Organellar signaling expands plant phenotypic variation and increases the potential for breeding the epigenome

MUTS HOMOLOGUE 1 (MSH1) is a nuclear gene unique to plants that functions in mitochondria and plastids, where it confers genome stability. Phenotypic effects of MSH1 down- regulation were studied in sorghum inbreed line Tx430 and Arabidopsis ecotype Columbia-0, with the hypothesis that RNAi suppression of MSH1 triggers retrograde signaling from organelles to the nucleus, alters the epigenome, and derives heritable phenotypic variation suitable for artificial selection. An array of morphological traits and metabolic pathways was detected, including leaf variegation, male sterility and dwarfism, associated with altered gibberellic acid metabolism, higher levels of reactive oxygen species (ROS), and decreased synthesis of ATP. A phenotype that combines dwarf, increased branching, reduced stomatal density and delayed flowering was identified, and designated developmental reprogrammed (MSH1-dr). Reproducible in additional plant species, this phenotypic variation is partially reversed by exogenous GA. In sorghum, the phenotype displays complete penetrance under self-pollination, even after segregation of the transgene, whereas progeny of MSH1-dr transgene null plants x wildtype Tx430 display enhanced growth. Significant differences for agronomic traits and response to selection were observed in the tested F2 to F 4 generations, with mean values that surpass the wildtype up to 70% for grain yield/panicle and plant height, and 100% for biomass yield/plant. SSR marker analyses among the parental phenotypes Tx430 and MSH1-dr transgene null, and their derived lines, show no polymorphism, suggesting that the observed changes are non-genetic. In Arabidopsis, this enhanced growth is accompanied by genome methylation changes, whereas genetic hemi-complementation indicates that the novel phenotype results from chloroplast disruption