A Tale Of Three Phytopathogens: Impact Of Transposable Elements On Genome Evolution

Date

2010-07-19

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Biology

Abstract

The genus Phytophthora harbors some notorious plant pathogens like Phytophthora infestans (causal of Irish potato famine), Phytophthora sojae (soybean rot agent), and Phytophthora ramorum (responsible for sudden oak death) that have significant economic, ecological and environmental impact. These phytopathogens exhibit remarkable phenotypic instability and vary tremendously in genome size from 65 Mb (P. ramorum) to 240 Mb (P. infestans). Complete draft genome sequences revealed that a substantial portion of their genome is occupied by highly repetitive DNA. This extreme genome plasticity is due to an infestation of repetitive virus-like genomic parasites called transposable elements (TEs). TEs are sometimes called jumping genes due to their capacity to move from one place to another in the genome. TEs are usually perceived as potent mutagens and the result of their proliferation in genome is usually detrimental, although occasionally they can contribute to the evolution of the host in a variety of ways. One such mechanism is transduplication, whereby TEs capture host gene fragments, that is known to give rise to novel genes in plants. Pathogens are in a constant arms race due to their reliance on the host to reproduce and persist and the negative fitness that they impart. Therefore, it was hypothesized that the plastic P. infestans genome allows for a rapid response to the ever-changing environment imposed by this evolutionary arms race. To this end, we have employed bioinformatics tools (RepeatScout, RepeatMasker, BLAST tools) to identify different superfamilies of TEs and assess their distribution across three Phytophthora species. Much to our surprise, we found 21 TE families carrying host genes accounting for 2.4% of the P. infestans genome. Overall, we observe a strong preference of TEs to capture genes that are involved in epigenetic regulation and critical in plant pathogenesis cycle. We report on the detailed structure of these transduplicates and their capacity to encode a functional transposase. Our results show capture of whole cellular genes by TEs and the existence of transcript evidence for the genes captured. This observed pattern of transduplication is different from what is known in plants and other species, where the capture involves gene fragments that are usually pseudogenized. Moreover, detailed analysis of the captured genes show retention of introns confirming that the transduplication events occurred at a DNA level. Cross species and molecular phylogenetic analyses further reveal that a few capture events might have predated the split of P. infestans from P. sojae and P. ramorum. Hereby, we present an in-depth analysis of various transduplication events and the impact they had in shaping the evolutionary trajectory of these phytopathogens.

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