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Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host.

Pagán I, Montes N, Milgroom MG, García-Arenal F - PLoS Pathog. (2014)

Bottom Line: For the last three decades, evolutionary biologists have sought to understand which factors modulate the evolution of parasite virulence.Although theory has identified several of these modulators, their effect has seldom been analysed experimentally.This result is consistent with plant-virus co-evolution.

View Article: PubMed Central - PubMed

Affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA) and Departamento de Biotecnología, Campus Montegancedo, Universidad Politécnica de Madrid. Pozuelo de Alarcón, Madrid, Spain.

ABSTRACT
For the last three decades, evolutionary biologists have sought to understand which factors modulate the evolution of parasite virulence. Although theory has identified several of these modulators, their effect has seldom been analysed experimentally. We investigated the role of two such major factors-the mode of transmission, and host adaptation in response to parasite evolution-in the evolution of virulence of the plant virus Cucumber mosaic virus (CMV) in its natural host Arabidopsis thaliana. To do so, we serially passaged three CMV strains under strict vertical and strict horizontal transmission, alternating both modes of transmission. We quantified seed (vertical) transmission rate, virus accumulation, effect on plant growth and virulence of evolved and non-evolved viruses in the original plants and in plants derived after five passages of vertical transmission. Our results indicated that vertical passaging led to adaptation of the virus to greater vertical transmission, which was associated with reductions of virus accumulation and virulence. On the other hand, horizontal serial passages did not significantly modify virus accumulation and virulence. The observed increases in CMV seed transmission, and reductions in virus accumulation and virulence in vertically passaged viruses were due also to reciprocal host adaptation during vertical passages, which additionally reduced virulence and multiplication of vertically passaged viruses. This result is consistent with plant-virus co-evolution. Host adaptation to vertically passaged viruses was traded-off against reduced resistance to the non-evolved viruses. Thus, we provide evidence of the key role that the interplay between mode of transmission and host-parasite co-evolution has in determining the evolution of virulence.

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Related in: MedlinePlus

Bivariate analyses between seed transmission, virus accumulation and virulence across passages of vertical transmission.Significant regressions of seed transmission rate on virus accumulation (A), seed transmission rate on virulence (one minus the ratio of seed weight in infected to mock-inoculated plants, 1−[SWi/SWm]) (B), and virulence on virus accumulation (C), for each virus strain: Fny-CMV (blue squares), De72-CMV (red triangle) and LS-CMV (green diamonds). Note the different scales depending on the trait and the virus strain.
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ppat-1004293-g003: Bivariate analyses between seed transmission, virus accumulation and virulence across passages of vertical transmission.Significant regressions of seed transmission rate on virus accumulation (A), seed transmission rate on virulence (one minus the ratio of seed weight in infected to mock-inoculated plants, 1−[SWi/SWm]) (B), and virulence on virus accumulation (C), for each virus strain: Fny-CMV (blue squares), De72-CMV (red triangle) and LS-CMV (green diamonds). Note the different scales depending on the trait and the virus strain.

Mentions: The analyses above strongly suggest that increases in seed transmission rate might be accompanied by reductions in virus accumulation and virulence. To explore this relationship, we analysed the association between these traits during the serial vertical transmission passages considering all strains together and independently (Figure 3). Regression analyses indicated that the seed transmission rate was negatively (exponentially) correlated with virus accumulation for all strains together (r = −0.32; P = 0.005) and separately (r≤−0.40; P≤0.049) (Figure 3a). In addition, seed transmission rate was also negatively (linearly) correlated with virulence in all CMV strains (r≤−0.56; P≤0.006) (Figure 3b). Finally, virus accumulation and virulence were always positively (exponentially) correlated (r≥0.45; P≤0.034) (Figure 3c). Overall, these results indicate that the increase of seed transmission rate through vertical passages is associated with a reduction of virus accumulation and virulence in Arabidopsis. These changes might be due to virus evolution and/or host evolution. In the next sections we address these possibilities.


Vertical transmission selects for reduced virulence in a plant virus and for increased resistance in the host.

Pagán I, Montes N, Milgroom MG, García-Arenal F - PLoS Pathog. (2014)

Bivariate analyses between seed transmission, virus accumulation and virulence across passages of vertical transmission.Significant regressions of seed transmission rate on virus accumulation (A), seed transmission rate on virulence (one minus the ratio of seed weight in infected to mock-inoculated plants, 1−[SWi/SWm]) (B), and virulence on virus accumulation (C), for each virus strain: Fny-CMV (blue squares), De72-CMV (red triangle) and LS-CMV (green diamonds). Note the different scales depending on the trait and the virus strain.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4117603&req=5

ppat-1004293-g003: Bivariate analyses between seed transmission, virus accumulation and virulence across passages of vertical transmission.Significant regressions of seed transmission rate on virus accumulation (A), seed transmission rate on virulence (one minus the ratio of seed weight in infected to mock-inoculated plants, 1−[SWi/SWm]) (B), and virulence on virus accumulation (C), for each virus strain: Fny-CMV (blue squares), De72-CMV (red triangle) and LS-CMV (green diamonds). Note the different scales depending on the trait and the virus strain.
Mentions: The analyses above strongly suggest that increases in seed transmission rate might be accompanied by reductions in virus accumulation and virulence. To explore this relationship, we analysed the association between these traits during the serial vertical transmission passages considering all strains together and independently (Figure 3). Regression analyses indicated that the seed transmission rate was negatively (exponentially) correlated with virus accumulation for all strains together (r = −0.32; P = 0.005) and separately (r≤−0.40; P≤0.049) (Figure 3a). In addition, seed transmission rate was also negatively (linearly) correlated with virulence in all CMV strains (r≤−0.56; P≤0.006) (Figure 3b). Finally, virus accumulation and virulence were always positively (exponentially) correlated (r≥0.45; P≤0.034) (Figure 3c). Overall, these results indicate that the increase of seed transmission rate through vertical passages is associated with a reduction of virus accumulation and virulence in Arabidopsis. These changes might be due to virus evolution and/or host evolution. In the next sections we address these possibilities.

Bottom Line: For the last three decades, evolutionary biologists have sought to understand which factors modulate the evolution of parasite virulence.Although theory has identified several of these modulators, their effect has seldom been analysed experimentally.This result is consistent with plant-virus co-evolution.

View Article: PubMed Central - PubMed

Affiliation: Centro de Biotecnología y Genómica de Plantas (UPM-INIA) and Departamento de Biotecnología, Campus Montegancedo, Universidad Politécnica de Madrid. Pozuelo de Alarcón, Madrid, Spain.

ABSTRACT
For the last three decades, evolutionary biologists have sought to understand which factors modulate the evolution of parasite virulence. Although theory has identified several of these modulators, their effect has seldom been analysed experimentally. We investigated the role of two such major factors-the mode of transmission, and host adaptation in response to parasite evolution-in the evolution of virulence of the plant virus Cucumber mosaic virus (CMV) in its natural host Arabidopsis thaliana. To do so, we serially passaged three CMV strains under strict vertical and strict horizontal transmission, alternating both modes of transmission. We quantified seed (vertical) transmission rate, virus accumulation, effect on plant growth and virulence of evolved and non-evolved viruses in the original plants and in plants derived after five passages of vertical transmission. Our results indicated that vertical passaging led to adaptation of the virus to greater vertical transmission, which was associated with reductions of virus accumulation and virulence. On the other hand, horizontal serial passages did not significantly modify virus accumulation and virulence. The observed increases in CMV seed transmission, and reductions in virus accumulation and virulence in vertically passaged viruses were due also to reciprocal host adaptation during vertical passages, which additionally reduced virulence and multiplication of vertically passaged viruses. This result is consistent with plant-virus co-evolution. Host adaptation to vertically passaged viruses was traded-off against reduced resistance to the non-evolved viruses. Thus, we provide evidence of the key role that the interplay between mode of transmission and host-parasite co-evolution has in determining the evolution of virulence.

Show MeSH
Related in: MedlinePlus