Parallel evolution of the POQR prolyl oligo peptidase gene conferring plant quantitative disease resistance.

Thomas Badet,Pierre Sadon,Dominique Roby,Malick Mbengue,Justine Sucher,Sylvain Raffaele,Marielle Barascud,Claudine Balagué,Derry Voisin

doi:10.1371/journal.pgen.1007143

Abstract

Plant pathogens with a broad host range are able to infect plant lineages that diverged over 100 million years ago. They exert similar and recurring constraints on the evolution of unrelated plant populations. Plants generally respond with quantitative disease resistance (QDR), a form of immunity relying on complex genetic determinants. In most cases, the molecular determinants of QDR and how they evolve is unknown. Here we identify in Arabidopsis thaliana a gene mediating QDR against Sclerotinia sclerotiorum, agent of the white mold disease, and provide evidence of its convergent evolution in multiple plant species. Using genome wide association mapping in A. thaliana, we associated the gene encoding the POQR prolyl-oligopeptidase with QDR against S. sclerotiorum. Loss of this gene compromised QDR against S. sclerotiorum but not against a bacterial pathogen. Natural diversity analysis associated POQR sequence with QDR. Remarkably, the same amino acid changes occurred after independent duplications of POQR in ancestors of multiple plant species, including A. thaliana and tomato. Genome-scale expression analyses revealed that parallel divergence in gene expression upon S. sclerotiorum infection is a frequent pattern in genes, such as POQR, that duplicated both in A. thaliana and tomato. Our study identifies a previously uncharacterized gene mediating QDR against S. sclerotiorum. It shows that some QDR determinants are conserved in distantly related plants and have emerged through the repeated use of similar genetic polymorphisms at different evolutionary time scales.

Highlights

Plant pathogens are major threats to biodiversity in natural ecosystems and to food security worldwide
Plant exhibit a response designated as quantitative disease resistance (QDR) when challenged by S. sclerotiorum, the molecular bases of which are largely unknown
We used genome wide association mapping a natural population of Arabidopsis thaliana host

Summary

Introduction

Plant pathogens are major threats to biodiversity in natural ecosystems and to food security worldwide. For some important plant diseases, especially those caused by necrotrophic and broad host range pathogens, R genes of major effect are unknown. QDR is based on complex inheritance, involving numerous genes of small effect [4,5,6]. QDR is frequent in crops and natural plant populations, and is of practical importance in agriculture because it is often more durable than R-mediated resistance [7]. The identification of genes underlying QDR is expected to provide fundamental insights into the diversity of plant immune responses and prediction of evolutionary trajectories of natural populations. The molecular bases of QDR have been identified only in few cases and involve remarkably diverse molecular functions [6,8,9]

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Conclusion