MaC2H2‐IDD regulates fruit softening and involved in softening disorder induced by cold stress in banana.

SUMMARY: Chilling stress causes banana fruit softening disorder and severely impairs fruit quality. Various factors, such as transcription factors, regulate fruit softening. Herein, we identified a novel regulator, MaC2H2‐IDD, whose expression is closely associated with fruit ripening and softening disorder. MaC2H2‐IDD is a transcriptional activator located in the nucleus. The transient and ectopic overexpression of MaC2H2‐IDD promoted "Fenjiao" banana and tomato fruit ripening. However, transient silencing of MaC2H2‐IDD repressed "Fenjiao" banana fruit ripening. MaC2H2‐IDD modulates fruit softening by activating the promoter activity of starch (MaBAM3, MaBAM6, MaBAM8, MaAMY3, and MaISA2) and cell wall (MaEXP‐A2, MaEXP‐A8, MaSUR14‐like, and MaGLU22‐like) degradation genes. DLR, Y1H, EMSA, and ChIP‐qPCR assays validated the expression regulation. MaC2H2‐IDD interacts with MaEBF1, enhancing the regulation of MaC2H2‐IDD to MaAMY3, MaEXP‐A2, and MaGLU22‐like. Overexpressing/silencing MaC2H2‐IDD in banana and tomato fruit altered the transcript levels of the cell wall and starch (CWS) degradation genes. Several differentially expressed genes (DEGs) were authenticated between the overexpression and control fruit. The DEGs mainly enriched biosynthesis of secondary metabolism, amino sugar and nucleotide sugar metabolism, fructose and mannose metabolism, starch and sucrose metabolism, and plant hormones signal transduction. Overexpressing MaC2H2‐IDD also upregulated protein levels of MaEBF1. MaEBF1 does not ubiquitinate or degrade MaC2H2‐IDD. These data indicate that MaC2H2‐IDD is a new regulator of CWS degradation in "Fenjiao" banana and cooperates with MaEBF1 to modulate fruit softening, which also involves the cold softening disorder. Significance Statement: MaC2H2‐IDD/MaEBF1 complex modulates banana fruit softening by regulating genes related to starch and cell wall degradation. Chilling stress severely represses the activation of softening‐related genes, causing fruit ripening disorder and impairing the texture quality. [ABSTRACT FROM AUTHOR]