Tolerance to Plant Pathogens: Theory and Experimental Evidence

Abstract

The two major mechanisms of plant defense against pathogens are resistance (the host's ability to limit pathogen multiplication) and tolerance (the host's ability to reduce the effect of infection on its fitness regardless of the level of pathogen multiplication). There is abundant literature on virtually every aspect of plant resistance to pathogens. Although tolerance to plant pathogens is comparatively less understood, studies on this plant defense strategy have led to major insights into its evolution, mechanistic basis and genetic determinants. This review aims at summarizing current theories and experimental evidence on the evolutionary causes and consequences of plant tolerance to pathogens, as well as the existing knowledge on the genetic determinants and mechanisms of tolerance. Our review reveals that (i) in plant-pathogen systems, resistance and tolerance generally coexist, i.e., are not mutually exclusive; (ii) evidence of tolerance polymorphisms is abundant regardless of the pathogen considered; (iii) tolerance is an efficient strategy to reduce the damage on the infected host; and (iv) there is no evidence that tolerance results in increased pathogen multiplication. Taken together, the work discussed in this review indicates that tolerance may be as important as resistance in determining the dynamics of plant-pathogen interactions. Several aspects of plant tolerance to pathogens that still remain unclear and which should be explored in the future, are also outlined.

Keywords: plant defense responses; range and point tolerance; tolerance mechanisms to pathogens; tolerance to plant pathogens.

Figure 1

Range versus point tolerance. Depending on the scenario, range tolerance and point tolerance do not necessarily lead to the same conclusion. (A) Host genotype a₁ (blue) has higher fitness than genotype a₂ (red) when uninfected and at every pathogen load, but range tolerance is the same in both genotypes. Point tolerance will always indicate higher tolerance of genotype a₁; (B) Host genotype a₁ and a₂ have the same fitness when uninfected, but range tolerance is higher in a₁ than in a₂. Point tolerance will agree with range tolerance at every pathogen load. Genotype a₃ (green) overcompensates detrimental effects of infection at every pathogen load (positive slope of the reaction norm); (C) Host genotype a₁ has lower fitness than genotype a₂ when uninfected, but range tolerance is higher for genotype a₁ than for a₂. Point tolerance will agree with range tolerance at higher, but not at lower, pathogen load; (D) Both genotypes have the same fitness when uninfected. Range tolerance is linear for genotype a₁ but not for genotype a₂. Genotype a₂ has lower range tolerance than a₁ in the exponential part, but higher in the plateau, of the reaction norm. Point tolerance will always be higher for genotypes a₁. Genotype a₃ overcompensates the detrimental effect of pathogen infection up to a maximum.