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Down-regulation of defense genes and resource allocation into infected roots as factors for compatibility between Fagus sylvatica and Phytophthora citricola

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Abstract

Phytophthora citricola is a wide spread and highly aggressive pathogen of Fagus sylvatica. The hemibiotrophic oomycete infects the roots and establishes a compatible interaction with F. sylvatica. To investigate the transcriptional changes associated with P. citricola infection, 68 custom oligo-microarray measurements were conducted. Hierarchical as well as non-hierarchical clustering was carried out to analyze the expression profiles. Experimental setup includes a time scale covering the biotrophic and necrotrophic stages of interaction as well as comparative analyses of the local and systemic responses. The local reaction of F. sylvatica is characterized by a striking lack of defense gene induction leading to the conclusion that P. citricola escapes the main recognition systems and/or suppresses the host's response. The analysis of the systemic reaction revealed a massive shift in gene expression patterns during the biotrophic phase that is interpreted as evidence of resource allocation into the roots to support the increased sink caused by pathogen growth. Defense genes known to be responsive to salicylic acid (effective against biotrophs), jasmonic acid, and ethylene (effective against necrotrophs and herbivores) are represented on the arrays. All significant changes in gene expression measured for salicylic acid responsive genes were down-regulations in roots and leaves while some jasmonic acid responsive genes showed a very late up-regulation only in leaves, probably caused by the desiccation shortly before plant death. Together, these expression changes could explain the success of the pathogen.

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Abbreviations

CNB hypothesis:

Carbon nutrient balance hypothesis

cRNA:

Complimentary RNA

dpi:

Days post infection

ET:

Ethylene

hpi:

Hours post infection

HR:

Hypersensitive response

ISR:

Induced systemic resistance

JA:

Jasmonic acid

PCD:

Programmed cell death

PR:

Pathogenesis related proteins

SA:

Salicylic acid

SAR:

Systemic acquired resistance

SSH:

Suppression subtractive hybridization

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Acknowledgements

I would like to thank Eliane Escher for excellent technical assistance. Advice in statistical analysis from Cristina-Maria Vâlcu and Mihai Vâlcu is gratefully acknowledged. I also thank the Editor-in-Chief Prof. Rudi Appels and two anonymous reviewers for helpful comments on the manuscript. This study was financially supported by the German Research Foundation (DFG) as part of the Collaborative Research Centre (SFB) 607 project A9.

Note added in proof

The Phytophthora isolate used in this study has just recently been identified to belong to the new species of Phytophthora plurivora sp. nov. (Jung T, Burgess TI (2009) Reevaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species, Phytophthora plurivora sp. nov. Persoonia 22: 95–110).

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Authors and Affiliations

  1. Forest Genetics, Center of Life and Food Sciences Weihenstephan, Technische Universität München, Hans-Carl-von-Carlowitz-Platz 2, 85354, Freising, Germany

    Katja Schlink

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Correspondence to Katja Schlink.

Electronic supplementary materials

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Supplementary Table 1

Array results for all genes with significant expression change in roots during the course of infection (in vitro infection) (XLS 745 kb)

Supplementary Table 2

Array results for all genes with significant expression change in leaves during the course of infection (in vitro infection) (XLS 850 kb)

Supplementary Table 3

Array results for all genes with significant expression change in leaves after soil infection (XLS 26.5 kb)

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Schlink, K. Down-regulation of defense genes and resource allocation into infected roots as factors for compatibility between Fagus sylvatica and Phytophthora citricola . Funct Integr Genomics 10, 253–264 (2010). https://doi.org/10.1007/s10142-009-0143-x

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