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Protein & Peptide Letters

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ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

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Research Article

Polyproline II Helix as a Recognition Motif of Plant Peptide Hormones and Flagellin Peptide flg22

Author(s): Norio Matsushima*, Hiroki Miyashita, Shinsuke Tamaki and Robert H. Kretsinger

Volume 26, Issue 9, 2019

Page: [684 - 690] Pages: 7

DOI: 10.2174/0929866526666190408125441

Price: $65

Abstract

Background: Plant peptide hormones play a crucial role in plant growth and development. A group of these peptide hormones are signaling peptides with 5 - 23 amino acids. Flagellin peptide (flg22) also elicits an immune response in plants. The functions are expressed through recognition of the peptide hormones and flg22. This recognition relies on membrane localized receptor kinases with extracellular leucine rich repeats (LRR-RKs). The structures of plant peptide hormones - AtPep1, IDA, IDL1, RGFs 1- 3, TDIF/CLE41 - and of flg22 complexed with LRR domains of corresponding LRR-RKs and co-receptors SERKs have been determined. However, their structures are well not analyzed and characterized in detail. The structures of PIP, CEP, CIF, and HypSys are still unknown.

Objective: Our motivation is to clarify structural features of these plant, small peptides and Flg22 in their bound states.

Methods: In this article, we performed secondary structure assignments and HELFIT analyses (calculating helix axis, pitch, radius, residues per turn, and handedness) based on the atomic coordinates from the crystal structures of AtPep1, IDA, IDL1, RGFs 1- 3, TDIF/CLE41 - and of flg22. We also performed sequence analysis of the families of PIP, CEP, CIF, and HypSys in order to predict their secondary structures.

Results: Following AtPep1 with 23 residues adopts two left handed polyproline helices (PPIIs) with six and four residues. IDA, IDL1, RGFs 1 - 2, and TDIF/CLE41 with 12 or 13 residues adopt a four residue PPII; RGF3 adopts two PPIIs with four residues. Flg22 with 22 residues also adopts a six residue PPII. The other peptide hormones – PIP, CEP, CIF, and HypSys – that are rich in proline or hydroxyproline presumably prefer PPII.

Conclusion: The present analysis indicates that PPII helix in the plant small peptide hormones and in flg22 is crucial for recognition of the LRR domains in receptors.

Keywords: Plant small signaling peptides, flg22, left handed polyproline II helix, proline / hydroxyproline rich sequence, leucine rich repeats (LRR-RKs), secondary structures.

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[1]
Zhang, H.; Han, Z.; Song, W.; Chai, J. Structural insight into recognition of plant peptide hormones by receptors. Mol. Plant, 2016, 9(11), 1454-1463.
[http://dx.doi.org/10.1016/j.molp.2016.10.002] [PMID: 27743937]
[2]
Hirakawa, Y.; Torii, K.U.; Uchida, N. Mechanisms and strategies shaping plant peptide hormones. Plant Cell Physiol., 2017, 58(8), 1313-1318.
[http://dx.doi.org/10.1093/pcp/pcx069] [PMID: 28961990]
[3]
Matsubayashi, Y. Exploring peptide hormones in plants: identification of four peptide hormone-receptor pairs and two post-translational modification enzymes. Proc. Jpn. Acad., Ser. B, Phys. Biol. Sci., 2018, 94(2), 59-74.
[http://dx.doi.org/10.2183/pjab.94.006] [PMID: 29434080]
[4]
He, Y.; Zhou, J.; Shan, L.; Meng, X. Plant cell surface receptor-mediated signaling - a common theme amid diversity. J. Cell Sci., 2018, 131(2) pii: jcs209353
[http://dx.doi.org/10.1242/jcs.209353] [PMID: 29378836]
[5]
Matsubayashi, Y. Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol., 2011, 52(1), 5-13.
[http://dx.doi.org/10.1093/pcp/pcq169] [PMID: 21071428]
[6]
Sun, Y.; Li, L.; Macho, A.P.; Han, Z.; Hu, Z.; Zipfel, C.; Zhou, J.M.; Chai, J. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science, 2013, 342(6158), 624-628.
[http://dx.doi.org/10.1126/science.1243825] [PMID: 24114786]
[7]
Matsushima, N.; Miyashita, H. Leucine-Rich Repeat (LRR) domains containing intervening motifs in plants. Biomolecules, 2012, 2(2), 288-311.
[http://dx.doi.org/10.3390/biom2020288] [PMID: 24970139]
[8]
Tang, J.; Han, Z.; Sun, Y.; Zhang, H.; Gong, X.; Chai, J. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res., 2015, 25(1), 110-120.
[http://dx.doi.org/10.1038/cr.2014.161] [PMID: 25475059]
[9]
Santiago, J.; Brandt, B.; Wildhagen, M.; Hohmann, U.; Hothorn, L.A.; Butenko, M.A.; Hothorn, M. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife, 2016, 5e15075
[http://dx.doi.org/10.7554/eLife.15075] [PMID: 27058169]
[10]
Song, W.; Liu, L.; Wang, J.; Wu, Z.; Zhang, H.; Tang, J.; Lin, G.; Wang, Y.; Wen, X.; Li, W.; Han, Z.; Guo, H.; Chai, J. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res., 2016, 26(6), 674-685.
[http://dx.doi.org/10.1038/cr.2016.62] [PMID: 27229311]
[11]
Zhang, H.; Lin, X.; Han, Z.; Qu, L.J.; Chai, J. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Res., 2016, 26(5), 543-555.
[http://dx.doi.org/10.1038/cr.2016.45] [PMID: 27055373]
[12]
Morita, J.; Kato, K.; Nakane, T.; Kondo, Y.; Fukuda, H.; Nishimasu, H.; Ishitani, R.; Nureki, O. Crystal structure of the plant receptor-like kinase TDR in complex with the TDIF peptide. Nat. Commun., 2016, 7, 12383.
[http://dx.doi.org/10.1038/ncomms12383] [PMID: 27498761]
[13]
Li, Z.; Chakraborty, S.; Xu, G. Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions. PLoS One, 2017, 12(4)e0175317
[http://dx.doi.org/10.1371/journal.pone.0175317] [PMID: 28384649]
[14]
Enkhbayar, P.; Miyashita, H.; Kretsinger, R.H.; Matsushima, N. Helical parameters and correlations of tandem leucine rich repeats in proteins. J. Proteomics Bioinform., 2014, 7, 139-150.
[http://dx.doi.org/10.4172/jpb.1000314]
[15]
Fraser, R.D.B.; MacRae, T.P. Conformation in fibrous proteins and related synthetic polypeptides; Academic Press: New York, 1973, pp. 1-628.
[16]
Adzhubei, A.A.; Sternberg, M.J.; Makarov, A.A. Polyproline-II helix in proteins: structure and function. J. Mol. Biol., 2013, 425(12), 2100-2132.
[http://dx.doi.org/10.1016/j.jmb.2013.03.018] [PMID: 23507311]
[17]
Narwani, T.J.; Santuz, H.; Shinada, N.; Melarkode Vattekatte, A.; Ghouzam, Y.; Srinivasan, N.; Gelly, J.C.; de Brevern, A.G. Recent advances on polyproline II. Amino Acids, 2017, 49(4), 705-713.
[http://dx.doi.org/10.1007/s00726-017-2385-6] [PMID: 28185014]
[18]
Esipova, N.G.; Tumanyan, V.G. Omnipresence of the polyproline II helix in fibrous and globular proteins. Curr. Opin. Struct. Biol., 2017, 42, 41-49.
[http://dx.doi.org/10.1016/j.sbi.2016.10.012] [PMID: 27815983]
[19]
Mansiaux, Y.; Joseph, A.P.; Gelly, J.C.; de Brevern, A.G. Assignment of PolyProline II conformation and analysis of sequence--structure relationship. PLoS One, 2011, 6(3)e18401
[http://dx.doi.org/10.1371/journal.pone.0018401] [PMID: 21483785]
[20]
Srinivasan, R.; Rose, G.D. A physical basis for protein secondary structure. Proc. Natl. Acad. Sci. USA, 1999, 96(25), 14258-14263.
[http://dx.doi.org/10.1073/pnas.96.25.14258] [PMID: 10588693]
[21]
Cubellis, M.V.; Cailliez, F.; Lovell, S.C. Secondary structure assignment that accurately reflects physical and evolutionary characteristics. BMC Bioinformatics, 2005, 6(Suppl. 4), S8.
[http://dx.doi.org/10.1186/1471-2105-6-S4-S8] [PMID: 16351757]
[22]
King, S.M.; Johnson, W.C. Assigning secondary structure from protein coordinate data. Proteins, 1999, 35(3), 313-320.
[http://dx.doi.org/10.1002/(SICI)1097-0134(19990515)35:3<313:AID-PROT5>3.0.CO;2-1] [PMID: 10328266]
[23]
Kumar, P.; Bansal, M. Identification of local variations within secondary structures of proteins. Acta Crystallogr. D Biol. Crystallogr., 2015, 71(Pt 5), 1077-1086.
[http://dx.doi.org/10.1107/S1399004715003144] [PMID: 25945573]
[24]
Enkhbayar, P.; Damdinsuren, S.; Osaki, M.; Matsushima, N. HELFIT: Helix fitting by a total least squares method. Comput. Biol. Chem., 2008, 32(4), 307-310.
[http://dx.doi.org/10.1016/j.compbiolchem.2008.03.012] [PMID: 18467178]
[25]
Batkhishig, D.; Bilguun, K.; Enkhbayar, P.; Miyashita, H.; Kretsinger, R.H.; Matsushima, N. Super secondary structure consisting of a polyproline II helix and a beta-turn in leucine rich repeats in bacterial type III secretion system effectors. Protein J., 2018, 37(3), 223-236.
[http://dx.doi.org/10.1007/s10930-018-9767-9] [PMID: 29651716]
[26]
Chebrek, R.; Leonard, S.; de Brevern, A.G.; Gelly, J.C. PolyprOnline: polyproline helix II and secondary structure assignment database. Database (Oxford) , 2014, 2014, 2014.
[http://dx.doi.org/10.1093/database/bau102] [PMID: 25380779]
[27]
Enkhbayar, P.; Boldgiv, B.; Matsushima, N. omega-Helices in proteins. Protein J., 2010, 29(4), 242-249.
[http://dx.doi.org/10.1007/s10930-010-9245-5] [PMID: 20496104]
[28]
Enkhbayar, P.; Hikichi, K.; Osaki, M.; Kretsinger, R.H.; Matsushima, N. 3(10)-helices in proteins are parahelices. Proteins, 2006, 64(3), 691-699.
[http://dx.doi.org/10.1002/prot.21026] [PMID: 16783793]
[29]
Finn, R.D.; Attwood, T.K.; Babbitt, P.C.; Bateman, A.; Bork, P.; Bridge, A.J.; Chang, H.Y.; Dosztányi, Z.; El-Gebali, S.; Fraser, M.; Gough, J.; Haft, D.; Holliday, G.L.; Huang, H.; Huang, X.; Letunic, I.; Lopez, R.; Lu, S.; Marchler-Bauer, A.; Mi, H.; Mistry, J.; Natale, D.A.; Necci, M.; Nuka, G.; Orengo, C.A.; Park, Y.; Pesseat, S.; Piovesan, D.; Potter, S.C.; Rawlings, N.D.; Redaschi, N.; Richardson, L.; Rivoire, C.; Sangrador-Vegas, A.; Sigrist, C.; Sillitoe, I.; Smithers, B.; Squizzato, S.; Sutton, G.; Thanki, N.; Thomas, P.D.; Tosatto, S.C.; Wu, C.H.; Xenarios, I.; Yeh, L.S.; Young, S.Y.; Mitchell, A.L. InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res., 2017, 45(D1), D190-D199.
[http://dx.doi.org/10.1093/nar/gkw1107] [PMID: 27899635]
[30]
Ogilvie, H.A.; Imin, N.; Djordjevic, M.A. Diversification of the C-Terminally Encoded Peptide (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genomics, 2014, 15, 870.
[http://dx.doi.org/10.1186/1471-2164-15-870] [PMID: 25287121]
[31]
Pearce, G. Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors. Curr. Protein Pept. Sci., 2011, 12(5), 399-408.
[http://dx.doi.org/10.2174/138920311796391106] [PMID: 21418016]
[32]
Crooks, G.E.; Hon, G.; Chandonia, J.M.; Brenner, S.E. WebLogo: a sequence logo generator. Genome Res., 2004, 14(6), 1188-1190.
[http://dx.doi.org/10.1101/gr.849004] [PMID: 15173120]
[33]
Lori, M.; van Verk, M.C.; Hander, T.; Schatowitz, H.; Klauser, D.; Flury, P.; Gehring, C.A.; Boller, T.; Bartels, S. Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: interfamily incompatibility of perception but compatibility of downstream signalling. J. Exp. Bot., 2015, 66(17), 5315-5325.
[http://dx.doi.org/10.1093/jxb/erv236] [PMID: 26002971]
[34]
Butenko, M.A.; Patterson, S.E.; Grini, P.E.; Stenvik, G.E.; Amundsen, S.S.; Mandal, A.; Aalen, R.B. 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.
[http://dx.doi.org/10.1105/tpc.014365] [PMID: 12972671]
[35]
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.
[http://dx.doi.org/10.1126/science.1191132] [PMID: 20798316]
[36]
Sun, J.Q.; Jiang, H.L.; Li, C.Y. Systemin/Jasmonate-mediated systemic defense signaling in tomato. Mol. Plant, 2011, 4(4), 607-615.
[http://dx.doi.org/10.1093/mp/ssr008] [PMID: 21357647]
[37]
Pearce, G.; Siems, W.F.; Bhattacharya, R.; Chen, Y.C.; Ryan, C.A. Three hydroxyproline-rich glycopeptides derived from a single petunia polyprotein precursor activate defensin I, a pathogen defense response gene. J. Biol. Chem., 2007, 282(24), 17777-17784.
[http://dx.doi.org/10.1074/jbc.M701543200] [PMID: 17449475]
[38]
van Holst, G.J.; Varner, J.E. Reinforced polyproline ii conformation in a hydroxyproline-rich cell wall glycoprotein from carrot root. Plant Physiol., 1984, 74(2), 247-251.
[http://dx.doi.org/10.1104/pp.74.2.247] [PMID: 16663405]
[39]
Kay, B.K.; Williamson, M.P.; Sudol, M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J., 2000, 14(2), 231-241.
[http://dx.doi.org/10.1096/fasebj.14.2.231] [PMID: 10657980]
[40]
Williamson, M.P. The structure and function of proline-rich regions in proteins. Biochem. J., 1994, 297(Pt 2), 249-260.
[http://dx.doi.org/10.1042/bj2970249] [PMID: 8297327]

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