Continua of specificity and virulence in plant host–pathogen interactions: causes and consequences

Abstract

Contents Summary 513 Introduction 513 Continua in plant host–pathogen interactions 514 Mechanisms underlying continua in specificity and virulence 516 Ecological consequences 519 Evolutionary patterns and processes 520 Conclusions 524 Acknowledgements 525 References 525 Summary Ecological, evolutionary and molecular models of interactions between plant hosts and microbial pathogens are largely based around a concept of tightly coupled interactions between species pairs. However, highly pathogenic and obligate associations between host and pathogen species represent only a fraction of the diversity encountered in natural and managed systems. Instead, many pathogens can infect a wide range of hosts, and most hosts are exposed to more than one pathogen species, often simultaneously. Furthermore, outcomes of pathogen infection vary widely because host plants vary in resistance and tolerance to infection, while pathogens are also variable in their ability to grow on or within hosts. Environmental heterogeneity further increases the potential for variation in plant host–pathogen interactions by influencing the degree and fitness consequences of infection. Here, we describe these continua of specificity and virulence inherent within plant host–pathogen interactions. Using this framework, we describe and contrast the genetic and environmental mechanisms that underlie this variation, outline consequences for epidemiology and community structure, explore likely ecological and evolutionary drivers, and highlight several key areas for future research.

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

“…Whether considering multi-parasitized hosts or multi-host parasites, field studies are needed because it is clear from many host-parasite systems that environmental variation mediates host-parasite interactions (either directly by resource-dependent variation in parasite growth and host defence, or indirectly through parasite-mediated competition, and thereby fitness impacts on host). In addition, oppportunities for interspecies transmission in multi-host parasites can be greatly modulated by environmental heterogeneity (Barrett et al 2009;Hall et al 2009). Cross-disciplinary approaches, including the tools of epidemiology and animal behaviour, have proved their efficiency in understanding the spread and virulence in a natural multi-host pathogen (e.g.…”

“…For example, the emergence of new virulent diseases has occurred in cultivated plants via betweenspecies recombination in virus and fungal pathogens (references in Barrett et al (2009)). Within-host interspecific interactions may favour between-strain recombination in one of the interacting parasites, leading to more virulent or transmissible strains of parasites, as suggested by the study of Escribano et al (2001).…”

Adaptation to enemy shifts: rapid resistance evolution to local Vibrio spp. in invasive Pacific oysters

“…Vibrio are ubiquitous in the marine realm and pathogenic strains are often generalists with a broad host range [43] that encounter a vast range of resistance mechanisms from alternative host species [44]. Indeed, Vibrio communities associated with benthic marine invertebrates including oyster populations used here were not host specific and rather reflected a random assemblage of Vibrio spp.…”

Phylogenetic congruence between subtropical trees and their associated fungi

“…Whereas networks of multiple pathogens with multiple hosts dominate natural systems (Barrett et al., 2009; Vacher, Piou, & Desprez‐Loustau, 2008), most previous work has emphasized single‐pathogen infections in a single plant species. Some recent studies have provided a window into the structure of bipartite networks of belowground plant–fungal interactions dominated by mycorrhizal fungi (e.g., Montesinos‐Navarro, Segarra‐Moragues, Valiente‐Banuet, & Verdú, 2012; Taylor et al., 2014; Toju, Guimarães, Olesen, & Thompson, 2014; Toju, Sato, et al., 2013, Toju, Yamamoto, et al., 2013), but such networks have included <2% putative pathogens.…”