Amino Acid Catabolism in Plants

Hildebrandt, Tatjana M.; Nunes‐Nesi, Adriano; Araújo, Wagner L.; Braun, Hans‐Peter

doi:10.1016/j.molp.2015.09.005

Cited by 964 publications

(793 citation statements)

References 109 publications

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“…and Lotus japonicus (Kreuzwieser et al, 2009;Rocha et al, 2010). Indeed, in senescing leaves, increased protein breakdown and amino acid catabolism coincide with increased amino acid content (Watanabe et al, 2013;Hildebrandt et al, 2015). Similarly, in petioles of submerged R. acetosa plants, a large increase in free ammonia was observed upon submergence, suggesting an increased amino acid breakdown (van Veen et al, 2013).…”

Section: Alternative Metabolic Reserve Mobilization As a Coordinated mentioning

confidence: 97%

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

et al. 2016

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ORCID IDs: 0000-0002-6709-6436 (S.H.); 0000-0001-6777-6565 (M.E.S.); 0000-0002-8568-7125 (J.B.-S.); 0000-0002-6940-0657 (R.S.).Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness-and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.

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Section: Alternative Metabolic Reserve Mobilization As a Coordinated mentioning

confidence: 97%

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

et al. 2016

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“…First, amino acids in leaves are not known to be oxidized for respiration except during carbon starvation or senescence (Hildebrandt et al, 2015). Given that stores of starch and organic acids remain at early points in the night, it is unlikely that amino acids would represent major substrates for the night respiration measurements performed in this study.…”

Section: Protein Synthesis Is Not a Major Determinant Of Mature Arabimentioning

confidence: 99%

Variation in Leaf Respiration Rates at Night Correlates with Carbohydrate and Amino Acid Supply

et al. 2017

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Plant respiration can theoretically be fueled by and dependent upon an array of central metabolism components; however, which ones are responsible for the quantitative variation found in respiratory rates is unknown. Here, large-scale screens revealed 2-fold variation in nighttime leaf respiration rate (R N ) among mature leaves from an Arabidopsis (Arabidopsis thaliana) natural accession collection grown under common favorable conditions. R N variation was mostly maintained in the absence of genetic variation, which emphasized the low heritability of R N and its plasticity toward relatively small environmental differences within the sampling regime. To pursue metabolic explanations for leaf R N variation, parallel metabolite level profiling and assays of total protein and starch were performed. Within an accession, R N correlated strongly with stored carbon substrates, including starch and dicarboxylic acids, as well as sucrose, major amino acids, shikimate, and salicylic acid. Among different accessions, metabolite-R N correlations were maintained with protein, sucrose, and major amino acids but not stored carbon substrates. A complementary screen of the effect of exogenous metabolites and effectors on leaf R N revealed that (1) R N is stimulated by the uncoupler FCCP and high levels of substrates, demonstrating that both adenylate turnover and substrate supply can limit leaf R N , and (2) inorganic nitrogen did not stimulate R N , consistent with limited nighttime nitrogen assimilation. Simultaneous measurements of R N and protein synthesis revealed that these processes were largely uncorrelated in mature leaves. These results indicate that differences in preceding daytime metabolic activities are the major source of variation in mature leaf R N under favorable controlled conditions. Few plant metabolic fluxes are readily accessible to routine measurement. The major exceptions to this are fluxes involving gas exchange, such as respiration and photosynthesis. Measurements of respiratory gas exchange (i.e. mitochondrial oxygen uptake or CO 2 release in the absence of photorespiration) are useful from a metabolic perspective because they can be interpreted in terms of the underlying carbon fluxes and the generation of ATP by oxidative phosphorylation (Sweetlove et al., 2013). The biochemical reactions of respiration that produce CO 2 and lead to oxygen consumption are well understood (Plaxton and Podestá, 2006;Sweetlove et al., 2010;Millar et al., 2011;Tcherkez et al., 2012). The stoichiometries of the reactions and the connections between them are known, which provides us with a metabolic map of respiration that includes glycolysis, the oxidative pentose phosphate pathway, the citric acid cycle, the mitochondrial electron transport chain (mETC), ATP synthase, and several other surrounding reactions. In plants, carbohydrates are the dominant respiratory substrates, whereas lipids are rarely respired (Plaxton and Podestá, 2006). Carbohydrate oxidation proceeds via organic acids, which serve many purposes in plant...

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“…Besides amino acid biosynthesis, plants also can break down all 20 amino acids. Amino acid catabolism is especially relevant in the context of germination (the conversion of storage proteins into carbohydrates), senescence (the recycling of energy-rich compounds), and in the context of stress reactions (Hildebrandt et al, 2015). The synthesis of some amino acids is massively induced upon drought and salt stress, most of all proline, because they can serve as compatible osmolytes (Szabados and Savouré, 2010).…”

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confidence: 99%

3-Hydroxyisobutyrate Dehydrogenase Is Involved in Both, Valine and Isoleucine Degradation in Arabidopsis thaliana

2017

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In plants, amino acid catabolism is especially relevant in metabolic stress situations (e.g. limited carbohydrate availability during extended darkness). Under these conditions, amino acids are used as alternative substrates for respiration. Complete oxidation of the branched-chain amino acids (BCAAs) leucine, isoleucine (Ile), and valine (Val) in the mitochondria efficiently allows the formation of ATP by oxidative phosphorylation. However, the metabolic pathways for BCAA breakdown are largely unknown so far in plants. A systematic search for Arabidopsis (Arabidopsis thaliana) genes encoding proteins resembling enzymes involved in BCAA catabolism in animals, fungi, and bacteria as well as proteomic analyses of mitochondrial fractions from Arabidopsis allowed the identification of a putative 3-hydroxyisobutyrate dehydrogenase, AtHDH1 (At4g20930), involved in Val degradation. Systematic substrate screening analyses revealed that the protein uses 3-hydroxyisobutyrate but additionally 3-hydroxypropionate as substrates. This points to a role of the enzyme not only in Val but possibly also in Ile metabolism. At4g20930 knockdown plants were characterized to test this conclusion. Root toxicity assays revealed increased root growth inhibition of the mutants if cultivated in the presence of Val or Ile but not in the presence of leucine. We conclude that AtHDH1 has a dual role in BCAA metabolism in plants.

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Amino Acid Catabolism in Plants

Cited by 964 publications

References 109 publications

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

Variation in Leaf Respiration Rates at Night Correlates with Carbohydrate and Amino Acid Supply

3-Hydroxyisobutyrate Dehydrogenase Is Involved in Both, Valine and Isoleucine Degradation in Arabidopsis thaliana

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