Redesigning a S‐nitrosylated pyruvate‐dependent GABA transaminase 1 to generate high‐malate and saline–alkali‐tolerant tomato

• Published in: The New phytologist 2024-06, Vol.242 (5), p.2148-2162
• Main Authors: Liu, Minghui, Cao, Bili, Wei, Jin‐Wei, Gong, Biao
• Format: Article
• Language: English
• Subjects: 4-Aminobutyrate transaminase; 4-Aminobutyrate Transaminase - genetics; 4-Aminobutyrate Transaminase - metabolism; Agricultural development; Alkalies - pharmacology; Aluminium; Aluminum; Exudation; Food quality; Fruit - drug effects; Fruit - genetics; Fruits; GABA; gamma-Aminobutyric Acid - metabolism; Gene Expression Regulation, Plant - drug effects; Malate; Malates - metabolism; Nitric oxide; Nitric Oxide - metabolism; Plant breeding; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Roots - drug effects; Plant Roots - metabolism; Pyruvic acid; Roots; saline–alkali; Solanum lycopersicum - drug effects; Solanum lycopersicum - genetics; Stress, Physiological - drug effects; tomato; Tomatoes; Transaminase; Transaminases; γ-Aminobutyric acid
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.19693

Summary Although saline–alkali stress can improve tomato quality, the detailed molecular processes that balance stress tolerance and quality are not well‐understood. Our research links nitric oxide (NO) and γ‐aminobutyric acid (GABA) with the control of root malate exudation and fruit malate storage, mediated by aluminium‐activated malate transporter 9/14 (SlALMT9/14). By modifying a specific S‐nitrosylated site on pyruvate‐dependent GABA transaminase 1 (SlGABA‐TP1), we have found a way to enhance both plant's saline–alkali tolerance and fruit quality. Under saline–alkali stress, NO levels vary in tomato roots and fruits. High NO in roots leads to S‐nitrosylation of SlGABA‐TP1/2/3 at Cys316/258/316, reducing their activity and increasing GABA. This GABA then reduces malate exudation from roots and affects saline–alkali tolerance by interacting with SlALMT14. In fruits, a moderate NO level boosts SlGABA‐TP1 expression and GABA breakdown, easing GABA's block on SlALMT9 and increasing malate storage. Mutants of SlGABA‐TP1C316S that do not undergo S‐nitrosylation maintain high activity, supporting malate movement in both roots and fruits under stress. This study suggests targeting SlGABA‐TP1Cys316 in tomato breeding could significantly improve plant's saline–alkali tolerance and fruit quality, offering a promising strategy for agricultural development.