Abstract
Key message
We analyzed the evolutionary pattern of cysteine-rich peptides (CRPs) to infer the relationship between CRP copy number and plant ecotype, and the origin of bi-domains CRPs.
Abstract
Plants produce cysteine-rich peptides (CRPs) that have long-lasting broad-spectrum antimicrobial activity to protect themselves from various groups of pathogens. We analyzed 240 plant genomes, ranging from algae to eudicots, and discovered that CRPs are widely distributed in plants. Our comparative genomics results revealed that CRP genes have been amplified through both whole genome and local tandem duplication. The copy number of these genes varied significantly across lineages and was associated with the plant ecotype. This may be due to their resistance to changing pathogenic environments. The conserved and lineage-specific CRP families contribute to diverse antimicrobial activities. Furthermore, we investigated the unique bi-domain CRPs that result from unequal crossover events. Our findings provide a unique evolutionary perspective on CRPs and insights into their antimicrobial and symbiosis characteristics.
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References
Alunni B, Gourion B (2016) Terminal bacteroid differentiation in the legume-rhizobium symbiosis: nodule-specific cysteine-rich peptides and beyond. New Phytol 211:411–417. https://doi.org/10.1111/nph.14025
Arias T, Pires C (2012) A fully resolved chloroplast phylogeny of the brassica crops and wild relatives (Brassicaceae: Brassiceae): novel clades and potential taxonomic implications. Taxon 61:980–988. https://doi.org/10.1002/tax.615005
Berrocal Lobo M, Segura A, Moreno M et al (2002) Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol 128:951–961. https://doi.org/10.1104/pp.010685
Broekaert WF, Terras FRG, Cammue BPA, Osborn RW (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108:1353–1358. https://doi.org/10.1104/pp.108.4.1353
Cammue BPA, De Bolle MFC, Terras FRG et al (1992) Isolation and characterization of a novel class of plant antimicrobial peptides from Mirabilis jalapa L. seeds. J Biol Chem 267:2228–2233. https://doi.org/10.1016/s0021-9258(18)45866-8
Campos ML, De Souza CM, De Oliveira KBS et al (2018) The role of antimicrobial peptides in plant immunity. J Exp Bot 69:4997–5011. https://doi.org/10.1093/jxb/ery294
Cantalapiedra CP, Hern̗andez-Plaza A, Letunic I et al (2021) eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 38:5825–5829. https://doi.org/10.1093/molbev/msab293
Chase MW, Christenhusz MJM, Fay MF et al (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20. https://doi.org/10.1111/boj.12385
Chen C, Chen H, Zhang Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537–552. https://doi.org/10.1038/nri.2016.77
Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511. https://doi.org/10.1146/annurev-arplant-050213-040012
Czernic P, Gully D, Cartieaux F et al (2015) Convergent evolution of endosymbiont differentiation in dalbergioid and inverted repeat-lacking clade legumes mediated by nodule-specific cysteine-rich peptides. Plant Physiol 169:1254–1265. https://doi.org/10.1104/pp.15.00584
Delaux PM, Schornack S (2021) Plant evolution driven by interactions with symbiotic and pathogenic microbes. Science. https://doi.org/10.1126/science.aba6605
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:1–14. https://doi.org/10.1186/s13059-015-0721-2
Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:1–14. https://doi.org/10.1186/s13059-019-1832-y
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:29–37. https://doi.org/10.1093/nar/gkr367
Florack DEA, Stiekema WJ (1994) Thionins: properties, possible biological roles and mechanisms of action. Plant Mol Biol 26:25–37. https://doi.org/10.1007/BF00039517
Haag AF, Kerscher B, Dall’Angelo S et al (2012) Role of cysteine residues and disulfide bonds in the activity of a legume root nodule-specific, cysteine-rich peptide. J Biol Chem 287:10791–10798. https://doi.org/10.1074/jbc.M111.311316
Hammami R, Ben Hamida J, Vergoten G, Fliss I (2009) PhytAMP: a database dedicated to antimicrobial plant peptides. Nucleic Acids Res 37:963–968. https://doi.org/10.1093/nar/gkn655
Islam KT, Velivelli SLS, Berg RH et al (2017) A novel bi-domain plant defensin MtDef5 with potent broad-spectrum antifungal activity binds to multiple phospholipids and forms oligomers. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-16508-w
Johnson LS, Eddy SR, Portugaly E (2010) Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinform 11:1471–2105. https://doi.org/10.1186/1471-2105-11-431
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Knapp S, Chase MW, Clarkson JJ (2004) Nomenclatural changes and a new sectional classification in Nicotiana (Solanaceae). Taxon 53:73–82. https://doi.org/10.2307/4135490
Kovaleva V, Bukhteeva I, Kit OY, Nesmelova IV (2020) Plant defensins from a structural perspective. Int J Mol Sci 21:1–23. https://doi.org/10.3390/ijms21155307
Kumar S, Suleski M, Craig JM et al (2022) TimeTree 5: an expanded resource for species divergence times. Mol Biol Evol 39:1–6. https://doi.org/10.1093/molbev/msac174
Lay F, Anderson M (2005) Defensins—components of the innate immune system in plants. Curr Protein Pept Sci 6:85–101. https://doi.org/10.2174/1389203053027575
Lim KY, Kovarik A, Matyasek R et al (2007) Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol 175:756–763. https://doi.org/10.1111/j.1469-8137.2007.02121.x
Liu C, Yuan D, Liu T et al (2020) Characterization and Comparative Analysis of RWP-RK Proteins from Arachis duranensis, Arachis ipaensis, and Arachis hypogaea. Int J Genom 2020:2568640. https://doi.org/10.1155/2020/2568640
Liu Y, Zeng Z, Zhang YM et al (2021) An angiosperm NLR Atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion. Mol Plant 14:2015–2031. https://doi.org/10.1016/j.molp.2021.08.001
Luo X, Chen S, Zhang Y (2022) PlantRep: a database of plant repetitive elements. Plant Cell Rep 41:1163–1166. https://doi.org/10.1007/s00299-021-02817-y
Mahelka V, Kopeck D, Patová L (2011) On the genome constitution and evolution of intermediate wheatgrass (Thinopyrum intermedium: Poaceae, Triticeae). BMC Evol Biol 11:1–17. https://doi.org/10.1186/1471-2148-11-127
Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J Exp Bot 62:1677–1686. https://doi.org/10.1093/jxb/err002
Matsumura M, Signor G, Matthews BW (1989) Substantial increase of protein stability by multiple disulphide bonds. Nature 342:291–293. https://doi.org/10.1038/342291a0
Mergaert P, Nikovics K, Kelemen Z et al (2003) A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–173. https://doi.org/10.1104/pp.102.018192
Molina A, Segura A, García-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316:119–122. https://doi.org/10.1016/0014-5793(93)81198-9
Montiel J, Downie JA, Farkas A et al (2017) Morphotype of bacteroids in different legumes correlates with the number and type of symbiotic NCR peptides. Proc Natl Acad Sci USA 114:5041–5046. https://doi.org/10.1073/pnas.1704217114
Nawrot R, Barylski J, Nowicki G et al (2014) Plant Antimicrobial Peptides. Folia Microbiol (praha) 59:181–196. https://doi.org/10.1007/s12223-013-0280-4
Pan H (2019) More than antimicrobial: Nodule cysteine-rich peptides maintain a working balance between legume plant hosts and rhizobia bacteria during nitrogen-fixing symbiosis. In: de Bruijn FJ (ed) The model Legume Medicago truncatula, 1st edn. Wiley, Changsha, pp 617–626
Pan H, Wang D (2017) Nodule cysteine-rich peptides maintain a working balance during nitrogen-fixing symbiosis. Nat Plants 3:1–6. https://doi.org/10.1038/nplants.2017.48
Qiu YL, Taylor AB, McManus HA (2012) Evolution of the life cycle in land plants. J Syst Evol 50:171–194. https://doi.org/10.1111/j.1759-6831.2012.00188.x
Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84. https://doi.org/10.1093/oxfordjournals.molbev.a003984
Roy P, Achom M, Wilkinson H et al (2020) Symbiotic outcome modified by the diversification from 7 to over 700 nodule-specific cysteine-rich peptides. Genes (basel) 11:1–16
Rozewicki J, Li S, Amada KM et al (2019) MAFFT-DASH: Integrated protein sequence and structural alignment. Nucleic Acids Res 47:W5–W10. https://doi.org/10.1093/nar/gkz342
Sanjur OI, Piperno DR, Andres TC, Wessel-Beaver L (2002) Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: implications for crop plant evolution and areas of origin. Proc Natl Acad Sci USA 99:535–540. https://doi.org/10.1073/pnas.012577299
Scheres B, van Engelen F, van der Knaap E et al (1990) Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2:687–700. https://doi.org/10.1105/tpc.2.8.687
Schoch CL, Ciufo S, Domrachev M et al (2020) NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database 2020:1–21. https://doi.org/10.1093/database/baaa062
Shelenkov AA, Slavokhotova AA, Odintsova TI (2018) Cysmotif searcher pipeline for antimicrobial peptide identification in plant transcriptomes. Biochem 83:1424–1432. https://doi.org/10.1134/S0006297918110135
Silverstein KAT, Moskal WA, Wu HC et al (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51:262–280. https://doi.org/10.1111/j.1365-313X.2007.03136.x
Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100. https://doi.org/10.1038/nri3141
Srivastava S, Dashora K, Ameta KL et al (2021) Cysteine-rich antimicrobial peptides from plants: the future of antimicrobial therapy. Phyther Res 35:256–277. https://doi.org/10.1002/ptr.6823
Takahashi Y, Somta P, Muto C et al (2016) Novel genetic resources in the genus vigna unveiled from gene bank accessions. PLoS ONE 11:1–18. https://doi.org/10.1371/journal.pone.0147568
Tam JP, Wang S, Wong KH, Tan WL (2015) Antimicrobial peptides from plants. Pharmaceuticals 8:711–757. https://doi.org/10.3390/ph8040711
Terras FRG, Goderis IJ, Van Leuven F et al (1992) In vitro antifungal activity of a radish (Raphanus sativus L.) seed protein homologous to nonspecific lipid transfer proteins. Plant Physiol 100:1055–1058. https://doi.org/10.1104/pp.100.2.1055
Terras FRG, Eggermont K, Kovaleva V et al (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588. https://doi.org/10.2307/3870116
van Dongen S (2000) A cluster algorithm for graphs. Inf Syst [INS] R 0010:1–40
Van de Velde W, Zehirov G, Szatmari A et al (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126. https://doi.org/10.4159/harvard.9780674333987.c22
Van Parijs J, Broekaert WF, Goldstein IJ, Peumans WJ (1991) Hevein: an antifungal protein from rubber-tree (Hevea brasiliensis) latex. Planta 183:258–264. https://doi.org/10.1007/BF00197797
Velivelli SLS, Islam KT, Hobson E, Shah DM (2018) Modes of action of a Bi-domain plant defensin MtDef5 against a bacterial pathogen Xanthomonas campestris. Front Microbiol 9:1–9. https://doi.org/10.3389/fmicb.2018.00934
Wang D, Griffitts J, Starker C et al (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327:1126–1130. https://doi.org/10.1126/science.1184096
Yang MQ, van Velzen RV, Bakker FT et al (2013) Molecular phylogenetics and character evolution of Cannabaceae. Taxon 62:473–485. https://doi.org/10.12705/623.9
Yu X, Feng B, He P, Shan L (2017) From Chaos to harmony: responses and signaling upon microbial pattern recognition. Annu Rev Phytopathol 55:109–137. https://doi.org/10.1146/annurev-phyto-080516-035649
Zhang Y, Xia R, Kuang H, Meyers BC (2016) The diversification of plant NBS-LRR defense genes directs the evolution of MicroRNAs that target them. Mol Biol Evol 33:2692–2705. https://doi.org/10.1093/molbev/msw154
Zhang H, Zhang F, Yu Y et al (2020) A comprehensive online database for exploring ∼20,000 public Arabidopsis RNA-Seq libraries. Mol Plant 13:1231–1233. https://doi.org/10.1016/j.molp.2020.08.001
Zhu S, Gao B, Tytgat J (2005) Phylogenetic distribution, functional epitopes and evolution of the CSαβ superfamily. Cell Mol Life Sci 62:2257–2269. https://doi.org/10.1007/s00018-005-5200-6
Zhuang W, Shu X, Zhang M et al (2020) Characterization of the complete chloroplast genome of Populus deltoides Zhonglin 2025. Mitochondrial DNA Part B Resour 5:3723–3724. https://doi.org/10.1080/23802359.2020.1833773
Acknowledgements
We thank Joanna Friesner for helping to revise the grammar.
Funding
This work was supported by the National Natural Science Foundation of China (32070250), the Natural Science Foundation of Guangdong Province (2020A1515011030, 2022A1515110240) and the open research project of “Cross-Cooperative Team” of the Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences.
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YZ, HH, BCM, and DS planned and designed the research. HM and YF performed the bioinformatic analysis. HM and YF analyzed the data. QC contributed to data collection. HM wrote the manuscript. JJ contributed to sort out the literature. MA contributed to revise the grammar. All authors read and approved the manuscript.
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All collected data used for this project were taken from available public databases. All other analysis scripts are available at https://github.com/Ma-hz/Evolution-of-plant-CRPs.
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Communicated by Ajit Kumar Shasany.
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Ma, H., Feng, Y., Cao, Q. et al. Evolution of antimicrobial cysteine-rich peptides in plants. Plant Cell Rep 42, 1517–1527 (2023). https://doi.org/10.1007/s00299-023-03044-3
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DOI: https://doi.org/10.1007/s00299-023-03044-3