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. 2020 Mar 18;6(1):veaa019.
doi: 10.1093/ve/veaa019. eCollection 2020 Jan.

Trade-offs Between Host Tolerances to Different Pathogens in Plant-Virus Interactions

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Free PMC article

Trade-offs Between Host Tolerances to Different Pathogens in Plant-Virus Interactions

Nuria Montes et al. Virus Evol. .
Free PMC article

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.

Keywords: Arabidopsis thaliana; Cucumber mosaic virus (CMV); Turnip mosaic virus (TuMV); evolution of tolerance; resistance; tolerance-tolerance trade-offs.

Figures

Figure 1.
Figure 1.
Which way to go? According to the life-history theory, hosts would modify their time to reproduction in opposite ways in order to achieve tolerance: when infected by a highly virulent pathogen (red line), hosts would bring forward reproduction to produce progeny before death; and when infected by a low virulent pathogen (blue line), host would delay reproduction so they can reallocate resourced from growth to reproduction. These strategies would maximize fitness in the presence of one virus at the cost of reducing fitness in the presence of the other (crossed dotted lines), establishing a tolerance-tolerance trade-off.
Figure 2.
Figure 2.
Arabidopsis fecundity and mortality tolerance to UK1-TuMV, LS-CMV and JPN1-TuMV. Panel A: values of fecundity tolerance to UK1-TuMV (blue), to JPN1-TuMV (green) and to LS-CMV (red) measured as the slope of the SW to virus accumulation linear regression. Panel B: values of mortality tolerance to the same three viruses measured as the slope of the LP to virus accumulation linear regression. Steeper slopes (lower values) indicate lower tolerance. Data are presented for allometric Groups 1 and 2, and for Subgroups 1a and 1b, and are mean ± standard errors across plant genotypes. Black dots indicate values non-different from zero. Note the different scales for tolerance to TuMV and to CMV.
Figure 3.
Figure 3.
Effect of UK1-TuMV, LS-CMV and JPN1-TuMV infection on life-history traits for Arabidopsis allometric groups and subgroups. (A–C) Effect of viral infection on RW, IW and SW. (D–F) Effect of viral infection on GP, RP and PRP. (G–I) Effect of infection on the ratios IW/RW, SW/RW, RP/GP and PRP/GP. All effects were estimated as the ratio between infected (i) and mock-inoculated (m) plants. Data are presented for allometric Groups 1 and 2, and for Subgroups 1a and 1b, and are mean ± standard errors of plant genotype means. All values were different from zero except IW ratios for Group 1, and Subgroups 1a and 1b, in panel A.
Figure 4.
Figure 4.
Trade-offs between Arabidopsis tolerances to UK1-TuMV, LS-CMV and JPN1-TuMV. (A–C) Pairwise linear regressions between fecundity tolerance to UK1-TuMV, LS-CMV and JPN1-TuMV. (D–F) Pairwise linear regressions between mortality tolerance to UK1-TuMV, LS-CMV and JPN1-TuMV. Data are slope of the SW (fecundity tolerance) and LP (mortality tolerance) to virus accumulation regression for each Arabidopsis genotype. Grey dots correspond to outlier values, which were excluded from the analyses.

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References

    1. Agnew P., Koella J. C., Michalakis Y. (2000) ‘Host Life History Responses to Parasitism’, Microbes and Infection, 2: 891–6. - PubMed
    1. Akiyama R., Ågren J. (2014) ‘Conflicting Selection on the Timing of Germination in a Natural Population of Arabidopsis thaliana’, Journal of Evolutionary Biology, 27: 193–9. - PubMed
    1. Anderson P. K. et al. (2004) ‘Emerging Infectious Diseases of Plants: Pathogen Pollution, Climate Change and Agrotechnology Drivers’, Trends in Ecology & Evolution, 19: 535–44. - PubMed
    1. Antonovics J. (2009) ‘The Effect of Sterilizing Diseases on Host Abundance and Distribution along Environmental Gradients’, Proceedings of the Royal Society B: Biological Sciences, 276: 1443–8. - PMC - PubMed
    1. Bates D. et al. (2015) ‘Fitting Linear Mixed-Effects Models Using lme4’, Journal of Statistic Software, 67: 1–48.
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