Are plant pathogen populations adapted for encounter with their host? A case study of phenological synchrony between oak and an obligate fungal parasite along an altitudinal gradient

Abstract

Biotrophic fungal pathogens are expected to have adapted to their host plants for phenological synchrony, to optimize the possibility of contacts leading to infections. We investigated the patterns and causes of variation in phenological synchrony in the oak‐powdery mildew pathosystem, a major disease in natural ecosystems. The study was carried out along an altitudinal gradient, representing a wide temperature range, in mature oak stands. Both sporulation (pathogen infective stage) and oak flushing (host susceptible stage) were delayed with increasing elevation, but with a significantly different sensitivity for the two species. This resulted in a variable host–pathogen synchrony along the gradient. A common garden experiment did not give evidence of among‐population genetic differentiation (past adaptation) for fungal phenology. This could be explained by the high phenotypic variation in phenology within host populations, precluding selection on fungal phenology at the population scale, but possibly favouring adaptation at the within‐population scale. Phenotypic plasticity was the major cause of the observed variation in the phenology of the fungal populations.

Interspecific and intraspecific diversity in oak powdery mildews in Europe: coevolution history and adaptation to their hosts

“…The occurrence of powdery mildew fungi on the model plant Arabidopsis thaliana has prompted many studies on the plant side but few on pathogen populations (Adam et al 1999;Micali et al 2008). The E. alphitoidesQuercus robur interaction was recently investigated in two studies, in Finland and France (Roslin et al 2007;Marçais et al 2009, Desprez-Loustau et al 2010a. A common objective of these studies was to test the hypothesis of a local adaptation of powdery mildew to its host.…”

“…In temperate regions with strong seasonality, biotrophic foliar pathogens such as powdery mildews are expected to have adapted to their host plants for phenological synchrony to optimize the possibility of contacts leading to infections. The study by Desprez-Loustau et al (2010a) investigated phenological synchrony (flushingascospore dispersal) in the Q. robur-E. alphitoides pathosystem, along an altitudinal gradient in the Pyrenees, with a high phenological variation within and between host populations. Host-pathogen phenological matching was shown to vary between and within sites at different altitudes.…”

European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change

“…Indeed, the peak of ascospore production from chasmothecia, which represent the primary inoculum re-initiating the annual epidemics, was shown to occur up to 30-50 days after budburst of the first oak flush in several French locations Desprez-Loustau et al 2010a). Phenological synchrony between host growth and ascospore production was shown to be an important factor explaining disease severity for Q. petraea (DesprezLoustau et al 2010a).…”

“…Furthermore, disruption in phenological synchrony could occur in some interactions, in particular if both partners do not respond in a similar way to temperature (Van Ash and Visser 2007;Both et al 2009). Indeed, E. alphitoides was shown to respond less strongly to a temperature gradient than its host Q. petraea, resulting in differences in synchrony and disease severity along the gradient (Desprez-Loustau et al 2010a). Increased phenological synchrony might be an explanation for the high report of powdery mildew on mature nondefoliated oaks in southwest France in mild years such as 1990, 2001, and 2007 (see §2.3).…”

Spatial variation in disease resistance: from molecules to metapopulations

“…It has also been suggested that genetic hitchhiking resulting from linkage between resistance genes and other traits under even more intense selection may affect the genetic composition of plant populations, where selection on resistance is swamped by these processes (Burdon & Thompson 1995). Alternatively, disease could impose selection on traits other than resistance, for example on demography or phenology, when larger or earlier emerging plants are more likely to become infectedand may support higher levels of infection,and hence may suffer higher mortality (Burdon & Thompson 1995; Desprez-Loustau et al . 2010).…”