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1. Water deficit changes the relationships between epidemiological traits of Cauliflower mosaic virus across diverse Arabidopsis thaliana accessions

Author

Sandy E. Bergès, Denis Vile, Michel Yvon, Diane Masclef, Myriam Dauzat, and Manuella van Munster

Subjects
Medicine, Science
Abstract

Abstract Changes in plant abiotic environments may alter plant virus epidemiological traits, but how such changes actually affect their quantitative relationships is poorly understood. Here, we investigated the effects of water deficit on Cauliflower mosaic virus (CaMV) traits (virulence, accumulation, and vectored-transmission rate) in 24 natural Arabidopsis thaliana accessions grown under strictly controlled environmental conditions. CaMV virulence increased significantly in response to water deficit during vegetative growth in all A. thaliana accessions, while viral transmission by aphids and within-host accumulation were significantly altered in only a few. Under well-watered conditions, CaMV accumulation was correlated positively with CaMV transmission by aphids, while under water deficit, this relationship was reversed. Hence, under water deficit, high CaMV accumulation did not predispose to increased horizontal transmission. No other significant relationship between viral traits could be detected. Across accessions, significant relationships between climate at collection sites and viral traits were detected but require further investigation. Interactions between epidemiological traits and their alteration under abiotic stresses must be accounted for when modelling plant virus epidemiology under scenarios of climate change.

Published
2021
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2. Natural variation of Arabidopsis thaliana responses to Cauliflower mosaic virus infection upon water deficit.

Author

Sandy E Bergès, François Vasseur, Alexis Bediée, Gaëlle Rolland, Diane Masclef, Myriam Dauzat, Manuella van Munster, and Denis Vile

Subjects
Immunologic diseases. Allergy, RC581-607, Biology (General), QH301-705.5
Abstract

Plant virus pathogenicity is expected to vary with changes in the abiotic environment that affect plant physiology. Conversely, viruses can alter the host plant response to additional stimuli from antagonism to mutualism depending on the virus, the host plant and the environment. Ecological theory, specifically the CSR framework of plant strategies developed by Grime and collaborators, states that plants cannot simultaneously optimize resistance to both water deficit and pathogens. Here, we investigated the vegetative and reproductive performance of 44 natural accessions of A. thaliana originating from the Iberian Peninsula upon simultaneous exposure to soil water deficit and viral infection by the Cauliflower mosaic virus (CaMV). Following the predictions of Grime's CSR theory, we tested the hypothesis that the ruderal character of a plant genotype is positively related to its tolerance to virus infection regardless of soil water availability. Our results showed that CaMV infection decreased plant vegetative performance and annihilated reproductive success of all accessions. In general, water deficit decreased plant performance, but, despite differences in behavior, ranking of accessions tolerance to CaMV was conserved under water deficit. Ruderality, quantified from leaf traits following a previously published procedure, varied significantly among accessions, and was positively correlated with tolerance to viral infection under both well-watered and water deficit conditions, although the latter to a lesser extent. Also, in accordance with the ruderal character of the accession and previous findings, our results suggest that accession tolerance to CaMV infection is positively correlated with early flowering. Finally, plant survival to CaMV infection increased under water deficit. The complex interactions between plant, virus and abiotic environment are discussed in terms of the variation in plant ecological strategies at the intraspecific level.

Published
2020
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3. Leaf economics and slow-fast adaptation across the geographic range of Arabidopsis thaliana

Author

Marianne Gerard, Kevin Sartori, Oscar Javier Ayala-Garay, Etienne Baron, Laura Garcia de Jalon, Maria Del Rey Granado, Agathe Chassagneux, Elena Kazakou, Denis Vile, François Vasseur, Diane Masclef, Nick P. Rowe, Cyrille Violle, Ananda Christophe, Erwan Harscouet, Maladies infectieuses et vecteurs : écologie, génétique, évolution et contrôle (MIVEGEC), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Écophysiologie des Plantes sous Stress environnementaux (LEPSE), Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro), Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD [France-Sud]), AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Botanique et Modélisation de l'Architecture des Plantes et des Végétations (UMR AMAP), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut National de la Recherche Agronomique (INRA)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD [France-Sud]), INRA Dpt EA grant, European Research Council (ERC) (‘CONSTRAINTS’: grant ERC-StG-2014-639706-CONSTRAINTS), French Agency for Research (ANR grant ANR-17-CE02-0018-01, ‘AraBreed’), ANR-17-CE02-0018,AraBreed,Exploration des réponses évolutives des plantes à des changements environnementaux à la lumière des théories écologiques : un test expérimental chez l'espèce modèle Arabidopsis thaliana(2017), European Project: 609398,EC:FP7:PEOPLE,FP7-PEOPLE-2013-COFUND,AGREENSKILLSPLUS(2014), European Project: 639706,H2020,ERC-2014-STG,CONSTRAINTS(2015), Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Université Paul-Valéry - Montpellier 3 (UM3)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Université Paul-Valéry - Montpellier 3 (UPVM)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École Pratique des Hautes Études (EPHE), and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)

Subjects
0301 basic medicine, allocation de ressources, media_common.quotation_subject, Biodiversité et Ecologie, Arabidopsis, lcsh:Medicine, Biology, Plant Physiological Phenomena, Article, Life history theory, Biodiversity and Ecology, adaptation au climat, 03 medical and health sciences, Plant evolution, 0302 clinical medicine, écologie fonctionnelle, Plant ecology, lcsh:Science, media_common, 2. Zero hunger, Functional ecology, Multidisciplinary, Ecology, Geography, arabidopsis thaliana, fungi, lcsh:R, Longevity, Ecological genetics, food and beverages, Interspecific competition, 15. Life on land, Arid, Plant Leaves, 030104 developmental biology, Natural variation in plants, Habitat, comparaison intraspécifique, 13. Climate action, lcsh:Q, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Slow Growing, 030217 neurology & neurosurgery
Abstract

International audience; Life history strategies of most organisms are constrained by resource allocation patterns that follow a 'slow-fast continuum'. It opposes slow growing and long-lived organisms with late investment in reproduction to those that grow faster, have earlier and larger reproductive effort and a short longevity. In plants, the Leaf Economics Spectrum (LES) depicts a leaf-level trade-off between the rate of carbon assimilation and leaf lifespan, as stressed in functional ecology from interspecific comparative studies. However, it is still unclear how the LES is connected to the slow-fast syndrome. Interspecific comparisons also impede a deep exploration of the linkage between Les variation and adaptation to climate. Here, we measured growth, morpho-physiological and life-history traits, at both the leaf and whole-plant levels, in 378 natural accessions of Arabidopsis thaliana. We found that the Les is tightly linked to variation in whole-plant functioning, and aligns with the slow-fast continuum. A genetic analysis further suggested that phenotypic differentiation results from the selection of different slow-fast strategies in contrasted climates. slow growing and long-lived plants were preferentially found in cold and arid habitats while fast growing and short-lived ones in more favorable habitats. Our findings shed light on the role of the slow-fast continuum for plant adaptation to climate. More broadly, they encourage future studies to bridge functional ecology, genetics and evolutionary biology to improve our understanding of plant adaptation to environmental changes. Investigations of the genetic and phenotypic differentiation of plant lineages along environmental gradients is crucial for the understanding of plant evolutionary responses to current and future climate variations. As plants cannot simultaneously optimize competing eco-physiological functions, an important question is how plant adaptation occurs under the influence of major trade-offs between traits. The slow-fast continuum is a pervasive trade-off between resource allocation to growth, reproduction and survival , spread across the tree of life 1. The slow end of this continuum is characterized by slow growing, long-lived species and low reproductive output, while species at the fast end reach reproductive maturity faster and produce more offsprings. In plants, the leaf economics spectrum (LES hereafter) 2-4 is thought to reflect the physiological basis of the slow-fast continuum 4. The LES arrays plant species along a continuum of leaf trait syndromes going from short-lived leaves with fast metabolism to the reverse syndrome 3. Core LES traits include leaf dry mass per area (LMA), leaf lifespan (LLS) and net photosynthetic rate per mass unit (A mass) 3,5-7. LES traits are widely used in comparative ecology to infer whole-plant ecological strategies 4,8-12. However, the extent to which leaf-level resource economics reflects whole-plant physiology, performance, and ultimately fitness, is still under debate 13. Many processes can lead to a mismatch between LES and whole-plant functioning 14 , including the impact of self-shading among leaves and resource allocation patterns, such as carbon investment in non-photosynthetic tissues 15,16. To gain insights into the robustness of the slow-fast continuum at different organizational levels, we need

Published
2019

4. Leaf economics guides slow-fast adaptation across the geographic range of A. thaliana

Author

Erwan Harscouet, Denis Vile, François Vasseur, Agathe Chassagneux, Etienne Baron, Kevin Sartori, Maria Del Rey Granado, Oscar J. Ayala-Garay, Cyrille Violle, Diane Masclef, Nick P. Rowe, Ananda Christophe, Marianne Gerard, Elena Kazakou, Laura Garcia de Jalon, Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry - Montpellier 3 (UPVM)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Écophysiologie des Plantes sous Stress environnementaux (LEPSE), Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), INRA, CNRS, European Research Council (ERC) (‘CONSTRAINTS’: grant ERC-StG-2014-639706-CONSTRAINTS, European Project: 609398,EC:FP7:PEOPLE,FP7-PEOPLE-2013-COFUND,AGREENSKILLSPLUS(2014), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD [France-Sud]), Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)

Subjects
0106 biological sciences, Genetic differentiation, 010603 evolutionary biology, 01 natural sciences, Genetic analysis, Plant adaptation, Carbon assimilation, Relative growth rate, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, Arabidopsis thaliana, Life history, 2. Zero hunger, Continuum (measurement), biology, Intraspecific variability, Plant performance, fungi, food and beverages, 15. Life on land, biology.organism_classification, Eco-physiological trade-off, Evolutionary biology, Trait, Plant functional trait, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, Adaptation, 010606 plant biology & botany
Abstract

SummaryThe slow-fast continuum describes how resource allocation constrains life-history strategies in many organisms. In plants, it is reflected by a trade-off at the leaf level between the rate of carbon assimilation and lifespan, the so-called Leaf Economics Spectrum (LES). However, it is still unclear how the LES is connected to the slow-fast syndrome, and reflects adaptation to climate. Here, we measured growth, morpho-physiological and life-history traits at both leaf and whole-plant levels in 384 natural accessions of Arabidopsis thaliana. We examined the extent to which the LES continuum parallels the slow-fast continuum, and compared trait variation to neutral genetic differentiation between lineages. We found that the LES is tightly linked to variation in whole-plant functioning, relative growth rate and life history. A genetic analysis further suggested that phenotypic differentiation is linked to the evolution of different slow-fast strategies in contrasted climates. Together, our findings shed light on the physiological bases of the slow-fast continuum, and its role for plant adaptation to climate.

Published
2018
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