Bet Hedging as a Mechanism of Pathogenic Variation in the Rice Blast Fungus

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Fungal phytopathogens are notorious for their pathogenic variability. As an example, the rice blast fungus Magnaporthe oryzae rapidly defeats newly deployed, disease resistant rice varieties. Studies have shown that such virulence gains can occur through the mutation or loss of key avirulence (Avr) effectors that would normally be recognized by cognate resistance receptors in rice [1-3]. Recent data from my lab suggest that clonal variation in effector expression (CVEE) could serves as an epigenetic mechanism underlying pathogenic variability. The M. oryzae genome codes for hundreds of secreted proteins, many of which are expressed during infection and potentially could trigger host resistance. Our preliminary data leads me to hypothesize that the fungus avoids this problem by bet-hedging, whereby clonal individuals express different sets of secreted effectors, thereby spreading the risk of host recognition among the pathogen population. Further, I posit that CVEE may be universal in M. oryzae:host interactions (and possibly in other pathosystems) constituting an important layer of plant:pathogen recognition that has been systematically overlooked due to epistasis from Avr genes not subject to CVEE. If true, this would dramatically alter our understanding of plant:microbe recognition; and, for M. orzyae and other pathogens, it could explain widely studied, but poorly understood phenomena such as quantitative (or partial, horizontal, etc.) resistance and mesothetic reactions (where a single plant is both susceptible and resistant to the same pathogen strain). Most importantly, however, it introduces the general and transformative concept that interactions between a single pathogen strain and a single plant genotype may typically involve recognition between many Avr-R-protein pairs, with a majority of Avr effectors being variably expressed among different infection sites. Under this model, the observed plant response (susceptible versus resistant), rather than being binary (as supposed by the current recognition model), instead represents an aggregate of different cellular responses (ranging from effector-triggered immunity to no response) at multiple individual infection sites. Clonal variation in gene expression has been documented in many organisms, including bacteria, fungi and mammals [4-6]. A comprehensive study of protein levels in single yeast cells revealed that the proteins with the noisiest expression tended to be ones whose products responded to environmental change [5]. This led to the idea that gene expression heterogeneity could be a key component of bet-hedging mechanisms that enhance organismal adaptability [7]. In biology, bet-hedging has been described as "reversible epigenetic phenotypic heterogeneity that results in decreased arithmetic mean fitness and increased geometric mean fitness of the population across environments" [8]. A recent study nicely illustrated this principle by showing that yeast cells exhibit heterogeneity in the expression of Tls1p, which regulates synthesis of the cytoprotectant sugar, trehalose. Cells with abundant Tls1p grew extremely slowly in a benign environment but preferentially survived heat stress. Surviving colonies then largely converted to fast growth (and Tls1p deficiency) once the stress was relieved [8], thereby resetting the mechanism. Recently, a number of additional papers have reported that bet-hedging underlies adaptation to various other stresses in organisms ranging from bacteria [9, 10], to fungi [11, 12], to an insect [13]. Undoubtedly, many more examples will soon surface.
Effective start/end date8/1/157/31/17


  • National Science Foundation: $100,814.00


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