Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato

Authors: YUAN, YUJIN - Chongqing University; XU, XIN - Chongqing University; GONG, ZEHAO - Chongqing University; TANG, YUWEI - Chongqing University; WU, MENGBO - Chongqing University; YAN, FANG - Chongqing University; ZHANG, XIAOLAN - Chongqing University; ZHANG, QIAN - Chongqing University; YANG, FENGQING - Chongqing University; HU, XIAOWEI - Chongqing University; YANG, QICHEN - Chongqing University; LUO, YINGQING - Chongqing University; MEI, LIHUA - Chongqing University; ZHANG, WENFA - Chongqing University; Jiang, Cai-Zhong; LU, WANGJIN - Chongqing University; LI, ZHENGGUO - Chongqing University; DENG, WEI - Chongqing University

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/17/2019
Publication Date: 7/11/2019
Citation: Yuan, Y., Xu, X., Gong, Z., Tang, Y., Wu, M., Yan, F., Zhang, X., Zhang, Q., Yang, F., Hu, X., Yang, Q., Luo, Y., Mei, L., Zhang, W., Jiang, C., Lu, W., Li, Z., Deng, W. 2019. Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato. Horticulture Research. 6. https://doi.org/10.1038/s41438-019-0167-x.
DOI: https://doi.org/10.1038/s41438-019-0167-x

Interpretive Summary: Tomato is the world’s second largest vegetable crop rich in nutrients. Tomato fruit development includes three stages. The first stage is characterized by an increase in cell number and starch accumulation, followed by cell enlargement with starch degradation and soluble sugar accumulation in the second stage. Fruit ripening is the last stage, associated with the accumulation of soluble sugars, carotenoids, organic acids, and volatile organic compounds in fruits. The chlorophyll accumulation and photosynthetic activity of green fruits influence the nutritional components and flavor of ripening tomato fruits. Some genes have been reported to affect chlorophyll accumulation, chloroplast development and fruit quality. For example, the tomato GOLDEN2-LIKE transcription factors play an important role in chloroplast formation and chlorophyll accumulation. Auxin is an important phytohormone involved in flower fertilization, fruit setting, fruit initiation and development. Auxin is also essential in the regulation of cell division and expansion, controlling final fruit size. Auxin modulates plant development through transcriptional regulation of auxin-responsive genes, including auxin response factors (ARFs). ARFs can act as either an activator or a repressor of the transcription of auxin-responsive genes. However, the function of SlARF6 in the regulation of fruit development is still not well understood. In this study, we performed functional characterization of SlARF6A in tomato. Overexpression of SlARF6A increased chlorophyll contents in the fruits and leaves of tomato plants, whereas downregulation of SlARF6A decreased chlorophyll contents compared with those of wild-type (WT) plants. Analysis of chloroplasts using transmission electron microscopy indicated increased sizes of chloroplasts in SlARF6A-overexpressing plants and decreased numbers of chloroplasts in SlARF6A-downregulated plants. Overexpression of SlARF6A increased the photosynthesis rate and accumulation of starch and soluble sugars, whereas knockdown of SlARF6A resulted in opposite phenotypes in tomato leaves and fruits. RNA-sequence analysis showed that regulation of SlARF6A expression altered the expression of genes involved in chlorophyll metabolism, photosynthesis and sugar metabolism. Overexpression of SlARF6A also inhibited fruit ripening and ethylene production, whereas downregulation of SlARF6A increased fruit ripening and ethylene production. Taken together, these results expand our understanding of ARFs with regard to photosynthesis, sugar accumulation and fruit development and provide a potential target for genetic engineering to improve fruit nutrition in horticulture crops.

Technical Abstract: Auxin response factors (ARFs) are involved in auxin-mediated transcriptional regulation in plants. In this study, we performed functional characterization of SlARF6A in tomato. SlARF6A is located in the nucleus and exhibits transcriptional activator activity. Overexpression of SlARF6A increased chlorophyll contents in the fruits and leaves of tomato plants, whereas downregulation of SlARF6A decreased chlorophyll contents compared with those of wild-type (WT) plants. Analysis of chloroplasts using transmission electron microscopy indicated increased sizes of chloroplasts in SlARF6A-overexpressing plants and decreased numbers of chloroplasts in SlARF6A-downregulated plants. Overexpression of SlARF6A increased the photosynthesis rate and accumulation of starch and soluble sugars, whereas knockdown of SlARF6A resulted in opposite phenotypes in tomato leaves and fruits. RNA-sequence analysis showed that regulation of SlARF6A expression altered the expression of genes involved in chlorophyll metabolism, photosynthesis and sugar metabolism. SlARF6A directly bound to the promoters of SlGLK1, CAB and RbcS genes and positively regulated the expression of these genes. Overexpression of SlARF6A also inhibited fruit ripening and ethylene production, whereas downregulation of SlARF6A increased fruit ripening and ethylene production. SlARF6A directly bound to the SAMS1 promoter and negatively regulated SAMS1 expression. Taken together, these results expand our understanding of ARFs with regard to photosynthesis, sugar accumulation and fruit development and provide a potential target for genetic engineering to improve fruit nutrition in horticulture crops.