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Plant Peptide Hormones

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Abstract

In addition to classic phytohormones, such as auxin, cytokinin, ethylene, gibberellin, and abscisic acid, plant peptide hormones are also involved in various aspects of growth and development. This group of phytohormones is represented by short peptides, which are, as a rule, ligands for receptor kinases that initiate a signaling cascade, regulating plant development in response to stimuli from an external or internal environment. The review examines the peptide phytohormones known to date, their structure, synthesis features, receptors, and their role in plant development.

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REFERENCES

  1. Pearce, G., Strydom, D., Johnson, S., and Ryan, C.A., A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins, Science, 1991, vol. 253, pp. 895–897.

    Article  CAS  PubMed  Google Scholar 

  2. Matsubayashi, Y. and Sakagami, Y., Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L., Proc. Natl. Acad. Sci. USA, 1996, vol. 93, pp. 7623–7627.

    Article  CAS  PubMed  Google Scholar 

  3. Fletcher, J.C., Brand, U., Running, M.P., Simon, R., and Meyerowitz, E.M., Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems, Science, 1999, vol. 283, pp. 1911–1914.

    Article  CAS  PubMed  Google Scholar 

  4. Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K., Sawa, S., Dohmae, N., and Fukuda, H., Dodeca-CLE peptides as suppressors of plant stem cell differentiation, Science, 2006, vol. 313, pp. 842–845.

    Article  CAS  PubMed  Google Scholar 

  5. Matsubayashi, Y., Posttranslationally modified small-peptide signals in plants, Annu. Rev. Plant Biol., 2014, vol. 65, pp. 385–413.

    Article  CAS  PubMed  Google Scholar 

  6. Lease, K.A. and Walker, J.C., The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics, Plant Physiol., 2006, vol. 142, pp. 831–838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Schardon, K., Hohl, M., Graff, L., Pfannstiel, J., Schulze, W., Stintzi, A., and Schaller, A., Precursor processing for plant peptide hormone maturation by subtilisin-like serine proteinases, Science, 2016, vol. 354, pp. 1594–1597.

    Article  CAS  PubMed  Google Scholar 

  8. Tamaki, T., Betsuyaku, S., Fujiwara, M., Fukao, Y., Fukuda, H., and Sawa, S., SUPPRESSOR OF LLP1 1‑mediated C-terminal processing is critical for CLE19 peptide activity, Plant J., 2013, vol. 76, pp. 970–981.

    Article  CAS  PubMed  Google Scholar 

  9. Okamoto, S., Shinohara, H., Mori, T., Matsubayashi, Y., and Kawaguchi, M., Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase, Nat. Commun., 2013, vol. 4: 2191.

    Article  CAS  PubMed  Google Scholar 

  10. Gorres, K.L. and Raines, R.T., Prolyl 4-hydroxylase, Crit. Rev. Biochem. Mol. Biol., 2010, vol. 45, pp. 106–124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Santiago, J., Brandt, B., Wildhagen, M., Hohmann, U., Hothorn, L.A., Butenko, M.A., and Hothorn, M., Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission, Elife, 2016, vol. 5: e15075.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Amano, Y., Tsubouchi, H., Shinohara, H., Ogawa, M., and Matsubayashi, Y., Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in A-rabidopsis, Proc. Natl. Acad. Sci. USA, 2007, vol. 104, pp.  18333–18338.

    Article  PubMed  Google Scholar 

  13. Song, W., Liu, L., Wang, J., Wu, Z., Zhang, H., Tang, J., Lin, G., Wang, Y., Wen, X., Li, W., Han, Z., Guo, H., and Chai, J., Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth, Cell Res., 2016, vol. 26, pp. 674–685.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A., and Matsubayashi, Y., Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis, Science, 2010, vol. 329, pp. 1065–1067.

    Article  CAS  PubMed  Google Scholar 

  15. Hirakawa, Y., Torii, K.U., and Uchida, N., Mechanisms and strategies shaping plant peptide hormones, Plant Cell Physiol., 2017, vol. 58, pp. 1313–1318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ma, X., Xu, G., He, P., and Shan, L., SERKing coreceptors for receptors, Trends Plant Sci., 2016, vol. 21, pp. 1017–1033.

    Article  CAS  PubMed  Google Scholar 

  17. Yamaguchi, Y.L., Ishida, T., and Sawa, S., CLE peptides and their signaling pathways in plant development, J. Exp. Bot., 2016, vol. 67, pp. 4813–4826.

    Article  CAS  PubMed  Google Scholar 

  18. Kucukoglu, M. and Nilsson, O., CLE peptide signaling in plants—the power of moving around, Physiol. Plant., 2015, vol. 155, pp. 74–87.

    Article  CAS  PubMed  Google Scholar 

  19. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F., Jürgens, G., and Laux, T., The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes, Cell, 2000, vol. 100, pp. 635–644.

    Article  CAS  PubMed  Google Scholar 

  20. Stahl, Y., Wink, R.H., Ingram, G.C., and Simon, R., A signaling module controlling the stem cell niche in Arabidopsis root meristems, Curr. Biol., 2009, vol. 19, pp. 909–914.

    Article  CAS  PubMed  Google Scholar 

  21. Pi, L., Aichinger, E., van der Graaff, E., Llavata-Peris, C.I., Weijers, D., Hennig, L., Groot, E., and Laux, T., Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression, Dev. Cell, 2015, vol. 33, pp. 576–588.

    Article  CAS  PubMed  Google Scholar 

  22. Kondo, Y. and Fukuda, H., The TDIF signaling network, Curr. Opin. Plant Biol., 2015, vol. 28, pp. 106–110.

    Article  CAS  PubMed  Google Scholar 

  23. Kondo, Y., Hirakawa, Y., Kieber, J.J., and Fukuda, H., CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling, Plant Cell Physiol., 2011, vol. 52, pp. 37–48.

    Article  CAS  PubMed  Google Scholar 

  24. Fiers, M., Hause, G., Boutilier, K., Casamitjana-Martinez, E., Weijers, D., Offringa, R., van der Geest, L., van Lookeren Campagne, M., and Liu, C.M., M-is‑expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem, Gene, 2004, vol. 327, pp. 37–49.

    Article  CAS  PubMed  Google Scholar 

  25. Gancheva, M.S., Dodueva, I.E., Lebedeva, M.A., Tvorogova, V.E., Tkachenko, A.A., and Lutova, L.A., Identification, expression, and functional analysis of CLE genes in radish (Raphanus sativus L.) storage root, BMC Plant Biol., 2016, vol. 16, suppl. 1: 7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shinohara, H., Moriyama, Y., Ohyama, K., and Matsubayashi, Y., Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKS, Plant J., 2012, vol. 70, pp. 845–854.

    Article  CAS  PubMed  Google Scholar 

  27. Osipova, M.A., Mortier, V., Demchenko, K.N., Tsyganov, V.E., Tikhonovich, I.A., Lutova, L.A., Dolgikh, E.A., and Goormachtig, S., WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation, Plant Physiol., 2012, vol. 158, pp. 1329–1341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Araya, T., Miyamoto, M., Wibowo, J., Suzuki, A., Kojima, S., Tsuchiya, Y.N., Sawa, S., Fukuda, H., von Wiren, N., and Takahashi, H., CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner, Proc. Natl. Acad. Sci. USA, 2014, vol. 111, pp. 2029–2034.

    Article  CAS  PubMed  Google Scholar 

  29. Samorodova, A.P., Tvorogova, V.E., Tkachenko, A.A., Potsenkovskaya, E.A., Lebedeva M.A., Tikhono-vich, I.A., and Lutova, L., Agrobacterial tumors interfere with nodulation and demonstrate the expression of nodulation-induced CLE genes in pea, J. Plant Physiol., 2017, vol. 221, pp. 94–100.

    Article  CAS  PubMed  Google Scholar 

  30. Wang, X., Mitchum, M.G., Gao, B., Li, C., Diab, H., Baum, T.J., Hussey, R.S., and Davis, E.L., A parasitism gene from a plant–parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana, Mol. Plant Pathol., 2005, vol. 6, pp. 187–191.

    Article  PubMed  Google Scholar 

  31. Replogle, A., Wang, J., Paolillo, V., Smeda, J., Kinoshita, A., Durbak, A., Tax, F.E., Wang, X., Sawa, S., and Mitchum, M.G., Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis, Mol. Plant–Microbe Interact., 2013, vol. 26, pp. 87–96.

    Article  CAS  PubMed  Google Scholar 

  32. Meng, L., Buchanan, B.B., Feldman, L.J., and Luan, S., CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 1760–1765.

    Article  PubMed  Google Scholar 

  33. Whitford, R., Fernandez, A., Tejos, R., Perez, A.C., Kleine-Vehn, J., Vanneste, S., Drozdzecki, A., Leitner, J., Abas, L., Aerts, M., Hoogewijs, K., Baster, P., de Groodt, R., Lin, Y.C., Storme, V., et al., GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses, Dev. Cell, 2012, vol. 22, pp. 678–685.

    Article  CAS  PubMed  Google Scholar 

  34. Shinohara, H., Mori, A., Yasue, N., Sumida, K., and Matsubayashi, Y., Identification of three LRR-RKS involved in perception of root meristem growth factor in Arabidopsis, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, pp. 3897–3902.

    Article  CAS  PubMed  Google Scholar 

  35. Yang, H., Matsubayashi, Y., Nakamura, K., and Sakagami, Y., Oryza sativa PSK gene encodes a precursor of phytosulfokine-α, a sulfated peptide growth factor found in plants, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 13560–13565.

    Article  CAS  PubMed  Google Scholar 

  36. Matsubayashi, Y., Morita, A., Matsunaga, E., Furuya, A., Hanai, N., and Sakagami, Y., Physiological relationships between auxin, cytokinin, and a peptide growth factor, phytosulfokine-α, in stimulation of asparagus cell proliferation, Planta, 1999, vol. 207, pp. 559–565.

    Article  CAS  Google Scholar 

  37. Yu, L., Liu, Y., Liu, Y., Li, Q., Tang, G., and Luo, L., Overexpression of phytosulfokine-α induces male sterility and cell growth by regulating cell wall development in Arabidopsis, Plant Cell Rep., 2016, vol. 35, pp. 2503–2512.

    Article  CAS  PubMed  Google Scholar 

  38. Matsubayashi, Y., Ogawa, M., Kihara, H., Niwa, M., and Sakagami, Y., Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth, Plant Physiol., 2006, vol. 142, pp. 45–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Srivastava, R., Liu, J.X., and Howell, S.H., Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis, Plant J., 2008, vol. 56, pp. 219–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sauter, M., Phytosulfokine peptide signalling, J. Exp. Bot., 2015, vol. 66, pp. 5161–5169.

    Article  CAS  PubMed  Google Scholar 

  41. Wang, J., Li, H., Han, Z., Zhang, H., Wang, T., Lin, G., Chang, J., Yang, W., and Chai, J., Allosteric receptor activation by the plant peptide hormone phytosulfokine, Nature, 2015, vol. 525, pp. 265–268.

    Article  CAS  PubMed  Google Scholar 

  42. Oehlenschlæger, C.B., Gersby, L.B.A., Ahsan, N., Pedersen, J.T., Kristensen, A., Solakova, T.V., Thelen, J.J., and Fuglsang, A.T., Activation of the LRR receptor-like kinase PSY1R requires transphosphorylation of residues in the activation loop, Front. Plant Sci., 2017, vol. 8: 2005.

  43. Mosher, S. and Kemmerling, B., PSKR1 and PSY1R-mediated regulation of plant defense responses, Plant Signal. Behav., 2013, vol. 8: e24119. https://doi.org/10.4161/psb.24119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Roberts, I., Smith, S., de Rybel, B., van den Broeke, J., Smet, W., de Cokere, S., Mispelaere, M., de Smet, I., and Beeckman, T., The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development, J. Exp. Bot., 2013, vol.  64, pp. 5371–5381.

    Article  CAS  PubMed  Google Scholar 

  45. Tabata, R., Sumida, K., Yoshii, T., Ohyama, K., Shinohara, H., and Matsubayashi, Y., Perception of root-derived peptides by shoot LRR-RKS mediates systemic N-demand signaling, Science, 2014, vol. 346, pp. 343–346.

    Article  CAS  PubMed  Google Scholar 

  46. Ohkubo, Y., Tanaka, M., Tabata, R., Ogawa-Ohnishi, M., and Matsubayashi, Y., Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition, Nat. Plants, 2017, vol. 3: 17029.

    Article  CAS  PubMed  Google Scholar 

  47. Imin, N., Mohd-Radzman, N.A., Ogilvie, H.A., and Djordjevic, M.A., The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula, J. Exp. Bot., 2013, vol. 64, pp. 5395–5409.

    Article  CAS  PubMed  Google Scholar 

  48. Huault, E., Laffont, C., Wen, J., Mysore, K.S., Ratet, P., Duc, G., and Frugier, F., Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase, PLoS Genet., 2014, vol. 10: e1004891.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Bobay, B.G., DiGennaro, P., Scholl, E., Imin, N., Djordjevic, M.A., and Bird, D.McK., Solution NMR studies of the plant peptide hormone CEP inform function, FEBS Lett., 2013, vol. 587, pp. 3979–3985.

    Article  CAS  PubMed  Google Scholar 

  50. Vie, A.K., Najafi, J., Liu, B., Winge, P., Butenko, M.A., Hornslien, K.S., Kumpf, R., Aalen, R.B., Bones, A.M., and Brembu, T., The IDA/IDA-LIKE and PIP/PIP-LIKE gene families in Arabidopsis: phylogenetic relationship, expression patterns, and transcriptional effect of the PIPL3 peptide, J. Exp. Bot., 2015, vol. 66, pp. 5351–5365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Stenvik, G.-E., Tandstad, N.M., Guo, Y., Shi, C.L., Kristiansen, W., Holmgren, A., Clark, S.E., Aalen, R.B., and Butenko, M.A., The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2, Plant Cell, 2008, vol. 20, pp. 1805–1817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cho, S.K., Larue, C.T., Chevalier, D., Wang, H., Jinn, T.L., Zhang, S., and Walker, J.C., Regulation of floral organ abscission in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 15629–15634.

    Article  PubMed  Google Scholar 

  53. Butenko, M.A., Shi, C.L., and Aalen, R.B., KNAT1, KNAT2 and KNAT6 act downstream in the ID-A‑HAE/HSL2 signaling pathway to regulate floral organ abscission, Plant Signal. Behav., 2012, vol. 7, pp. 135–138.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Kumpf, R.P., Shi, C.L., Larrieu, A., Stø, I.M., Butenko, M.A., Péret, B., Riiser, E.S., Bennett, M.J., and Aalen, R.B., Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence, Proc. Natl. Acad. Sci. USA, 2013, vol. 110, pp. 5235–5240.

    Article  PubMed  Google Scholar 

  55. Wang, X., Hou, S., Wu, Q., Lin, M., Acharya, B.R., Wu, D., and Zhang, W., IDL6-HAE/HSL2 impacts pectin degradation and resistance to Pseudomonas syringae pv tomato DC3000 in Arabidopsis leaves, Plant J., 2017, vol. 89, pp. 250–263.

    Article  CAS  PubMed  Google Scholar 

  56. Hou, S., Wang, X., Chen, D., Yang, X., Wang, M., Turrà, D., di Pietro, A., and Zhang, W., The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7, PLoS Pathog., 2014, vol. 10, no. 9. https://www. ncbi.nlm.nih.gov/pmc/articles/PMC4154866/, Accessed November 17, 2017.

  57. Doblas, V.G., Smakowska-Luzan, E., Fujita, S., Alassimone, J., Barberon, M., Madalinski, M., Belkhadir, Y., and Geldner, N., Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor, Science, 2017, vol. 355, pp. 280–284.

    Article  CAS  PubMed  Google Scholar 

  58. Nakayama, T., Shinohara, H., Tanaka, M., Baba, K., Ogawa-Ohnishi, M., and Matsubayashi, Y., A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots, Science, 2017, vol. 355, pp. 284–286.

    Article  CAS  PubMed  Google Scholar 

  59. Pearce, G., Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors, Curr. Protein Pept. Sci., 2011, vol. 12, pp. 399–408.

    Article  CAS  PubMed  Google Scholar 

  60. Higashiyama, T., Peptide signaling in pollen–pistil interactions, Plant Cell Physiol., 2010, vol. 51, pp. 177–189.

    Article  CAS  PubMed  Google Scholar 

  61. Qu, L.J., Li, L., Lan, Z., and Dresselhaus, T., Peptide signalling during the pollen tube journey and double fertilization, J. Exp. Bot., 2015, vol. 66, pp. 5139–5150.

    Article  CAS  PubMed  Google Scholar 

  62. Stotz, H.U., Thomson, J.G., and Wang, Y., Plant defensins: defense, development and application, Plant Signal. Behav., 2009, vol. 4, pp. 1010–1012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Olsen, A.N., Mundy, J., and Skriver, K., Peptomics, identification of novel cationic Arabidopsis peptides with conserved sequence motifs, In Silico Biol., 2002, vol. 2, pp. 441–451.

    CAS  PubMed  Google Scholar 

  64. Dressano, K., Ceciliato, P.H.O., Silva, A.L., Guerrero-Abad, J.C., Bergonci, T., Ortiz-Morea, F.A., Bürger, M., Silva-Filho, M.C., and Moura, D.S., BAK1 is involved in AtRALF1-induced inhibition of root cell expansion, PLoS Genet., 2017, vol. 13: e1007053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Murphy, E. and de Smet, I., Understanding the RALF family: a tale of many species, Trends Plant Sci., 2014, vol. 19, pp. 664–671.

    Article  CAS  PubMed  Google Scholar 

  66. Murphy E., Vu L.D., van den Broeck L., Lin Z., Ramakrishna P., van de Cotte B., Gaudinier A., Goh T., Slane D., Beeckman T., Inzé D., Brady S.M., Fukaki H., and de Smet, I. RALFL34 regulates formative cell divisions in Arabidopsis pericycle during lateral root initiation, J. Exp. Bot., 2016, vol. 67, pp. 4863–4875.

  67. Thynne, E., Saur, I.M.L., Simbaqueba, J., Ogilvie, H.A., Gonzalez-Cendales, Y., Mead, O., Taranto, A., Catanzariti, A.-M., McDonald, M.C., Schwessinger, B., Jones, D.A., Rathjen, J.P., and Solomon, P.S., Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides, Mol. Plant Pathol., 2017, vol. 18, pp. 811–824.

    Article  CAS  PubMed  Google Scholar 

  68. Sugano, S.S., Shimada, T., Imai, Y., Okawa, K., Tamai, A., Mori, M., and Hara-Nishimura, I., Stomagen positively regulates stomatal density in Arabidopsis, Nature, 2010, vol. 463, pp. 241–244.

    Article  CAS  PubMed  Google Scholar 

  69. Shimada, T., Sugano, S.S., and Hara-Nishimura, I., Positive and negative peptide signals control stomatal density, Cell. Mol. Life Sci., 2011, vol. 68, pp. 2081–2088.

    Article  CAS  PubMed  Google Scholar 

  70. Murphy, E., Smith, S., and de Smet, I., Small signaling peptides in Arabidopsis development: how cells communicate over a short distance, Plant Cell, 2012, vol. 24, pp. 3198–3217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kondo, T., Kajita, R., Miyazaki, A., Hokoyama, M., Nakamura-Miura, T., Mizuno, S., Masuda, Y., Irie, K., Tanaka, Y., Takada, S., Kakimoto, T., and Sakagami, Y., Stomatal density is controlled by a mesophyll-derived signaling molecule, Plant Cell Physiol., 2010, vol. 51, pp. 1–8.

    Article  CAS  PubMed  Google Scholar 

  72. Lin, G., Zhang, L., Han, Z., Yang, X., Liu, W., Li, E., Chang, J., Qi, Y., Shpak, E.D., and Chai, J., A receptor-like protein acts as a specificity switch for the regulation of stomatal development, Genes Dev., 2017, vol. 31, pp. 927–938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Jewaria, P.K., Hara, T., Tanaka, H., Kondo, T., Betsuyaku, S., Sawa, S., Sakagami, Y., Aimoto, S., and Kakimoto, T., Differential effects of the peptides Stomagen, EPF1 and EPF2 on activation of MAP kinase MPK6 and the SPCH protein level, Plant Cell Physiol., 2013, vol. 54, pp. 1253–1262.

    Article  CAS  PubMed  Google Scholar 

  74. Yang, S.L., Jiang, L., Puah, C.S., Xie, L.F., Zhang, X.Q., Chen, L.Q., Yang, W.C., and Ye, D., Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with excess microsporocytes1/extra sporogenous cells, Plant Physiol., 2005, vol. 139, pp. 186–191.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Huang, J., Zhang, T., Linstroth, L., Tillman, Z., Otegui, M.S., Owen, H.A., and Zhao, D., Control of anther cell differentiation by the small protein ligand TPD1 and its receptor EMS1 in Arabidopsis, PLoS Genet., 2016, vol. 12: e1006147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Li, Z., Wang, Y., Huang, J., Ahsan, N., Biener, G., Paprocki, J., Thelen, J.J., Raicu, V., and Zhao, D., Two SERK receptor-like kinases interact with EMS1 to control anther cell fate determination, Plant Physiol., 2017, vol. 173, pp. 326–337.

    Article  CAS  PubMed  Google Scholar 

  77. Wheeler, M.J., de Graaf, B.H.J., Hadjiosif, N., Perry, R.M., Poulter, N.S., Osman, K., Vatovec, S., Harper, A., Franklin, F.C.H., and Franklin-Tong, V.E., Identification of the pollen self-incompatibility determinant in Papaver rhoeas, Nature, 2009, vol. 459, pp. 992–995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Lin, Z., Eaves, D.J., Sanchez-Moran, E., Fran-klin, F.C.H., and Franklin-Tong, V.E., The Papaver rhoeas S determinants confer self-incompatibility to Arabidopsis thaliana in planta, Science, 2015, vol. 350, pp. 684–687.

    Article  CAS  PubMed  Google Scholar 

  79. Tang, W., Kelley, D., Ezcurra, I., Cotter, R., and McCormick, S., LeSTIG1, an extracellular binding partner for the pollen receptor kinases LEPRK1 and LEPRK2, promotes pollen tube growth in vitro, Plant J., 2004, vol. 39, pp. 343–353.

    Article  CAS  PubMed  Google Scholar 

  80. Huang, W.J., Liu, H.K., McCormick, S., and Tang, W.H., Tomato pistil factor STIG1 promotes in vivo pollen tube growth by binding to phosphatidylinositol 3-phosphate and the extracellular domain of the pollen receptor kinase LePRK2, Plant Cell, 2014, vol. 26, pp. 2505–2523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Márton, M.L., Cordts, S., Broadhvest, J., and Dresselhaus, T., Micropylar pollen tube guidance by egg apparatus 1 of maize, Science, 2005, vol. 307, pp. 573–576.

  82. Uebler, S., Márton, M.L., and Dresselhaus, T., Classification of EA1-box proteins and new insights into their role during reproduction in grasses, Plant Reprod., 2015, vol. 28, pp. 183–197.

    Article  CAS  PubMed  Google Scholar 

  83. Okuda, S., Tsutsui, H., Shiina, K., Sprunck, S., Takeuchi, H., Yui, R., Kasahara, R.D., Hamamura, Y., Mizukami, A., Susaki, D., Kawano, N., Sakakibara, T., Namiki, S., Itoh, K., Otsuka, K., et al., Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cell, Nature, 2009, vol. 458, pp. 357–361.

    Article  CAS  PubMed  Google Scholar 

  84. Takeuchi, H. and Higashiyama, T., Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis, Nature, 2016, vol. 531, pp. 245–248.

    Article  CAS  PubMed  Google Scholar 

  85. Chae, K. and Lord, E.M., Pollen tube growth and guidance: roles of small, secreted proteins, Ann. Bot., 2011, vol. 108, pp. 627–636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Tousheh, M., Miroliaei, M., Asghar Rastegari, A., Ghaedi, K., Esmaeili, A., and Matkowski, A., Computational evaluation on the binding affinity of non-specific lipid-transfer protein-2 with fatty acids, Comput. Biol. Med., 2013, vol. 43, pp. 1732–1738.

    Article  CAS  PubMed  Google Scholar 

  87. Sprunck, S., Rademacher, S., Vogler, F., Gheyselinck, J., Grossniklaus, U., and Dresselhaus, T., Egg cell-secreted EC1 triggers sperm cell activation during double fertilization, Science, 2012, vol. 338, pp. 1093–1097.

    Article  CAS  PubMed  Google Scholar 

  88. Mori, T. and Igawa, T., Gamete attachment process revealed in flowering plant fertilization, Plant Signal. Behav., 2014, vol. 9: e977715.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Costa, L.M., Marshall, E., Tesfaye, M., Silverstein, K.A.T., Mori, M., Umetsu, Y., Otterbach, S.L., Papareddy, R., Dickinson, H.G., Boutiller, K., Vandenbosch, K.A., Ohki, S., and Gutierrez-Marcos, J.F., Central cell-derived peptides regulate early embryo patterning in flowering plants, Science, 2014, vol. 344, pp. 168–172.

    Article  CAS  PubMed  Google Scholar 

  90. Musielak, T.J. and Bayer, M., YODA signalling in the early Arabidopsis embryo, Biochem. Soc. Trans., 2014, vol. 42, pp. 408–412.

    Article  CAS  PubMed  Google Scholar 

  91. Corrado, G., Sasso, R., Pasquariello, M., Iodice, L., Carretta, A., Cascone, P., Ariati, L., Digilio, M.C., Guerrieri, E., and Rao, R., Systemin regulates both systemic and volatile signaling in tomato plants, J. Chem. Ecol., 2007, vol. 33, pp. 669–681.

    Article  CAS  PubMed  Google Scholar 

  92. Li, C., Liu, G., Xu, C., Lee, G.I., Bauer, P., Ling, H.Q., Ganal, M.W., and Howe, G.A., The tomato Suppressor of prosystemin-mediated responses2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression, Plant Cell, 2003, vol. 15, pp. 1646–1661.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Yamaguchi, Y., Huffaker, A., Bryan, A.C., Tax, F.E., and Ryan, C.A., PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis, Plant Cell, 2010, vol. 22, pp. 508–522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Wang, Y., Wang, L., Zou, Y., Chen, L., Cai, Z., Zhang, S., Zhao, F., Tian, Y., Jiang, Q., Ferguson, B.J., Gresshoff, P.M., and Li, X., Soybean miR172c targets the repressive AP2 transcription factor NNC1 to activate ENOD40 expression and regulate nodule initiation, Plant Cell, 2014, vol. 26, pp. 4782–4801.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Batut, J., Mergaert, P., and Masson-Boivin, C., Peptide signalling in the rhizobium–legume symbiosis, Curr. Opin. Microbiol., 2011, vol. 14, pp. 181–187.

    Article  CAS  PubMed  Google Scholar 

  96. Wen, J., Lease, K.A., and Walker, J.C., DVL, a novel class of small polypeptides: overexpression alters Ar-abidopsis development, Plant J., 2004, vol. 37, pp. 668–677.

    Article  CAS  PubMed  Google Scholar 

  97. Ikeuchi, M., Yamaguchi, T., Kazama, T., Ito, T., Horiguchi, G., and Tsukaya, H., ROTUNDIFOLIA4 regulates cell proliferation along the body axis in Ar-abidopsis shoot, Plant Cell Physiol., 2011, vol. 52, pp. 59–69.

    Article  CAS  PubMed  Google Scholar 

  98. Valdivia, E.R., Chevalier, D., Sampedro, J., Taylor, I., Niederhuth, C.E., and Walker, J.C., DVL genes play a role in the coordination of socket cell recruitment and differentiation, J. Exp. Bot., 2012, vol. 63, pp. 1405–1412.

    Article  CAS  PubMed  Google Scholar 

  99. Liu, J., Mehdi, S., Topping, J., Friml, J., and Lindsey, K., Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development, Front. Plant Sci., 2013, vol. 4: 75.

    PubMed  PubMed Central  Google Scholar 

  100. Chilley, P.M., Casson, S.A., Tarkowski, P., Hawkins, N., Wang, K.L.-C., Hussey, P.J., Beale, M., Ecker, J.R., Sandberg, G.K., and Lindsey, K., The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling, Plant Cell, 2006, vol. 18, pp. 3058–3072.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

The research was supported by grants from the Russian Science Foundation (project no. 16-16-1001), and the Russian Foundation for Basic Research (project nos. 18-04-01017, 15-29-02737, and 18-34-00020).

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  1. St. Petersburg State University, Department of Genetics Biotechnology, 199034, St. Petersburg, Russia

    M. S. Gancheva, Yu. V. Malovichko, L. O. Poliushkevich, I. E. Dodueva & L. A. Lutova

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  1. M. S. Gancheva
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  2. Yu. V. Malovichko
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  3. L. O. Poliushkevich
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  4. I. E. Dodueva
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  5. L. A. Lutova
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Correspondence to M. S. Gancheva.

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Translated by M. Shulskaya

Supplementary materials are available for this article at 10.1134/S1021443719010072.

Abbreviations: AA—amino acid; CRP—cysteine-rich peptides; LRR-RLK—Leucin Reach Repeats containing Receptor-Like Kinase; NSSP—nonsecreted signal peptides; PTMP—posttranslationally modified peptides; TF—transcription factor.

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Gancheva, M.S., Malovichko, Y.V., Poliushkevich, L.O. et al. Plant Peptide Hormones. Russ J Plant Physiol 66, 171–189 (2019). https://doi.org/10.1134/S1021443719010072

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  • DOI: https://doi.org/10.1134/S1021443719010072

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