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 dao 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 AUXIN RESPONSE FACTOR 18 ( OsARF18 ) and OsARF2 is significantly up- and down-regulated, respectively, in the lodicule of dao mutant. Overexpression of OsARF18 or knocking out of OsARF2 phenocopies the dao mutant. We demonstrate that OsARF2 regulates the expression of OsSUT1 through direct binding to the sugar-responsive elements (SuREs) in the OsSUT1 promoter and that OsARF18 represses the expression of OsARF2 and OsSUT1 via direct binding to the auxin-responsive element (AuxRE) or SuRE in their promoters, respectively. Furthermore, overexpression of OsSUT1 in the dao and Osarf2 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.

Biosynthesis‐ and transport‐mediated dynamic auxin distribution during seed development controls seed size in Arabidopsis

“…A previous study suggested that auxin might regulate sucrose phloem unloading during rice seed development (Deng et al., 2021). Another recent study further demonstrated that the rice auxin signaling components OsARF2 and OsARF18 directly regulate the expression of the sucrose transporter OsSUT1 to organize sucrose transport and reproductive organ development (Zhao et al., 2022). Auxin also has been found to control anther dehiscence timing by regulating anther endothecium lignification (Cecchetti et al., 2013).…”

Transcriptome and Proteome Analysis Revealed That Hormone and Reactive Oxygen Species Synergetically Regulate Dormancy of Introgression Line in Rice (Oryza sativa L.)

“…Transcriptome analysis plays an important role in the study of rice molecular mechanisms [ 45 , 46 ]. For example, RNA-Seq sequencing detected a significant down-regulation of OsSUT1 expression in dao mutants and further verified that OsSUT1 can directly regulate the source-sink allocation of sucrose in plants [ 47 ]. Transcriptome data analysis also revealed that OsNCED3 mainly regulates rice dormancy through hormone and signal transduction [ 42 ].…”

Auxin regulation on crop: from mechanisms to opportunities in soybean breeding

“…Knockdown of tomato SlARF4 enhances sugar accumulation in fruit, implying a connection between sugar partitioning and auxin signaling (Sagar et al 2013). Zhao et al recently found that rice dao mutant, which failed to convert IAA into OxIAA, had defects in sugar partition between source (leaf) to sink (spikelet) tissue (Zhao et al 2022c). dao mutant upregulates auxin signaling component OsARF18 but downregulates OsARF2.…”

“…Strikingly, the cis-element motif of SuREs (GTCTC) shows high sequence similarity with auxin-responsive elements (AuxREs: TGTCTC), implying a synergistic or antagonistic regulation between auxin and sugar on transcriptional level. OsARF18 acts as a repressor of OsARF2-OsSUT1 complex, feedback regulates sugar transport through auxin signaling (Zhao et al 2022c). Hence, auxin signaling cascade is also involved in carbohydrate partitioning, providing an important implication for raising seed quality.…”