Skip to main content
Log in

Production mechanisms, structural features and post-translational modifications of plant peptides

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Accumulated evidence suggests that peptides play diverse roles in various aspects of plant growth and development. Therefore, many research groups have developed and utilized new methods for the identification of peptides in different organisms. Nevertheless, the number and diversity of identified peptides remain lower than expected. In addition, the number of identified peptides is underestimated because of their low endogenous concentrations and, consequently, technical difficulties with their isolation. Additionally, while some types of peptides undergo functional maturation via proteolytic processing or post-translational modifications, which are important for their biological activity, most of the enzymes involved in the maturation of peptides have not yet been identified. Together, these factors indicate that the investigation of peptides is in its beginning stages in plants, as in other organisms. This review summarizes the biosynthesis mechanisms, identification tools, post-translational modifications, and biological functions of plant peptides, and the importance of post-translational modifications in peptide activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Albert M (2013) Peptides as triggers of plant defence. J Exp Bot 64:5269–5279

    CAS  PubMed  Google Scholar 

  • Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104:18333–18338

    CAS  PubMed  Google Scholar 

  • Andrews SJ, Rothnagel JA (2014) Emerging evidence for functional peptides encoded by short open reading frames. Nat Rev Genet 15:193–204

    CAS  PubMed  Google Scholar 

  • Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H, Aalen RB, Felix G (2014) Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26:1838–1847

    CAS  PubMed  PubMed Central  Google Scholar 

  • Corcilius L, Hastwell AH, Zhang M, Williams J, Mackay JP, Gresshoff PM, Ferguson BJ, Payne RJ (2017) Arabinosylation modulates the growth-regulating activity of the peptide hormone CLE40a from Soybean. Cell Chem Biol 24:1347–1355

    CAS  PubMed  Google Scholar 

  • Czyzewicz N, Yue K, Beeckman T, De Smet I (2013) Message in a bottle: small signalling peptide outputs during growth and development. J Exp Bot 64:5281–5296

    CAS  PubMed  Google Scholar 

  • Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, Belkhadir Y, Geldner N (2017) Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355:280–284

    CAS  PubMed  Google Scholar 

  • Egelund J, Obel N, Ulvskov P, Geshi N, Pauly M, Bacic A, Petersen BL (2007) Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants, rra1 and rra2, which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue. Plant Mol Biol 64:439–451

    CAS  PubMed  Google Scholar 

  • El Oirdi M, Abd El Rahman T, Rigano L, El Hadrami A, Rodriguez MC, Daayf F, Vojnov A, Bouarab K (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell 23:2405–2421

    PubMed  PubMed Central  Google Scholar 

  • Fan SK, Fang XZ, Guan MY, Ye YQ, Lin XY, Du ST, Jin CW (2014) Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5:721

    PubMed  PubMed Central  Google Scholar 

  • Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–1914

    CAS  PubMed  Google Scholar 

  • Fuglsang AT, Kristensen A, Cuin A, Schulze WX, Persson J, Thuesen KH, Ytting CK, Oehlenschlæger CB, Mahmood K, Sondergaard TE, Shabala S, Palmgren MG (2014) Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. Plant J 80:951–964

    CAS  PubMed  Google Scholar 

  • Gille S, Hansel U, Ziemann M, Pauly M (2009) Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc Natl Acad Sci USA 106:14699–14704

    CAS  PubMed  Google Scholar 

  • Grillet L, Lan P, Li W, Mokkapati G, Schmidt W (2018) IRON MAN is a ubiquitous family of peptides that control iron transport in plants. Nat Plants 4:953–963

    CAS  PubMed  Google Scholar 

  • Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ (2006) Protein disulfide isomerase: the structure of oxidative folding. Trends Biochem Sci 31:455–464

    CAS  PubMed  Google Scholar 

  • Guillén G, Díaz-Camino C, Loyola-Torres CA, Aparicio-Fabre R, Hernández-López A, Díaz-Sánchez M, Sanchez F (2013) Detailed analysis of putative genes encoding small proteins in legume genomes. Front Plant Sci 4:208

    PubMed  PubMed Central  Google Scholar 

  • Hahn M, Stachelhaus T (2004) Selective interaction between nonribosomal peptide synthetases is facilitated by short communication-mediating domains. Proc Natl Acad Sci USA 101(44):15585–15590

    CAS  PubMed  Google Scholar 

  • Hellens RP, Brown CM, Chisnall MAW, Waterhouse PM, Macknight RC (2016) The emerging world of small ORFs. Trends Plant Sci 21:317–328

    CAS  PubMed  Google Scholar 

  • Hirayama T, Lei GJ, Yamaji N, Nakagawa N, Ma JF (2018) The putative peptide gene FEP1 regulates iron deficiency response in Arabidopsis. Plant Cell Physiol 59:1739–1752

    CAS  PubMed  Google Scholar 

  • Huffaker A, Pearce G, Ryan CA (2006) An endogenous peptide signal in arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103:10098–10103

    CAS  PubMed  Google Scholar 

  • Igarashi D, Tsuda K, Katagiri F (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71:194–204

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kageyama Y, Kondo T, Hashimoto Y (2011) Coding vs non-coding: Translatability of short ORFs found in putative non-coding transcripts. Biochimie 93:1981–1986

    CAS  PubMed  Google Scholar 

  • Kastin AJ (2013) Handbook of Biologically Active Peptides (2nd ed.). Elsevier. ISBN 978–0–12–385095–9.

  • Kaufmann C, Sauter M (2019) Sulfated plant peptide hormones. J Exp Bot 70(16):4267–4277

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kehoe JW, Bertozzi CR (2000) Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem Biol 7:R57–R61

    CAS  PubMed  Google Scholar 

  • Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106:15067–15072

    CAS  PubMed  Google Scholar 

  • Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848

    CAS  PubMed  Google Scholar 

  • Kutschmar A, Rzewuski G, Stührwohldt N, Beemster GTS, Inze D, Sauter M (2009) PSK-alpha promotes root growth in Arabidopsis. New Phytol 181:820–831

    CAS  PubMed  Google Scholar 

  • Kurihara Y, Makita Y, Shimohira H, Fujita T, Iwasaki S, Matsui M (2020) Translational landscape of protein-coding and non-protein-coding RNAs upon light exposure in Arabidopsis. Plant Cell Physiol 61(3):536–545

    PubMed  Google Scholar 

  • Lease KA, Walker JC (2006) The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol 142:831–838

    CAS  PubMed  PubMed Central  Google Scholar 

  • Loivamaki M, Stührwohldt N, Deeken R, Steffens B, Roitsch T, Hedrich R, Sauter M (2010) A role for PSK signaling in wounding and microbial interactions in arabidopsis. Physiol Plant 139:348–357

    PubMed  Google Scholar 

  • Matsubayashi Y (2011) Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol 52(1):5–13

    CAS  PubMed  Google Scholar 

  • Matsubayashi Y (2012) Recent progress in research on small post-translationally modified peptide signals in plants. Genes Cells 17:1–10

    CAS  PubMed  Google Scholar 

  • Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol 65:385–413

    PubMed  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93(15):7623–7627

    CAS  PubMed  Google Scholar 

  • Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y (2010) Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–1067

    CAS  PubMed  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52(1):711–760

    CAS  PubMed  Google Scholar 

  • Mohd-Radzman NA, Binos S, Truong TT, Imin N, Mariani M, Djordjevic MA (2015) Novel MtCEP1 peptides produced in vivo differentially regulate root development in Medicago truncatula. J Exp Bot 66:5289–5300

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mosher S, Kemmerling B (2013) PSKR1 and PSY1R-mediated regulation of plant defense responses. Plant Signal Behav 8:e24119

    PubMed  PubMed Central  Google Scholar 

  • Myllyharju J (2003) Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 22:15–24

    CAS  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    CAS  PubMed  Google Scholar 

  • Niarchou A, Alexandridou A, Athanasiadis E, Spyrou G (2013) C-PAmP: large scale analysis and database construction containing high scoring computationally predicted antimicrobial peptides for all the available plant species. PLoS ONE 8:e79728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y (2013) Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat Chem Biol 9:726–730

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J 55:152–160

    CAS  PubMed  Google Scholar 

  • Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Okamoto S, Tabata R, Matsubayashi Y (2016) Long-distance peptide signaling essential for nutrient homeostasis in plants. Curr Opin Plant Biol 34:35–40

    CAS  PubMed  Google Scholar 

  • Patel N, Mohd-Radzman NA, Corcilius L, Crossett B, Connolly A, Cordwell SJ, Ivanovici A, Taylor K, Williams J, Binos S, Mariani M, Payne RJ, Djordjevic MA (2018) Diverse peptide hormones affecting root growth identified in the Medicago truncatula secreted peptidome. Mol Cell Proteom 17:160–174

    CAS  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA (2001a) Production of mutlitple plant hormones from a single polyprotein precursor. Nature 411:817–820

    CAS  PubMed  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA (2001b) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98:12843–12847

    CAS  PubMed  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–897

    CAS  PubMed  Google Scholar 

  • Pueyo JI, Magny EG, Couso JP (2016) New peptides under the s(ORF)ace of the genome. Trends Biochem Sci 41:665–678

    CAS  PubMed  Google Scholar 

  • Rehemtulla A, Kaufman RJ (1992) Protein processing within the secretory pathway. Curr Opin Biotechnol 3:560–565

    CAS  PubMed  Google Scholar 

  • Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA, Butenko MA, Hothorn M (2016) Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. ELife 5:e15075

    PubMed  PubMed Central  Google Scholar 

  • Sawa S, Kinoshita A, Betsuyaku S, Fukuda H (2008) A large family of genes that share homology with CLE domain in Arabidopsis and rice. Plant Signal Behav 3:337–339

    PubMed  PubMed Central  Google Scholar 

  • Shimizu M, Igasaki T, Yamada M, Yuasa K, Hasegawa J, Kato T, Tsukagoshi H, Nakamura K, Fukuda H, Matsuoka K (2005) Experimental determination of proline hydroxylation and hydroxyproline arabinogalactosylation motifs in secretory proteins. Plant J 42:877–889

    CAS  PubMed  Google Scholar 

  • Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y (2012) Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J 70:845–854

    CAS  PubMed  Google Scholar 

  • Silva J, Fernandes R, Romão L (2019) Translational regulation by upstream open reading frames and human diseases. Adv Exp Med Biol 1157:99–116

    CAS  PubMed  Google Scholar 

  • Stührwohldt N, Dahlke RI, Kutschmar A, Peng X, Sun MX, Sauter M (2015) Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiol Plant 153:643–653

    PubMed  Google Scholar 

  • Stührwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M (2011) Phytosulfokine-alpha controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS ONE 6:e21054

    PubMed  PubMed Central  Google Scholar 

  • Stührwohldt N, Hartmann J, Dahlke RI, Oecking C, Sauter M (2014) The PSI family of nuclear proteins is required for growth in Arabidopsis. Plant Mol Biol 86:289–302

    PubMed  Google Scholar 

  • Stührwohldt N, Hohl M, Schardon K, Stintzi A, Schaller A (2018) Post-translational maturation of IDA, a peptide signal controlling floral organ abscission in Arabidopsis. Commun Integr Biol 11(1):e1395119

    Google Scholar 

  • Su M, Ling Y, Yu J, Wu J, Xiao J (2013) Small proteins: untapped area of potential biological importance. Front Genet 4:286

    PubMed  PubMed Central  Google Scholar 

  • Süssmuth RD, Andi Mainz A (2017) Nonribosomal peptide synthesis-principles and prospects. Angew Chem Int Ed 56:3770–3821

    Google Scholar 

  • Takahashi F, Hanada K, Kondo T, Shinozaki T (2019) Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol 51:88–95

    CAS  PubMed  Google Scholar 

  • Tavormina P, de Coninck B, Nikonorova N, de Smet I, Cammue BPA (2015) The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27:2095–2118

    CAS  PubMed  PubMed Central  Google Scholar 

  • Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, Pol-Fachin L, Egelund J, Gille S, Harholt J, Ciancia M, Verli H, Pauly M, Bacic A, Olsen CE, Ulvskov P, Petersen BL, Somerville C, Iusem ND, Estevez JM (2011) O-glycosylated cell wall proteins are essential in root hair growth. Science 332:1401–1403

    CAS  PubMed  Google Scholar 

  • von Arnim AG, Jia Q, Vaughn JN (2014) Regulation of plant translation by upstream open reading frames. Plant Sci 214:1–12

    Google Scholar 

  • Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, Chang J, Yang W, Chai J (2015) Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–268

    CAS  PubMed  Google Scholar 

  • Wang P, Yao S, Kosami KI, Guo T, Li J, Zhang Y, Fukao Y, Kaneko-Kawano T, Zhang H, She YM, Wang P, Xing W, Hanada K, Liu R, Kawano Y (2019) Identification of endogenous small peptides involved in rice immunity through transcriptomics- and proteomics-based screening. Plant Biotechnol J 18(2):415–428

    PubMed  PubMed Central  Google Scholar 

  • Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J, Vanneste S, Drozdzecki A, Leitner J, Abas L, Aerts M, Hoogewijs K, Baster P, de Groodt R, Lin YC, Storme V, van de Peer Y, Beeckman T, Madder A, Devreese B, Luschnig C, Friml J, Hilson P (2012) GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell 22:678–685

    CAS  PubMed  Google Scholar 

  • Xu C, Liberatore KL, MacAlister CA, Huang Z, Chu YH, Jiang K, Brooks C, Ogawa-Ohnishi M, Xiong G, Pauly M, van Eck J, Matsubayashi Y, van der Knaap E, Lippman ZB (2015) A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat Genet 47:784–792

    CAS  PubMed  Google Scholar 

  • Yang X, Tschaplinski TJ, Hurst GB, Jawdy S, Abraham PE, Lankford PK, Adams RM, Shah MB, Hettich RL, Lindquist E, Kalluri UC, Gunter LE, Pennacchio C, Tuskan GA (2011) Discovery and annotation of small proteins using genomics, proteomics, and computational approaches. Genome Res 21:634–641

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Zhang Y, Chen X, Chen Y (2019) Plant Noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell Dev Biol 35:407–431

    CAS  PubMed  Google Scholar 

  • Zhang H, Hu Z, Lei C, Zheng C, Wang J, Shao S, Li X, Xia X, Cai X, Zhou J, Zhou Y, Yu J, Foyer CH, Shi K (2018) A plant phytosulfokine peptide initiates Auxin-dependent immunity through cytosolic Ca2 + signaling in tomato. Plant Cell 30:652–667

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Han Z, Song W, Chai J (2016) Structural insight into recognition of plant peptide hormones by receptors. Mol Plant 9(11):1454–1463

    CAS  PubMed  Google Scholar 

  • Zhou W, Wei L, Xu J, Zhai Q, Jiang H, Chen R, Chen Q, Sun J, Chu J, Zhu L, Liu CM, Li C (2010) Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22:3692–4370

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center no. PJ01327601), Rural Development Administration, Republic of Korea. This work was also supported by a grant from the Next-Generation BioGreen 21 Program (Plant Molecular Breeding Center no. PJ01330802), Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

Authors

Contributions

HSS designed the manuscript. KHL, DHK and HSS wrote the manuscript. KHL, DHK, JTS and HSS evaluated the manuscript.

Corresponding author

Correspondence to Hak Soo Seo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, K.H., Kwon, D.H., Song, J.T. et al. Production mechanisms, structural features and post-translational modifications of plant peptides. J. Plant Biol. 63, 259–265 (2020). https://doi.org/10.1007/s12374-020-09255-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-020-09255-5

Keywords

Navigation