All Mold Is Not Alike: The Importance of Intraspecific Diversity in Necrotrophic Plant Pathogens

Pathogens commonly possess naturally occurring intraspecific variation for traits associated with pathogenicity or virulence. Studies of host–pathogen interactions frequently fail to acknowledge this variation, particularly in studies of necrotrophic plant pathogens, where the molecular bases of defense are largely unknown. Necrotrophic plant pathogens, in contrast to obligate parasites of living plant cells known as biotrophs, kill plant cells before consuming them and may survive in the absence of living host cells in dormant or saprophytic states [1–4]. Necrotrophs may kill host cells using an array of toxins, although it is also proposed that these pathogens may activate plant immune responses designed to work against biotrophic pathogens, thus encouraging plant cells to kill themselves [5–9]. While many pathogen species cannot be clearly classified as either biotrophic or necrotrophic, as they shift lifestyles over the course of interactions with their hosts, commonly recognized necrotrophic plant pathogens include various species of Botrytis and Alternaria, as well as Sclerotinia sclerotiorum, Pythium irregulare, and Plectosphaerella cucurmerina [2,10]. Of these, Botrytis cinerea, a highly generalist pathogen, and Alternaria brassicicola, a specialist pathogen of Brassica, dominate research on molecular mechanisms of plant defense against necrotrophic pathogens. Plant immune responses against biotrophic pathogens are predominantly mediated by specific recognition of the products of pathogen ‘‘avirulence’’ (avr) genes directly or indirectly by the products of plant ‘‘resistance’’ (R) genes; localized cell death is believed to restrict the growth of obligate (biotrophic) parasites [11,12]. Intraspecific variation in pathogen avr genes is common, as these genes are believed to confer a selective pathogen advantage in the absence of the corresponding plant R gene [13–15]. Currently, specific recognition of necrotrophic pathogens by similar mechanisms has not been documented, although similar evolutionary dynamics may shape the interplay between variable plant sensitivity to some necrotroph-produced toxins (called ‘‘host selective toxins’’) and variable production of these toxins by the pathogen [15–17]. This lack of identified specific recognition has generated a prevailing view in the plant molecular defense research community that as necrotrophic pathogens are not reported to engage in specific interactions with host plants, all isolates of a particular necrotrophic pathogen species are equivalent. This opinion manifests itself in a lack of use of necrotrophic diversity in published studies, as well as a lack of reporting of identifying pathogen data, despite published evidence that necrotrophic pathogens show intraspecific variation affecting pathogenesisor virulence-related traits [18–24]. We suggest that the limited use of pathogen diversity biases our understanding of plant–necrotroph interactions. The research community should enforce detailed reporting of identifying pathogen data for studies of plant–necrotroph interactions and encourage the use of multiple pathogen genotypes.