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

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.

Transcription Factor Networks in Leaves of Cichorium endivia: New Insights into the Relationship between Photosynthesis and Leaf Development

“…CeARF_11, a homologue of Arabidopsis ARF16, was also co-expressed with several photosynthetic downstream genes and with one of the top-ranked genes in the GCN, CeARF_9. Auxin response regulators have been recently shown to play antagonistic roles in photosynthesis regulation in tomato, and the SlARF6A gene was shown to positively affects photosynthesis in fruits and leaves of tomato plants [63]. Our data are consistent with a major role of auxin response in coordinating photosynthesis and leaf development.…”

Comparative Transcriptomic Analysis of Two Bottle Gourd Accessions Differing in Fruit Size

“…The role of auxin in plant cell expansion is well established [20]. Many studies have demonstrated the role of auxin response factors (ARFs), the main regulators of auxin, in cell division and plant growth [21,23,24,62]. We identified eight auxin-related genes showing significant differential expression among the two cultivars.…”

“…An increase in auxin and cytokinin levels in seeds is correlated with fruit growth stages [19]. The role of auxin in cell expansion during fruit development stages is well established [20,21]. Numerous studies have demonstrated the role of auxin response factors (ARFs), the main regulators of auxin, in cell division and growth during fruit development [20][21][22][23][24].…”

“…The role of auxin in cell expansion during fruit development stages is well established [20,21]. Numerous studies have demonstrated the role of auxin response factors (ARFs), the main regulators of auxin, in cell division and growth during fruit development [20][21][22][23][24]. Transcription factors also regulate genes related to fruit development [8,25,26].…”

Regulatory network of fruit ripening: current understanding and future challenges

“…Although both SlARF2A and SlARF2B contribute to tomato fruit ripening, the SlARF2A transcript is responsive to exogenous ethylene, auxin and ABA, suggesting that SlARF2A intercorrelates auxin, ethylene and ABA signalling during fruit ripening (Breitel et al, 2016). Moreover, SlARF4 negatively regulates chlorophyll accumulation and starch biosynthesis in tomato fruit, whereas SlARF10 and SlARF6A positively regulate chlorophyll content and sugar accumulation (Sagar et al, 2013;Yuan et al, 2018Yuan et al, , 2019. In addition, ABA is also involved in ethylene signalling, with exogenous ABA application inducing the ethylene biosynthesis genes (Zhang et al, 2009).…”