Trade-offs between host tolerances to different pathogens in plant–virus interactions

Abstract

Although accumulating evidence indicates that tolerance is a plant defence strategy against pathogens as widespread as resistance, how plants evolve tolerance is poorly understood. Theory predicts that hosts will evolve to maximize tolerance or resistance, but not both. Remarkably, most experimental works failed in finding this trade-off. We tested the hypothesis that the evolution of tolerance to one virus is traded-off against tolerance to others, rather than against resistance and identified the associated mechanisms. To do so, we challenged eighteen Arabidopsis thaliana genotypes with Turnip mosaic virus (TuMV) and Cucumber mosaic virus (CMV). We characterized plant life-history trait modifications associated with reduced effects of TuMV and CMV on plant seed production (fecundity tolerance) and life period (mortality tolerance), both measured as a norm of reaction across viral loads (range tolerance). Also, we analysed resistance-tolerance and tolerance-tolerance trade-offs. Results indicate that tolerance to TuMV is associated with changes in the length of the pre-reproductive and reproductive periods, and tolerance to CMV with resource reallocation from growth to reproduction; and that tolerance to TuMV is traded-off against tolerance to CMV in a virulence-dependent manner. Thus, this work provides novel insights on the mechanisms of plant tolerance and highlights the importance of considering the combined effect of different pathogens to understand how plant defences evolve.

Arabidopsis thaliana Genes Associated with Cucumber mosaic virus Virulence and Their Link to Virus Seed Transmission

“…RTFL13 has been shown to be a regulator of flowering time that is expressed during cambium formation in Arabidopsis inflorescences [ 70 ]. There is ample evidence of the link between flowering time and the effect of virus infection on seed production [ 25 , 26 , 91 ]. Although the genetic bases are unknown, flowering genes are thought to control this process [ 18 ].…”

“…Certainly, the development of plant symptoms in vegetative structures may potentially impact plant fitness and it is likely that both traits have genetic associations [ 10 ]. However, the effect of infection on plant growth and on plant reproduction are not necessarily linked, e.g., [ 20 , 25 , 26 ]. Hence, the host genetic determinants of virulence as the effect of virus infection on plant progeny production are still poorly understood.…”

“…Accordingly, substantial genetic variation has been described for relevant adaptive traits including diversity for responses to pathogens [ 23 , 32 , 33 , 34 ]. For instance, the infection of ten Iberian Arabidopsis genotypes, representing the variation of the species in this region, with different CMV and TuMV strains showed that virulence (quantitatively measured as the effect of infection on viable seed production) is also controlled by both virus and host genetic determinants [ 4 , 23 , 26 ].…”

Host population structure for tolerance determines the evolution of plant–virus interactions

“…Numerous experimental analyses have indicated that phenotypic structure for tolerance in animal and plant populations varies along a continuum from fixation (Roy et al ., 2000 ; Carr et al ., 2003 ; Lefèvre et al ., 2011 ) to no tolerance (Montes et al ., 2020 ), with a range of intermediate levels in between (Råberg et al ., 2007 ; Pagán et al ., 2008 ; Hayward et al ., 2014 ). It is thought that structure for tolerance can be maintained in the host population if tolerance has a cost in terms of host fitness or by reducing defences to other pathogens (Restif & Koella, 2003 ; Fornoni et al ., 2004 ; Vitale & Best, 2019 ), and evidence of such costs have been reported in several plant–pathogen (including virus) interactions (Simms & Triplett, 1994 ; Koskella et al ., 2002 ; Montes et al ., 2020 ). These observations strongly suggest that pathogens commonly face heterogeneous plant population structures for tolerance; yet analyses of pathogen evolution in response such structure are scant and sometimes contradictory, particularly for plant viruses.…”

“…TuMV is commonly found in wild populations of Arabidopsis, mostly in a single infection, at up to 60% prevalence (Pagán et al ., 2010 ), indicating that the Arabidopsis–TuMV interaction is significant in nature. TuMV infection affects Arabidopsis flower and silique viability, which may severely reduce plant fertility and often prevents reproduction (Sánchez et al ., 2015 ; Montes et al ., 2020 ). Also, virus infection greatly shortens plant lifespan (Vijayan et al ., 2017 ), and particularly the Arabidopsis reproductive period, thereby affecting progeny production (Montes et al ., 2020 ).…”