Abstract
Maintaining metabolic homeostasis is critical for plant growth and development. Here we report proteome and metabolome changes when the metabolic homeostasis is perturbed due to gene-dosage dependent mutation of Arabidopsis isopropylmalate dehydrogenases (IPMDHs). By integrating complementary quantitative proteomics and metabolomics approaches, we discovered that gradual ablation of the oxidative decarboxylation step in leucine biosynthesis caused imbalance of amino acid homeostasis, redox changes and oxidative stress, increased protein synthesis, as well as a decline in photosynthesis, which led to rearrangement of central metabolism and growth retardation. Disruption of IPMDHs involved in aliphatic glucosinolate biosynthesis led to synchronized increase of both upstream and downstream biosynthetic enzymes, and concomitant repression of the degradation pathway, indicating metabolic regulatory mechanisms in controlling glucosinolate biosynthesis.
Highlights
Amino acid homeostasis is pivotal for plant growth and development
Our previous study discovered that the imdh2 ipmdh3 mutant was lethal in male gametophytes and had reduced transmission through female gametophytes, probably caused by the decrease of Leu biosynthesis [7]
This result supports the direct involvement of isopropylmalate dehydrogenases (IPMDHs) in de novo Leu biosynthesis, and suggests that other pathways are not adequate to sustain the Leu homeostasis in planta
Summary
Among the essential amino acids, leucine (Leu), valine (Val) and isoleucine (Ile) constitute a small group of branched-chain amino acids (BCAAs). The motivations driving the advancement in this area include: 1) human and other animals cannot synthesize these essential amino acids, and have to obtain them directly or indirectly from plants [1,2]; 2) enzymes in their biosynthetic pathways are targets of several economically important herbicides [3]. Val and Ile are synthesized in two parallel pathways using a single set of enzymes catalyzing the reactions with different substrates. Similar 2-oxoacid-based chain-elongation reactions are used in other biosynthetic pathways, such as the tricarboxylic acid (TCA) cycle, lysine (Lys) biosynthesis in fungi and methionine (Met) chain-elongation in the biosynthesis of aliphatic glucosinolates found in Brassicaceae plants including Arabidopsis thaliana [1]. The notion that Met chainelongation cycle is evolutionarily recruited from Leu biosynthetic pathway has been well supported by several independent experiments [4,5,6,7,8]
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