Cereal Killers Thomas D

NEWS & ANALYSIS GENOME WATCH Cereal killers Thomas D. Otto and Adam J. Reid This month’s Genome Watch traces the B. graminis f. sp. hordei and compared them molecular trick to further characterize the evolutionary history of powdery mildew to an existing reference sequence3. In both role of effectors in host–pathogen interac- and highlights the ‘arms race’ of this wheat and barley pathogens, which are sepa- tions. The model plant Arabidopsis thaliana is fungal pathogen with its wheat and barley rated by ~6.3 million years of evolution, the usually resistant to B. graminis, but knock- hosts. genomes display a mosaic of evolutionarily ing out three immune defence genes makes it young and old haplotypes (regions with rela- susceptible to infection. Resistance can then Blumeria graminis is a widespread plant path- tively few SNPs and regions with many SNPs, be reconsituted by supplying the mildew ogen that causes powdery mildew in grasses, respectively). Younger parts of the genome resistance locus A 1 (MLA1) gene from bar- including wheat, barley and other cereals. diverged around 10,000 years ago, coinciding ley. By analysing the transcriptomes of the Two recent studies have examined the evo- with the domestication of the wheat and bar- host and the pathogen, the authors identified lution of B. graminis to reveal high genetic ley hosts, whereas older parts diverged more two waves of effector gene expression: a first adaptibility and flexibility, which enable than 100,000 years ago during the last ice age, wave during penetration of the plant epider- this fungus to infect a range of hosts and to when wild cereals were locally confined. mis and a second during formation of the overcome host defences. Both studies suggest that B. graminis haustorium (which is a fungal appendage that Powdery mildew fungi are grouped into populations maintain a high level of genetic takes up nutrients from the plant). When the so-called formae speciales (f. sp.) according variation by clonal propagation and infre- fungus tried to invade the resistant MLA1- to their respective host species. Wicker et al.1 quent sexual reproduction, thus only rarely expressing A. thaliana, the second wave of sequenced and assembled the genome of breaking up combinations of potentially ben- effector genes was downregulated, whereas B. graminis f. sp. tritici, which infects wheat, eficial alleles that would otherwise be lost by plant defence genes were upregulated. and compared isolates from different coun- recombination during meiosis. Other crop Interestingly, the effector genes expressed at tries, whereas Hacquard et al.2 pathogens such as potato blight have under- this stage — early in haustorium formation sequenced two isolates of gone substantial diversifying selection fol- — are those under the greatest selective pres- the barley pathogen lowing host domestication. The modern sure, which suggests that this is a key phase of forms of B. graminis, however, can still host–pathogen interactions. infect wild cereals and their genomes These findings provide insight into the do not show signs of the diversity- ease with which powdery mildew fungi have reducing genetic bottlenecks associated adapted to infect domesticated cereals and with speciation. give us clues as to how we might combat them Many parasitic organisms have a in the future to improve food security. range of effector proteins to mediate, for Thomas D. Otto and Adam J. Reid are at the example, host entry, immune evasion Sanger Institute, Wellcome Trust Genome Campus, and nutrient acquisition. Both studies Hinxton, Cambridge CB10 1SA, UK. indicate that the effector repertoire of e‑mail: [email protected] B. graminis is under positive selec- doi:10.1038/nrmicro3144 tive pressure with effector genes 1. Wicker, T. et al. The wheat powdery mildew genome among the most polymorphic shows the unique evolution of an obligate biotroph. genes in the genome. This is sug- Nature Genet. 45, 1092–1096 (2013). 2. Hacquard, S. et al. Mosaic genome structure of the gestive of an ‘arms race’ in which barley powdery mildew pathogen and conservation of the fungus must constantly transcriptional programs in divergent hosts. Proc. Natl Acad. Sci. USA 110, E2219– E2228 (2013). diversify its ‘weaponry’ when 3. Spanu, P. D. et al. Genome expansion and gene loss in the plant becomes powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543–1546 (2010). NPG resistant to effectors. H a c q u a r d Competing interests statement et al.2 used a clever The authors declare no competing financial interests. 744 | NOVEMBER 2013 | VOLUME 11 www.nature.com/reviews/micro © 2013 Macmillan Publishers Limited. All rights reserved.

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