Sucrose and ABA regulate starch biosynthesis in maize through a novel transcription factor, ZmEREB156

Huang, Huanhuan; Xie, Sidi; Xiao, Qianlin; Wei, Bin; Zheng, Lanjie; Wang, Yongbin; Cao, Yujin; Zhang, Xiangge; Long, Tiandan; Li, Yangping; Hu, Yu‐Feng; Yu, Guowu; Liu, Hanmei; Liu, Yanping; Huang, Zhi; Zhang, Junjie; Huang, Yubi

doi:10.1038/srep27590

Cited by 86 publications

(60 citation statements)

References 54 publications

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“…On the other hand, thus far there have been only a few reports regarding transcriptional regulation of starch synthesis in cereals. Among them, one barley WRKY transcription factor, SUSIBA2, and three maize transcription factors, ZmNAC36, ZmbZIP91, and ZmEREB156, are thought to regulate the expression of starch-synthetic genes based on transcriptional activation and/or EMSA assays of their promoters (22)(23)(24)(25). Recently, a study in rice showed that OsbZIP58, the closest homologous protein of maize O2, regulates the expression of multiple genes in the starch biosynthetic pathways, and its null mutants cause abnormal seed morphology with decreased amounts of seed starch (26).…”

Section: Significancementioning

confidence: 99%

Maize endosperm-specific transcription factors O2 and PBF network the regulation of protein and starch synthesis

Zhang

Zheng

Yang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

147

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The maize endosperm-specific transcription factors opaque2 (O2) and prolamine-box binding factor (PBF) regulate storage protein zein genes. We show that they also control starch synthesis. The starch content in the PbfRNAi and o2 mutants was reduced by ∼5% and 11%, respectively, compared with normal genotypes. In the doublemutant PbfRNAi;o2, starch was decreased by 25%. Transcriptome analysis reveals that >1,000 genes were affected in each of the two mutants and in the double mutant; these genes were mainly enriched in sugar and protein metabolism. Pyruvate orthophosphate dikinase 1 and 2 (PPDKs) and starch synthase III (SSIII) are critical components in the starch biosynthetic enzyme complex. The expression of PPDK1, PPDK2, and SSIII and their protein levels are further reduced in the double mutants as compared with the single mutants. When the promoters of these genes were analyzed, we found a prolamine box and an O2 box that can be additively transactivated by PBF and O2. Starch synthase IIa (SSIIa, encoding another starch synthase for amylopectin) and starch branching enzyme 1 (SBEI, encoding one of the two main starch branching enzymes) are not directly regulated by PBF and O2, but their protein levels are significantly decreased in the o2 mutant and are further decreased in the double mutant, indicating that o2 and PbfRNAi may affect the levels of some other transcription factor(s) or mRNA regulatory factor(s) that in turn would affect the transcript and protein levels of SSIIa and SBEI. These findings show that three important traits-nutritional quality, calories, and yieldare linked through the same transcription factors.gene regulation | zein | starch synthesis | yield | breeding strategy

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Section: Significancementioning

confidence: 99%

Maize endosperm-specific transcription factors O2 and PBF network the regulation of protein and starch synthesis

Zhang

Zheng

Yang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

159

147

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“…Both MYB and NAC homologs in Arabidopsis and maize regulate secondary cell wall deposition and components (Zhong et al, 2008(Zhong et al, , 2011. Their homologs in maize also affect starch metabolism in endosperm (Huang et al, 2016). Furthermore, several candidate genes involved in metabolism were introgressed and associated with the T6P signal in R9188/ BTx406.…”

Section: Candidate Genes Regulating T6p Pathwaymentioning

confidence: 99%

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

Wang

Feng

et al. 2018

Plant Biotechnology Journal

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Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.

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“…The previous studies also tried to identify TFs regulating synthetic starch genes by coexpression analysis and biochemistry experiments, like the Electrophoretic Mobility Shift Assay (EMSA) and the Dual-Luciferase Reporter (DLR) assay. There have been candidate TFs, including one barley WRKY transcription factor of SUSIBA2, and three maize transcription factors of ZmNAC36, ZmbZIP91, and ZmEREB156, although their regulatory function on starch synthesis remains to be validated (20)(21)(22)(23).…”

mentioning

confidence: 99%

NAC-type transcription factors regulate accumulation of starch and protein in maize seeds

Zhang

Dong

Chen

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

139

126

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Grain starch and protein are synthesized during endosperm development, prompting the question of what regulatory mechanism underlies the synchronization of the accumulation of secondary and primary gene products. We found that two endosperm-specific NAC transcription factors, ZmNAC128 and ZmNAC130, have such a regulatory function. Knockdown of expression of ZmNAC128 and ZmNAC130 with RNA interference (RNAi) caused a shrunken kernel phenotype with significant reduction of starch and protein. We could show that ZmNAC128 and ZmNAC130 regulate the transcription of Bt2 and then reduce its protein level, a rate-limiting step in starch synthesis of maize endosperm. Lack of ZmNAC128 and ZmNAC130 also reduced accumulation of zeins and nonzeins by 18% and 24% compared with nontransgenic siblings, respectively. Although ZmNAC128 and ZmNAC130 affected expression of zein genes in general, they specifically activated transcription of the 16-kDa γ-zein gene. The two transcription factors did not dimerize with each other but exemplified redundancy, whereas individual discovery of their function was not amenable to conventional genetics but illustrated the power of RNAi. Given that both the Bt2 and the 16-kDa γ-zein genes were activated by ZmNAC128 or ZmNAC130, we could identify a core binding site ACGCAA contained within their target promoter regions by combining Dual-Luciferase Reporter and Electrophoretic Mobility Shift assays. Consistent with these properties, transcriptomic profiling uncovered that lack of ZmNAC128 and ZmNAC130 had a pleiotropic effect on the utilization of carbohydrates and amino acids. maize endosperm | gene regulation | starch synthesis | protein

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Sucrose and ABA regulate starch biosynthesis in maize through a novel transcription factor, ZmEREB156

Cited by 86 publications

References 54 publications

Maize endosperm-specific transcription factors O2 and PBF network the regulation of protein and starch synthesis

Maize endosperm-specific transcription factors O2 and PBF network the regulation of protein and starch synthesis

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

NAC-type transcription factors regulate accumulation of starch and protein in maize seeds

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