Nearly all plants play host to a myriad of parasites. They can suffer from bacterial, viral and fungal attack, but fungal parasites are by far the most prevalent plant pathogenic organism. Over 20,000 species of fungi are parasites and cause disease in crops and plants. Parasitic fungi require a living host to survive. This forces them to achieve a delicate balance, extracting enough nutrients to ensure their own survival but not so much that they kill the plant. Common plant fungi such as powdery mildews, rusts and smuts require a living plant to sustain them.
The genomes of the hemibiotrophic (Magnaporthe oryzae, Leptopshaeria maculans, Fusarium spp., Mycosphaerella spp.) and necrotrophic (Stagnospora nodorum, Botrytis cinerea, Nectria haematoccoca), fungal plant pathogens have been released at a regular pace over the last five years and allowed a better understanding of the evolution of pathogenesis. These studies highlighted the value of comparative genomics in identifying important virulence genes with host-specific functions. Given that almost nothing is known about the molecular basis or evolution of obligate biotrophy in plant pathogens, the recent publication of papers describing the genomes of three pathogens representing two independent evolutions of obligate biotrophy in the powdery mildews [Blumeria graminis, Spanu et al. (2010)] and the rusts [Puccinia graminis f. sp tritici & Melampsora larici-populina, Duplessis et al. (2011)] is a key step in our understanding of plant-pathogen interactions.
The genome analysis of the barley powdery mildew (Blumeria graminis) revealed a genome size expansion caused by transposon proliferation concomitant with a striking reduction in gene content, i.e., genes encoding sugar-cleaving enzymes, transporters and assimilatory enzymes for inorganic nitrate and sulfur (Spanu et al., 2010). To identify the genetic idiosyncrasies underlying pathogenesis and biotrophic ability of rust pathogens, we have analyzed the genome sequences of the rust fungi M. larici-populina and P. graminis f. sp. tritici. in a joint collaboration between the JGI and the MIT Broad Institute (see my previous post). Our comparisons of M. larici-populina and P. graminis f. sp. tritici to other saprotrophic, pathogenic, and symbiotic basidiomycetes indicate that developmental innovations in the rust fungi lineages did not involve major changes in the ancestral repertoire of conserved proteins with known function. However, gene family expansions observed for oligopeptide transporters, auxin efflux carriers and signaling elements could reflect specific adaptations to this extreme parasitic lifestyle of these fungi. No massive gene loss was observed in M. larici-populina and P. graminis f. sp. tritici,
However, our comparisons of these three genomes with genomes from non-obligate fungal relatives have confirmed several startling commonalities amongst powdery mildews and rusts:
- Dramatic reduction of plant cell-wall degrading enzymes and other pathogenicity genes (i.e., evolution for “stealth”).
- Loss of sulphite and nitrite assimilation genes (i.e., metabolic dependency on the host).
- The massive proliferation of (retro)transposable elements which lead to significant enlargement of the overall genome size (the increase in genetic, heritable variability may confers an adaptive advantage to obligate life on a live host).
- The deployment of large arrays of secreted effector proteins that act within and outside of host cells to counteract plant immunity and may facilitate other processes that are integral to survival within a hostile host.
Our study on the wheat and poplar rusts is the latest in a series of papers that investigates genomic attributes of biotrophy in obligate plant parasites. Another recent works focused on the oomycete Hyaloperonospora arabidopsidis, which causes downy mildew of Arabidopsis (Baxter et al., 2010). Interestingly, the genomic features discussed above were also identified in this non-fungal lineage. Collectively, these draft genomes of these microbial parasites thus provided the first opportunity to gain insight into the genomic signatures and convergent evolution of obligate biotrophy.
A series of papers describing the transcriptome and secretome of the poplar rust will soon be published. Now, it remains to determine the role of hundreds of effector-like secreted proteins released in planta by M. larici-populina and P. graminis.
John McDowell’s comparison of our and Pietro’s papers appears as an invited Commentary in the PNAS early edition published online the week of May 16.
Duplessis et al. (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Ntl Acad Sci USA, Published online before print May 2, 2011, doi:10.1073/pnas.1019315108.
Spanu et al. (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330: 1543–1546.
Baxter et al. (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549-1551.
McDowell JM (2011) Genomes of obligate plant pathogens reveal adaptations for obligate parasitism. Proc Ntl Acad Sci USA, doi:10.1073/pnas.1105802108, published ahead of print May 16, 2011.
Photo: A poplar leaf infected by the leaf rust M. larici-populina (© F Martin).