Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana

Glaring, Mikkel A.; Skryhan, Katsiaryna; Kötting, Oliver; Zeeman, Samuel C.; Blennow, Andreas

doi:10.1016/j.plaphy.2012.06.017

Cited by 63 publications

(59 citation statements)

References 48 publications

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“…This could indicate that Trx f1 and NTRC may participate in the diurnal regulation of starch degradation in addition to starch synthesis. This is in line with previous in vitro studies reporting that several enzymes in the pathway of starch degradation are subject to thiol redox regulation (Valerio et al, 2011;Glaring et al, 2012), including a plastid-targeted b-amylase, which has been shown to be regulated by both Trx f1 and NTRC (Valerio et al, 2011). It remains to be determined whether a similar mechanism is operational in vivo.…”

Section: Discussionsupporting

confidence: 90%

Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions

et al. 2015

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Two different thiol redox systems exist in plant chloroplasts, the ferredoxin-thioredoxin (Trx) system, which depends on ferredoxin reduced by the photosynthetic electron transport chain and, thus, on light, and the NADPH-dependent Trx reductase C (NTRC) system, which relies on NADPH and thus may be linked to sugar metabolism in the dark. Previous studies suggested, therefore, that the two different systems may have different functions in plants. We now report that there is a previously unrecognized functional redundancy of Trx f1 and NTRC in regulating photosynthetic metabolism and growth. In Arabidopsis (Arabidopsis thaliana) mutants, combined, but not single, deficiencies of Trx f1 and NTRC led to severe growth inhibition and perturbed light acclimation, accompanied by strong impairments of Calvin-Benson cycle activity and starch accumulation. Light activation of key enzymes of these pathways, fructose-1,6-bisphosphatase and ADP-glucose pyrophosphorylase, was almost completely abolished. The subsequent increase in NADPH-NADP + and ATP-ADP ratios led to increased nitrogen assimilation, NADP-malate dehydrogenase activation, and light vulnerability of photosystem I core proteins. In an additional approach, reporter studies show that Trx f1 and NTRC proteins are both colocalized in the same chloroplast substructure. Results provide genetic evidence that light-and NADPH-dependent thiol redox systems interact at the level of Trx f1 and NTRC to coordinately participate in the regulation of the Calvin-Benson cycle, starch metabolism, and growth in response to varying light conditions. Reversible disulfide bond formation between two Cys residues regulates structure and function of many proteins in diverse organisms (Cook and Hogg, 2013). Thiol disulfide exchange is controlled by thioredoxins (Trxs), which are small proteins containing a redoxactive disulfide group in their active site (Holmgren, 1985;Baumann and Juttner, 2002). The latter can be reduced to a dithiol by Trx reductases using NADPH or ferredoxin (Fdx) as electron donors. Due to their low redox midpoint potential, reduced Trxs are able to reductively cleave disulfide bonds in many target proteins and, thus, modulate their functions.Plants contain the most versatile Trx system found in all organisms with respect to the multiplicity of different isoforms and reduction systems (Buchanan and Balmer, 2005;Nikkanen and Rintamäki, 2014;Geigenberger and Fernie, 2014). The Arabidopsis (Arabidopsis thaliana) genome contains a complex family of Trxs, including up to 20 different isoforms grouped into seven subfamilies (Schürmann and Buchanan, 2008;Dietz and Pfannschmidt, 2011). Trxs f1-2, m1-4, x, y1-2, and z are located exclusively in the chloroplast, and Trx o is located exclusively in the mitochondria, while the eight Trx h representatives are distributed between the cytosol, nucleus, endoplasmic reticulum, and mitochondria (Meyer et al., 2012). The different Trxs can be reduced by two different redox systems, dependent on Fdx and Fdx-Trx reductase in the chlorop...

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Section: Discussionsupporting

confidence: 90%

Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions

et al. 2015

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“…In cereals, the SBEII class is subdivided into two distinct gene products, SBEIIa and SBEIIb, each with different kinetic characteristics and tissue expression patterns. SBEII isoforms transfer shorter chains (DP [6][7][8][9][10][11][12][13][14] and prefer amylopectin as a substrate (29). These characteristics have also been shown in a variety of other plant species, for example, rice (Oryza sativa L.; ref.…”

Section: Mode Of Action and Properties Of Sbesmentioning

confidence: 84%

“…Citrate can activate SS activity, by lowering the K m for the a-glucan primer, and can stimulate both spinach leaf (Spinacia oleracea L.) and bean (Phaseolus vulgaris) SBEs (6,26). The activity of a number of starch biosynthetic enzymes has been shown to be modified by redox state, and activities of Arabidopsis SBE 2.1 and 2.2 were enhanced under reducing conditions (10). Redox modulation of the pathway may play a role in diurnal starch regulation in leaves, although its role in regulation of storage starch biosynthesis in nonphotosynthetic tissues is not clear.…”

Section: Figmentioning

confidence: 99%

A review of starch‐branching enzymes and their role in amylopectin biosynthesis

2014

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Starch-branching enzymes (SBEs) are one of the four major enzyme classes involved in starch biosynthesis in plants and algae, and their activities play a crucial role in determining the structure and physical properties of starch granules. SBEs generate a-1,6-branch linkages in a-glucans through cleavage of internal a-1,4 bonds and transfer of the released reducing ends to C-6 hydroxyls. Starch biosynthesis in plants and algae requires multiple isoforms of SBEs and is distinct from glycogen biosynthesis in both prokaryotes and eukaryotes which uses a single branching enzyme (BE) isoform. One of the unique characteristics of starch structure is the grouping of a-1,6-branch points in clusters within amylopectin. This is a feature of SBEs and their interplay with other starch biosynthetic enzymes, thus facilitating formation of the compact water-insoluble semicrystalline starch granule. In this respect, the activity of SBE isoforms is pivotal in starch granule assembly. SBEs are structurally related to the aamylase superfamily of enzymes, sharing three domains of secondary structure with prokaryotic Bes: the central (b/a) 8 -barrel catalytic domain, an NH 2 -terminal domain involved in determining the size of a-glucan chain transferred, and the C-terminal domain responsible for catalytic capacity and substrate preference. In addition, SBEs have conserved plant-specific domains, including phosphorylation sites which are thought to be involved in regulating starch metabolism. SBEs form heteromeric protein complexes with other SBE isoforms as well as other enzymes involved in starch synthesis, and assembly of these protein complexes is regulated by protein phosphorylation. Phosphorylated SBEIIb is found in multienzyme complexes with isoforms of glucan-elongating starch synthases, and these protein complexes are implicated in amylopectin cluster formation. This review presents a comparative overview of plant SBEs and includes a review of their properties, structural and functional characteristics, and recent developments on their posttranslational regulation.

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“…In addition to AGPase, reductive activation by thiol/ disulfide modulation has also been demonstrated for other enzymes involved in the pathway of starch synthesis downstream of AGPase, such as SS 1 and SS 3, SBE 2, and ISA 1 and ISA 2, by using comprehensive in vitro studies (115). This enables a co-ordinated activation of the supply and the use of ADPGlc for starch synthesis by Trx-dependent redox regulation, linking external factors such as light and sucrose to redox activation of the whole pathway.…”

Section: Starch Metabolismmentioning

confidence: 99%

Metabolic Control of Redox and Redox Control of Metabolism in Plants

Geigenberger

Fernie

2014

Antioxidants & Redox Signaling

139

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Significance: Reduction-oxidation (Redox) status operates as a major integrator of subcellular and extracellular metabolism and is simultaneously itself regulated by metabolic processes. Redox status not only dominates cellular metabolism due to the prominence of NAD(H) and NADP(H) couples in myriad metabolic reactions but also acts as an effective signal that informs the cell of the prevailing environmental conditions. After relay of this information, the cell is able to appropriately respond via a range of mechanisms, including directly affecting cellular functioning and reprogramming nuclear gene expression. Recent Advances: The facile accession of Arabidopsis knockout mutants alongside the adoption of broad-scale post-genomic approaches, which are able to provide transcriptomic-, proteomic-, and metabolomic-level information alongside traditional biochemical and emerging cell biological techniques, has dramatically advanced our understanding of redox status control. This review summarizes redox status control of metabolism and the metabolic control of redox status at both cellular and subcellular levels. Critical Issues: It is becoming apparent that plastid, mitochondria, and peroxisome functions influence a wide range of processes outside of the organelles themselves. While knowledge of the network of metabolic pathways and their intraorganellar redox status regulation has increased in the last years, little is known about the interorganellar redox signals coordinating these networks. A current challenge is, therefore, synthesizing our knowledge and planning experiments that tackle redox status regulation at both inter-and intracellular levels. Future Directions: Emerging tools are enabling ever-increasing spatiotemporal resolution of metabolism and imaging of redox status components. Broader application of these tools will likely greatly enhance our understanding of the interplay of redox status and metabolism as well as elucidating and characterizing signaling features thereof. We propose that such information will enable us to dissect the regulatory hierarchies that mediate the strict coupling of metabolism and redox status which, ultimately, determine plant growth and development.

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Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana

Cited by 63 publications

References 48 publications

Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions

Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions

A review of starch‐branching enzymes and their role in amylopectin biosynthesis

Metabolic Control of Redox and Redox Control of Metabolism in Plants

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