MQ, et al. Small epidermal patterning factor-like 2 peptides regulate awn development in rice. Plant Physiology. 2022;190(1):516–531. DOI: 10.1093/plphys/kiac278.
  150. Le J, Zou J, Yang K, Wang M. Signaling to stomatal initiation and cell division. Frontiers in Plant Science. 2014;5:297. DOI: 10.3389/fpls.2014.00297.
  151. Hunt L, Bailey KJ, Gray JE. The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytologist. 2010;186(3):609–614. DOI: 10.1111/j.1469-8137.2010.03200.x.
  152. Kosentka PZ, Overholt A, Maradiaga R, Mitoubsi O, Shpak ED. EPFL signals in the boundary region of the SAM restrict its size and promote leaf initiation. Plant Physiology. 2019;179(1):265–279. DOI: 10.1104/pp.18.00714.
  153. Nahirnak V, Almasia NI, Hopp HE, Vazquez-Rovereet C. Snakin/GASA proteins: involvement in hormone crosstalk and redox homeostasis. Plant Signaling and Behavior. 2012;7(8):1004–1008. DOI: 10.4161/psb.20813.
  154. Wigoda N, Ben-Nissan G, Granot D, Schwartz A, Weiss D. The gibberellin-induced, cysteine-rich protein GIP2 from Petunia hybrida exhibits in planta antioxidant activity. Plant Journal. 2006;48(5):796–805. DOI: 10.1111/j.1365-313X.2006.02917.x.
  155. Sun S, Wang H, Yu H, Zhong C, Zhang X, Peng J, et al. GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. Journal of Experimental Botany. 2013;64(6):1637–1647. DOI: 10.1093/jxb/ert021.
  156. Silverstein KAT, Moskal WA Jr, Wu HC, Underwood BA, Graham MA, Town CD, et al. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant Journal. 2007;51(2):262–280. DOI: 10.1111/j.1365-313X. 2007.03136.x.
  157. Ahmad MZ, Sana A, Jamil A, Nasir JA, Ahmed S, Hameed MU, et al. A genome-wide approach to the comprehensive analysis of GASA gene family in Glycine max. Plant Molecular Biology. 2019;100(6):607–620. DOI: 10.1007/s11103-019-00883-1.
  158. Bouteraa MT, Romdhane WB, Hsouna AB, Amor F, Ebel C, Saad RB, et al. Genome-wide characterization and expression profiling of GASA gene family in Triticum turgidum ssp. durum (Desf.) Husn. (durum wheat) unveils its involvement in environmental stress responses. Phytochemistry. 2023;206:113544. DOI: 10.1016/j.phytochem.2022.113544.
  159. Bouteraa MT, Romdhane WB, Baazaoui N, Alfaifi MY, Chouaibi Y, Akacha BB, et al. GASA proteins: review of their functions in plant environmental stress tolerance. Plants. 2023;12(10):2045. DOI: 10.3390/plants12102045.
  160. Qu J, Kang SG, Hah C, Jang J-C. Molecular and cellular characterization of GA-stimulated transcripts GASA4 and GASA6 in Arabidopsis thaliana. Plant Science. 2016;246:1–10. DOI: 10.1016/j.plantsci.2016.01.009.
  161. Nagai K, Mori Y, Ishikawa S, Furuta T, Gamuyao R, Niimi Y, et al. Antagonistic regulation of the gibberellic acid response during stem growth in rice. Nature. 2020;584(7819):109–114. DOI: 10.1038/s41586-020-2501-8.
  162. Butenko MA, Patterson SE, Grini PE, Stenvik G-E, Amundsen SS, Mandal A, et al. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell. 2003;15(10):2296–2307. DOI: 10.1105/tpc.014365.
  163. Zhu Q, Shao Y, Ge S, Zhang M, Zhang T, Hu X, et al. A MAPK cascade downstream of IDA-HAE/HSL2 ligand-receptor pair in lateral root emergence. Nature Plants. 2019;5:414–423. DOI: 10.1038/s41477-019-0396-x.
  164. Patharkar OR, Walker JC. Core mechanisms regulating developmentally timed and environmentally triggered abscission. Plant Physiology. 2016;172(1):510–520. DOI: 10.1104/pp.16.01004.
  165. Mishima M, Takayama S, Sasaki K-I, Jee J-G, Kojima C, Isogai A, et al. Structure of the male determinant factor for Brassica self-incompatibility. Journal of Biological Chemistry. 2003;278(38):36389–36395. DOI: 10.1074/jbc.M305305200.
  166. Kemp BP, Doughty J. S cysteine-rich (SCR) binding domain analysis of the Brassica self-incompatibility S-locus receptor kinase. New Phytologyst. 2007;175(4):619–629. DOI: 10.1111/j.1469-8137.2007.02126.x.
  167. Ma R, Han Z, Hu Z, Lin G, Gong X, Zhang H, et al. Structural basis for specific self-incompatibility response in Brassica. Cell Research. 2016;26:1320–1329. DOI: 10.1038/cr.2016.129.
  168. Gully K, Pelletier S, Guillou M-C, Ferrand M, Aligon S, Pokotylo I, et al. The SCOOP12 peptide regulates defense response and root elongation in Arabidopsis thaliana. Journal of Experimental Botany. 2019;70(4):1349–1365. DOI: 10.1093/jxb/ery454.
  169. Rhodes J, Yang H, Moussu S, Boutrot F, Santiago J, Zipfel C. Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2. Nature Communications. 2021;12:705. DOI: 10.1038/s41467-021-20932-y.
  170. Stahl E, Martin AF, Glauser G, Guillou M-C, Aubourg S, Renou J-P, et al. The MIK2/SCOOP signaling system contributes to Arabidopsis resistance against herbivory by modulating jasmonate and indole glucosinolate biosynthesis. Frontiers in Plant Science. 2022;13:852808. DOI: 10.3389/fpls.2022.852808.
  171. Guillou M-C, Vergne E, Aligon S, Pelletier S, Simonneau F, Rolland A, et al. The peptide SCOOP12 acts on reactive oxygen species homeostasis to modulate cell division and elongation in Arabidopsis primary root. Journal of Experimental Botany. 2022;73(18): 6115–6132. DOI: 10.1093/jxb/erac240.
  172. Guillou M-C, Balliau T, Vergne E, Canut H, Chourré J, Herrera-León C, et al. The PROSCOOP10 gene encodes two extracellular hydroxylated peptides and impacts flowering time in Arabidopsis. Plants. 2022;11:3554. DOI: 10.3390/plants11243554.
  173. Chen YL, Lee C-Y, Cheng K-T, Chang W-H, Huang R-N, Nam HG, et al. Quantitative peptidomics study reveals that a woundinduced peptide from PR-1 regulates immune signaling in tomato. Plant Cell. 2014;26(10):4135–4148. DOI: 10.1105/tpc.114.131185.
  174. Chien PS, Nam HG, Chen Y-R. A salt-regulated peptide derived from the CAP superfamily protein negatively regulates saltstress tolerance in Arabidopsis. Journal of Experimental Botany. 2015;66(17):5301–5313. DOI: 10.1093/jxb/erv263.
Published
2024-07-05
Keywords: plant peptide hormones, signaling mechanisms, regulation of growth and development, plant resistance
How to Cite
Filiptsova, H. G. (2024). Role of peptide hormones in regulation of plant growth and development and their adaptation to environmental factors. Experimental Biology and Biotechnology, 2, 4-23. Retrieved from https://journals.bsu.by/index.php/biology/article/view/6123