Esca grapevine disease involves leaf hydraulic failure and represents a unique premature senescence process

Tree Physiology, vol. 43, pp. 441–451

Abstract

Xylem anatomy may change in response to environmental or biotic stresses. Vascular occlusion, an anatomical modification of mature xylem, contributes to plant resistance and susceptibility to different stresses. In woody organs, xylem occlusions have been examined as part of the senescence process, but their presence and function in leaves remain obscure. In grapevine, many stresses are associated with premature leaf senescence inducing discolorations and scorched tissue in leaves. However, we still do not know whether the leaf senescence process follows the same sequence of physiological events and whether leaf xylem anatomy is affected in similar ways. In this study, we quantified vascular occlusions in midribs from leaves with symptoms of the grapevine disease esca, magnesium deficiency and autumn senescence. We found higher amounts of vascular occlusions in leaves with esca symptoms (in 27% of xylem vessels on average), whereas the leaves with other symptoms (as well as the asymptomatic controls) had far fewer occlusions (in 3% of vessels). Therefore, we assessed the relationship between xylem occlusions and esca leaf symptoms in four different countries (California in the USA, France, Italy and Spain) and eight different cultivars. We monitored the plants over the course of the growing season, confirming that vascular occlusions do not evolve with symptom age. Finally, we investigated the hydraulic integrity of leaf xylem vessels by optical visualization of embolism propagation during dehydration. We found that the occlusions lead to hydraulic dysfunction mainly in the peripheral veins compared with the midribs in esca symptomatic leaves. These results open new perspectives on the role of vascular occlusions during the leaf senescence process, highlighting the uniqueness of esca leaf symptoms and its consequence on leaf physiology.

Authors 9

1. Giovanni Bortolami Aachen Naturalis Biodiversity Center

   Naturalis Biodiversity Center · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Santé et Agroécologie du Vignoble

   Affiliation as printed

   INRAE, BSA, ISVV, SAVE , 33882 Villenave d’Ornon , France

   Naturalis Biodiversity Center , PO Box 9517, 2300 RA Leiden, Th e Netherlands

2. Nathalie Ferrer

   Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Santé et Agroécologie du Vignoble

   Affiliation as printed

   INRAE, BSA, ISVV, SAVE , 33882 Villenave d’Ornon , France

3. Kendra Baumgartner

   Agricultural Research Service · United States Department of Agriculture

   Affiliation as printed

   Crops Pathology and Genetics Research Unit United States Department of Agriculture-Agricultural Research Service, , Davis, CA 95616 , USA

4. Sylvain Delzon

   Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · UMR BIOdiversity, GEnes & Communities

   Affiliation as printed

   Univ. Bordeaux, INRAE, BIOGECO , 33615 Pessac , France

5. David Gramaje

   Consejo Superior de Investigaciones Científicas · Universidad de La Rioja · Instituto de Ciencias de la Vid y del Vino

   Affiliation as printed

   University of La Rioja and Government of La Rioja Institute of Grapevine and Wine Sciences (ICVV), Spanish National Research Council (CSIC), , Logroño 26007 , Spain

6. Laurent J. Lamarque

   Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · UMR BIOdiversity, GEnes & Communities · Université du Québec à Trois-Rivières

   Affiliation as printed

   Univ. Bordeaux, INRAE, BIOGECO , 33615 Pessac , France

   Université du Québec à Trois-Rivières, Trois-Rivières Département des Sciences de l’Environnement, , Québec, G9A 5H7 , Canada

7. Gianfranco Romanazzi

   Marche Polytechnic University

   Affiliation as printed

   Marche Polytechnic University Department of Agricultural, Food and Environmental Sciences, , Ancona , Italy

8. Gregory Alan Gambetta

   Université de Bordeaux · Ecophysiologie et Génomique Fonctionnelle de la Vigne · Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · École Nationale Supérieure des Sciences Agronomiques de Bordeaux-Aquitaine

   Affiliation as printed

   EGFV, Bordeaux-Sciences Agro, INRAE, Université de Bordeaux, ISVV , 33882 Villenave d’Ornon , France

9. Chloé E. L. Delmas corresponding

   Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement · Santé et Agroécologie du Vignoble

   Affiliation as printed

   INRAE, BSA, ISVV, SAVE , 33882 Villenave d’Ornon , France