Utilizing MutS HOMOLOG 1 (MSH1) Derived Epigenetic Variation in Breeding for Yield and Stress Adaptability

Plant responses to a multitude of environmental changes have potential adaptive and agronomic benefits. The epigenetic component of this response is not well understood, but dynamic methylome changes may contribute towards modulating stress-responsive gene regulation and potentially give rise to transgenerational epigenetic information. Down-regulation of a nuclear-encoded gene MutS HOMOLOG 1 (MSH1) causes similar developmental phenotypes in multiple crop species accompanied by modulation of defense, phytohormone, stress responsive gene expression and heritable changes in DNA methylation patterns. In Arabidopsis T-DNA MSH1 mutants, strong phenotypes emerge after two generations of homozygosity and transcript profiling identified pathways associated with phytohormone signaling, abiotic and biotic stress responses, photosynthetic function, and circadian rhythm. Consistent with gene expression changes, mutants display enhanced tolerance for abiotic stress including drought and salt stress, while showing susceptibility to freezing stress and bacterial pathogen Pseudomonas syringae. Under prolonged cold stress, msh1 display increased variation in DNA methylation, particularly CHH hypomethylation in the heterochromatin. Interestingly, this increased variation in non-CG methylation pattern divergence does not seem to have any significant effect on the previously described msh1-derived enhanced growth after mutants are crossed with isogenic wild type, emphasizing the role of CG methylation changes in msh1 derived enhanced vigor. RNAi suppression of the MSH1 in soybean produces a wide range of developmental changes including dwarfing, delayed flowering and crinkled leaves. These msh1 developmentally reprogrammed phenotypes are independent of transgene segregation, giving rise to transgene-null memory lines. Crossing these memory lines to wild type produces increased variation in adaptive traits that respond to selection. Selected epi-lines show an increase in yield up to 14% and show evidence of reduced epitype-by- environment interaction, indicating higher yield stability. Transcriptome profiling of epi-lines identified putative signatures of enhanced growth behavior across generations. Sucrose biosynthesis and auxin-responsive genes, particularly SMALL AUXIN UP RNAs (SAURs) were differentially expressed in epi-F2:4 lines that showed increased yield when compared to epi-F2:6. Taken together, these data support the utility of MSH1-derived epigenetic variation in plant breeding for enhanced yield and yield stability