Natural allelic variation of NAC transcription factor 22 regulates starch biosynthesis and properties in sweetpotato.

Abstract

Sweetpotato (Ipomoea batatas) starch is in high demand globally as a food and industrial product. However, the regulatory mechanisms governing starch biosynthesis and starch properties in this important crop remain largely unknown. Here we identified a natural allelic variant in the promoter of IbNAC22, encoding a NAC (NAM, ATAF1/2, and CUC2) transcription factor, which is closely linked to starch content in sweetpotato. In high-starch sweetpotato varieties, the T/C haplotype and a 13-bp deletion in the IbNAC22 promoter resulted in higher transcriptional activity. The high-starch IbNAC22 haplotype is more prevalent in regions of China where the sweetpotato starch industry is well developed, indicating that this advantageous allele type has been utilized in breeding starchy sweetpotato varieties in China. IbNAC22 is highly expressed in storage roots and starch-rich sweetpotato accessions. Overexpression of IbNAC22 significantly improved starch and amylose contents, as well as granule size and gelatinization temperature, and decreased starch crystallinity, whereas IbNAC22 knockdown had the opposite effects. IbNAC22 directly activates the expression of IbGBSSI, a key gene for amylose biosynthesis, but suppresses the expression of IbSBEI, a key gene for amylopectin biosynthesis. IbNAC22 directly interacts with IbNF-YA10. Overexpressing of IbNF-YA10 significantly improved starch and amylose contents, and starch gelatinization temperature, but decreased granule size, crystallinity, and amylopectin chain length distribution. IbNF-YA10 directly activates IbAGPL and IbGBSSI, which are key genes involved in starch and amylose biosynthesis. IbNAC22-IbNF-YA10 heterodimers further enhance the IbNF-YA10-induced activation of IbAGPL and IbGBSSI. These findings increase our understanding of starch biosynthesis and starch properties and provide strategies and candidate genes for the improvement of starchy root and tuber crops.