MicroRNA172 plays a critical role in wheat spike morphogenesis and grain threshability

Authors: DEBERNARDI, JUAN - University Of California, Davis; LIN, HUIQIONG - University Of California, Davis; CHUCK, GEORGE - University Of California; Faris, Justin; DUBCOVSKY, JORGE - University Of California, Davis

Submitted to: Development
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2017
Publication Date: 5/4/2017
Publication URL: https://handle.nal.usda.gov/10113/5801902
Citation: Debernardi, J.M., Lin, H., Chuck, G., Faris, J.D., Dubcovsky, J. 2017. MicroRNA172 plays a critical role in wheat spike morphogenesis and grain threshability. Development. 144:1966-1975.

Interpretive Summary: Wheat domestication from wild species involved mutations in the Q gene. Wild, undomesticated wheats have a primitive form of the Q gene that renders the grains non-free-threshing, meaning that the seeds are not easily separated from the hulls. About 10,000 years ago, mutations in the Q gene occurred that altered its function and led to free-threshing grains. However, previous studies have indicated that multiple mutations have occurred within the gene, and they have not conclusively demonstrated which of the mutation(s) were responsible for acquisition of the free-threshing trait, and thus the domestication of wheat. Here we show that one mutation in the Q gene that interacts with a secondary molecule known as microRNA172 (miR172) plays a critical role in determining expression of traits associated with development and domestication. The inhibition of miR172 activity led to overexpression of the Q gene and associated traits, whereas overexpression of miR172 led to under-expression of Q and traits similar to those observed in wild wheats with the primitive form of the gene. We propose that the selection of the Q gene mutation at the miR172 binding site responsible for free-threshing grains led to fully domesticated wheat.

Technical Abstract: Wheat domestication from wild species involved mutations in the Q gene. The q allele (wild wheats) is associated with elongated spikes and hulled grains, whereas the mutant Q allele (domesticated wheats) confers subcompact spikes and free-threshing grains. Previous studies showed that Q encodes an AP2-like transcription factor, but the causal polymorphism of the domestication traits remained unclear. Here we show that the interaction between microRNA172 (miR172) and the Q allele is reduced by an SNP in the miRNA binding site. The inhibition of miR172 activity by a miRNA target mimic resulted in compact spikes and transition from glumes to florets in distal spikelets. By contrast, overexpression of miR172 was sufficient to induce elongated spikes and non-free-threshing grains, similar to those observed in three Q loss-of-function mutations. These lines showed transitions from florets to glumes in the basal spikelets. These localized homeotic changes were associated with opposing miR172/ Q gradients along the spike. We propose that the selection of a nucleotide change at the miR172 binding site contributed to subcompact spikes and free-threshing grains during wheat domestication.