Blocking IbmiR319a Impacts Plant Architecture and Reduces Drought Tolerance in Sweet Potato

MicroRNA319 (miR319) plays a key role in plant growth, development, and multiple resistance by repressing the expression of targeted TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) genes. Two members, IbmiR319a and IbmiR319c, were discovered in the miR319 gene family in sweet potato (Ipomoea batatas [L.] Lam). Here, we focused on the biological function and potential molecular mechanism of the response of IbmiR319a to drought stress in sweet potato. Blocking IbmiR319a in transgenic sweet potato (MIM319) resulted in a slim and tender phenotype and greater sensitivity to drought stress. Microscopic observations revealed that blocking IbmiR319a decreased the cell width and increased the stomatal distribution in the adaxial leaf epidermis, and also increased the intercellular space in the leaf and petiole. We also found that the lignin content was reduced, which led to increased brittleness in MIM319. Quantitative real-time PCR showed that the expression levels of key genes in the lignin biosynthesis pathway were much lower in the MIM319 lines than in the wild type. Ectopic expression of IbmiR319a-targeted genes IbTCP11 and IbTCP17 in Arabidopsis resulted in similar phenotypes to MIM319. We also showed that the expression of IbTCP11 and IbTCP17 was largely induced by drought stress. Transcriptome analysis indicated that cell growth-related pathways, such as plant hormonal signaling, were significantly downregulated with the blocking of IbmiR319a. Taken together, our findings suggest that IbmiR319a affects plant architecture by targeting IbTCP11/17 to control the response to drought stress in sweet potato.