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Literature Sharing | Transcription factor ZmGBF1 enhances heat stress tolerance in maize by directly increasing expression of ZmCXE2 involved in GA pathway

Release time:

2025-05-16

This study revealed that the transcription factor ZmGBF1 plays a positive role in maize heat stress (HS) tolerance. Through transcriptome analysis, DNA affinity purification sequencing, yeast one-hybrid, and dual-luciferase assays, ZmGBF1 was shown to directly bind to the promoter of ZmCXE2 and enhance its expression, thereby promoting the HS response. Both ZmGBF1 and ZmCXE2 were upregulated by gibberellin (GA), suggesting hormonal involvement in this regulatory pathway. The findings propose an improved model in which ZmGBF1 enhances maize heat tolerance by activating ZmCXE2, helping to balance growth and environmental stress responses.

This study identified heat stress (HS)-responsive transcription factors by performing RNA-seq on five maize inbred lines exposed to 45°C for one day. A total of 17,062 differentially expressed genes (DEGs) were detected. Using weighted gene co-expression network analysis (WGCNA), these DEGs were grouped into 19 modules. Among them, the turquoise module, containing 6,089 DEGs, showed the most significant and consistent upregulation under HS. GO enrichment analysis revealed that genes in this module were associated with heat and reactive oxygen species responses, indicating their key role in maize HS tolerance.

Fig. 1 Co-expression analysis and gene regulatory networks of the maize HS response constructed by WGCNA

To explore the role of ZmGBF1 in HS response, we created overexpressing lines of ZmGBF1 in the B104 background. For further analysis, two overexpression lines, ZmGBF1-OE3 and ZmGBF1-OE5 with higher expression levels were selected based on their relative expression level (Fig. 2A). Both overexpression line (ZmGBF1-OE3 and ZmGBF1-OE5) exhibited a heat-tolerant phenotype compared to WT (Fig 2D), with relatively high survival rate (Fig. 2E), accompanied by decreased percentage of ion leakage (Fig. 2F), less MDA and H2O2 accumulation (Fig. 2G), higher SOD and POD enzyme activities (Fig. 2H).

Fig. 2 Heat tolerance is modulated by ZmGBF1

To identify target genes directly regulated by ZmGBF1, transcriptome analysis was performed on wild-type and ZmGBF1 overexpression (OE) lines. Among 62 differentially expressed genes, ZmCXE2 showed the most significant upregulation. GO analysis revealed enrichment in hormone and signal response pathways. DAP-seq identified six genes with ZmGBF1 binding peaks in their promoters, with ZmCXE2, ZmMYBAS2, and ZmARF3 upregulated, and ZmFMO1 and ZmPYL10 downregulated in OE lines. ZmCXE2 was the most responsive. Hormone treatments showed that GA and IAA significantly increased the expression of ZmGBF1 and ZmCXE2, especially under GA. These findings suggest that ZmGBF1 enhances heat tolerance by modulating hormone-responsive genes, particularly ZmCXE2.

Fig. 3 Transcriptomic analysis of WT and ZmGBF1-OE3 under normal and HS treatment

ZmCXE2 expression was strongly induced by heat stress and by the transcription factor ZmGBF1. Both yeast one-hybrid and luciferase assays confirmed that ZmGBF1 directly activates the ZmCXE2 promoter, demonstrating that ZmGBF1 promotes ZmCXE2 transcription.

Fig. 4. Heat tolerance is modulated by ZmCXE2, a downstream target gene of ZmGBF1.

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