A pear S1-bZIP transcription factor PpbZIP44 modulates carbohydrate metabolism, amino acid, and flavonoid accumulation in fruits

Abstract

Fruit quality is defined by attributes that give value to a commodity. Flavor, texture, nutrition, and shelf life are key quality traits that ensure market value and consumer acceptance. In pear fruit, soluble sugars, organic acids, amino acids, and total flavonoids contribute to flavor and overall quality. Transcription factors (TFs) regulate the accumulation of these metabolites during development or in response to the environment. Here, we report a novel TF, PpbZIP44, as a positive regulator of primary and secondary metabolism in pear fruit. Analysis of the transient overexpression or RNAi-transformed pear fruits and stable transgenic tomato fruits under the control of the fruit-specific E8 promoter demonstrated that PpZIP44 substantially affected the contents of soluble sugar, organic acids, amino acids, and flavonoids. In E8::PpbZIP44 tomato fruit, genes involved in carbohydrate metabolism, amino acid, and flavonoids biosynthesis were significantly induced. Furthermore, in PpbZIP44 overexpression or antisense pear fruits, the expression of genes in the related pathways was significantly impacted. PpbZIP44 directly interacted with the promoter of PpSDH9 and PpProDH1 to induce their expression, thereby depleting sorbitol and proline, decreasing citrate and malate, and enhancing fructose contents. PpbZIP44 also directly bound to the PpADT and PpF3H promoters, which led to the carbon flux toward phenylalanine metabolites and enhanced phenylalanine and flavonoid contents. These findings demonstrate that PpbZIP44 mediates multimetabolism reprogramming by regulating the gene expression related to fruit quality compounds.

Acknowledgements

We thank Prof. Songling Bai for kindly providing the genome database of ‘Cuiguan’ pear. We thank Chuan-Bei Jiang (Gene-pioneer Biotechnologies, Nanjing 210014, China) for providing bioinformatics analysis. This work was supported by Jiangsu Agri- cultural Science and Technology Independent Innovation Fund [Grant No. CX(22)3010], the General Program of National Natural Science Foundation of China (Grant No. 31872078, 32272669), Jiangsu Modern Agricultural Industry Technology System (Grant No. JATS[2022]437, JATS[2022]438), Jiangsu Agricultural Key New Varieties Innovation (Grant No. PZCZ201726), Jiangsu Province Seed Industry Revitalization Unveiled Project: Breeding of New Pear Cultivars with High-quality and Extreme Early Ripening (Grant No. JBGS[2021]084). The funders had no role in study design, data collection, and analysis.

Author Contributions

H.W., L.J., and C.Z.J. designed and supervised the research. W.J., B.L.S., and Y.H.C. suggested the research. H.W. and K.X.X. wrote the manuscript. B.B.U. and C.Z.J. revised the manuscript. W.H. conducted the RNA-seq library and metabolites preparation, pro- cessed the RNA-seq data and metabolites data, gene clone, trans- formation, HPLC, EMSA, dual luciferase assay, and statistics. K.X.X. performed RT-qPCR and physiology experiments. H.W. and G.F.Y. performed transient transformation. Y.D.W. performed sequences analysis. Q.S.Y. and X.G.L. prepared pear fruits. All authors read and approved the final manuscript.

Data availability

All the RNA-seq data are available and have been deposited in the National Center for Biotechnology Information Sequence Reads Archive (PRJNA947778). Other relevant data are presented within the paper and its supplementary files.

Conflict of Interest

The authors declare that they have no conflict of interest.

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