PbrbZIP15 promotes sugar accumulation in pear via activating the transcription of the glucose isomerase gene PbrXylA1.

Luting Jia, Xu Zhang, Zan Zhang, Weiqi Luo, Savithri U Nambeesan, Qionghou Li, Xin Qiao, Bing Yang, Libin Wang, Shaoling Zhang

Journal: The Plant journal : for cell and molecular biology 2024;117(5):1392-1412

PMID: 38044792

Abstract

The composition and abundance of soluble sugars in mature pear (Pyrus) fruit are important for its acceptance by consumers. However, our understanding of the genes responsible for soluble sugar accumulation remains limited. In this study, a S1-group member of bZIP gene family, PbrbZIP15, was characterized from pear genome through the combined analyses of metabolite and transcriptome data followed by experimental validation. PbrbZIP15, located in nucleus, was found to function in fructose, sucrose, and total soluble sugar accumulation in pear fruit and calli. After analyzing the expression profiles of sugar-metabolism-related genes and the distribution of cis-acting elements in their promoters, the glucose isomerase 1 gene (PbrXylA1), whose corresponding protein catalyzed the isomerization of glucose and fructose in vitro, was identified as a downstream target gene of PbrbZIP15. PbrbZIP15 could directly bind to the G-box element in PbrXylA1 promoter and activate its transcription, as evidenced by chromatin immunoprecipitation-quantitative PCR, yeast one-hybrid, electrophoretic mobility shift assay, and dual-luciferase assay. PbrXylA1, featuring a leucine-rich signal peptide in its N-terminal, was localized to the endoplasmic reticulum. It was validated to play a significant role in fructose, sucrose, and total soluble sugar accumulation in pear fruit and calli, which was associated with the upregulated fructose/glucose ratio. Further studies revealed a positive correlation between the sucrose content and the expression levels of several sucrose-biosynthesis-related genes (PbrFRK3/8, PbrSPS1/3/4/8, and PbrSPP1) in PbrbZIP15-/PbrXylA1-transgenic fruit/calli. In conclusion, our results suggest that PbrbZIP15-induced soluble sugar accumulation during pear development is at least partly attributed to the activation of PbrXylA1 transcription.

© 2023 Society for Experimental Biology and John Wiley & Sons Ltd.

Address: National Key Laboratory of Crop Genetics and Germplasm Enhancement and Utilization, Sanya Institute of Nanjing Agricultural University, College of Horticulture, Nanjing Agricultural University, Nanjing, Jiangsu, 210095, China.; U.S. Horticultural Research Laboratory, ARS-USDA, Ft. Pierce, Florida, 34945, USA.; CIPM, NC State University, Raleigh, North Carolina, 27606, USA.; Department of Horticulture, University of Georgia, Athens, Georgia, 30602, USA.

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