NaCl promotes tomato fruit coloring by relieving SlSR3-induced transcriptional inhibition of lycopene synthesis-related genes

Abstract

Although salt stress has an adverse effect on plant growth and development, mild salt stress acts as an elicitor of biosynthesis and thus improves fruit quality. To date, the role and mechanism of NaCl in accelerating tomato (Solanum lycopersicum) fruit coloring remain unclear. This study found that 50 mM NaCl treatment (moderate salt stress) reduced the chlorophyll content, increased the carotenoid and lycopene content, and accelerated tomato color transition without decreasing yield. Moreover, NaCl treatment downregulated calmodulin-binding transcription activator (CAMTA5)/signal responsive (SR3). Knockout of SlSR3 by CRISPR/Cas 9 (sr3 mutant) accelerated chlorophyll degradation and carotenoid and lycopene accumulation and upregulated chlorophyll degradation (PPH) and lycopene synthesis (PSY2, PDS, and ZDS) genes in tomato fruit, thereby accelerating tomato coloring. However, SlSR3 overexpression had the opposite effect. Although NaCl treatment decreased chlorophyll, increased carotenoids, and upregulated PPH, PSY2, PDS, and ZDS in wild type and OE-sr3 fruit, these changes were not observed in sr3 mutant fruit. Therefore, PPH, PSY2, PDS, and ZDS might be involved in SR3-regulated coloring under moderate salt stress. Further results showed that SlSR3 could directly bind to the promoter of PSY2 and ZDS via the CG-1 domain, thereby downregulating PSY2 and ZDS. However, NaCl treatment reversed the transcriptional inhibition of SlSR3 on PSY2 and ZDS expression, thereby upregulating PSY2 and ZDS. Collectively, our results suggest that the promoting effects of NaCl on fruit coloring may be dependent on SlSR3-induced transcriptional regulation of lycopene synthesis-related genes PSY2 and ZDS. Therefore, our study provides a better understanding of the function of SlSR3 in tomato coloring and offers insights on the molecular mechanism underlying the effects of moderate salt stress on tomato color transformation.