Breakdown of scavina resistance in Bahia caused by the evolution of Moniliophthora perniciosa

Abstract

Resistant clones to witches' broom disease of cacao (WBD), caused by the basidiomycete fungus Moniliophthora perniciosa (Mp) is the most practical and cost efficient strategy for WBD management, but their use is currently restricted to very limited clones, mostly, Scavina's descendants. Scavina resistance has proved inadequate or unstable, as, for example, in Rondônia in the Amazon basin, in Ecuador during the 1980s, and in Bahia in 2002. In this paper, we present evidences, through several independent studies, that the Scavinas' resistance have been overcome because of changes in the pathogen population. Using molecular markers in studies of 40 isolates of the fungus, collected from brooms from five resistant and two susceptible cocoa genotypes, a clear genetic differentiation was observed between fungal isolates from primarily resistant clones and from susceptible ones. Further, a study carried out to characterize temporal genetic variability of Mp populations in Bahia, Brazil, over four consecutive years (2001 to 2004), in several locations, have shown that there was a shift in the genetic composition of the Mp populations. Pathogenic variability through cross inoculation experiments using -isolates derived from Scavinas (Scavina 6 and descendants), non scavina, and from SIC, a susceptible clone, showed that Scavina isolates caused more disease on the Scavinas genotypes, whereas the isolate derived from SIC was less pathogenic on the Scavinas and more pathogenic on its respective host. These results allowed us to conclude that the increase in susceptibility in Scavina descendants was the result of the buildup of resistance-breaking pathogen's strains capable of overcoming the resistance of Scavina. Also, temporal observations of natural infections between 2003 and 2010 in a F2 Scavina 6 x ICS1 showed that the major QTL identified in the LG9 had its effect decreased year by year; moving from a LOD of 9 in 2003 to a non significant LOD in 2010. The same results were found under artificial inoculations with specific strains of Mp and using a new F2 population created in 2007. The present study provides the first evidences that Scavinas WB resistance breakdown is due to the adaptation of the Mp field populations. These studies, besides proving the change in the Mp population in Bahia, they are also a warning call that the efficiency of resistant cultivars in WBD management is limited by Mp variability and an incentive to design breeding programs for durable resistance. Different sources of resistance have been identified and are being used in the cacao breeding program to associate distinct genes of resistance. (Résumé d'auteur