Control of Starch Synthesis in Cereals: Metabolite Analysis of Transgenic Rice Expressing an Up-Regulated Cytoplasmic ADP-Glucose Pyrophosphorylase in Developing Seeds

Nagai, Yasuko; Sakulsingharoj, Chotipa; Edwards, Gerald E.; Satoh, Hiroyuki; Greene, Thomas W.; Blakeslee, Beth; Okita, Thomas W.

doi:10.1093/pcp/pcp021

Cited by 44 publications

(35 citation statements)

References 23 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…LC-MS/MS analysis of soluble sugars in plants was carried out essentially as described previously (Nagai et al, 2009) except that 100 mg of fresh leaf tissue per sample was used. The analyzed sugars included Suc, Fru, Glc, ADPGlc, GDP-Glc, UDP-Glc, Glc-1-P, and Glc-6-P. Each biological sample was assayed in triplicate.…”

Section: Total Starch and Lc-ms/ms Metabolite Analysismentioning

confidence: 99%

The Protein Kinase SnRK2.6 Mediates the Regulation of Sucrose Metabolism and Plant Growth in Arabidopsis

et al. 2010

View full text Add to dashboard Cite

In higher plants, three subfamilies of sucrose nonfermenting-1 (Snf1)-related protein kinases have evolved. While the Snf1-related protein kinase 1 (SnRK1) subfamily has been shown to share pivotal roles with the orthologous yeast Snf1 and mammalian AMP-activated protein kinase in modulating energy and metabolic homeostasis, the functional significance of the two plant-specific subfamilies SnRK2 and SnRK3 in these critical processes is poorly understood. We show here that SnRK2.6, previously identified as crucial in the control of stomatal aperture by abscisic acid (ABA), has a broad expression pattern and participates in the regulation of plant primary metabolism. Inactivation of this gene reduced oil synthesis in Arabidopsis (Arabidopsis thaliana) seeds, whereas its overexpression increased Suc synthesis and fatty acid desaturation in the leaves. Notably, the metabolic alterations in the SnRK2.6 overexpressors were accompanied by amelioration of those physiological processes that require high levels of carbon and energy input, such as plant growth and seed production. However, the mechanisms underlying these functionalities could not be solely attributed to the role of SnRK2.6 as a positive regulator of ABA signaling, although we demonstrate that this kinase confers ABA hypersensitivity during seedling growth. Collectively, our results suggest that SnRK2.6 mediates hormonal and metabolic regulation of plant growth and development and that, besides the SnRK1 kinases, SnRK2.6 is also implicated in the regulation of metabolic homeostasis in plants.Plants are constantly confronted by biotic and abiotic stresses and nutrient deprivation that disrupt metabolic and energy homeostasis or diminish carbon and energy availability for maintaining cell vitality, growth, and proliferation. It is believed that maintaining energy balance and availability at the cellular and organism levels is critical for optimizing plant growth and development. This underscores the cellular and physiological importance of energy sensors that control energy balance through regulating fundamental metabolic pathways in response to nutritional and environmental stresses.At present, a prevailing view is that energy sensors are evolutionarily conserved in eukaryotes, which are represented by Snf1 (for sucrose nonfermenting-1) in yeast, AMPK (for AMP-activated protein kinase) in

show abstract

Section: Total Starch and Lc-ms/ms Metabolite Analysismentioning

confidence: 99%

The Protein Kinase SnRK2.6 Mediates the Regulation of Sucrose Metabolism and Plant Growth in Arabidopsis

et al. 2010

View full text Add to dashboard Cite

show abstract

“…30) Although the regulation of extracellular invertase activity and the involvement of plastidial PGM is still poorly understood, the increased extracellular invertase activity of the PGM lines possibly enhances sink strength, eventually resulting in hexose accumulation in the lower leaves. That extracellular invertase activity is also elevated by overexpression of ADP-glucose pyrophosphorylase, one of the rate-limiting enzymes for starch synthesis, 33) also suggests a relationship between starch synthesis and extracellular invertase activity.…”

Section: Discussionmentioning

confidence: 99%

Alteration of Photosynthate Partitioning by High-Level Expression of Phosphoglucomutase in Tobacco Chloroplasts

Uematsu

Suzuki

Iwamae

et al. 2012

Bioscience, Biotechnology, and Biochemistry

View full text Add to dashboard Cite

Plastidial phosphoglucomutase (PGM) plays an important role in starch synthesis and degradation. Nonetheless, the impact of enhanced plastidial PGM activity on metabolism in photosynthetic tissue is yet to be elucidated. In this study, we generated transplastomic tobacco plants overproducing Arabidopsis thaliana plastidial PGM (AtptPGM) in chloroplasts and analyzed the consequent metabolic and physiological parameters in the transplastomic plants. AtptPGM accumulated in the chloroplasts to up to 16% of total soluble protein in the leaves. PGM activity in leaves increased 100-fold relative to that of wild-type plants. The transplastomic plants were phenotypically indistinguishable in their growth rates, photosynthetic activities, and starch synthesis from wild-type plants, but hexose partitioning in the light period was dramatically different. Furthermore, alteration of extracellular invertase activity was observed in the lower leaves of the transplastomic plants. These observations suggest that high-level expression of plastidial PGM alters hexose partitioning in light periods via modification of extracellular invertase activity.Key words: chloroplast; hexose partitioning; Nicotiana tabacum; phosphoglucomutase; transplastomic plant Phosphoglucomutase (PGM, EC 2.7.5.1) is a widely distributed enzyme in all life forms, catalyzing the nearequilibrium reversible interconversion between glucose 1-phosphate (Glc1P) and glucose 6-phosphate (Glc6P). There are two types of PGMs in plant cells: one cytosolic and the other plastidial.1) Cytosolic PGM participates in sucrose and hexose sugar metabolism and provides intermediates for glycolysis and building blocks for cellular components.2) In contrast, plastidial PGM functions in starch synthesis and degradation. 3)Starch is synthesized in leaf chloroplasts during the day via photosynthetic CO 2 fixation and is degraded at night as a major source of the sucrose required for dark metabolism.4) Lack of plastidial PGM results in a starchless phenotype characterized by a significant decrease in starch content and a high level of soluble sugar accumulation in the leaves during the day. 5,6) These mutants exhibit repressed carbon assimilation and altered growth characteristics. 5,7,8) A transgenic potato expressing the plastidial PGM gene in the antisense orientation has the same lowered rate of photosynthesis of starchless mutants as other plant species, as well as altered compartmentation of photosynthetic metabolites in the cytosol and plastids relative to the wildtype. 9,10) Plastidial PGM, therefore, not only catalyzes an essential reaction for starch synthesis, but also regulates photosynthesis through leaf starch synthesis.Enzymes that catalyze the near-equilibrium reversible reaction in carbohydrate synthesis were thought not to exert much influence on pathway flux, but recent studies have demonstrated that such enzymes as plastidial aldolase, 11,12) transketolase 13) and isocitrate lyase 14) do exert significant metabolic control. Expressing bacterial PGM in the potato c...

show abstract

“…Thus SuSy is a major determinant of sink strength that highly controls the channelling of incoming sucrose into starch [9,10]. The UDPGlc is converted to adenosine 5'-diphosphate glucose (ADPGlc) in the cytosol by the stepwise reactions of UDPGlc pyrophosphorylase and ADPGlc pyrophosphorylase (AGPase), while the conversion of fructose to ADPGlc involves hexokinase, phosphoglucoisomerase and phosphoglucomutase [11]. Although UDP is the preferred nucleoside diphosphate substrate for SuSy, ADP could also be an acceptor molecule of this sucrolytic enzyme to produce ADPGlc [12][13][14].…”

Section: Sucrose Synthase (Susy)mentioning

confidence: 99%

“…This may be due to the greater number of branches, the transferred chains being too short or the branch points incorrectly positioned. DBEs are theorised to selectively remove errantly-placed branch points, thereby facilitating crystallization; however, there is no evidence as yet to indicate, which branch points are removed, how these are selected or how this contributes to amylopectin synthesis [42,11,112]. The finding of numerous short chains on the surface of immature starch granules supports this model [65].…”

Section: Starch Debranching Enzymes (Dbes)mentioning

confidence: 99%

“…It starts with individual chains as the first level, which are formed by ADP-glucose through (1→4)-α-glycosidic linkages. Those chains in amylopectin have been further denoted as C chains having the reducing end, A chains (degree of polymerization, DP, [6][7][8][9][10][11][12] carrying no branches, B1 chains (DP [13][14][15][16][17][18][19][20][21][22][23][24] carrying A chains, B2 chains (DP DOI 10.1515/amylase-2017-0006 [25][26][27][28][29][30][31][32][33][34][35][36] carrying B1 chains, B3 chains (DP > 36) carrying B2 chains, and so on (for a recent review, see [2]). Although still occasionally one finds statements to the contrary, amylose is not solely linear, but contains a small but significant number of long-chain branches [3].…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Recent progress toward understanding the role of starch biosynthetic enzymes in the cereal endosperm

Li¹,

Powell²,

Gilbert

2017

Amylase

View full text Add to dashboard Cite

Abstract:Starch from cereal endosperm is a major energy source for many mammals. The synthesis of this starch involves a number of different enzymes whose mode of action is still not completely understood. ADPglucose pyrophosphorylase is involved in the synthesis of starch monomer (ADP-glucose), a process, which almost exclusively takes place in the cytosol. ADPglucose is then transported into the amyloplast and incorporated into starch granules by starch synthase, starch-branching enzyme and debranching enzyme. Additional enzymes, including starch phosphorylase and disproportionating enzyme, may be also involved in the formation of starch granules, although their exact functions are still obscure. Interactions between these enzymes in the form of functional complexes have been proposed and investigated, resulting more complicated starch biosynthetic pathways. An overall picture and recent advances in understanding of the functions of these enzymes is summarized in this review to provide insights into how starch granules are synthesized in cereal endosperm.

show abstract

Control of Starch Synthesis in Cereals: Metabolite Analysis of Transgenic Rice Expressing an Up-Regulated Cytoplasmic ADP-Glucose Pyrophosphorylase in Developing Seeds

Cited by 44 publications

References 23 publications

The Protein Kinase SnRK2.6 Mediates the Regulation of Sucrose Metabolism and Plant Growth in Arabidopsis

The Protein Kinase SnRK2.6 Mediates the Regulation of Sucrose Metabolism and Plant Growth in Arabidopsis

Alteration of Photosynthate Partitioning by High-Level Expression of Phosphoglucomutase in Tobacco Chloroplasts

Recent progress toward understanding the role of starch biosynthetic enzymes in the cereal endosperm

Contact Info

Product

Resources

About