Skip to main content
Log in

In Silico Identification of Gene Families Encoding Cysteine-Rich Peptides in Solanum lycopersicum L.

  • PLANT GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Plant cysteine-rich peptides (CRP) play a key role in protection of plants from pathogens and abiotic stress, in symbiosis with bacteria, and in plant development and reproduction. The composition and role of CRPs in tomato Solanum lycopersicum, one of the most important vegetable, has not been studied so far. In this paper, using two approaches, hidden Markov models and regular expressions, in silico identification of tomato CRP families was performed. A bioinformatic analysis of NCBI databases revealed 191 CRP precursors. The peptides found belong to the families of antimicrobial and signaling peptides. Among the antimicrobial peptides, defensins and defensin-like peptides, nonspecific lipid-transfer proteins, thionins, snakins, and hevein- and knottin-like peptides were found. Among signaling peptides, the peptides belonging to the RALF, Ole e 1, Ole e 6, and MEG families were discovered. In addition, peptides with new cysteine motifs were identified. All discovered CRPs are synthesized as pre- or preproproteins. The predicted mature peptides were characterized by cysteine motifs, antimicrobial activity, and domain structure. Thus, for the first time, using bioinformatic approaches, systemic data on the arsenal of CRPs in the tomato genome were obtained, which creates a basis for further functional studies of these peptides and their subsequent use in agriculture to develop new strategies for increasing tomato pathogen resistance, as well as in medicine to create next-generation drugs.

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.

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Farrokhi, N., Whitelegge, J.P., and Brusslan, J.A., Plant peptides and peptidomics, Plant Biotechnol. J., 2008, vol. 6, no. 2, pp. 105—134. https://doi.org/10.1111/j.1467-7652.2007.00315.x

    Article  CAS  PubMed  Google Scholar 

  2. Silverstein, K.A., Moskal, W.A.Jr., Wu, H.C., et al., Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants, Plant J., 2007, vol. 51, no. 2, pp. 262—280. https://doi.org/10.1111/j.1365-313X.2007.03136.x

    Article  CAS  PubMed  Google Scholar 

  3. Koehbach, J. and Jackson, K.A.V., Unravelling peptidomes by in silico mining, Peptidomics, 2015, vol. 2, no. 1, pp. 17—25. https://doi.org/10.1515/ped-2015-0002

    Article  Google Scholar 

  4. Choksi, P.M. and Joshi, V.Y., A review on lycopene—extraction, purification, stability and applications, Int. J. Food Prop., 2007, vol. 10, pp. 289—298. https://doi.org/10.1080/10942910601052699

    Article  CAS  Google Scholar 

  5. Rowles, J.L. III, Ranard, K.M., Smith, J.W., et al., Increased dietary and circulating lycopene are associated with reduced prostate cancer risk: a systematic review and meta-analysis, Prostate Cancer Prostatic Dis., 2017, vol. 20, no. 4, pp. 361—377. https://doi.org/10.1038/pcan.2017.25

    Article  CAS  PubMed  Google Scholar 

  6. Cavallini, C., Trettene, M., Degan, M., et al., Anti-angiogenic effects of two cystine-knot miniproteins from tomato fruit, Br. J. Pharmacol., 2011, vol. 162, no. 6, pp. 1261—1273. https://doi.org/10.1111/j.1476-5381.2010.01154.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Odintsova, T.I., Slezina, M.P., Istomina, E.A., et al., Defensin-like peptides in wheat analyzed by whole-transcriptome sequencing: a focus on structural diversity and role in induced resistance, Peer J., 2019, vol. 7. e6125. https://doi.org/10.7717/peerj.6125

    Article  CAS  PubMed  Google Scholar 

  8. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S., Improved prediction of signal peptides: SignalP 3.0, J. Mol. Biol., 2004, vol. 340, no. 4, pp. 783—795. https://doi.org/10.1016/j.jmb.2004.05.028

    Article  CAS  PubMed  Google Scholar 

  9. Kozlowski, L.P., IPC—Isoelectric Point Calculator, Biol. Direct., 2016, vol. 11, no. 55. https://doi.org/10.1186/s13062-016-0159-9

  10. Porto, W.F., Pires, Á.S., and Franco, O.L., CS-AMPPred: an updated SVM model for antimicrobial activity prediction in cysteine-stabilized peptides, PLoS One, 2012, vol. 7, no. 12. e51444. https://doi.org/10.1371/journal.pone.0051444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Waghu, F.H., Barai, R.S., Gurung, P., and Idicula-Thomas, S., CAMPR3: a database on sequences, structures, and signatures of antimicrobial peptides, Nucleic Acids Res., 2016, vol. 44, no. D1, pp. D1094—D1097. https://doi.org/10.1093/nar/gkv1051

    Article  CAS  PubMed  Google Scholar 

  12. Gasteiger, E., Hoogland, C., Gattiker, A., et al., Protein identification and analysis tools on the ExPASy server, The Proteomics Protocols Handbook / Ed. Walker John M. Humana Press, 2005, pp. 571—607.

  13. Hirokawa, T., Boon-Chieng, S., and Mitaku, S., SOSUI: classification and secondary structure prediction system for membrane proteins, Bioinformatics, 1998, vol. 14, no. 4, pp. 378—379.

    Article  CAS  Google Scholar 

  14. Wang, G., Li, X., and Wang, Z., APD3: the antimicrobial peptide database as a tool for research and education, Nucleic Acids Res., 2016, vol. 44, no. D1, pp. D1087—D1093. https://doi.org/10.1093/nar/gkv1278

    Article  CAS  PubMed  Google Scholar 

  15. Quevillon, E., Silventoinen, V., Pillai, S., et al., InterProScan: protein domains identifier, Nucleic Acids Res., 2005, vol. 33, pp. W116—W120. https://doi.org/10.1093/nar/gki442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lay, F.T. and Anderson, M.A., Defensins—components of the innate immune system in plants, Curr. Protein Pept. Sci., 2005, vol. 6, no. 1, pp. 85—101. https://doi.org/10.2174/1389203053027575

    Article  CAS  PubMed  Google Scholar 

  17. Parisi, K., Shafee, T.M.A., Quimbar, P., et al., The evolution, function and mechanisms of action for plant defensins, Semin. Cell Dev. Biol., 2019, vol. 88, pp. 107—118. https://doi.org/10.1016/j.semcdb.2018.02.004

    Article  CAS  PubMed  Google Scholar 

  18. Stotz, H.U., Spence, B., and Wang, Y., A defensin from tomato with dual function in defense and development, Plant Mol. Biol., 2009, vol. 71, nos. 1–2, pp. 131—143. https://doi.org/10.1007/s11103-009-9512-z

    Article  CAS  PubMed  Google Scholar 

  19. Harris, F., Dennison, S.R., and Phoenix, D.A., Anionic antimicrobial peptides from eukaryotic organisms, Curr. Protein Pept. Sci., 2009, vol. 10, no. 6, pp. 585—606. https://doi.org/10.2174/138920309789630589

    Article  CAS  PubMed  Google Scholar 

  20. Kader, J.C., Lipid-transfer proteins in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1996, vol. 47, pp. 627—654. https://doi.org/10.1146/annurev.arplant.47.1.627

    Article  CAS  PubMed  Google Scholar 

  21. Slavokhotova, A.A., Shelenkov, A.A., Andreev, Y.A., and Odintsova, T.I., Hevein-like antimicrobial peptides of plants, Biochemistry (Moscow), 2017, vol. 82, no. 13, pp. 1659—1674. https://doi.org/10.1134/S0006297917130065

    Article  CAS  PubMed  Google Scholar 

  22. Van den Bergh, K.P., Rougé, P., Proost, P., et al., Synergistic antifungal activity of two chitin-binding proteins from spindle tree (Euonymus europaeus L.), Planta, 2004, vol. 219, no. 2, pp. 221—232. https://doi.org/10.1007/s00425-004-1238-1

    Article  CAS  PubMed  Google Scholar 

  23. Slavokhotova, A.A., Naumann, T.A., Price, N.P., et al., Novel mode of action of plant defense peptides—hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases, FEBS J., 2014, vol. 281, no. 20, pp. 4754—4764. https://doi.org/10.1111/febs.13015

    Article  CAS  PubMed  Google Scholar 

  24. Harris, P.W., Yang, S.H., Molina, A., et al., Plant antimicrobial peptides snakin-1 and snakin-2: chemical synthesis and insights into the disulfide connectivity, Chemistry, 2014, vol. 20, no. 17, pp. 5102—5210. https://doi.org/10.1002/chem.201303207

    Article  CAS  PubMed  Google Scholar 

  25. Berrocal-Lobo, M., Segura, A., Moreno, M., et al., Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection, Plant Physiol., 2002, vol. 128, no. 3, pp. 951—961. https://doi.org/10.1104/pp.010685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Segura, A., Moreno, M., Madueño, F., et al., Snakin-1, a peptide from potato that is active against plant pathogens, Mol. Plant—Microbe Interact., 1999, vol. 12, no. 1, pp. 16—23. https://doi.org/10.1094/MPMI.1999.12.1.16

    Article  CAS  PubMed  Google Scholar 

  27. Almasia, N.I., Bazzini, A.A., Hopp, H.E., and Vazquez-Rovere, C., Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants, Mol. Plant Pathol., 2008, vol. 9, no. 3, pp. 329—338.

    Article  CAS  Google Scholar 

  28. Nahirñak, V., Almasia, N.I., Fernandez, P.V., et al., Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition, Plant Physiol., 2012, vol. 158, no. 1, pp. 252—263. https://doi.org/10.1104/pp.111.186544

    Article  CAS  PubMed  Google Scholar 

  29. Tam, J.P., Wang, S., Wong, K.H., and Tan, W.L., Antimicrobial peptides from plants, Pharmaceuticals (Basel), 2015, vol. 8, no. 4, pp. 711—757. https://doi.org/10.3390/ph8040711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Cotabarren, J., Tellechea, M.E., Tanco, S.M., et al., Biochemical and MALDI-TOF mass spectrometric characterization of a novel native and recombinant cystine knot miniprotein from Solanum tuberosum subsp. andigenum cv. Churqueña, Int. J. Mol. Sci., 2018, vol. 19, no. 3. pii: E678. https://doi.org/10.3390/ijms19030678

    Article  CAS  PubMed  Google Scholar 

  31. Stec, B., Plant thionins—the structural perspective, Cell. Mol. Life Sci., 2006, vol. 63, no. 12, pp. 1370—1385. https://doi.org/10.1007/s00018-005-5574-5

    Article  CAS  PubMed  Google Scholar 

  32. Pearce, G., Moura, D.S., Stratmann, J., and Ryan, C.A., Jr., RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development, Proc. Natl. Acad. Sci. U.S.A., 2001, vol. 98, no. 22, pp. 12843—12847. https://doi.org/10.1073/pnas.201416998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bedinger, P.A., Pearce, G., and Covey, P.A., RALFs: peptide regulators of plant growth, Plant Signal. Behav., 2010, vol. 5, no. 11, pp. 1342—1346. https://doi.org/10.4161/psb.5.11.12954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen, L.Y., Small peptides, big roles—RALFs regulate pollen tube growth and burst in plant reproduction, J. Genet. Genomics, 2018, vol. 45, no. 3, pp. 121—123. https://doi.org/10.1016/j.jgg.2018.02.006

    Article  PubMed  Google Scholar 

  35. Quiralte, J., Palacios, L., Rodríguez, R., et al., Modelling diseases: the allergens of Olea europaea pollen, J. Invest. Allergol. Clin. Immunol., 2007, vol. 17, suppl. 1, pp. 76—82.

    Google Scholar 

  36. Villalba, M., Batanero, E., Monsalve, R.I., et al., Cloning and expression of Ole e I, the major allergen from olive tree pollen: polymorphism analysis and tissue specificity, J. Biol. Chem., 1994, vol. 269, no. 21, pp. 15217—15222.

    CAS  PubMed  Google Scholar 

  37. Treviño, M.A., García-Mayoral, M.F., Barral, P., et al., NMR solution structure of Ole e 6, a major allergen from olive tree pollen, J. Biol. Chem., 2004, vol. 279, no. 37, pp. 39035—39041. https://doi.org/10.1074/jbc.M406045200

    Article  CAS  PubMed  Google Scholar 

  38. Gutiérrez-Marcos, J.F., Costa, L.M., Biderre-Petit, C., et  al., maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression, Plant Cell, 2004, vol. 16, no. 5, pp. 1288—1301. https://doi.org/10.1105/tpc.019778

    Article  PubMed  PubMed Central  Google Scholar 

  39. Milligan, S.B. and Gasser, C.S., Nature and regulation of pistil-expressed genes in tomato, Plant Mol. Biol., 1995, vol. 28, no. 4, pp. 691—711.

    Article  CAS  Google Scholar 

  40. Baxter, A.A., Richter, V., Lay, F.T., et al., The tomato defensin TPP3 binds phosphatidylinositol (4,5)-bisphosphate via a conserved dimeric cationic grip conformation to mediate cell lysis, Mol. Cell. Biol., 2015, vol. 35, no. 11, pp. 1964—1978. https://doi.org/10.1128/MCB.00282-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Rigano, M.M., Romanelli, A., Fulgione, A., et al., A novel synthetic peptide from a tomato defensin exhibits antibacterial activities against Helicobacter pylori,J. Pept. Sci., 2012, vol. 18, no. 12, pp. 755—762. https://doi.org/10.1002/psc.2462

    Article  CAS  PubMed  Google Scholar 

  42. Tomassen, M.M., Barrett, D.M., van der Valk, H.C., and Woltering, E.J., Isolation and characterization of a tomato non-specific lipid transfer protein involved in polygalacturonase-mediated pectin degradation, J. Exp. Bot., 2007, vol. 58, no. 5, pp. 1151—1160. https://doi.org/10.1093/jxb/erl288

    Article  CAS  PubMed  Google Scholar 

  43. Mitton, F.M., Pinedo, M.L., and de la Canal, L., Phloem sap of tomato plants contains a DIR1 putative ortholog, J. Plant Physiol., 2009, vol. 166, no. 5, pp. 543—547.

    Article  CAS  Google Scholar 

  44. Volpicella, M., Leoni, C., Fanizza, I., et al., Expression and characterization of a new isoform of the 9 kDa allergenic lipid transfer protein from tomato (variety San Marzano), Plant Physiol. Biochem., 2015, vol. 96, pp. 64—71. https://doi.org/10.1016/j.plaphy.2015.07.019

    Article  CAS  PubMed  Google Scholar 

  45. Balaji, V. and Smart, C.D., Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhances tolerance to Clavibacter mi-chiganensis subsp. michiganensis in transgenic tomato (Solanum lycopersicum), Transgenic Res., 2012, vol. 21, no. 1, pp. 23—37. https://doi.org/10.1007/s11248-011-9506-x

    Article  CAS  PubMed  Google Scholar 

  46. Herbel, V., Sieber-Frank, J., and Wink, M., The antimicrobial peptide snakin-2 is upregulated in the defense response of tomatoes (Solanum lycopersicum) as part of the jasmonate-dependent signaling pathway, J. Plant Physiol., 2017, vol. 208, pp. 1—6. https://doi.org/10.1016/j.jplph.2016.10.006

    Article  CAS  PubMed  Google Scholar 

  47. Díez-Díaz, M., Conejero, V., Rodrigo, I., et al., Isolation and characterization of wound-inducible carboxypeptidase inhibitor from tomato leaves, Phytochemistry, 2004, vol. 65, no. 13, pp. 1919—1924. https://doi.org/10.1016/j.phytochem.2004.06.007

    Article  CAS  PubMed  Google Scholar 

  48. Molesini, B., Rotino, G.L., Dusi, V., et al., Two metallocarboxypeptidase inhibitors are implicated in tomato fruit development and regulated by the Inner No Outer transcription factor, Plant Sci., 2018, vol. 266, pp. 19—26. https://doi.org/10.1016/j.plantsci.2017.10.011

    Article  CAS  PubMed  Google Scholar 

  49. Muschietti, J., Dircks, L., Vancanneyt, G., and McCormick, S., LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization, Plant J., 1994, vol. 6, no. 3, pp. 321—338.

    Article  CAS  Google Scholar 

  50. Shelenkov, A.A., Slavokhotova, A.A., and Odintsova, T.I., Cysmotif searcher pipeline for antimicrobial peptide identification in plant transcriptomes, Biochemistry (Moscow), 2018, vol. 83, no. 11, pp. 1424—1432. https://doi.org/10.1134/S0006297918110135

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the Russian Science Foundation (grant no. 16-16-00032).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. I. Odintsova.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Istomina, E.A., Slezina, M.P., Kovtun, A.S. et al. In Silico Identification of Gene Families Encoding Cysteine-Rich Peptides in Solanum lycopersicum L.. Russ J Genet 56, 572–579 (2020). https://doi.org/10.1134/S1022795420050063

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795420050063

Keywords:

Navigation