The different interactions of Colletotrichum gloeosporioides with two strawberry varieties and the involvement of salicylic acid

Qing-Yu Zhang , Li-Qing Zhang , Li-Li Song , Ke Duan , Na Li , Yan-Xiu Wang , Qing-Hua Gao

Horticulture Research ›› 2016, Vol. 3 ›› Issue (1) : 16007

PDF (1802KB)
Horticulture Research ›› 2016, Vol. 3 ›› Issue (1) :16007 DOI: 10.1038/hortres.2016.7
Article
research-article
The different interactions of Colletotrichum gloeosporioides with two strawberry varieties and the involvement of salicylic acid
Author information +
History +
PDF (1802KB)

Abstract

The disease symptoms recognized as ‘Anthracnose’ are caused by Colletotrichum spp. and lead to large-scale strawberry (Fragaria × ananassa Duchesne) losses worldwide in terms of both quality and production. Little is known regarding the mechanisms underlying the genetic variations in the strawberry– Colletotrichum spp. interaction. In this work, Colletotrichum gloeosporioides (C. gloeosporioides) infection was characterized in two varieties exhibiting different susceptibilities, and the involvement of salicylic acid (SA) was examined. Light microscopic observation showed that C. gloeosporioides conidia germinated earlier and faster on the leaf surface of the susceptible cultivar compared with the less-susceptible cultivar. Several PR genes were differentially expressed, with higher-amplitude changes observed in the less-susceptible cultivar. The less-susceptible cultivar contained a higher level of basal SA, and the SA levels increased rapidly upon infection, followed by a sharp decrease before the necrotrophic phase. External SA pretreatment reduced susceptibility and elevated the internal SA levels in both varieties, which were sharply reduced in the susceptible cultivar upon inoculation. The less-susceptible cultivar also displayed a more sensitive and marked increase in the transcripts of NB-LRR genes to C. gloeosporioides, and SA pretreatment differentially induced transcript accumulation in the two varieties during infection. Furthermore, SA directly inhibited the germination of C. gloeosporioides conidia; NB-LRR transcript accumulation in response to SA pretreatment was both dose- and cultivar-dependent. The results demonstrate that the less-susceptible cultivar showed reduced conidia germination. The contribution of SA might involve microbial isolate-specific sensitivity to SA, cultivar/tissue-specific SA homeostasis and signaling, and the sensitivity of R genes and the related defense network to SA and pathogens.

Cite this article

Download citation ▾
Qing-Yu Zhang, Li-Qing Zhang, Li-Li Song, Ke Duan, Na Li, Yan-Xiu Wang, Qing-Hua Gao. The different interactions of Colletotrichum gloeosporioides with two strawberry varieties and the involvement of salicylic acid. Horticulture Research, 2016, 3 (1) : 16007 DOI:10.1038/hortres.2016.7

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Münch S, Lingner U, Floss DS . The hemibiotrophic lifestyle of Colletotrichum species. J Plant Physiol 2008; 165: 41-51.

[2]

Freeman S, Katan T . Identification of Colletotrichum species responsible for anthracnose and root necrosis of strawberry in Israel. Phytopathology 1997; 87: 516-521.

[3]

Xie L, Zhang JZ, Wan Y . Identification of Colletotrichum spp. isolated from strawberry in Zhejiang Province and Shanghai City, China. J Zhejiang Univ Sci B 2010; 11: 61-70.

[4]

Dodds PN, Rathjen JP . Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 2010; 11: 539-548.

[5]

Amil-Ruiz F, Blanco-Portales R, Muñoz-Blanco J et al. The strawberry plant defense mechanism: a molecular review. Plant Cell Physiol 2011; 52: 1873-1903.

[6]

Jones JD, Dangl JL . The plant immune system. Nature 2006; 444: 323-329.

[7]

Heidel AJ, Clarke JD, Antonovics J et al. Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 2004; 168: 2197-2206.

[8]

Tao Y, Xie Z, Chen W . Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 2003; 15: 317-330.

[9]

DebRoy S, Thilmony R, Kwack YB . A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci USA 2004; 101: 9927-9932.

[10]

Loake G, Grant M . Salicylic acid in plant defense: the players and protagonists. Curr Opin Plant Biol 2007; 10: 466-472.

[11]

Tsuda K, Sato M, Stoddard T et al. Network properties of robust immunity in plants. Plos Genet 2009; 5: e1000772.

[12]

Durrant WE, Dong X . Systemic acquired resistance. Annu Rev Phytopathol 2004; 42: 185-209.

[13]

Návarová H, Bernsdorff F, Döring AC . Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 2012; 24: 5123-5141.

[14]

Shah J, Zeier J . Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci 2013; 4: 30.

[15]

Wu Y, Zhang D, Chu JY . The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 2012; 1: 639-647.

[16]

Fu ZQ, Yan S, Saleh A . NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 2012; 486: 228-232.

[17]

An C, Mou Z . Salicylic acid and its function in plant immunity. J Integr Plant Biol 2011; 53: 412-428.

[18]

DeYoung BJ, Innes RW . Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 2006; 7: 1243-1249.

[19]

Eitas TK, Dangl JL . NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 2010; 13: 472-477.

[20]

Li X, Clarke JD, Zhang Y . Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 2001; 14: 1131-1139.

[21]

Bonardi V, Tang S, Stallmann A . Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci USA 2011; 108: 16463-16468.

[22]

Salazar S, Castagnaro A, Arias M . Induction of a defense response in strawberry mediated by an avirulent strain of Colletotrichum. Eur J Plant Pathol 2007; 117: 109-122.

[23]

Tortora ML, Díaz-Ricci JC, Pedraza RO . Azospirillum brasilense siderophores with antifungal activity against Colletotrichum acutatum. Arch Microbiol 2011; 193: 275-286.

[24]

Grellet-Bournonville CF, Martinez-Zamora MG, Castagnaro AP . Temporal accumulation of salicylic acid activates the defense response against Colletotrichum in strawberry. Plant Physiol Biochem 2012; 54: 10-16.

[25]

Mamaní A, Filippone MP, Grellet C . Pathogen-induced accumulation of an ellagitannin elicits plant defense response. Mol Plant Microbe Interact 2012; 25: 1430-1439.

[26]

Widiastuti A, Yoshino M, Saito H, Maejima K, Zhou S, Odani H et al. Heat shock-induced resistance in strawberry against crown rot fungus Colletotrichum gloeosporioides. Physiol Mol Plant Pathol 2013; 84: 86-91.

[27]

Babalar M, Asghari M, Talaei A, Khosroshahi A . Effect of pre- and postharvest salicylic acid treatment on ethylene production, fungal decay and overall quality of Selva strawberry fruit. Food Chem 2007; 105: 449-453.

[28]

Asghari MR, Babalar M . Use of salicylic acid to increase strawberry fruit total antioxidant activity. Acta Hort 2010; 877: 1117-1122.

[29]

Cao SF, Hu ZC, Zheng YH, Li XW, Wang HO, Pang B . Effect of post-harvest treatment with BTH on fruit decay, microbial populations, and the maintenance of quality in strawberry. J Hortic Sci Biotech 2010; 85: 185-190.

[30]

Casado-Díaz A, Encinas-Villarejo S, de los Santos B, Schilirò E, Yubero-Serrano E-M, Amil-Ruíz F et al. Analysis of strawberry genes differentially expressed in response to Colletotrichum infection. Physiol Plant 2006; 4: 633-650.

[31]

Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F et al. Evidence for a positive regulatory role of strawberry (Fragaria × ananassa) FaWRKY1 and Arabidopsis AtWRKY75 proteins in resistance. J Exp Bot 2009; 60: 3043-3065.

[32]

Guidarelli M, Carbone F, Mourgues F, Perrotta G, Rosati C, Bertolini P et al. Colletotrichum acutatum interactions with unripe and ripe strawberry fruits and differential responses at histological and transcriptional levels. Plant Pathol 2011; 60: 685-697.

[33]

Fang X, Chen W, Xin Y . Proteomic analysis of strawberry leaves infected with Colletotrichum fragariae. J Proteomics 2012; 75: 4074-4090.

[34]

Nimchuk Z, Eulgem T, Holt BF III . Recognition and response in the plant immune system. Annu Rev Genet 2003; 37: 579-609.

[35]

Mysore KS, Ryu CM . Nonhost resistance: how much do we know? Trends Plant Sci 2004; 9: 97-104.

[36]

Li J, Zhang QY, Gao ZH, Wang F, Duan K, Ye ZW et al. Genome-wide identification and comparative expression analysis of NBS-LRR-encoding genes upon Colletotrichum gloeosporioides infection in two ecotypes of Fragaria vesca. Gene 2013; 527: 215-227.

[37]

Zhang QY, Liu FC, Duan K . Effects of salicylic acid on the expression of FaNBS20 gene responsive to Colletotrichum gloeosporioides infection in Fragaria × ananassa. Acta Hortic Sinica 2014; 41: 53-62 Chinese.

[38]

Eddleman H. Making bacteria media from potato. Indiana Biolab 1998.

[39]

Müller A, Düchting P, Weiler EW . A multiplex GC-MS/MS technique for the sensitive and quantitative single-run analysis of acidic phytohormones and related compounds, and its application to Arabidopsis thaliana. Planta 2002; 216: 44-56.

[40]

Ge Y, Guest DI . Light and scanning electron microscopy studies on the infection process of melon leaves by Colletotrichum lagenarium. Physiol Mol Plant Pathol 2011; 76: 67-74.

[41]

Amil-Ruiz F, Garrido-Gala J, Blanco-Portales R . Identification and validation of reference genes for transcript normalization in strawberry (Fragaria × ananassa) defense responses. PLoS One 2013; 8: e70603.

[42]

Glazebrook J . Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005; 43: 205-227.

[43]

Osherov N, May GS . The molecular mechanisms of conidial germination. FEMS Microbiol Lett 2001; 199: 153-160.

[44]

Kim YK, Li D, Kolattukudy PE . Induction of Ca+2 calmodulin signaling by hard-surface contact primes Colletotrichum gloeosporioides conidia to germinate and form appressoria . J Bacteriol 1998; 180: 5144-5150.

[45]

Zhang H, Ma L, Jiang S . Enhancement of biocontrol efficacy of Rhodotorula glutinis by salicylic acid against gray mold spoilage of strawberries. Int J Food Microbiol 2010; 141: 122-125.

[46]

Landi L, Feliziani E, Romanazzi G . Expression of defense genes in strawberry fruits treated with different resistance inducers. J Agric Food Chem 2014; 62: 3047-3056.

[47]

Vos IA, Pieterse CMJ, van Wees SCM . Costs and benefits of hormone-regulated plant defences. Plant Pathol 2013; 62: 43-55.

[48]

Yan J, Jessica T, Shao Y, Xu K, Liu C, Yuan Y et al. Effects of variety and cultivated conditions on salicylic acid content of strawberry (Fragaria × ananassa Duch.) fruits. Chin Agric Sci Bull 2009; 25: 199-204 Chinese.

[49]

Amil-Ruiz F. Molecular mechanisms of strawberry plant defense against Colletotrichum acutatum, PhD thesis, Universidad de Córdoba: Córdoba, Spain, 2013.

[50]

Ludwig-Müller J. Auxin and the interaction between plants and microorganisms. In: Zažímalová E, Petrášek J, Benková E (eds). Auxin and Its Role in Plant Development. Springer Press, Cham Switzerland, 2014, pp 413-429.

[51]

Koornneef A, Leon-Reyes A, Ritsema T et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 2008; 147: 1358-1368.

[52]

Tsuda K, Sato M, Glazebrook J . Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 2008; 53: 763-775.

[53]

Adams KL, Cronn R, Percifield R . Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 2003; 100: 4649-4654.

[54]

Creusot F, Macadré C, Ferrier Cana E . Cloning and molecular characterization of three members of the NBS-LRR subfamily located in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris. Genome 1999; 42: 254-264.

[55]

Pollegioni P, Van der Linden G, Belisario A . Mechanisms governing the responses to anthracnose pathogen in Juglans spp. J Biotechnol 2012; 159: 251-264.

[56]

Yang S, Gao M, Xu C . Alfalfa benefits from Medicago truncatula: the RCT1 gene from M. truncatula confers broad-spectrum resistance to anthracnose in alfalfa. Proc Natl Acad Sci USA 2008; 105: 12164-12169.

PDF (1802KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/