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Dynamics of growth regulators during infection of apple leaves by Alternaria alternata apple pathotype

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Abstract

Alternaria blotch of apple caused by Alternaria alternata apple pathotype has a severe negative effect on apple production. It can cause tissue necrosis on leaves, young shoots and fruit. Recent studies on this pathogen have mostly focused on phytotoxicity and pathogenicity. There are few reports on the roles of signaling and metabolism in the process of infection. In this paper, a filial generation with substantial differences in resistance between individuals with similar genetic background was used as a host. An aggressive strain of A. alternate, that can complete the infection process 72 h after inoculation, served as the pathogen. A reproducible and reliable in vitro inoculation system for plant growth regulator determination was established to overcome the difficulties of inoculation of attached leaves. Alterations in growth regulator concentrations were detected, including indole-3-acetic acid (IAA), zeatin riboside (ZR), gibberellin A3 (GA3), abscissic acid (ABA) and the polyamines, putrescine (Put), spermidine (Spd) and spermine (Spm). Results indicated the plant growth regulators interacted with each other to modulate signaling and metabolic networks. A biotrophic-like phase was inferred to exist before necrosis developed. Gibberellin A3 and ABA appeared to be involved in the phase transformation from the biotrophic-like stage to the necrotrophic stage. Cytokinin, Put and Spd appeared to be related to disease resistance. This study advances our knowledge of the pathological mechanisms of Alternaria blotch on apple and provides useful resources for development of disease control and prevention.

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Abbreviations

SA:

salicylic acid

JA:

jasmonic acid

ET:

ethylene

PGRs:

plant growth regulators

AOS:

activated oxygen species

SEM:

scanning electron microscopy

ELISA:

enzyme-linked immunosorbent assay

HPLC:

high-performance liquid chromatography

PI:

post inoculation

IAA:

indole-3-acetic acid

ZR:

zeatin riboside

GA3 :

gibberellin A3

CK:

cytokinin

ABA:

abscissic acid

Put:

putrescine

Spd:

spermidine

Spm:

spermine

References

  • Abe K, Iwanami H, Kotoda N, Moriya S, Takahashi SS (2010) Evaluation of apple genotypes and Malus species for resistance to Alternaria blotch caused by Alternaria alternata apple pathotype using detached- leaf method. Plant Breed 129:208–218

    Article  CAS  Google Scholar 

  • Angelini R, Federico R (1989) Histochemical evidence of polyamine oxidation and generation of hydrogen peroxide in the cell wall. J Plant Physiol 135:212–217

    Article  CAS  Google Scholar 

  • Bagni N, Tassoni A (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids 20:301–317

    Article  PubMed  CAS  Google Scholar 

  • Banno K, Ishikawa H, Hamauzu Y, Tabira H (1999) Identification of a RAPD marker linked to the susceptible gene of black spot disease in Japanese pear. J Jpn Soc Hortic Sci 68:476–481

    Article  CAS  Google Scholar 

  • Davies P (1987) Plant hormones and their role in plant growth and development M. Nijhoff, the University of Michigan

  • de Torres-Zabala M, Truman W, Bennett M, Lafforgue G, Mansfield J, Egea P, Bogre L, Grant M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J 26:1434–1443

    Article  PubMed  Google Scholar 

  • Dickens J, Cook R (1995) Japanese pear black spot and apple alternaria blotch. EPPO Bull 25:651–659

    Article  Google Scholar 

  • Egusa M, Akamatsu H, Tsuge T, Otani H, Kodama M (2008) Induced resistance in tomato plants to the toxin-dependent necrotrophic pathogen Alternaria alternata. Physiol Mol Plant Pathol 73:67–77

    Article  CAS  Google Scholar 

  • Egusa M, Ochi H, Tsuge T, Otani H, Kodama M (2009) Identification of putative defense-related genes in Japanese pear against Alternaria alternata infection using suppression subtractive hybridization and expression analysis. J Gen Plant Pathol 75:119–124

    Article  CAS  Google Scholar 

  • El Ghachtouli N, Paynot M, Martin-Tanguy J, Morandi D, Gianinazzi S (1996) Effect of polyamines and polyamine biosynthesis inhibitors on spore germination and hyphal growth of Glomus mosseae. Mycol Res 100:597–600

    Article  Google Scholar 

  • Filajdić N, Sutton T (1991) Identification of distribution of Alternaria mali on apples in North Carolina and susceptibility of different varieties of apples to Alternaria blotch. Plant Dis 75:1045–1048

    Article  Google Scholar 

  • Filajdić N, Sutton T (1992) Chemical control of Alternaria blotch of apples caused by Alternaria mali. Plant Dis 76:126–130

    Article  Google Scholar 

  • Flores H, Galston A (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701

    Article  PubMed  CAS  Google Scholar 

  • Flors V, Ton J, Van Doorn R, Jakab G, García–Agustín P, Mauch–Mani B (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54:81–92

    Article  PubMed  CAS  Google Scholar 

  • Forcat S, Bennett M, Mansfield J, Grant M (2008) A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4:16

    Article  PubMed  Google Scholar 

  • Gaudinová A, Malbeck J, Dobrev P, Kubelková D, Spak J, Vanková R (2008) Cytokinin, auxin, and abscisic acid dynamics during flower development in white and red currants infected with Blackcurrant reversion virus. Physiol Mol Plant Pathol 73:119–125

    Article  Google Scholar 

  • Guan L, Zhao J, Scandalios J (2000) Cis–elements and trans–factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. Plant J 22:87–95

    Article  PubMed  CAS  Google Scholar 

  • Johnson R, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K (2000) Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 13:742–753

    Article  PubMed  CAS  Google Scholar 

  • Jones A, Aldwinckle H (1990) Compendium of apple and pear diseases. APS Press

  • Kępczyńska E (1995) The effects of spermidine biosynthetic inhibitor methyl bis-(guanylhydrazone) on spore germination, growth and ethylene production in Alternaria consortiale. Plant Growth Regul 16:263–266

    Article  Google Scholar 

  • Kepczyńska E, Kepczyński J (2005) Inhibitory effect of methyl jasmonate on development of phytopathogen Alternaria alternata (Fr.) Keissl. and its reversal by ethephon and ACC. Acta Physiol Plant 27:491–496

    Article  Google Scholar 

  • López M, Bannenberg G, Castresana C (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr Opin Plant Biol 11:420–427

    Article  PubMed  Google Scholar 

  • Mansvelt EL, Hattingh M (1989) Scanning electron microscopy of invasion of apple leaves and blossoms by Pseudomonas syringae pv. syringae. Appl Environ Microbiol 55:533

    PubMed  CAS  Google Scholar 

  • Mehdy M (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467

    PubMed  CAS  Google Scholar 

  • Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA (2008) Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell Online 20:1708–1724

    Article  CAS  Google Scholar 

  • Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd N, Jones J (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol 18:650–655

    Article  PubMed  CAS  Google Scholar 

  • Nishimura S, Kohmoto K (1983) Host-specific toxins and chemical structures from Alternaria species. Annu Rev Phytopathol 21:87–116

    Article  CAS  Google Scholar 

  • Otani H, Kohmoto K, Kodama M (1995) Alternaria toxins and their effects on host plants. Can J Bot 73:453–458

    Article  Google Scholar 

  • Pieterse C, Leon-Reyes A, Van der Ent S, Van Wees S (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    Article  PubMed  CAS  Google Scholar 

  • Roberts J (1924) Morphological characters of Alternaria mali Roberts. J Agric Res 27:699–708

    Google Scholar 

  • Saito A, Nakazawa N, Suzuki M (2001) Selection of mutants resistant to Alternaria blotch from in vitro-cultured apple shoots irradiated with X-and [gamma]-rays. J Plant Physiol 158:391–400

    Article  CAS  Google Scholar 

  • Sasabe M, Takeuchi K, Kamoun S, Ichinose Y, Govers F, Toyoda K, Shiraishi T, Yamada T (2000) Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur J Biochem 267:5005–5013

    Article  PubMed  CAS  Google Scholar 

  • Sawamura K (1972) Studies on apple Alternaria blotch caused by Alternaria mali Roberts. Faculty of Agric Hirosaki Univ Bull 18:152–235

    Google Scholar 

  • Shan X, Yan J, Xie D (2011) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol

  • Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmülling T, Parniske M, Ludwig-Müller J (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol Plant Microbe Interact 19:480–494

    Article  PubMed  CAS  Google Scholar 

  • Sutton T, Filajdić N, Brown E (1994) Current status of the management of summer diseases of apples. Norwegian Journal of Agricultural Sciences (Norway)

  • Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A, Terauchi R, Kusano T (2004) A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J 40:586–595

    Article  PubMed  CAS  Google Scholar 

  • Thomma B (2003) Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236

    Article  PubMed  CAS  Google Scholar 

  • Thomma B, Eggermont K, Penninckx I, Mauch-Mani B, Vogelsang R, Cammue B, Broekaert W (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

    Article  PubMed  CAS  Google Scholar 

  • Walters D (2003) Resistance to plant pathogens: possible roles for free polyamines and polyamine catabolism. New Phytol 159:109–115

    Article  CAS  Google Scholar 

  • Walton JD (1996) Host-selective toxins: agents of compatibility. The Plant Cell 8:1723

    Article  PubMed  CAS  Google Scholar 

  • Weiler EW (1980a) Radioimmunoassays for the differential and direct analysis of free and conjugated abscisic acid in plant extracts. Planta 148:262–272

    Article  CAS  Google Scholar 

  • Weiler EW (1980b) Radioimmunoassays for trans-zeatin and related cytokinins. Planta 149:155–162

    Article  CAS  Google Scholar 

  • Xin-ru W, Wei B, Zhi-jun Q, Ya-su Z (2008) Controlling effects of serveral fungicides against Apple Alternaria Leaf Spot. Acta Agriculturae Boreali-Occidentalis Sinica 5

  • Yamagishi D, Otani H, Kodama M (2006) G protein signaling mediates developmental processes and pathogenesis of Alternaria alternata. Mol Plant Microbe Interact 19:1280–1288

    Article  PubMed  CAS  Google Scholar 

  • Yoda H, Fujimura K, Takahashi H, Munemura I, Uchimiya H, Sano H (2009) Polyamines as a common source of hydrogen peroxide in host-and nonhost hypersensitive response during pathogen infection. Plant Mol Biol 70:103–112

    Article  PubMed  CAS  Google Scholar 

  • You-Ming Y, Chu-Nian X, Bao-Min W, Jun-Zhen J (2001) Effects of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regul 35:233–237

    Article  Google Scholar 

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Acknowledgement

We would like to thank Guodong Kang and Qiang Wang for help with apple breeding, the Institute of Pomology, Chinese Academy of Agricultural Sciences for sample collection, and Zongshan Zhou for assistance in preparing fungal strains. The authors are grateful to the electron microscopy lab at the Institute of Agro-food Science & Technology, Chinese Academy of Agricultural Sciences (Beijing, P. R. China, 100094), and the Changli Institute of Pomology, Hebei Academy of Agriculture and Forest (Changli, Hebei Province, China, 066600) for equipment and technical assistance. We also would like to thank Dr. Herb S. Aldwinckle, Kerik D. Cox, Jonathan Oliver and Lisa Jones from Cornell University for editorial assistance. This work was supported by the National Natural Science Foundation of China (30900968).

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Correspondence to P. Cong.

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Chen, Y., Zhang, C. & Cong, P. Dynamics of growth regulators during infection of apple leaves by Alternaria alternata apple pathotype. Australasian Plant Pathol. 41, 247–253 (2012). https://doi.org/10.1007/s13313-012-0128-4

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