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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 #408944

Research Project: Biochemistry and Physiology of Crop Adaptation to Soil-Based Abiotic Stresses

Location: Plant, Soil and Nutrition Research

Title: Alternative splicing underpins ALMT9 function for vacuolar malic acid accumulation in apple

Author
item LI, CHUNLONG - Cornell University
item KRISHNAN, SRINIVASAN - Boyce Thompson Institute
item ZHANG, MENGXIA - Cornell University
item HU, DAGANG - Cornell University
item MENG, DONG - Cornell University
item RIEDELSBERGER, JANIN - University Of Talca
item Dougherty, Laura
item XU, KENONG - Cornell University
item Pineros, Miguel
item CHENG, LAILIANG - Cornell University

Submitted to: Advanced Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/24/2023
Publication Date: 3/21/2024
Citation: Li, C., Krishnan, S., Zhang, M., Hu, D., Meng, D., Riedelsberger, J., Dougherty, L.E., Xu, K., Pineros, M., Cheng, L. 2024. Alternative splicing underpins ALMT9 function for vacuolar malic acid accumulation in apple. Advanced Science. vol. 11, 2310159. https://doi.org/10.1002/advs.202310159.
DOI: https://doi.org/10.1002/advs.202310159

Interpretive Summary: In apple, fruit acidity is determined based on the levels of malic acid present. Malic acid levels can vary among apple cultivars and is the main reason certain apples taste tart. In cells, malic acid is stored in the vacuole but the mechanism underlying malic acid accumulation has not been fully characterized. The major transporter gene responsible for transporting the malic acid into the vacuole is called ALMT9 or Ma1. When more transporters were present in the fruit, more malic acid did not accumulate in the vacuole as expected. In this study we determined that key gene interactions with Ma1 are active in a feedback loop that influences the malic acid transporter gene, leading to more or less malic acid accumulation in apple fruit.

Technical Abstract: Malate transport into the vacuole largely determines fruit acidity of apple and other fleshy fruits. ALUMINUM-ACTIVATED MALATE TRANSPORTER 9 (ALMT9/Ma1) underlies Ma, a major genetic locus for fruit acidity in apple, but how the transporter works is still unclear. Here we show that overexpression of Ma1 cDNA drastically decreases fruit acidity in ‘Royal Gala’ apple, leading us to uncover how alternative splicing underpins Ma1’s function. Alternative splicing generates two isoforms, Ma1' being 68 amino acids shorter than the full length Ma1'. Ma1' is not functional itself, but interacts with the functional Ma1' to form heterodimers, creating a synergy with Ma1' for malate transport. Ma1' overexpression triggers a feedback loop via transcription factor MYB73 to down-regulate the expression of native Ma1, decreasing Ma1' to lower levels that reduce Ma1 function and malic acid accumulation. These findings reveal an essential role of alternative splicing in ALMT9-mediated malate transport underlying apple fruit acidity.