A stepwise route to domesticate rice by controlling seed shattering and panicle shape

Abstract

Asian rice (<i>Oryza sativa</i> L.) is consumed by more than half of the world's population. Despite its global importance, the process of early rice domestication remains unclear. During domestication, wild rice (<i>Oryza rufipogon</i> Griff.) acquired non-seed-shattering behavior, allowing humans to increase grain yield. Previous studies argued that a reduction in seed shattering triggered by the <i>sh4</i> mutation led to increased yield during rice domestication, but our experiments using wild introgression lines show that the domesticated <i>sh4</i> allele alone is insufficient for shattering loss in <i>O</i>. <i>rufipogon</i>. The interruption of abscission layer formation requires both <i>sh4</i> and <i>qSH3</i> mutations, demonstrating that the selection of shattering loss in wild rice was not as simple as previously suggested. Here we identified a causal single-nucleotide polymorphism at <i>qSH3</i> within the seed-shattering gene <i>OsSh1</i>, which is conserved in <i>indica</i> and <i>japonica</i> subspecies but absent in the <i>circum</i>-aus group of rice. Through harvest experiments, we further demonstrated that seed shattering alone did not significantly impact yield; rather, yield increases were observed with closed panicle formation controlled by <i>SPR3</i> and further augmented by nonshattering, conferred by integration of <i>sh4</i> and <i>qSH3</i> alleles. Complementary manipulation of panicle shape and seed shattering results in a mechanically stable panicle structure. We propose a stepwise route for the earliest phase of rice domestication, wherein selection of visible <i>SPR3</i>-controlled closed panicle morphology was instrumental in the sequential recruitment of <i>sh4</i> and <i>qSH3</i>, which together led to the loss of shattering.