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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]

Banana is a typical subtropical fruit, sensitive to chilling injuries and prone to softening disorder. However, the underlying regulatory mechanisms of the softening disorder caused by cold stress remain obscure. Herein, we found that BEL1‐LIKE HOMEODOMAIN transcription factor 1 (MaBEL1) and its associated proteins regulate the fruit softening and ripening process. The transcript and protein levels of MaBEL1 were up‐regulated with fruit ripening but severely repressed by the chilling stress. Moreover, the MaBEL1 protein interacted directly with the promoters of the cell wall and starch degradation‐related genes, such as MaAMY3, MaXYL32, and MaEXP‐A8. The transient overexpression of MaBEL1 alleviated fruit chilling injury and ripening disorder caused by cold stress and promoted fruit softening and ripening of "Fenjiao" banana by inducing ethylene production and starch and cell wall degradation. The accelerated ripening was also validated by the ectopic overexpression in tomatoes. Conversely, MaBEL1‐silencing aggravated the chilling injury and ripening disorder and repressed fruit softening and ripening by inhibiting ethylene production and starch and cell wall degradation. MaABI5‐like and MaEBF1, the two positive regulators of the fruit softening process, interacted with MaBEL1 to enhance the promoter activity of the starch and cell wall degradation‐related genes. Moreover, the F‐box protein MaEBF1 does not modulate the degradation of MaBEL1, which regulates the transcription of MaABI5‐like protein. Overall, we report a novel MaBEL1‐MaEBF1‐MaABI5‐like complex system that mediates the fruit softening and ripening disorder in "Fenjiao" bananas caused by cold stress. [ABSTRACT FROM AUTHOR]

• The MaC2H2-like is closely related to fruit ripening disorder by chilling stress. • MaC2H2-like activates the transcription level of fruit softening-related genes. • MaEBF1 interacting MaC2H2-like enhanced the expression of softening-related genes. • MaC2H2-like- overexpressing promotes fruit ripening in 'Fenjiao' banana. As one of the largest transcription factor families, C2H2 zinc finger proteins contain a zinc finger motif and a conserved DNA-binding homeodomain. Although C2H2 zinc finger proteins have been found to play an essential role in ethylene biosynthetic and cold stress in banana fruit, their transcriptional regulatory mechanisms involved in the softening of 'Fenjiao' banana remain largely elusive. In this study, a new MaC2H2-like gene was identified, which is closely related to fruit softening. MaC2H2-like localizes in the nucleus. MaC2H2-like activated the transcription of four starch (MaBAM4 , MaBAM6 , MaISA2 and MaPWD1) and five cell wall (MaEXP-A2 , MaEXP-A8 , MaSUR14 , MaSUR14-like and MaXYL32) degradation-related genes, by specifically interacting with their promoters. Protein-protein interaction assays showed that MaC2H2-like cooperates with ethylene-insensitive 3-binding F-box protein (MaEBF1) in vitro and vivo , and their interaction enhanced the binding and activated the promoter activities of MaBAM4 , MaPWD1 , MaISA2 , MaEXP-A2 , MaSUR14-like and MaXYL32. The transient overexpression of MaC2H2-like in 'Fenjiao' banana fruit promoted fruit ripening and softening by accelerating ethylene production, decreasing fruit firmness and inducing the transcription of starch and cell wall degradation-related genes. Collectively, we uncovered a novel module of MaC2H2-like-MaEBF1 that cooperates in actively impacting starch and cell wall degradation by up-regulating the transcript level of genes related to the degradation of starch and cell walls. [ABSTRACT FROM AUTHOR]