Catabolism of Branched Chain Amino Acids Supports Respiration but Not Volatile Synthesis in Tomato Fruits

Abstract

The branched-chain amino acid transaminases (BCATs) have a crucial role in metabolism of the branched-chain amino acids leucine, isoleucine, and valine. These enzymes catalyze the last step of synthesis and the initial step of degradation of these amino acids. Although the biosynthetic pathways of branched chain amino acids in plants have been extensively investigated and a number of genes have been characterized, their catabolism in plants is not yet completely understood. We previously characterized the branched chain amino acid transaminase gene family in tomato, revealing both the subcellular localization and kinetic properties of the enzymes encoded by six genes. Here, we examined possible functions of the enzymes during fruit development. We further characterized transgenic plants differing in the expression of branched chain amino acid transaminases 1 and 3, evaluating the rates of respiration in fruits deficient in BCAT1 and the levels of volatiles in lines overexpressing either BCAT1 or BCAT3. We quantitatively tested, via precursor and isotope feeding experiments, the importance of the branched chain amino acids and their corresponding keto acids in the formation of fruit volatiles. Our results not only demonstrate for the first time the importance of branched chain amino acids in fruit respiration, but also reveal that keto acids, rather than amino acids, are the likely precursors for the branched chain flavor volatiles.

System-Wide Hypersensitive Response-Associated Transcriptome and Metabolome Reprogramming in Tomato

“…7A; Supplemental Table S2). The catabolism of Leu, Ile, and Val generates acetyl-CoA, which in the tricarboxylic acid cycle generates energy, a process widely observed during starvation and stress (Aubert et al, 1996;Fujiki et al, 2001;Taylor et al, 2004;Kochevenko et al, 2012). Our data suggest that the highly induced hydroxycinnamic acid-derived secondary metabolite biosynthesis pathways are for the greater part responsible for the alterations in aromatic amino acids and carbon skeleton fluxes.…”

A Regulatory Hierarchy of the Arabidopsis Branched-Chain Amino Acid Metabolic Network

“…In plants, BCAAs and their derivatives contribute to growth, defense, and the production of food flavor components (Kang et al, 2006;Yoshikawa et al, 1995;Zeier, 2013;Kimball and Jefferson, 2006;Gonda et al, 2010;Galili et al, 2016). In addition, BCAA catabolism provides an alternative source of energy in plants under long-term dark treatment conditions (Peng et al, 2015;Kochevenko et al, 2012). Moreover, acetohydroxyacid synthase (AHAS), the committed enzyme of Val biosynthesis, is the target of four classes of commercial herbicides, and numerous plant herbicide resistance AHAS alleles have been reported (Jander et al, 2003).…”

The Impact of the Branched-Chain Ketoacid Dehydrogenase Complex on Amino Acid Homeostasis in Arabidopsis

“…Plants synthesize BCAAs and are the main source of these essential nutrients in the diets of humans and agriculturally important animals. In addition to their nutritional value, BCAAs and BCAA-derived metabolites such as glucosinolates, fatty acids, and acyl sugars contribute to plant growth, development, defense, and flavor (Mikkelsen and Halkier, 2003;Taylor et al, 2004;Ishizaki et al, 2005;Slocombe et al, 2008;Araújo et al, 2010;Ding et al, 2012;Kochevenko et al, 2012).The BCAA biosynthetic pathway and its regulation have been investigated in Arabidopsis (Arabidopsis thaliana) and other plants for the past two decades, in large part because of the commercial importance of herbicides that inhibit acetohydroxy acid synthase, which is the committing enzyme of BCAA biosynthesis (Singh and Shaner, 1995;Aubert et al, 1997;Singh, 1999;McCourt et al, 2006;Tan et al, 2006;Binder, 2010;Chen et al, 2010;Yu et al, 2010). Strong correlations between the levels of free BCAAs were found in wildtype Arabidopsis seeds and tomato (Solanum lycopersicum) fruits Lu et al, 2008), which suggests coregulation of biosynthesis and/or degradation.…”

“…Plants synthesize BCAAs and are the main source of these essential nutrients in the diets of humans and agriculturally important animals. In addition to their nutritional value, BCAAs and BCAA-derived metabolites such as glucosinolates, fatty acids, and acyl sugars contribute to plant growth, development, defense, and flavor (Mikkelsen and Halkier, 2003;Taylor et al, 2004;Ishizaki et al, 2005;Slocombe et al, 2008;Araújo et al, 2010;Ding et al, 2012;Kochevenko et al, 2012).…”