Effective tolerance based on resource reallocation is a virus‐specific defence in Arabidopsis thaliana

Abstract

Plant viruses often harm their hosts, which have developed mechanisms to prevent or minimize the effects of virus infection. Resistance and tolerance are the two main plant defences to pathogens. Although resistance to plant viruses has been studied extensively, tolerance has received much less attention. Theory predicts that tolerance to low-virulent parasites would be achieved through resource reallocation from growth to reproduction, whereas tolerance to high-virulent parasites would be attained through shortening of the pre-reproductive period. We have shown previously that the tolerance of Arabidopsis thaliana to Cucumber mosaic virus (CMV), a relatively low-virulent virus in this host, accords to these predictions. However, whether other viruses trigger the same response, and how A. thaliana copes with highly virulent virus infections remains unexplored. To address these questions, we challenged six A. thaliana wild genotypes with five viruses with different genomic structures, life histories and transmission modes. In these plants, we quantified virus multiplication, virulence, and the effects of infection on plant growth and reproduction, and on the developmental schedule. Our results indicate that virus multiplication varies according to the virus × host genotype interaction. Conversely, effective tolerance is observed only on CMV infection, and is associated with resource reallocation from growth to reproduction. Tolerance to the other viruses is observed only in specific host-virus combinations and, at odds with theoretical predictions, is linked to longer pre-reproductive periods. These findings only partially agree with theoretical predictions, and contribute to a better understanding of pathogenic processes in plant-virus interactions.

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

“…It should be noted that upon UK1-TuMV infection, infected plants of tolerant Arabidopsis genotypes produced on average 30% of the seeds produced by mock individuals. It could be argued that this level of fecundity tolerance is not effective, i.e., seed production of infected plants is far from that of uninfected ones ( Shuckla et al, 2018 ). However, mathematical models on the evolution of tolerance to sterilizing pathogens predict that optimal levels of tolerance will not surpass 50% of the progeny produced by uninfected individuals, regardless of tolerance being modelled as a function of host mortality, lifespan or transmission rate ( Restif & Koella, 2004; Hall et al, 2007; Best et al, 2010 ).…”

“…Tolerance to CMV varies across Arabidopsis genotypes as a quantitative trait; and long-lived genotypes with low seed production to total biomass ratio (Group 1 genotypes) are generally more tolerant than short-lived genotypes that have high seed to biomass ratio (Group 2 genotypes) ( Pagán et al, 2008; Hily et al, 2016 ). Tolerance to CMV in Group 1 genotypes is attained through modifications of life-history traits, mainly the reallocation of resources from growth to reproduction and, to a lesser extent, elongation of the pre-reproductive period ( Pagán et al, 2008; Shuckla et al, 2018 ). Virus-induced resource reallocation appears to be CMV-specific, and it is not triggered upon TuMV infection ( Shuckla et al, 2018 ).…”

“…Tolerance to CMV in Group 1 genotypes is attained through modifications of life-history traits, mainly the reallocation of resources from growth to reproduction and, to a lesser extent, elongation of the pre-reproductive period ( Pagán et al, 2008; Shuckla et al, 2018 ). Virus-induced resource reallocation appears to be CMV-specific, and it is not triggered upon TuMV infection ( Shuckla et al, 2018 ). However, these authors used a reduced set of Arabidopsis genotypes, and did not test virulence-specific modifications of other life-history traits that would confer tolerance, and their potential trade-offs.…”

“…Conversely, plant mortality tolerance might be less relevant upon infection with a milder pathogen such as CMV, as infected plants generally reach the adult stage and reproduce. However, in most experimental analyses of tolerance to plant pathogens host fitness was measured only as progeny production ( Pagán & García-Arenal, 2018 ), and the relationship between fecundity tolerance and mortality tolerance have been seldom analysed (Pagán et al, 2008; Shuckla et al, 2018 ). Another point under debate in the literature on plant tolerance is how it is quantified.…”

A tradeoff between tolerance and resistance to a major fungal pathogen in elite wheat cultivars

“…Since the concept of tolerance was first coined more than a century ago (Cobb, 1894), numerous studies (reviewed by Pagan & Garcia-Arenal, 2018) investigated tolerance to pathogens in crop plants (Caldwell et al, 1958;Schafer, 1971;Newton et al, 2000;Bingham et al, 2009;Ney et al, 2013;Newton, 2016), model plants (Kover & Schaal, 2002;Pagan et al, 2008;Shuckla et al, 2017) and wild plants Inglese & Paul, 2006;Carr et al, 2006). R aberg et al (2007) were the first to demonstrate tolerance to an infectious disease in animals.…”