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. 2019 May 28;15(5):e1007810.
doi: 10.1371/journal.ppat.1007810. eCollection 2019 May.

Cucumber Mosaic Virus Infection as a Potential Selective Pressure on Arabidopsis Thaliana Populations

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Free PMC article

Cucumber Mosaic Virus Infection as a Potential Selective Pressure on Arabidopsis Thaliana Populations

Nuria Montes et al. PLoS Pathog. .
Free PMC article

Abstract

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Geographic distribution of Arabidopsis thaliana populations analysed in this study.
Circles indicate population locations. Circles with asterisk indicate the 12 populations used for within/between population analyses, their names appearing next to them.
Fig 2
Fig 2. Variation for resistance and tolerance to CMV in A. thaliana.
Frequency distributions are for accumulation (μg RNA g fresh leaf weight-1) of (A) Cdc-CMV and (B) Lro-CMV RNA, and of the effect of infection by (C) Cdc-CMV and (D) to Lro-CMV on seed production.
Fig 3
Fig 3. Relationships between life-history traits and geographic or climatic factors.
Correlations are shown (A, B, C) for rosette weight (RW), (D, E, F) inflorescence weight (IW), (G, H, I) seed weight (SW) and (J, K, L) growth period (GP) with altitude, annual mean temperature and precipitation seasonality. Values are means of at least five replicates per plant genotype.
Fig 4
Fig 4. Variation for resistance and tolerance to CMV within and among wild A. thaliana populations.
Frequency distributions of resistance (virus accumulation, μg RNA g fresh leaf weight-1) and tolerance (SWi/SWm) to Cdc-CMV (blue) and Fny-CMV (red). Three-letter code for each population is as in Fig 1.
Fig 5
Fig 5. Genetic differentiation among wild A. thaliana populations for CMV resistance and tolerance traits, or for neutral markers.
Fig shows values of quantitative genetic differentiation (QST) for resistance (squares) and tolerance (triangles), to Cdc-CMV (blue) or Fny-CMV (red), and for neutral genetic differentiation (FST) (black circle), among ten A. thaliana populations. 95%CI are indicated.

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References

    1. Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet. 2002; 32: 569–577. 10.1038/ng1202-569 - DOI - PubMed
    1. Agnew P, Koella JC, Michalakis Y. Host life history responses to parasitism. Microb Infect. 2000; 2: 891–896. - PubMed
    1. Råberg L. How to Live with the Enemy: Understanding Tolerance to Parasites. PLoS Biol. 2014; 12: e1001989 10.1371/journal.pbio.1001989 - DOI - PMC - PubMed
    1. Pagán I, García-Arenal F. Tolerance to plant pathogens: theory and experimental evidences. Int J Mol Sci. 2018; 19: 810. - PMC - PubMed
    1. Fraile A, García-Arenal F. The coevolution of plants and viruses: Resistance and pathogenicity. Adv Virus Res. 2010; 76: 1–32. 10.1016/S0065-3527(10)76001-2 - DOI - PubMed

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Grant support

This work was funded by grants BFU2015-64018-R (Plan Estatal de I+D+i, MINECO, Spain) to FGA, and BIO2016-75754-P (Agencia Estatal de Investigación, Spain and FEDER, UE) to CAB. NM was in receipt of a FPI contract (BES-2009-026698) from MEC, Spain. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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