The endosperm-specific transcription factor TaNAC019 regulates glutenin and starch accumulation and its elite allele improves wheat grain quality

Abstract

In wheat (Triticum aestivum L.), breeding efforts have focused intensively on improving grain yield and quality. For quality, the content and composition of seed storage proteins (SSPs) determine the elasticity of wheat dough and flour processing quality. Moreover, starch levels in seeds are associated with yield. However, little is known about the mechanisms that coordinate SSP and starch accumulation in wheat. In this study, we explored the role of the endosperm-specific NAC transcription factor TaNAC019 in coordinating SSP and starch accumulation. TaNAC019 binds to the promoters of TaGlu-1 loci, encoding high molecular weight glutenin (HMW-GS), and of starch metabolism genes. Triple knock-out mutants of all three TaNAC019 homoeologs exhibited reduced transcript levels for all SSP types and genes involved in starch metabolism, leading to lower gluten and starch contents, and in flour processing quality parameters. TaNAC019 directly activated the expression of HMW-GS genes by binding to a specific motif in their promoters and interacting with the TaGlu-1 regulator TaGAMyb. TaNAC019 also indirectly regulated the expression of TaSPA, an ortholog of maize Opaque2 that activates SSP accumulation. Therefore, TaNAC019 regulation of starch- and SSP-related genes has key roles in wheat grain quality. Finally, we identified an elite allele (TaNAC019-BI) associated with flour processing quality, providing a candidate gene for breeding wheat with improved quality.

Conserved, divergent and heterochronic gene expression during Brachypodium and Arabidopsis embryo development

“…S5). Lastly, we examined the expression of the closest Brachypodium homologs of the Arabidopsis ZHOUPI (Yang et al 2008 ) and Wheat NAC019 (Gao et al 2021 ) genes, both of which are specifically expressed in endosperm. The Brachypodium homologs are likewise strongly expressed in the endosperm sample (Supplementary Fig.…”

Starch biosynthesis in cereal endosperms: An updated review over the last decade

“…ONAC127 and ONAC129 are not directly involved in starch synthesis in the rice endosperm, but they do form heterodimers that participate in apoplastic transport and the heat stress response to regulate rice grain filling, including starch accumulation ( Ren et al., 2021 ). In wheat, the endosperm-specific TaNAC019 was also found to regulate glutenin and starch accumulation by directly activating the expression of relevant genes ( Liu et al., 2020 ; Gao et al., 2021 ).…”

High molecular weight glutenin gene diversity in Aegilops tauschii demonstrates unique origin of superior wheat quality

“…The early expression and transcription of this allele are also higher than that of the other Glu-D1 alleles, in particular 2 + 12 16 . Other factors underlying the functionality of highmolecular weight glutenin alleles in quality have also been proposed, such as the length and composition of the central repeat domain 29,30 , the position and number of cysteine residues for disulfide bonds 31 , the glutamine composition for hydrogen bonds 31,32 , and promoter elements 33,34 . At this time, it is unclear which of these characteristics, or the combination and interaction of different features, lend to superior quality characteristics and laboratory testing of end-use quality is necessary to determine superior and inferior alleles.…”