Auxin regulates source-sink carbohydrate partitioning and reproductive organ development in rice

Abstract

Carbohydrate partitioning between the source and sink tissues plays an important role in regulating plant growth and development. However, the molecular mechanisms regulating this process remain poorly understood. In this study, we show that elevated auxin levels in the rice <i>dao</i> mutant cause increased accumulation of sucrose in the photosynthetic leaves but reduced sucrose content in the reproductive organs (particularly in the lodicules, anthers, and ovaries), leading to closed spikelets, indehiscent anthers, and parthenocarpic seeds. RNA sequencing analysis revealed that the expression of <i>AUXIN RESPONSE FACTOR 18</i> (<i>OsARF18</i>) and <i>OsARF2</i> is significantly up- and down-regulated, respectively, in the lodicule of <i>dao</i> mutant. Overexpression of <i>OsARF18</i> or knocking out of <i>OsARF2</i> phenocopies the <i>dao</i> mutant. We demonstrate that OsARF2 regulates the expression of <i>OsSUT1</i> through direct binding to the sugar-responsive elements (SuREs) in the <i>OsSUT1</i> promoter and that OsARF18 represses the expression of <i>OsARF2</i> and <i>OsSUT1</i> via direct binding to the auxin-responsive element (AuxRE) or SuRE in their promoters, respectively. Furthermore, overexpression of <i>OsSUT1</i> in the <i>dao</i> and <i>Osarf2</i> mutant backgrounds could largely rescue the spikelets' opening and seed-setting defects. Collectively, our results reveal an auxin signaling cascade regulating source-sink carbohydrate partitioning and reproductive organ development in rice.