MaBEL1 regulates banana fruit ripening by activating cell wall and starch degradation‐related genes

Abstract

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.

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

“…Thus, EBF1 may function as a transcriptional co‐factor that affects target gene transcription. MaEBF1 cooperates with ABI5‐like, MaC2H2‐like, MaNAC67‐like, MaBEL1 (Lai et al., 2022; Song et al., 2019, 2023; Song, Lai, Yao, et al., 2022), and MaC2H2‐IDD (this study), stimulating fruit softening by upregulating these CWS degradation genes (Figures 6 and 7).…”

“…In Arabidopsis , EBF1 is involved in ethylene signaling, which ubiquitination degradation EIN3/EIL1 and negatively regulates the ethylene signal (Guo & Ecker, 2004). A previous report proved that MaEBF1 does not ubiquitinate MaBEL1 and MaABI5‐like and positively regulates fruit ripening (Song et al., 2023; Song, Lai, Yao, et al., 2022). The in vivo and in vitro ubiquitination‐ and protein‐level of MaC2H2‐IDD were detected to verify whether MaC2H2‐IDD protein was ubiquitinated or degraded by MaEBF1.…”

“…MaEBF1 modulates banana fruit ripening and softening disorder (Song et al., 2019) and function as a co‐activator with MaC2H2‐like, MaABI5‐like, MaNAC67‐like, and MaBEL1 transcriptional factors, positively regulating banana fruit ripening (Lai et al., 2022; Song et al., 2019, 2023; Song, Lai, Yao, et al., 2022). Moreover, MaEBF1 (bait) selected MaC2H2‐IDD in a yeast cDNA library (Song et al., 2019).…”

“…Moreover, a previous study proved that MaC2H2‐like, MaNAC67‐like, MaABI5‐like, and MaBEL1 modulate CWS degradation and positively regulate fruit softening in “Fenjiao” banana (Lai et al., 2022; Song et al., 2019, 2023; Song, Lai, Yao, et al., 2022). Thus, this study identified another C2H2 gene, MaC2H2‐IDD , whose gene and protein levels are closely associated with CTS‐caused fruit ripening and softening disorder (Figure 1).…”

“…In banana, MaTCP20 cooperates with MaMPK2, and MaTCP5 interacts with MabZIP93, affecting the modulation of MaTCP20 and MabZIP93 to the cell wall modification‐related genes (Song et al., 2018; Wu et al., 2019). Previous studies indicated that MaEBF1 co‐activates and positively regulates banana fruit softening (Song et al., 2019, 2023; Song, Lai, Yao, et al., 2022). Thus, this study showed that MaEBF1 also cooperates with MaC2H2‐IDD, further activating the expression of MaAMY3 , MaEXP‐A2 , and MaGLU22‐like (Figure 7).…”