Hydroxyproline-rich glycopeptide signals in potato elicit signalling associated with defense against insects and pathogens

Plant Science

Volumn 207, Issue , 2013, Pages 88-97

  Bhattacharya, Ramcharan ^a   Koramutla, Murali krishna ^a   Negi, Manisha ^a   Pearce, Gregory ^b   Ryan, Clarence A ^b  

^a INDIAN AGRICULTURAL RESEARCH INSTITUTE   (India)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Glycopeptide signals; Herbivore defense; HypSys peptides; Innate immunity; Plant defense

Indexed keywords

GLYCOPEPTIDE; PLANT DNA; PROTEIN PRECURSOR;

AMINO ACID SEQUENCE; ARTICLE; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT DISEASE; POTATO; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BASE SEQUENCE; DISEASE RESISTANCE; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GLYCOPEPTIDES; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PROTEIN PRECURSORS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM;

HEXAPODA; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM; SOLANUM TUBEROSUM;

EID: 84875590983     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2013.03.002     Document Type: Article

References (60)

1. Pearce G., Strydom D., Johnson S., Ryan C.A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 1991, 253:895-897.
2. Schmelz E.A., LeClere S., Carroll M.J., Alborn H.T., Teal P.E. Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol. 2007, 144:793-805.
3. Constabel C.P., Yip L., Ryan C.A. Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol. Biol. 1998, 36:55-62.
4. Felix G., Boller T. Systemin induces rapid ion fluxes and ethylene biosynthesis in Lycopersicon peruvianum cells. Plant J. 1995, 7:381-389.
5. +-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell. 1999, 11:263-272.
6. Orozco-Cardenas M.L., McGurl B., Ryan C.A. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:8273-8276.
7. McGurl B., Orozco-Cardenas M., Pearce G., Ryan C.A. Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase-inhibitor synthesis. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:9799-9802.
8. Pearce G., Johnson S., Ryan C.A. Structure-activity of deleted and substituted systemin, an 18-amino acid polypeptide inducer of plant defensive genes. J. Biol. Chem. 1993, 268:212-216.
9. Pearce G., Moura D.S., Stratmann J., Ryan C.A. Production of multiple plant hormones from a single polyprotein precursor. Nature 2001, 411:817-820.
10. Pearce G., Ryan C.A. Systemic signaling in tomato plants for defense against herbivores: isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J. Biol. Chem. 2003, 278:30044-30050.
11. Pearce G. Systemin, hydroxyproline-rich systemin and the induction of protease inhibitors. Curr. Protein Pept. Sci. 2011, 12:399-408.
12. Narvaez-Vasquez J., Orozco-Cardenas M.L., Ryan C.A. Systemic wound signaling in tomato leaves is cooperatively regulated by systemin and hydroxyproline-rich glycopeptide signals. Plant Mol. Biol. 2007, 65:711-718.
13. 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, 282:17777-17784.
14. Chen Y.C., Siems W.F., Pearce G., Ryan C.A. Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J. Biol. Chem. 2008, 283:11469-11476.
15. Pearce G., Bhattacharya R., Chen Y.C., Barona G., Yamaguchi Y., Ryan C.A. Isolation and characterization of hydroxyproline-rich glycopeptides signals in black nightshade leaves. Plant Physiol. 2009, 150:1422-1433.
16. Narvaez-Vasquez J., Pearce G., Ryan C.A. The plant cell wall matrix harbours a precursor of defense signaling peptides. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:12974-12977.
17. Rocha-Granados M.D.C., Sanchez-Hernandez C., Sanchez-Hernandez C.V., Martinez-Gallardo N.A., Ochoa-Alejo N., Delano-Frier J.P. The expression of the hydroxyproline-rich glycopeptide systemin precursor A in response to (a)biotic stress and elicitors is indicative of its role in the regulation of the wound response in tobacco (Nicotiana tabacum L.). Planta 2005, 222:794-810.
18. Ryan C.A., Pearce G. Systemins: a functionally defined family of peptide signal that regulate defensive genes in Solanaceae species. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14577-14580.
19. Huffaker A., Pearce G., Ryan C.A. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10098-10103.
20. Doyle J.J., Doyle J.L. A rapid total DNA preparation procedure for fresh plant tissue. Focus 1990, 12:13-15.
21. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 1997, 11:1187-1194.
22. Alexieva V., Sergiev I., Mapelli S., Karanov E. Effect of drought and UV on pea and wheat the effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ. 2001, 24:1337-1344.
23. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
24. Beyer W.F., Fridovich I. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 1987, 161:559-566.
25. Giannopolitis C.N., Ries S.K. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 1977, 59:309-314.
26. Aebi H., Lester P. Catalase in vitro. Meth Enzymol. 1984, 105:121-126.
27. Nakano Y., Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981, 22. pp. 867-280.
28. Castillo F.J., Penel C., Greppin H. Peroxidase release induced by ozone in sedum album leaves. Plant Physiol. 1984, 74:846-851.
29. Hori K., Wada A., Shibuta T. Changes in phenoloxidase activities of the gals on leaves of Ulmus davidana formed by Tetraneura fusiformis (Homoptera: Eriosomatidae). Appl. Entomol. Zool. 1997, 32:365-371.
30. Dickerson D.P., Pascholati S.F., Hagerman A.E., Butler L.G., Nicholson R.L. Phenylalanine ammonia-lyase and hydroxycinnamate: CoA ligase in maize mesocotyls inoculated with Helminthosporium maydis or Helminthosporium carbonum. Physiol Plant Pathol. 1984, 25:111-123.
31. Larkin M., Blackshields G., Brown N., Chenna R., McGettigan P., McWilliam H., Valentinet F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
32. Alvarez M.E., Penell R.I., Meijer P.J., Ishikawa A., Dixon R.A., Lamb C. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 1998, 92:773-784.
33. Orozco-Cardenas M.L., Ryan C. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:6553-6557.
34. Smirnoff N. Antioxidant systems and plant response to the environment. Environment and Plant Metabolism: Flexibility and Acclimation 1995, 217-243. BIOS Scientific Publishers, Oxford. V. Smirnoff (Ed.).
35. Ali B., Hasan S.A., Hayat S., Hayat Q., Yadav S., Fariduddin Q., Ahmad A. A role for brassinosteroids in the amelioration of aluminium stress through antioxidant system in mung bean (Vigna radiata L. Wilczek). Environ. Exp. Bot. 2008, 62:153-159.
36. Lee S.H., Ahsan N., Lee K.W., Kim D.H., Lee D.G., Kwak S.S., Kwon S.Y., Kim T.H., Lee B.H. Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J. Plant Physiol. 2007, 164:1626-1638.
37. Han Y., Wang Y., Bi J.L., Yang X.Q., Huang Y., Zhao X., Hu Y., Cai Q.N. Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. J. Chem. Ecol. 2009, 35:176-182.
38. Mueller M.J. Enzymes involved in jasmonic acid biosynthesis. Physiol. Plant. 1997, 100:653-663.
39. Cortes H., Fisahn J., Willmitzer L. Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:4106-4113.
40. Constable C.P., Yip L., Patton J.J., Chirstopher M.E. Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol. 2000, 124:285-296.
41. Ren F., Lu Y.T. Overexpression of tobacco hydroxyproline-rich glycopeptide systemin A gene in transgenic tobacco enhances resistance against Helicoverpa armigera larvae. Plant Sci. 2006, 171:286-292.
42. Laudert D., Elmar W. Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J. 1998, 15:675-684.
43. Baker C.J., Orlandi E.W. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 1995, 33:299-321.
44. Jaleel C.A., Riadh K., Gopi R., Paramasivam M., Ines J., Al-Juburi H.J., Chang-Xing Z., Hong-Bo S., Panneerselvam R. Antioxidant defense responses: physiological plasticity in higher plants under abiotic constraints. Acta Physiol. Plant. 2009, 311:427-436.
45. Matern U., Kneusel R.E. Phenolic compounds in plant disease resistance. Phytoparasitica 1988, 16:153-170.
46. Howe G.A., Jander G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 2008, 59:41-66.
47. Cai K., Gao D., Luo S., Zeng R., Yang J., Zhu X. Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiol. Plant. 2008, 134:324-333.
48. Song W., Ma X., Tan H., Zhou J. Abscisic acid enhances resistance to Alternaria solani in tomato seedlings. Plant Physiol. Biochem. 2011, 49:693-700.
49. Huffaker A., Dafoe N.J., Schmelz E.A. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1 regulates maize innate immunity and enhances disease resistance. Plant Physiol. 2011, 155:1325-1338.
50. Yamaguchi Y., Barona G., Ryan C.A., Pearce G. GmPep914, an eight-amino acid peptide isolated from Soybean leaves, activates defense-related genes. Plant Physiol. 2011, 156:932-942.
51. Spoel S.H., Mou Z., Tada Y., Spivey N.W., Genschik P., Dong X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 2009, 137:860-872.
52. Glazebrook J., Zook M., Mert F., Kagan I., Rogers E.E., Crute I.R., Houlb E.B., Hammerschmidt R., Ausubel F.M. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 1997, 146:381-392.
53. Mauch F., Dudler R. Differential induction of distinct glutathione S-transferases of wheat by xenobiotics and by pathogen attack. Plant Physiol. 1993, 102:1193-1201.
54. Wagner U., Edwards R., Dixon D.P., Mauch F. Probing the diversity of the Arabidopsis glutathione S-transferase family. Plant Mol. Biol. 2002, 49:515-532.
55. Hughes R.K., West S.I., Hornostaj A.R., Lawson D.M., Fairhurst S.A., Sanchez R.O., Hough P., Robinson B.H., Casey R. Probing a novel potato lipoxygenase with dual positional specificity reveals primary determinants of substrate binding and requirements for a surface hydrophobic loop and has implications for the role of lipoxygenases in tubers. Biochem. J. 2001, 353:345-355.
56. Stumpe M., Gobel C., Demchenko K., Hoffmann M., Klosgen R.B., Pawlowski K. I Feussner, Identification of an allene oxide synthase (CYP74C) that leads to formation of alpha-ketols from 9-hydroperoxides of linoleic and linolenic acid in below-ground organs of potato. Plant J. 2006, 47:883-896.
57. Dammann C., Rojo E., Sanchez-Serrano J.J. Abscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathways. Plant J. 1997, 11:773-782.
58. Taylor J.L., Fritzemeier K.H., Hauser I., Kombrink E., Rohwer F., Schroder M., Strittmatter G., Hahlbrock K. Structural analysis and activation by fungal infection of a gene encoding a pathogenesis-related protein in potato. Mol. Plant Microbe Interact. 1990, 3:72-77.
59. Pajerowska K.M., Parker J.E., Gebhardt C. Potato homologs of Arabidopsis thaliana genes functional in defense signaling-identification, genetic mapping, and molecular cloning. Mol. Plant Microbe Interact. 2005, 18:1107-1119.
60. Drouin G., Dover G.A. Independent Gene Evolution in the Potato Actin Gene Family Demonstrated by Phylogenetic Procedures for Resolving Gene Conversions and the Phylogeny of Angiosperm Actin Genes. J. Mol. Evol. 1990, 31:132-150.