Brachypodium HISTONE DEACETYLASE 19.1 promotes yield, flowering, and freezing tolerance at the expense of drought tolerance

Antagonistic pleiotropy can lead to tradeoffs whereby changes at a single locus positively and negatively affect two fitness traits, respectively. In plants, hormone signaling genes are good candidates for such pleiotropy, as they often work at the expense of alternative hormone pathways. In Arabidopsis thaliana, HISTONE DEACETYLASE 19 (HDA19) stimulates growth at the expense of drought tolerance by repressing the brassinosteroid (BR) pathway. To determine if orthologous genes in grasses function in a similar manner, we characterized one of two HDAC19 genes in the temperate model grass Brachypodium distachyon. Partially supporting a molecular tradeoff in growth and reproduction versus drought tolerance, hdac19.1 mutants were late flowering and shorter with smaller/lighter seed under control conditions and proportionally larger with higher survival under drought conditions. Mutants also showed reduced growth sensitivity to brassinolide treatment. Evidence of weaker antagonistic pleiotropy was found between drought and freezing tolerance, in line with previous studies showing a tradeoff between these stressors in Pooideae grasses. By modulating brassinosteroid responsiveness, HDAC19.1 appears to act as a molecular lever governing the tradeoff between growth, reproductive output and freezing tolerance versus drought tolerance.