Balancing Selection at the Tomato RCR3 Guardee Gene Family Maintains Variation in Strength of Pathogen Defense

• Published in: PLoS genetics Vol. 8; no. 7; p. e1002813
• Main Authors: Hörger, Anja C., Ilyas, Muhammad, Stephan, Wolfgang, Tellier, Aurélien, van der Hoorn, Renier A. L., Rose, Laura E.
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.07.2012; Public Library of Science (PLoS)
• Subjects: Biology; Cladosporium - genetics; Cysteine Proteases - genetics; Evolution; Evolution, Molecular; Gene Conversion; Genes; Genetic aspects; Genetic diversity; Genetic Variation; Grants; Health aspects; Host-Pathogen Interactions - genetics; Hypotheses; Immune system; Lycopersicon esculentum - genetics; Lycopersicon esculentum - parasitology; Microbial genetics; Molecular Sequence Data; Multiculturalism & pluralism; Pathogenic microorganisms; Phylogeny; Physiological aspects; Plant Immunity - genetics; Plant Proteins - genetics; Polymorphism, Genetic; Proteinase Inhibitory Proteins, Secretory - genetics; Proteins; Selection, Genetic - genetics; Virulence (Microbiology); United Kingdom
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1002813

Coevolution between hosts and pathogens is thought to occur between interacting molecules of both species. This results in the maintenance of genetic diversity at pathogen antigens (or so-called effectors) and host resistance genes such as the major histocompatibility complex (MHC) in mammals or resistance (R) genes in plants. In plant-pathogen interactions, the current paradigm posits that a specific defense response is activated upon recognition of pathogen effectors via interaction with their corresponding R proteins. According to the "Guard-Hypothesis," R proteins (the "guards") can sense modification of target molecules in the host (the "guardees") by pathogen effectors and subsequently trigger the defense response. Multiple studies have reported high genetic diversity at R genes maintained by balancing selection. In contrast, little is known about the evolutionary mechanisms shaping the guardee, which may be subject to contrasting evolutionary forces. Here we show that the evolution of the guardee RCR3 is characterized by gene duplication, frequent gene conversion, and balancing selection in the wild tomato species Solanum peruvianum. Investigating the functional characteristics of 54 natural variants through in vitro and in planta assays, we detected differences in recognition of the pathogen effector through interaction with the guardee, as well as substantial variation in the strength of the defense response. This variation is maintained by balancing selection at each copy of the RCR3 gene. Our analyses pinpoint three amino acid polymorphisms with key functional consequences for the coevolution between the guardee (RCR3) and its guard (Cf-2). We conclude that, in addition to coevolution at the "guardee-effector" interface for pathogen recognition, natural selection acts on the "guard-guardee" interface. Guardee evolution may be governed by a counterbalance between improved activation in the presence and prevention of auto-immune responses in the absence of the corresponding pathogen.