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Repeat-Induced Point Mutation (RIP) as an Alternative Mechanism of Evolution Toward Virulence in Leptosphaeria maculans

August 2009 , Volume 22 , Number  8
Pages  932 - 941

Isabelle Fudal,1 Simon Ross,1 Hortense Brun,2 Anne-Laure Besnard,2 Magali Ermel,2 Marie-Line Kuhn,1 Marie-Hélène Balesdent,1 and Thierry Rouxel1

1INRA UMR 1290 BIOGER-CPP, F-78026 Versailles, France; 2UMR BIO3P, INRA, F- 35653 Le Rheu, France

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Accepted 21 March 2009.

Three avirulence genes, AvrLm1, AvrLm6, and AvrLm4-7, were recently identified in Leptosphaeria maculans and found to be localized as solo genes within large noncoding, heterochromatin-like regions mainly composed of retrotransposons, truncated and degenerated by repeat-induced point mutation (RIP). The Rlm6 resistance gene has been overcome within 3 years in outdoor experiments in France and, here, we investigate the molecular basis of evolution toward virulence at the AvrLm6 locus. A region of 235 kb was sequenced in a virulent isolate and showed the deletion of AvrLm6 and three divergent mosaics of retrotransposons. AvrLm6 was found to be absent from 66% of 70 virulent isolates, with multiple events of deletion. The sequencing of virulent alleles in 24 isolates revealed a few cases of point mutations that had created stop codons in the sequence. The most frequent mutation events, however, were RIP, leading to the modification of 4 to 9% of the bases compared with the avirulent allele and generating 2 to 4 stop codons. Thus, RIP is described for the first time as an efficient mechanism leading to virulence and the multiple patterns of mutation observed suggest that multiple RIP events could occur independently in a single field population during 1 year.

© 2009 The American Phytopathological Society