Increasing evidence indicates that tolerance is a host defense strategy against pathogens as widespread and successful as resistance. Since the concept of tolerance was proposed more than a century ...ago, it has been in continuous evolution. In parallel, our understanding of its mechanistic bases and its consequences for host and pathogen interactions, ecology, and evolution has grown. This review aims at summarizing the conceptual changes in the meaning of tolerance inside and outside the field of phytopathology, emphasizing difficulties in demonstrating and quantifying this trait. We also discuss evidence of tolerance and current knowledge on its genetic regulation, mechanisms, and role in host-pathogen coevolution, highlighting common patterns across hosts and pathogens. We hope that this comprehensive review attracts more plant pathologists to the study of this key plant defense response.
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.
It has been hypothesized that plant–virus interactions vary between antagonism and conditional mutualism according to environmental conditions. This hypothesis is based on scant experimental ...evidence, and to test it we examined the effect of abiotic factors on the Arabidopsis thaliana–Cucumber mosaic virus (CMV) interaction. Four Arabidopsis genotypes clustering into two allometric groups were grown under six environments defined by three temperature and two light‐intensity conditions. Plants were either CMV‐infected or mock‐inoculated, and the effects of environment and infection on temporal and resource allocation life‐history traits were quantified. Life‐history traits significantly differed between allometric groups over all environments, with group 1 plants tolerating abiotic stress better than those of group 2. The effect of CMV infection on host fitness (virulence) differed between genotypes, being lower in group 1 genotypes. Tolerance to abiotic stress and to infection was similarly achieved through life‐history trait responses, which resulted in resource reallocation from growth to reproduction. Effects of infection varied according to plant genotype and environment from detrimental to beneficial for host fitness. These results are highly relevant and demonstrate that plant viruses can be pleiotropic parasites along the antagonism–mutualism continuum, which should be considered in analyses of the evolution of plant–virus interactions.
Control strategies for plant viruses cannot eradicate widespread outbreaks of disease, or the emergence of new ones. Most of the reported emerging diseases of plants are caused by viruses, which ...stresses the need to model and forecast plant virus disease risk. High‐throughput sequencing technologies are one of many sources driving the generation of big data, and they are now inspiring investigations that promise a deeper understanding of what organises complex disease systems.
It has been proposed that in wild ecosystems viruses are often plant mutualists, whereas agroecosystems favour pathogenicity. We seek evidence for virus pathogenicity in wild ecosystems through the ...analysis of plant-virus coevolution, which requires a negative effect of infection on the host fitness. We focus on the interaction between Arabidopsis thaliana and Cucumber mosaic virus (CMV), which is significant in nature. We studied the genetic diversity of A. thaliana for two defence traits, resistance and tolerance, to CMV. A set of 185 individuals collected in 76 A. thaliana Iberian wild populations were inoculated with different CMV strains. Resistance was estimated from the level of virus multiplication in infected plants, and tolerance from the effect of infection on host progeny production. Resistance and tolerance to CMV showed substantial genetic variation within and between host populations, and depended on the virus x host genotype interaction, two conditions for coevolution. Resistance and tolerance were co-occurring independent traits that have evolved independently from related life-history traits involved in adaptation to climate. The comparison of the genetic structure for resistance and tolerance with that for neutral traits (QST/FST analyses) indicated that both defence traits are likely under uniform selection. These results strongly suggest that CMV infection selects for defence on A. thaliana populations, and support plant-virus coevolution. Thus, we propose that CMV infection reduces host fitness under the field conditions of the wild A. thaliana populations studied.
Summary
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.
Viruses constitute the largest group of emerging pathogens, and geminiviruses (plant viruses with circular, single-stranded DNA genomes) are the major group of emerging plant viruses. With their high ...potential for genetic variation due to mutation and recombination, their efficient spread by vectors, and their wide host range as a group, including both wild and cultivated hosts, geminiviruses are attractive models for the study of the evolutionary and ecological factors driving virus emergence. Studies on the epidemiological features of geminivirus diseases have traditionally focused primarily on crop plants. Nevertheless, knowledge of geminivirus infection in wild plants, and especially at the interface between wild and cultivated plants, is necessary to provide a complete view of their ecology, evolution, and emergence. In this review, we address the most relevant aspects of geminivirus variability and evolution in wild and crop plants and geminiviruses' potential to emerge in crops.
Summary
Specificity in plant–pathogen gene‐for‐gene (GFG) interactions is determined by the recognition of pathogen proteins by the products of plant resistance (R) genes. The evolutionary dynamics ...of R genes in plant–virus systems is poorly understood. We analyse the evolution of the L resistance locus to tobamoviruses in the wild pepper Capsicum annuum var. glabriusculum (chiltepin), a crop relative undergoing incipient domestication.
The frequency, and the genetic and phenotypic diversity, of the L locus was analysed in 41 chiltepin populations under different levels of human management over its distribution range in Mexico.
The frequency of resistance was lower in Cultivated than in Wild populations. L‐locus genetic diversity showed a strong spatial structure with no isolation‐by‐distance pattern, suggesting environment‐specific selection, possibly associated with infection by the highly virulent tobamoviruses found in the surveyed regions. L alleles differed in recognition specificity and in the expression of resistance at different temperatures, broad‐spectrum recognition of P0 + P1 pathotypes and expression above 32°C being ancestral traits that were repeatedly lost along L‐locus evolution.
Overall, loss of resistance co‐occurs with incipient domestication and broad‐spectrum resistance expressed at high temperatures has apparent fitness costs. These findings contribute to understand the role of fitness trade‐offs in plant–virus coevolution.
The term virulence has a conflicting history among plant pathologists. Here we define virulence as the degree of damage caused to a host by parasite infection, assumed to be negatively correlated ...with host fitness, and pathogenicity the qualitative capacity of a parasite to infect and cause disease on a host. Selection may act on both virulence and pathogenicity, and their change in parasite populations can drive parasite evolution and host-parasite co-evolution. Extensive theoretical analyses of the factors that shape the evolution of pathogenicity and virulence have been reported in last three decades. Experimental work has not followed the path of theoretical analyses. Plant pathologists have shown greater interest in pathogenicity than in virulence, and our understanding of the molecular basis of pathogenicity has increased enormously. However, little is known regarding the molecular basis of virulence. It has been proposed that the mechanisms of recognition of parasites by hosts will have consequences for the evolution of pathogenicity, but much experimental work is still needed to test these hypotheses. Much theoretical work has been based on evidence from cellular plant pathogens. We review here the current experimental and observational evidence on which to test theoretical hypotheses or conjectures. We compare evidence from viruses and cellular pathogens, mostly fungi and oomycetes, which differ widely in genomic complexity and in parasitism. Data on the evolution of pathogenicity and virulence from viruses and fungi show important differences, and their comparison is necessary to establish the generality of hypotheses on pathogenicity and virulence evolution.
The acquisition of new hosts provides a virus with more opportunities for transmission and survival but may be limited by across-host fitness trade-offs. Major causes of across-host trade-offs are ...antagonistic pleiotropy, that is, host differential phenotypic effects of mutations, a Genotype x Environment interaction, and epistasis, a Genotype x Genotype interaction. Here, we analyze if there are trade-offs, and what are the causes, associated with the acquisition by tobacco mild green mosaic virus (TMGMV) of a new host. For this, the multiplication of sympatric field isolates of TMGMV from its wild reservoir host
and from pepper crops was quantified in the original and the heterologous hosts. TMGMV isolates from
were adapted to their host, but pepper isolates were not adapted to pepper, and the acquisition of this new host was associated with a fitness penalty in the original host. Analyses of the collection of field isolates and of mutant genotypes derived from biologically active cDNA clones showed a role of mutations in the coat protein and the 3' untranslated region in determining within-host virus fitness. Fitness depended on host-specific effects of these mutations, on the genetic background in which they occurred, and on higher-order interactions of the type Genotype x Genotype x Environment. These types of effects had been reported to generate across-host fitness trade-offs under experimental evolution. Our results show they may also operate in heterogeneous natural environments and could explain why pepper isolates were not adapted to pepper and their lower fitness in
The acquisition of new hosts conditions virus epidemiology and emergence; hence it is important to understand the mechanisms behind host range expansion. Experimental evolution studies have identified antagonistic pleiotropy and epistasis as genetic mechanisms that limit host range expansion, but studies from virus field populations are few. Here, we compare the performance of isolates of tobacco mild green mosaic virus from its reservoir host,
and its new host, pepper, showing that acquisition of a new host was not followed by adaptation to it but was associated with a fitness loss in the original host. Analysis of mutations determining host-specific virus multiplication identified antagonistic pleiotropy, epistasis, and host-specific epistasis as mechanisms generating across-host fitness trade-offs that may prevent adaptation to pepper and cause a loss of fitness in
Thus, mechanisms determining trade-offs, identified under experimental evolution, could also operate in the heterogeneous environment in which natural plant virus populations occur.
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