Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana
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Whereas proline accumulates through de novo biosynthesis in plants subjected to osmotic stress, leucine, isoleucine, and valine accumulation in drought-stressed Arabidopsis thaliana is caused by abscisic acid-regulated protein degradation.
In response to several kinds of abiotic stress, plants greatly increase their accumulation of free amino acids. Although stress-induced proline increases have been studied the most extensively, the fold-increase of other amino acids, in particular branched-chain amino acids (BCAAs; leucine, isoleucine, and valine), is often higher than that of proline. In Arabidopsis thaliana (Arabidopsis), BCAAs accumulate in response to drought, salt, mannitol, polyethylene glycol, herbicide treatment, and nitrogen starvation. Plants that are deficient in abscisic acid signaling accumulate lower amounts of BCAAs, but not proline and most other amino acids. Previous bioinformatic studies had suggested that amino acid synthesis, rather than protein degradation, is responsible for the observed BCAA increase in osmotically stressed Arabidopsis. However, whereas treatment with the protease inhibitor MG132 decreased drought-induced BCAA accumulation, inhibition of BCAA biosynthesis with the acetolactate synthase inhibitors chlorsulfuron and imazapyr did not. Additionally, overexpression of BRANCHED-CHAIN AMINO ACID TRANSFERASE2 (BCAT2), which is upregulated in response to osmotic stress and functions in BCAA degradation, decreased drought-induced BCAA accumulation. Together, these results demonstrate that BCAA accumulation in osmotically stressed Arabidopsis is primarily the result of protein degradation. After relief of the osmotic stress, BCAA homeostasis is restored over time by amino acid degradation involving BCAT2. Thus, drought-induced BCAA accumulation is different from that of proline, which is accumulated due to de novo synthesis in an abscisic acid-independent manner and remains elevated for a more prolonged period of time after removal of the osmotic stress.
KeywordsAbscisic acid Drought Isoleucine Leucine Mannitol Protease Valine
Branched-chain amino acids
BRANCHED-CHAIN AMINO ACID TRANSFERASE2
This work was supported by the United States National Science Foundation [Grant Number MCB-1022017].
- Cohen H, Israeli H, Matityahu I, Amir R (2014) Seed-specific expression of a feedback-insensitive form of CYSTATHIONINE-gamma-SYNTHASE in Arabidopsis stimulates metabolic and transcriptomic responses associated with desiccation stress. Plant Physiol 166(3):1575–1592CrossRefPubMedPubMedCentralGoogle Scholar
- Martinelli T, Whittaker A, Bochicchio A, Vazzana C, Suzuki A, Masclaux-Daubresse C (2007) Amino acid pattern and glutamate metabolism during dehydration stress in the ‘resurrection’ plant Sporobolus stapfianus: a comparison between desiccation-sensitive and desiccation-tolerant leaves. J Exp Bot 58(11):3037–3046CrossRefPubMedGoogle Scholar
- Ranieri A, Bernardi R, Lanese P, Soldatini GF (1989) Changes in free amino acid content and protein pattern of maize seedlings under water stress. Environ Exp Biol 29(3):351–357Google Scholar
- Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53(1):11–28CrossRefPubMedGoogle Scholar
- Urano K, Maruyama K, Ogata Y, Morishita Y, Takeda M, Sakurai N, Suzuki H, Saito K, Shibata D, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57(6):1065–1078CrossRefPubMedGoogle Scholar