Pathogenic characteristics of isolates of

Aphanomyces euteiches from pea in France

E. Wicker

, M. Hullé

and F.Rouxel

a Union Nationale Interprofessionnelle des Plantes riches en Protéines (UNIP) – 12, Avenue Georges V, 75008 Paris

b Unité Mixte de Recherche INRA-ENSAR 'Biologie des Organismes et des Populations appliquée à la Protection des Plantes' - INRA –Centre de recherches de Rennes - Domaine de La Motte- BP 35327- 35653 Le Rheu Cédex, France

*To whom correspondence should be addressed

Email: wicker@rennes.inra.fr

Running title : Pathogenicity of Aphanomyces euteiches isolates on Legumes

Keywords: epidemiology, Fabacae, host specificity, Oomycota, pea common root rot, soilborne disease

ABSTRACT

Aphanomyces root rot (Aphanomyces euteiches) has become a very destructive disease in French pea crops since 1993. The host specificity of the French pea–infecting populations of this pathogen was investigated by inoculating pea, common vetch, alfalfa, broad bean and green bean with 91 pea-infecting A.euteiches isolates, originating from the main areas of infestation in France. These isolates were compared to 13 isolates from various countries and hosts (pea, green bean, alfalfa). Virulence phenotypes were defined according to the pathogenicity data on the different hosts: all isolates from France infected two to five legume species, with most infecting pea, vetch, alfalfa and broad bean. Four pathotypes were characterised within the French isolates: one type corresponded to broad-host range isolates, the second was composed of isolates preferentially agressive on pea/vetch/alfalfa and weakly aggressive on broad bean, and two others corresponding to more specialised isolates that preferentially infected pea/vetch or pea/vetch/alfalfa. Most isolates from France were preferentially pathogenic on pea, like the pea-infecting isolates from other countries, but were less specialised than the alfalfa- and green bean-infecting isolates from other countries. These results suggest that A. euteiches isolates may be maintained on wild or cultivated legumes other than pea in France.

INTRODUCTION

Aphanomyces euteiches, a soilborne oomycete, was described in 1925 as the causal agent of a soft root rot that affected pea crops (Pisum sativum) in Wisconsin, USA (Jones & Drechsler, 1925). It was considered to be primarily a pea root pathogen (Scott, 1961). More recently, A. euteiches has been identified in many other regions of the Midwestern, Central and Northwestern States of the USA (Holub et al., 1991; Kraft & Boge, 1994); Canada (Basu et al., 1973), Europe (Persson et al., 1997), Australia (Allen et al., 1987), New Zealand (Manning & Menzies, 1980) and Asia (Yokosawa et al., 1974), causing heavy losses, primarily on pea crops.

Several authors also reported A. euteiches to be a pathogen of alfalfa (Medicago

sativa) (Greenhalgh & Merriman, 1985), green bean (Phaseolus vulgaris) (Pfender &

pratense (Tofte et al., 1992), Trifolium subterraneum (Burnett et al., 1994)). Many control

measures have been tested (Papavizas & Ayers, 1974), but the only efficient way to control the disease identified to date is to avoid planting peas in contaminated fields and to ensure that there is an appropriate time interval between successive pea crops in the rotation (Carrouée et al., 1995).

Although it was first identified in France as early as 1933 (Labrousse, 1933), A.

euteiches has caused major losses in pea crops only since 1993 (Didelot & Chaillet, 1995),

probably due to the intensification of the spring pea crop from the 1980s, and climatic conditions very favourable to the disease (mild and wet springs). Initially affected areas were clustered and limited in extent (2 to 5 % of the total area under pea), in the Parisian Basin (Carrouée et al., 1995; Maufras et al., 1997), but the disease has since occurred in other regions (Brittany, Rhone-Alpes). To date however, A.euteiches has never been reported for any other crop, although many other legumes were cultivated in France before the expansion of the pea crop, and some are still cultivated in rotation with pea in some regions (e.g. pea-green bean rotations in Brittany and Picardy, pea-alfalfa rotations in Champagne).

This raises the question as to how this soilborne fungus, not expected to migrate over long distances (Papavizas & Ayers, 1974) (for example from the USA or even Scandinavia to France), developed epidemics so quickly in different parts of the country. A. euteiches can survive in the soil for up to 10 years (Papavizas & Ayers, 1974), in the form of oospores, which can withstand unfavourable conditions (e.g. dessication, freezing). It may also be maintained on one or several alternative hosts. Many species are infected by A. euteiches (Papavizas & Ayers, 1974), including weeds and pasture legumes that are colonised without symptoms (Chan & Close, 1987). However, these plants have not been clearly demonstrated to play a role in maintaining the fungus and renewing the inoculum.

Thus, several questions concerning the epidemiology of this disease in France remain unanswered. It is possible that there is a single population of A. euteiches which, although evident only on pea, has a much broader host range, and is harboured by various wild or cultivated legume species. Alternatively, there may be different subpopulations with different host specificities or host ranges, one of which has been favoured and selected by the recent shorter pea rotations.

Experimental evidence supporting this second hypothesis has been provided by the results of Malvick et al. (1998) in the Midwestern United States. Four genotypically and phenotypically different subpopulations were distinguished: 'alfalfa/red clover', 'alfalfa', 'green bean', 'non-pathogenic'. However, the differences between subpopulations were not large enough for them to be considered different formae speciales, (except for the 'green bean' subpopulation assimilated into f. sp. phaseoli). Moreover, the isolates pathogenic on pea (f. sp. pisi as defined by Pfender & Hagedorn (1982)) were not genotypically clustered together. The existence of different subpopulations may have major consequences in soils with A.

euteiches, in which growers are advised to replace pea by broad bean. To date, broad bean has

displayed complete field resistance to the pathogen, but it may maintain a proportion of the A.

euteiches population, or enable the pathogen to adapt to this new host.

The objectives of this work were: (i) to determine the degree of specialisation of the French populations of A. euteiches, (ii) to determine whether they are pathogenic on legume species other than pea and whether there are host preference groups and (iii) to compare these isolates with reference isolates from other countries.