Genome-wide association analysis identifies a natural variation in basic helix-loop-helix transcription factor regulating ascorbate biosynthesis via D-mannose/L-galactose

Authors: YE, JIE - Boyce Thompson Institute; LI, WANGFANG - Huazhong Agricultural University; AI, GUO - Huazhong Agricultural University; LI, CHANGZIN - Huazhong Agricultural University; LU, CHENGZHONG - Huazhong Agricultural University; CHEN, WEIFANG - Huazhong Agricultural University; WANG, BING - Huazhong Agricultural University; WANG, WENQIAN - Huazhong Agricultural University; LU, YONGEN - Huazhong Agricultural University; ZHANG, JUNHONG - Huazhong Agricultural University; LI, HANXIA - Huazhong Agricultural University; OUYANG, BO - Huazhong Agricultural University; ZHANG, HONGYAN - Huazhong Agricultural University; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James; ZHANG, YUYANG - Huazhong Agricultural University; YE, HUAZHONG - Huazhong Agricultural University

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/2/2019
Publication Date: 5/8/2019
Citation: Ye, J., Li, W., Ai, G., Li, C., Lu, C., Chen, W., Wang, B., Wang, W., Lu, Y., Zhang, J., Li, H., Ouyang, B., Zhang, H., Fei, Z., Giovannoni, J.J., Zhang, Y., Ye, H. 2019. Genome-wide association analysis identifies a natural variation in basic helix-loop-helix transcription factor regulating ascorbate biosynthesis via D-mannose/L-galactose. PLoS Genetics. 15(5):e1008149. https://doi.org/10.1371/journal.pgen.1008149.
DOI: https://doi.org/10.1371/journal.pgen.1008149

Interpretive Summary: Tomato represents an important source of nutrients and fiber for the human diet and is a model system for studying fruit biology as many things learned from tomato can be translated to other fruit crops. Cultivated tomatoes carry only a small fraction of the available genetic variation found in nature for this crop and breeders have primarily focused on fruit size and stress resistance but not flavor and other consumer quality traits. In the present study, we focused on 92 metabolic traits related to fruit quality in 302 diverse tomato accessions that were characterized in two different years and environments. We uncovered a novel transcription factor gene, SlbHLH59, for vitamin C levels in fruit. These findings provide new information on a specific gene influencing fruit quality that can now be selected by breeders to enhance fruit vitamin C content and provides a foundation for additional discovery related to genetic regulation of other metabolic traits associated with fruit flavor, color and nutrition.

Technical Abstract: Tomato (Solanum lycopersicum) is one of the highest-value vegetable crops worldwide. Understanding the genetic regulation of primary metabolite levels can inform efforts aimed toward improving the nutrition of commercial tomato cultivars, while maintaining key traits such as yield and stress tolerance. We identified 388 suggestive association loci (including 126 significant loci) for 92 metabolic traits including nutrition and flavor-related loci by genome-wide association study from 302 accessions in two different environments. Among them, an ascorbate quantitative trait locus TFA9 (TOMATO FRUIT ASCORBATEON CHROMOSOME 9) co-localized with SlbHLH59, which promotes high ascorbate accumulation by directly binding to the promoter of structural genes involved in the D-mannose/L-galactose pathway. The causal mutation of TFA9 is an 8-bp InDel, named InDel_8, located in the promoter region of SlbHLH59 and spanned a 5’UTR Py-rich stretch motif affecting its expression. Phylogenetic analysis revealed that differentially expressed SlbHLH59 alleles were selected during tomato domestication. Our results provide a dramatic illustration of how ascorbate biosynthesis can be regulated and was selected during the domestication of tomato. Furthermore, the findings provide novel genetic insights into natural variation of metabolites in tomato fruit, and will promote efficient utilization of metabolite traits in tomato improvement.