Christophe Le May

Diversification at the plot level, through the use of intercropping (mixtures of crops), is an alternative to the conventional system of intensive agriculture, based on monospecific, usually single-variety canopies. Intercropping has been shown to provide benefits in terms of disease control. However, competition phenomena and the heterogeneity of the associated crops raise new ecological questions, particularly with regard to the dynamics and evolution of parasite populations. No study has assessed the potential impact of these associations on the dynamics of pathogenic species complexes. Changes in the nutritional status of plants and therefore in their physiological susceptibility to infection within intercropping systems could contribute to an increased diversity of ecological niches and thus affect the composition of the parasitic complex and its spatiotemporal dynamics. In this review, focusing on foliar diseases of fungal origin, and after outlining some elements of the biology and epidemiology of these fungal diseases, we will (i) describe the mechanisms that contribute to the composition of disease clusters and that drive interactions, but we will also review the strategies that these foliar diseases have adopted to deal with these co-infections; (ii) define how intercropping can lead to changes in epidemic dynamics, in particular by presenting the mechanisms that have a direct and indirect effect on disease evolution; and (iii) present the approach that should be adopted to properly study intercropping correctly in a multi-infection situation.

Introduction: Aphanomyces euteiches Drechsler is an oomycete pathogen that affects legume crops, causing root rot, a severe disease of peas (Pisum sativum L.) worldwide. While significant research progress has been made in breeding pea-resistant varieties, there is still a need for a deeper understanding of the diversity of pathogen populations present in breeding nurseries located in various legume-growing regions around the world.Methods: We analysed the diversity of 51 pea-infecting isolates of A. euteiches, which were recovered from four American (Athena, OR; Le Sueur, MN; Mount Vernon, WA; Pullman, WA) and three French (Riec-sur-Belon, Templeux-le-Guérard, Dijon) resistance screening nurseries. Our study focused on evaluating their aggressiveness on two sets of differential hosts, comprising six pea lines and five Medicago truncatula accessions.Results: The isolates clustered into three groups based on their aggressiveness on the whole pea set, confirming the presence of pathotypes I and III. Pathotype I was exclusive to French isolates and American isolates from Athena and Pullman, while all isolates from Le Sueur belonged to pathotype III. Isolates from both pathotypes were found in Mount Vernon. The M. truncatula set clustered the isolates into three groups based on their aggressiveness on different genotypes within the set, revealing the presence of five pathotypes. All the isolates from the French nurseries shared the same Fr pathotype, showing higher aggressiveness on one particular genotype. In contrast, nearly all-American isolates were assigned to four other pathotypes (Us1, Us2, Us3, Us4), differing in their higher aggressiveness on two to five genotypes. Most of American isolates exhibited higher aggressiveness than French isolates within the M. truncatula set, but showed lower aggressiveness than French isolates within the P. sativum set.Discussion: These results provide valuable insights into A. euteiches pathotypes, against which the QTL and sources of resistance identified in these nurseries displayed effectiveness. They also suggest a greater adaptation of American isolates to alfalfa, a more widely cultivated host in the United States.

Multiple infections, either simultaneous or sequential, affecting a single plant or crop are now recognized to be common in plant disease epidemics. These multiple infections thus generate a range of competitive interactions (exploitation competition, apparent competition, or interference competition) that directly impact competitors’ life history traits, and hence fitness. While a theoretical framework, based primarily on three ecological theories—niche exclusion, the “tragedy of the commons”, and the virulence–transmission trade‐off, provides insights into potential outcomes of multiple infections on pathogen evolution and virulence and on disease dynamics, experimental observations, although rather rare so far, strongly suggest that unexpected outputs can also occur. This review therefore attempts to provide a comprehensive overview of both theoretical and empirical knowledge about multiple infection in plants. It highlights the need for a detailed assessment of pathogen life history traits and their modulation according to competition types, host receptivity, and pathogen life strategies for a better understanding and prediction of the evolutionary and demographic outcomes of multiple infections, as well as research questions still open in this emerging field of plant pathology.

Aphanomyces root rot is a major disease in many pea growing regions worldwide. Development of resistant varieties is necessary to manage the disease. Near isogenic lines (NILs) carrying resistance alleles at main quantitative trait loci (QTLs) were developed by marker-assisted backcrossing. This study aimed to evaluate the aggressiveness of diverse French isolates of Aphanomyces euteiches on NILs carrying different resistance QTLs. Forty-three A. euteiches isolates from different French pea growing regions were tested for aggressiveness on eight NILs carrying single or combinations of resistance QTLs and two susceptible or resistant control lines, in controlled conditions. Three clusters of isolates, unrelated to geographical origin, were identified, including 37, 56, and 7% of isolates with high, moderate, and low average levels of aggressiveness, respectively. Three groups of pea lines were also identified. The first group consisted of a pea resistant control line, moderately to highly resistant to all of the isolates. The second group included five NILs carrying a major-effect resistance allele at QTL Ae-Ps7.6, with a medium to broad range of effects on the isolates. The third group consisted of three NILs carrying minor-effect resistance alleles, with a narrow range of effects on the isolates. The results suggest that highly aggressive isolates occur naturally, which may be selected by future partially resistant pea varieties carrying QTLs and increase the risk of erosion of QTL effect. QTL pyramiding strategies for a higher level and a broader range of effect of quantitative resistance on A. euteiches populations will be required for breeding for durable pea resistant varieties.

Multi‐infections may result in either competitive exclusion or coexistence on the same host of pathogen genotypes belonging to the same or different species. Epidemiological consequences of multiple infections, particularly how the development and transmission of a pathogen can be modified by the presence of another pathogen, are well documented. However, understanding how life history strategies of each pathogen modulate co‐infection outcomes remains quite elusive. To analyze how co‐infection drives changes in life history traits and affects co‐existence in epidemic pathogens, we infected detached pea stipules with two fungal species, Peyronellaea pinodes and Phoma medicaginis var. pinodella (considering two strains per species), part of the ascochyta blight complex but presenting different life history strategies. All pairwise combinations (including self‐pairs) between two strains of each species were tested. Strains were inoculated simultaneously, but apart from one another on the stipule. For each strain, four life history traits were measured: incubation period, necrosis area six days after inoculation, latent period and offspring production. Results show that, in co‐infection, when resources are highly allocated to lesion development, the time between inoculation and the appearance of reproduction structures (latent period) and offspring production decreased, and vice‐versa relative to single infections. The direction and/or magnitude of these responses to co‐infection depend on the co‐infecting strains. Moreover, these changes were always higher in self‐pairs than in mixed co‐infections. These results suggest facilitation between co‐infecting strains, resulting in the selection of an intermediate level of virulence (here measured as the lesion development) at the expense of pathogen offspring production. This strategy allows the development and reproduction of each co‐infecting strain when sharing limited resources. However, the direction and strength of these life history traits variations in co‐infection depend on the life history strategy of the co‐infecting strains, with a clear difference between ‘opportunists', ‘scavengers' and ‘pioneer colonisers'.

Plant disease complexes are a playground to investigate coinfections in natural or cultivated systems. Pathogens of such complexes may affect each other through direct and/or indirect interactions and lead to changes in virulence or aggressiveness, offspring production, and transmission. As coinfections by sympatric host‐pathogens can strongly influence pathogen dynamics and their evolutionary trajectories, new insights into the mechanisms of their coexistence is thus of critical importance. In order to characterize differences in ecological niches liable to explain species coexistence on the same host, the inter‐ and intraspecific diversity of the life history traits in natural collections of the two main pathogens ( Peyronellaea (formerly Didymella ) pinodes [Dp] and Phoma medicaginis var. pinodella [Pmp]) of the ascochyta blight disease complex of pea was evaluated under controlled conditions. Dp strains developed 1.3 times faster and produced longer, mainly bicellular spores and in lower amounts (3.7 times less) than Pmp strains. Pmp strains were separated into two groups, one producing more pycnidiospores, mainly bicellular, with less resources, and the other with mainly unicellular ones. These three groups can be interpreted as three distinct life history strategies: pioneer colonizer (Dp), scavenger (large‐spored Pmp), and intermediate (small‐spored Pmp), allowing differentiation in access to and use of resources. While this experimental work provides new insight into coexistence of two species of the ascochyta blight disease complex of pea, it also raises the question of the benefit of having two distinct life history strategies for one species (Pmp).

Aphanomyces euteiches is a polyphagous, homothallic soilborne pathogen producing asexual (zoospores) and sexual (oospores) spores. Even if oospores are essential for disease development and survival, to date, no study has focused on the production rates of oospores or the quality of the offspring produced by oospores. In this study, a nonabrasive oospore extraction method from infected roots of leguminous species (pea, faba bean and vetch) was developed. This methodology includes steps of grinding and filtration. The quality of oospores (viable, dormant and dead) was assessed with tetrazolium bromide staining, and germination of oospores was tested using exudates of peas, faba bean and vetch. The average yield of the extraction method was approximately 21%. Staining revealed some differences between strains and between leguminous species. The germination percentage of oospores extracted from pea, faba bean and vetch was 25%, 62% and 70%, respectively, and a significant difference was observed according to the origin of A. euteiches‐inoculated strains. Application of exudates seems to stimulate the germination of oospores (2% for the control, 18% for pea exudates and 1% for vetch exudates). Differences observed between A. euteiches strains and leguminous species indicate that more knowledge concerning the biology of oospores is needed. This will help to better estimate evolution process of the pathogen and manage resistance and crop successions.