Virulence determines beneficial trade‐offs in the response of virus‐infected plants to drought via induction of salicylic acid

It has been hypothesized that plants can get beneficial trade‐offs from viral infections when grown under drought conditions. However, experimental support for a positive correlation between virus‐induced drought tolerance and increased host fitness is scarce. We investigated whether increased virul...

Full description

Saved in:
Bibliographic Details
Published in:Plant, cell and environment cell and environment, 2017-12, Vol.40 (12), p.2909-2930
Main Authors: Aguilar, Emmanuel, Cutrona, Carmen, Toro, Francisco J., Vallarino, José G., Osorio, Sonia, Pérez‐Bueno, María Luisa, Barón, Matilde, Chung, Bong‐Nam, Canto, Tomás, Tenllado, Francisco
Format: Article
Language:English
Subjects:
Abscisic acid
Abscisic Acid - metabolism
Arabidopsis
Arabidopsis - physiology
Arabidopsis - virology
Arabidopsis thaliana
Correlation
Drought
Drought resistance
Environmental impact
Fitness
Flowers & plants
host fitness
Host plants
Hypotheses
Infections
Mutation
Nicotiana - physiology
Nicotiana - virology
Nicotiana benthamiana
Offsets
Offspring
Plant Diseases - virology
Plant growth
Plant Growth Regulators - metabolism
Plant Transpiration - physiology
Plant viruses
Plants (botany)
Plum pox
Plum pox virus
Plum Pox Virus - pathogenicity
Plum Pox Virus - physiology
Potato virus X
Potatoes
Potexvirus - pathogenicity
Potexvirus - physiology
Reproductive fitness
Salicylic acid
Salicylic Acid - metabolism
Seeds - physiology
Seeds - virology
Stress, Physiological
Tradeoffs
Transpiration
Viral infections
Virulence
Viruses
virus‐induced drought tolerance
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Description
Summary:It has been hypothesized that plants can get beneficial trade‐offs from viral infections when grown under drought conditions. However, experimental support for a positive correlation between virus‐induced drought tolerance and increased host fitness is scarce. We investigated whether increased virulence exhibited by the synergistic interaction involving Potato virus X (PVX) and Plum pox virus (PPV) improves tolerance to drought and host fitness in Nicotiana benthamiana and Arabidopsis thaliana. Infection by the pair PPV/PVX and by PPV expressing the virulence protein P25 of PVX conferred an enhanced drought‐tolerant phenotype compared with single infections with either PPV or PVX. Decreased transpiration rates in virus‐infected plants were correlated with drought tolerance in N. benthamiana but not in Arabidopsis. Metabolite and hormonal profiles of Arabidopsis plants infected with the different viruses showed a range of changes that positively correlated with a greater impact on drought tolerance. Virus infection enhanced drought tolerance in both species by increasing salicylic acid accumulation in an abscisic acid‐independent manner. Viable offspring derived from Arabidopsis plants infected with PPV increased relative to non‐infected plants, when exposed to drought. By contrast, the detrimental effect caused by the more virulent viruses overcame potential benefits associated with increased drought tolerance on host fitness. It has been hypothesized that tolerance of virus‐infected plants to abiotic stresses is a conditional phenotype that could act as a pay‐off that offsets the detrimental effect of virus infection on plant fitness. However, this might not be the case if fitness costs associated with virulence outweigh the beneficial effects conferred by stress tolerance on plant growth. We experimentally tested the hypothesis that virus infection would increase the reproductive fitness of Arabidopsis thaliana and Nicotiana benthamiana under variable drought conditions. Our results challenge the general validity of the hypothesis that viruses behave as conditionally beneficial to their hosts and emphasize the need of considering the effect of virulence in the analysis of plant responses to combined abiotic and biotic stress.
ISSN:0140-7791
1365-3040
DOI:10.1111/pce.13028