A NAC transcription factor, PpNAC1, regulates the expression of PpMYB10.1 to promote anthocyanin biosynthesis in the leaves of peach trees in autumn

Abstract

AbstractRed leaves in autumn are characteristic of a very early-maturing ripening variety of peach (Prunus persica). Analysis of the genetic factors and molecular mechanisms associated with the red-leaf phenotype can help breed peach very early maturing peach varieties. This study investigated the mechanisms underlying the red- and green-leaf phenotypes in autumn. Red compounds accumulated in the older but not younger leaves in the extremely early-maturing peach variety, ‘99-30-33’, and the leaves of the medium-maturing variety, ‘Zhongtao5 (CP5)’. Metabolic analysis showed that cyanidin-3-O-glucoside was the most abundant anthocyanin in the red leaves. The segregation of the progenies obtained from crossing revealed that the red leaves are a unique hereditary phenomenon not in line with Mendel’s law. BSA-seq and RNA-seq analyses suggest that PpNAC1 was essential for enhancing anthocyanin biosynthesis and was highly upregulated in red than in green leaves. Similar to PpNAC1, the anthocyanin activator, PpMYB10.1, was the only gene highly expressed in red leaves. Moreover, the functional genes involved in anthocyanin biosynthesis, such as Prunus persica Flavonoid 3'-hydroxylase (PpF3'H), Prunus persicaDihydroflavonol reductase (PpDFR), Prunus persica Leucoantho-cyanidin dioxygenase (Pp LDOX), Prunus persica Glutathione S-transferase (PpGST), and Prunus persica UDP-glucose, flavonoid-3-O-glucosyltransferase (PpUFGT), were upregulated in the older red leaves of 99-30-33 but downregulated in the younger 99-30-33 and green CP5 leaves. Yeast one-hybrid and dual-luciferase assays further confirmed that PpNAC1, which refers to 'Prunus persica NAC (NAM、A TAF1/2、CUC1/2)' bound to the promoter of PpMYB10.1, PpMYB10.1 stands for 'Prunus persica MYB (v-myb avian myeloblastosis viral) 10.1' and activated its expression along with those of PpGST and PpUFGT. These results provide insights into the mechanisms responsible for the development of red color in peach leaves in autumn.