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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #345488
Title: An InDel in the promoter of Al-activated malate transporter 9 selected during tomato domestication determines fruit malate content and aluminum tolerance

Author
item YE, JIE - Huazhong Agricultural University
item WANG, XIN - Huazhong Agricultural University
item HU, TIXU - Huazhong Agricultural University
item ZHANG, FENXIA - Huazhong Agricultural University
item Giovannoni, James
item ZHANG, YUYANG - Huazhong Agricultural University
item YE, ZHIBIAO - Huazhong Agricultural University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/11/2017
Publication Date: 8/16/2017
Citation: Ye, J., Wang, X., Hu, T., Zhang, F., Giovannoni, J.J., Zhang, Y., Ye, Z. 2017. An InDel in the promoter of Al-activated malate transporter 9 selected during tomato domestication determines fruit malate content and aluminum tolerance. The Plant Cell. doi:10.1105/tpc.17.00211.

Interpretive Summary: Plants produce numerous metabolites that are important for plant growth and tolerance of environmental stress, and also serve as essential sources of fiber, energy, and nutrients in the human diet. For example, malic acid (or malate), affects plant growth, stress responses, and the flavor and nutrient quality of fruit. High malate contents protect plants from Aluminum toxicity. In addition, malate is essential for maintaining cellular osmotic pressure and charge balance in guard cells and thus directly regulates plant stress responses and photosynthesis. In this study, we analyzed a mapping population of tomato to identify genetic determinants of fruit malate content. Furthermore, we integrated numerous molecular techniques to functionally characterize a malate content-related gene that was uncovered. We call this gene TOMATO FRUIT MALATE ON CHROMOSOME 6 (TFM6), and found it to contribute high malate content in both fruit and root tissue. The resulting high malate content improved both fruit flavor and aluminum stress resistance in cultivated tomato plants harboring the naturally occurring TFM6 gene variant. This resulted in both greater understanding of the genetic regulation of fruit flavor and aluminum tolerance and provides a new target for improved tomato breeding.

Technical Abstract: Deciphering the mechanism of malate accumulation in plants would contribute to a greater understanding of plant chemistry, which has implications for improving flavor quality in crop species and enhancing human health benefits. However, the regulation of malate metabolism is poorly understood in crops such as tomato (Solanum lycopersicum). Here, we integrated a metabolite-based genome-wide association study (mGWAS) with linkage mapping and gene functional studies to characterize the genetics of malate accumulation in a global collection of tomato accessions with broad genetic diversity. We report that TFM6 (tomato fruit malate 6), which corresponds to Al-Activated Malate Transporter 9 (Sl-ALMT9 in tomato), is the major quantitative trait locus responsible for variation in fruit malate accumulation among tomato genotypes. A 3-bp indel in the promoter region of Sl-ALMT9 was linked to high fruit malate content. Further analysis indicated that this indel disrupts a W-box binding site in the Sl-ALMT9 promoter, which prevents binding of the WRKY transcription repressor Sl-WRKY42, thereby alleviating the repression of Sl-ALMT9 expression and promoting high fruit malate accumulation. Evolutionary analysis revealed that this highly expressed Sl-ALMT9 allele was selected for during tomato domestication. Furthermore, vacuole membrane–localized Sl-ALMT9 increases in abundance following Al treatment, thereby elevating malate transport and enhancing Al resistance.