Genetic and archaeological evidence indicates that cereal agriculture, including wheat (Triticum aestivum
) and rye (Secale cereale
) cultivation, originated in the Fertile Crescent 10,000 to 12,000
years ago [1
]. Since then, the nature of the agro-ecosystem itself has played a critical part in the emergence and spread of plant pathogens, by providing a more dense and genetically uniform host population [2
]. An example of such a plant pathogen is Blumeria graminis
, the causal agent of powdery mildew in cereals. This pathogen is a major problem in cereal production as it can reduce quality and yield [3
]. Management of the disease normally involves the use of fungicides, but this adds considerably to the cost of grain production.
is an obligate biotrophic fungus which implies that it depends on living plant cells for survival and reproduction. Penetration and biotrophic colonization of a plant is the result of highly specific recognition mechanisms in the gene-for-gene response involving avirulence (AVR
)- and resistance genes [5
]. Most known AVR
genes encode effectors that facilitate pathogenicity by suppressing pathogen-associated molecular pattern-triggered immunity which can result in the induction of effector-triggered immunity [6
]. Two AVR
genes have been isolated from B. graminis
and both have effector activity [8
]. The fungus also has a huge repertoire of homologues of these genes, which may function as effectors and contribute to parasite aggressiveness [10
In the long run, this mutual close interplay can result in co-evolution of host and pathogen. In this way, B. graminis
has evolved eight distinct formae speciales
(f.sp.) which display strict host specialization [11
]. For example, Triticum
spp. and Secale
spp. are appropriate hosts to B.g.
, respectively. Conversely, if plants are attacked by inappropriate formae speciales
, attempts to infect and colonize the plant will fail [13
Multilocus phylogenetic analysis identified lineages, closely matching the formae speciales
defined on the basis of host specialization [14
]. Additionally, Sacristan et al. [10
] found that B. graminis
avirulence genes (AVRk1
paralogs) have evolved differentially in the different formae speciales
and that the phylogeny of AVRa10
-like sequences corresponds with those of other genes. In particular, B.g.
are phylogenetically the most closely related formae speciales
In the last decade, several studies tried to tackle the co-evolutionary relationship of the different formae speciales
with their hosts [14
]. These studies resulted in a wide range of divergence time estimates between the different formae speciales
, which reflects the challenges to calculate an accurate divergence time of this pathogen. However, all these studies state that the divergence of the different formae speciales
is likely to be younger than the divergence of their hosts. This type of co-evolution is called host-tracking in contrast to co-speciation, where host and pathogen have diverged simultaneously [2
]. In spite of the discrepancy between divergence time of host and pathogen, Wyand and Brown [14
] concluded that the center of diversity of B. graminis
coincides with the center of origin of their hosts in the Middle East.
Triticale (× Triticosecale
Wittmack) is the intergeneric hybrid between the female parent wheat (Triticum
ssp.) and the male parent rye (Secale
ssp.). The aim of this hybrid breeding was to combine the cold and disease tolerance of rye and its adaption to unfavorable soils and climates with the productivity and nutritional qualities of wheat [16
]. This artificial cereal is, in contrast to wheat and rye, of very recent origin and was commercialized at the end of the 1960’s [19
]. During the last decade, triticale has gained considerable importance in Europe, as its production area has nearly doubled since 2000 (up to almost 3.6 million ha in 2009, [21
]). However, with the expansion of the triticale growing area, powdery mildew emerged on this new host and became a significant disease on triticale. This was simultaneously observed in several European countries, including Belgium, France and Poland [16
]. Recent research demonstrated that this powdery mildew on triticale has emerged most probably through a host range expansion of the wheat powdery mildew B.g.
]. This means that powdery mildew has evolved the capacity to colonize a new host species, triticale, which is phylogenetically closely related to its present host wheat.
Host range expansions are expected to occur rather frequently, because only a few modifications in the effector repertoire of the pathogen can suffice to adapt to a closely related plant species [22
]. Moreover, pathogen species with a large and diversified composition of effectors, which holds true for powdery mildew [23
], should have a higher chance to increase their host range [22
This study was initiated to gain more precise information about the evolutionary processes that led to this host range expansion. To address this question, we pursued a combined pathological and genetic approach. Powdery mildew isolates on triticale, wheat and rye were sampled from different breeding areas in Europe. Old isolates from the Middle East, the proposed centre of origin of cereals and B. graminis, were also included in this study, in order to be able to put the results in an evolutionary perspective. The first objective was to assess the host specificity and to determine the virulence profile of the powdery mildew populations on different hosts and regions in Europe. Documenting the true host range and virulence profile of this recently emerged pathogen is an important first step towards understanding the ecological context in which it has evolved. The second objective was to clarify the phylogenetic relationships and population structure of this recently emerged pathogen. We hypothesized that (i) the triticale powdery mildew population is structured by geography, host species or both and (ii) genetic diversity is higher in the wheat powdery mildew populations than in the recently emerged triticale powdery mildew populations.