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The salicylic acid-induced protection of non-climacteric unripe pepper fruit against Colletotrichum gloeosporioides is similar to the resistance of ripe fruit

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Abstract

The anthracnose fungus Colletotrichum gloeosporioides deleteriously affects unripe pepper fruit, but not ripe fruit. Here, we show that the induction of local acquired resistance (LAR) by salicylic acid (SA), 2,6-dichloroisonicotinic acid, or benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester pretreatment protects unripe pepper fruit against the fungus, while jasmonic acid (JA) does not. The SA-mediated LAR in the unripe fruit inhibited the fungal appressoria, resulting in protection against fungal infection. Microarray analysis revealed that 177 of 7,900 cDNA clones showed more than fourfold transcriptional accumulation in SA-treated unripe fruit. The reverse transcription-polymerase chain reaction showed that most of the SA-responsive genes (SRGs) were regulated by SA, but not by JA or ethylene-releasing ethephon. Furthermore, most of the SRGs were preferentially expressed in the ripe fruit. These results suggest that the SA-mediated transcriptional regulation of SRGs has a critical role in the resistance of ripe pepper fruit to fungal infection.

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Abbreviations

LAR:

Local acquired resistance

SA:

Salicylic acid

INA:

2,6-Dichloroisonicotinic acid

BTH:

Benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester

SRGs:

SA-responsive genes

JA:

Jasmonic acid

ET:

Ethylene

AR:

Acquired resistance

SAR:

Systemic acquired resistance

ISR:

Induced systemic resistance

RT-PCR:

Reverse transcription-polymerase chain reaction

DEPC:

Diethylpyrocarbonate

DAI:

Day after inoculation

PR:

Pathogenesis related

References

  • Bailey JA, O’Connell RJ, Pring RJ, Nash C (1992) Infection strategies of Colletotrichum species. In: Bailey JA, Jeger JA (eds) Colletotrichum: biology, pathology and control. CAB International, Wallingford, UK, pp 88–120

    Google Scholar 

  • Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12:2175–2190

    Article  PubMed  CAS  Google Scholar 

  • Cohen Y, Gisi U, Niederman T (1993) Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic-methyl-ester. Phytopathology 83:1054–1102

    Article  CAS  Google Scholar 

  • Daykin ME (1984) Infection in blueberry fruit by Colletotrichum gloeosporioides. Plant Dis 68:948–950

    Article  Google Scholar 

  • Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746

    PubMed  CAS  Google Scholar 

  • Dodd JC, Estrada A, Matcham A, Jeffries P, Jeger MJ (1991) The effect of environmental factors on Colletotrichum gloeosporioides, the causal agent of mango anthracnose, in the Philippines. Plant Pathol 40:568–575

    Article  Google Scholar 

  • Fils-Lycaon BR, Wiersma PA, Eastwell KC, Sautiere P (1996) A cherry protein and its gene, abundantly expressed in ripening fruit, have been identified as thaumatin-like. Plant Physiol 111:269–273

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr Opin Plant Biol 4:301–308

    Article  PubMed  CAS  Google Scholar 

  • Gorlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorp M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8:629–643

    Article  PubMed  CAS  Google Scholar 

  • Gupta V, Willits MG, Glazebrook J (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol Plant-Microbe Interact 13:503–511

    Article  PubMed  CAS  Google Scholar 

  • Hoffman T, Schmidt JS, Zheng X, Bent A (1999) Isolation of ethylene-insensitive soybean mutant that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiol 119:935–949

    Article  PubMed  CAS  Google Scholar 

  • Katz VA, Thulke OU, Conrath UA (1998) Benzothiadiazole primes parsley cells for augmented elicitation of defense responses. Plant Physiol 117:1333–1339

    Article  PubMed  CAS  Google Scholar 

  • Kim WG, Cho EK, Lee EJ (1986) Two strains of Colletotrichum gloeosporioides Penz. causing anthracnose on pepper fruits. Korean J Plant Pathol 2:107–113

    Google Scholar 

  • Kim KD, Oh BJ, Yang J (1999) Differential interactions of a Colletotrichum gloeosporioides isolate with green and red pepper fruits. Phytoparasitica 27:1–10

    Article  Google Scholar 

  • Knoester M, van Loon LC, van Den Heuvel J, Hennig J, Bol JF, Linthorst HJM (1998) Ethylene-insensitive tobacco lacks non-host resistance against soil-borne fungi. Proc Natl Acad Sci USA 95:1933–1937

    Article  PubMed  CAS  Google Scholar 

  • Kunkel BN, Brooks AM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  PubMed  CAS  Google Scholar 

  • Lawton KA, Beck J, Potter S, Ward E, Ryals J (1994) Regulation of cucumber class III chitinase gene expression. Mol Plant-Microbe Interact 7:48–57

    PubMed  CAS  Google Scholar 

  • Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T, Kessmann H, Staub T, Ryals J (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10:71–82

    Article  PubMed  CAS  Google Scholar 

  • Lee HI, Raskin I (1999) Purification, cloning, and expression of a pathogen inducible UDP-glucose:salicylic acid glucosyltransferase from tobacco. J Biol Chem 274:36637–36642

    Article  PubMed  CAS  Google Scholar 

  • Lund ST, Stall RE, Klee HJ (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10:371–382

    Article  PubMed  CAS  Google Scholar 

  • Manandhar JB, Hartman GL, Wang TC (1995) Conidial germination and appressorial formation of Colletotrichum capsici and C. gloeosporioides isolates from pepper. Plant Dis 79:361–366

    Google Scholar 

  • Mandal S, Mallick N, Mitra A (2009) Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol Biochem 47:642–649

    Article  PubMed  CAS  Google Scholar 

  • Marte M, Buonaurio R, Dellatorre G (1993) Induction of systemic resistance to tobacco powdery mildew by tobacco mosaic virus, tobacco necrosis virus or ethephon. J Phytopathol 138:137–144

    Article  CAS  Google Scholar 

  • Negre F, Kolosova N, Knoll J, Kish CM, Dudareva N (2002) Novel S-adenosyl-l-methionine:salicylic acid carboxyl methyltransferase, an enzyme responsible for biosynthesis of methyl salicylate and methyl benzoate, is not involved in floral scent production in snapdragon flowers. Arch Biochem Biophys 406:261–270

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell PJ, Jones JB, Antoine FR, Ciardi J, Klee HJ (2001) Ethylene-dependent salicylic acid regulates an expanded cell death response to a plant pathogen. Plant J 25:315–323

    Article  PubMed  Google Scholar 

  • Oh BJ, Kim KD, Kim YS (1998) A microscopic characterization of the infection of green and red pepper fruits by an isolate of Colletotrichum gloeosporioides. J Phytopathol 146:301–303

    Article  Google Scholar 

  • Oh BJ, Kim KD, Kim YS (1999) Effect of cuticular wax layers of green and red pepper fruits on infection by Colletotrichum gloeosporioides. J Phytopathol 147:547–552

    Article  Google Scholar 

  • Pallas J, Paiva N, Lamb C, Dixon R (1996) Tobacco plants epigenetically suppressed in phenylalanine amCommentary 93 monia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J 10:281–293

    Article  CAS  Google Scholar 

  • Park JY (2003) Expression of ripening genes in a variety of stress conditions studied by hot pepper cDNA microarray analysis. PhD thesis

  • Pieterse CMJ, van Pelt JA, van Wees SCM, Ton J, Leon-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, van der Sluis I, Bakker PAHM, van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression. Eur J Plant Pathol 107:51–61

    Article  Google Scholar 

  • Prusky D, Plumbley RA, Kobiler I (1991) The relationship between the antifungal diene levels and fungal inhibition during quiescent infection of Colletotrichum gloeosporioides in unripe avocado fruits. Plant Pathol 40:45–52

    Article  CAS  Google Scholar 

  • Rasmussen S, Dixon R (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11:1537–1551

    Article  PubMed  CAS  Google Scholar 

  • Robinson SP, Jacobs AK, Dry IB (1997) A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol 114:771–778

    Article  PubMed  CAS  Google Scholar 

  • Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    Article  PubMed  CAS  Google Scholar 

  • Salzman RA, Tikhonova I, Bordelon BP, Hasegawa PM, Bressan RA (1998) Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol 117:465–472

    Article  PubMed  CAS  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660

    Article  PubMed  CAS  Google Scholar 

  • Sticher L, Mauch-Mani B, Metraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270

    Article  PubMed  CAS  Google Scholar 

  • Swinburne TR (1983) Post-harvest pathology of fruits and vegetables. Academic Press, New York

    Google Scholar 

  • Tattersall DB, van Heeswijck R, Bordier Hoj P (1997) Identification and characterization of a fruit-specific, thaumatin-like protein that accumulates at very high levels in conjunction with the onset of sugar accumulation and berry softening in grapes. Plant Physiol 114:759–769

    Article  PubMed  CAS  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue CPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  PubMed  CAS  Google Scholar 

  • Tsuge S, Ochiai H, Inoue Y, Ohu T, Tsuno K, Kaku K, Kubo Y (2004) Involvement of phosphoglucose isomerase in pathogenicity of Xanthomonas oryzae pv. oryzae. Phytopathology 94:478–483

    Article  PubMed  CAS  Google Scholar 

  • Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusanrenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4:645–656

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by a grant (CG1134) from the Crop Functional Genomics Center of the 21st Century Frontier Research Program funded by Ministry of Science and Technology of Korean government and a grant (Code 20070401-034-026) from BioGreen 21 Program, Rural Development Administration, Republic of Korea.

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Correspondence to Young Hee Joung or Boung-Jun Oh.

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Communicated by J. R. Liu.

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Lee, S., Hong, JC., Jeon, W.B. et al. The salicylic acid-induced protection of non-climacteric unripe pepper fruit against Colletotrichum gloeosporioides is similar to the resistance of ripe fruit. Plant Cell Rep 28, 1573–1580 (2009). https://doi.org/10.1007/s00299-009-0756-5

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