An InDel variant in the promoter of the NAC transcription factor MdNAC18.1 plays a major role in apple fruit ripening.
Yue, QY (Yue, Qianyu) [1] , [2] ; Xie, YP (Xie, Yinpeng) [1] ; Yang, XY (Yang, Xinyue) [1] ; Zhang, YX (Zhang, Yuxin) [1] ; Li, ZX (Li, Zhongxing) [1] ; Liu, YX (Liu, Yunxiao) [1] ; Cheng, PD (Cheng, Pengda) [1] ; Zhang, RP (Zhang, Ruiping) [3] ; Yu, Y (Yu, Yue) [1] ; Wang, XF (Wang, Xiaofei) [2] ; Liao, L (Liao, Liao) [4] ; Han, YP (Han, Yuepeng) ; Zhao, T (Zhao, Tao) [1] ; Li, XW (Li, Xuewei) [1] ; Zhang, HT (Zhang, Hengtao) [3] ; Ma, FW (Ma, Fengwang) [1] ; Guan, QM (Guan, Qingmei) [1]
PLANT CELL
Abstract
A complex regulatory network governs fruit ripening, but natural variations and functional differentiation of fruit ripening genes remain largely unknown. Utilizing a genome-wide association study (GWAS), we identified the NAC family transcription factor MdNAC18.1, whose expression is closely associated with fruit ripening in apple (Malus x domestica Borkh.). MdNAC18.1 activated the transcription of genes related to fruit softening (Polygalacturonase, PG) and ethylene biosynthesis (1-aminocyclopropane-1-carboxylic acid synthase, ACS), thereby promoting fruit ripening of apple and tomato (Solanum lycopersicum). There were two single-nucleotide polymorphisms (SNP-1,545 and SNP-2,002) and a 58-bp insertion-deletion (InDel-58) in the promoter region of MdNAC18.1. Among these, InDel-58 serves as the main effector in activating the expression of MdNAC18.1 and driving fruit ripening. InDel-58 determines the binding affinity of the class D MADS-box protein AGAMOUS-LIKE 11 (MdAGL11), a negative regulator of fruit ripening. The InDel-58 deletion in the early-ripening genotype reduces the inhibitory effect of MdAGL11 on MdNAC18.1. Moreover, MdNAC18.1 and its homologous genes originated from a common ancestor across 61 angiosperms, with functional diversification attributed to tandem replications that occurred in basal angiosperms. In summary, our study revealed how a set of natural variations influence fruit ripening and explored the functional diversification of MdNAC18.1 during evolution.