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Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response

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Key message: During abiotic stress low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, darkness) and are degraded. Metabolic adaptation is crucial for abiotic stress resistance in plants, and accumulation of specific amino acids as well as secondary metabolites derived from amino acid metabolism has been implicated in increased tolerance to adverse environmental conditions. The role of proline, which is synthesized during Arabidopsis stress response to act as a compatible osmolyte, has been well established. However, conclusions drawn about potential functions of other amino acids such as leucine, valine, and isoleucine are not entirely consistent. This study reevaluates published datasets with a special emphasis on changes in the free amino acid pool and transcriptional regulation of the associated anabolic and catabolic pathways. In order to gain a comprehensive overview about the general direction of amino acid metabolism under abiotic stress conditions a complete map of all currently known enzymatic steps involved in amino acid synthesis and degradation was assembled including also the initial steps leading to the synthesis of secondary metabolites. Microarray datasets and amino acid profiles of Arabidopsis plants exposed to dehydration, high salinity, extended darkness, cold, and heat were systematically analyzed to identify trends in fluxes of amino acid metabolism. Some high abundant amino acids such as proline, arginine, asparagine, glutamine, and GABA are synthesized during abiotic stress to act as compatible osmolytes, precursors for secondary metabolites, or storage forms of organic nitrogen. In contrast, most of the low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, extended darkness) and are degraded.
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Plant Molecular Biology (2018) 98:121–135
https://doi.org/10.1007/s11103-018-0767-0
Synthesis versusdegradation: directions ofamino acid metabolism
duringArabidopsis abiotic stress response
TatjanaM.Hildebrandt1
Received: 17 April 2018 / Accepted: 15 August 2018 / Published online: 24 August 2018
© Springer Nature B.V. 2018
Abstract
Key message During abiotic stress low abundant amino acids are not synthesized but they accumulate due to
increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, darkness)
and are degraded.
Abstract Metabolic adaptation is crucial for abiotic stress resistance in plants, and accumulation of specific amino acids as
well as secondary metabolites derived from amino acid metabolism has been implicated in increased tolerance to adverse
environmental conditions. The role of proline, which is synthesized during Arabidopsis stress response to act as a compat-
ible osmolyte, has been well established. However, conclusions drawn about potential functions of other amino acids such as
leucine, valine, and isoleucine are not entirely consistent. This study reevaluates published datasets with a special emphasis
on changes in the free amino acid pool and transcriptional regulation of the associated anabolic and catabolic pathways. In
order to gain a comprehensive overview about the general direction of amino acid metabolism under abiotic stress conditions
a complete map of all currently known enzymatic steps involved in amino acid synthesis and degradation was assembled
including also the initial steps leading to the synthesis of secondary metabolites. Microarray datasets and amino acid profiles
of Arabidopsis plants exposed to dehydration, high salinity, extended darkness, cold, and heat were systematically analyzed
to identify trends in fluxes of amino acid metabolism. Some high abundant amino acids such as proline, arginine, aspara-
gine, glutamine, and GABA are synthesized during abiotic stress to act as compatible osmolytes, precursors for secondary
metabolites, or storage forms of organic nitrogen. In contrast, most of the low abundant amino acids are not synthesized
but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt
stress, extended darkness) and are degraded.
Keywords Arabidopsis· Abiotic stress· Amino acid profiles· Transcriptomics· Metabolomics
Introduction
Amino acids are involved in several physiological processes
in plants apart from constituting proteins. Most impor-
tantly, they act as precursors for a diverse set of second-
ary metabolites and are the transport and storage form for
organic nitrogen within the plant. Gln synthesis is the only
way to assimilate inorganic nitrogen into organic molecules
and thus prerequisite for the production of all other nitrogen
containing metabolites (Bernard and Habash 2009). Also,
amino acids are tightly linked to carbohydrate metabolism,
they are synthesized mainly from intermediates of the calvin
cycle and degraded to either TCA cycle intermediates or
their precursors (Pratelli and Pilot 2014; Hildebrandt etal.
2015; Supp. Fig.S1). Plants are able to synthesize all 20
proteinogenic amino acids de novo from inorganic carbon,
nitrogen, and sulfur compounds (Fig.1a). The set of sec-
ondary metabolites including non-protein amino acids that
can be produced via modification of these 20 amino acids
is extremely diverse and serves critical functions in plant
metabolism such as signaling, defense, structure, interac-
tion with other organisms, and protection from various abi-
otic stresses (D’Auria and Gershenzon 2005). For example,
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s1110 3-018-0767-0) contains
supplementary material, which is available to authorized users.
* Tatjana M. Hildebrandt
hildebrandt@genetik.uni-hannover.de
1 Institut für Pflanzengenetik, Leibniz Universität Hannover,
Herrenhäuser Straße 2, 30419Hannover, Germany
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Pools of free amino acids are tightly controlled through relevant pathways including amino acid and protein biosynthesis as well as degradation. The direction of amino acid metabolism and the size of free amino acid pools highly depends on the type of abiotic stress [20,28]. Combining transcriptome and metabolome data indicates which pathways are induced or repressed during abiotic stress and the source of free amino acid pools [28]. ...
... The direction of amino acid metabolism and the size of free amino acid pools highly depends on the type of abiotic stress [20,28]. Combining transcriptome and metabolome data indicates which pathways are induced or repressed during abiotic stress and the source of free amino acid pools [28]. While induced pathways may contribute to stress protection, repressed pathways and degraded molecules are rather irrelevant. ...
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Following a previous microbial inoculation, plants can induce broad-spectrum immunity to pathogen infection, a phenomenon known as systemic acquired resistance (SAR). SAR establishment in Arabidopsis thaliana is regulated by the Lys catabolite pipecolic acid (Pip) and flavin-dependent-monooxygenase1 (FMO1). Here, we show that elevated Pip is sufficient to induce an FMO1-dependent transcriptional reprogramming of leaves that is reminiscent of SAR. In planta and in vitro analyses demonstrate that FMO1 functions as a pipecolate N-hydroxylase, catalyzing the biochemical conversion of Pip to N-hydroxypipecolic acid (NHP). NHP systemically accumulates in plants after microbial attack. When exogenously applied, it overrides the defect of NHP-deficient fmo1 in acquired resistance and acts as a potent inducer of plant immunity to bacterial and oomycete infection. Our work has identified a pathogen-inducible L-Lys catabolic pathway in plants that generates the N-hydroxylated amino acid NHP as a critical regulator of systemic acquired resistance to pathogen infection.
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As sessile organisms, plants must cope with abiotic stress such as soil salinity, drought, and extreme temperatures. Core stress-signaling pathways involve protein kinases related to the yeast SNF1 and mammalian AMPK, suggesting that stress signaling in plants evolved from energy sensing. Stress signaling regulates proteins critical for ion and water transport and for metabolic and gene-expression reprogramming to bring about ionic and water homeostasis and cellular stability under stress conditions. Understanding stress signaling and responses will increase our ability to improve stress resistance in crops to achieve agricultural sustainability and food security for a growing world population.
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Amino acids have various prominent functions in plants. Besides their usage during protein biosynthesis they also represent building blocks for several other biosynthesis pathways and play pivotal roles during signaling processes as well as in plant stress response. In general, pool sizes of the 20 amino acids strongly differ and dynamically change depending on the developmental and physiological state of the plant cell. Besides amino acid biosynthesis, which already has been investigated in great detail, the catabolism of amino acids is of central importance for adjusting their pool sizes but so far has drawn much less attention. The degradation of amino acids also can substantially contribute to the energy state of plant cells during certain physiological conditions, e.g. carbon starvation. In this review we discuss the biological role of amino acid catabolism and summarize current knowledge on amino acid degradation pathways and their regulation in the context of the plant cell physiology.