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

Authors: WANG, HONG - Jiangsu Academy Agricultural Sciences; XU, KEXIN - Jiangsu Academy Agricultural Sciences; LI, XIAOGANG - Jiangsu Academy Agricultural Sciences; BLANCO-ULATE, BARBARA - University Of California, Davis; YANG, QINGSONG - Jiangsu Academy Agricultural Sciences; YAO, GAIFANG - Jiangsu Academy Agricultural Sciences; WEI, YIDUO - University Of California, Davis; WU, JUN - Nanjing Agricultural University; SHENG, BAOLONG - Jiangsu Academy Agricultural Sciences; CHANG, YOUHONG - Jiangsu Academy Agricultural Sciences; Jiang, Cai-Zhong; LIN, JING - Jiangsu Academy Agricultural Sciences

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/8/2023
Publication Date: 7/21/2023
Citation: Wang, H., Xu, K., Li, X., Blanco-Ulate, B., Yang, Q., Yao, G., Wei, Y., Wu, J., Sheng, B., Chang, Y., Jiang, C., Lin, J. 2023. A pear S1-bZIP transcription factor PpbZIP44 modulates carbohydrate metabolism, amino acid and flavonoid accumulation in fruits. Horticulture Research. 10(8):uhad140. https://doi.org/10.1093/hr/uhad140.
DOI: https://doi.org/10.1093/hr/uhad140

Interpretive Summary: Fruit quality influences consumer preference and market competitiveness. Therefore, improving fruit quality has been the cornerstone for breeders and scientists. Fruit quality includes taste, aroma, texture, and nutritional quality, in addition to shelf-life and other visual attributes. The content and species of soluble sugars and organic acids are the fundamental compounds for fruit growth, development, and ripening and determine the fruit flavor at the edible stage. Fatty acids, amino acids and vitamins, and secondary metabolites such as phenylpropanoids, flavonoids, and phenolics are vital factors in determining the health-promoting quality of fruits. As with most complex agronomic traits, fruit quality is affected by primary and secondary metabolic shifts. Elucidation of the underlying metabolic regulation responsible for changes in fruit attributes is essential for providing scientific guidance for improvement of fruit quality. Biosynthesis and accumulation of primary and secondary metabolites are regulated by transcription factors (TFs). TFs can activate the collaborative expression of multiple genes, thereby effectively regulating the reprogramming of primary or secondary metabolic pathways. Evidences suggest that one subgroup of the basic leucine zipper (bZIP) transcription factors (S1-bZIP group) mediates sugar-related regulatory gene expression and are required for sugar signaling, and plays important roles in the regulation of fruit quality and stress response. However, whether or how pear S1-bZIP TFs regulate primary and secondary metabolic shifts in fruit remains unclear. The discovery and identification of novel TFs are vital for successfully improving fruit quality, especially in woody plants that generate commercially superior fruits with better palatability, nutrient balance, and health benefits. Pear is a popular fruit worldwide. For several years, there has been increased interest in the consumption of pear fruits. Hence, cultivation areas have been increasing, production has intensified, and new cultivars have been developed. The great demand for pear fruit is associated with its taste, texture, and nutritional value. Asian pears desired traits include high sugar contents, moderate acidity, crispy, few stone cells, and high contents of amino acids, unsaturated fatty acids, phenylpropanoids, and flavonoids. Enhancing fruit quality through metabolite manipulation or breeding has been an essential in increasing Asian pear quality. We have recently developed the ‘Sucui 1’ [Pyrus pyrifolia (Burm.f.) Nakai.] variety by crossing ‘Huasu’ and ‘Cuiguan’. ‘Sucui 1’ fruits have improved quality and extrinsic features and an extremely short growth period, and could be used as an excellent material for studying the mechanism of fruit quality or other agronomy traits in pears. In this study, we identified a critical regulator, a member of the S1-bZIP group PpbZIP44, that affected fructose accumulation, organic acids contents, amino acid and flavonoid levels. Our finding provides new insights into understanding the regulatory mechanism for future metabolic engineering to improve fruit quality.

Technical 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 stable transgenic tomato fruits under the control of the fruit-specific E8 promoter and the transient overexpression or RNAi transformed pear fruits 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 were 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, enhancing fructose contents. PpbZIP44 also directly bound to the PpADT and PpF3H promoter, mediating carbon flux towards phenylalanine metabolites and enhancing phenylalanine and flavonoid contents. These findings illustrated that PpbZIP44 mediates multi-metabolism reprogramming by inducing related gene expression affecting the quality-related compounds substantially.