Glucose-6-Phosphate Dehydrogenases: The Hidden Players of Plant Physiology

Abstract

Glucose-6-phosphate dehydrogenase (G6PDH) catalyzes a metabolic hub between glycolysis and the pentose phosphate pathway (PPP), which is the oxidation of glucose-6-phosphate (G6P) to 6-phosphogluconolactone concomitantly with the production of nicotinamide adenine dinucleotide phosphate (NADPH), a reducing power. It is considered to be the rate-limiting step that governs carbon flow through the oxidative pentose phosphate pathway (OPPP). The OPPP is the main supplier of reductant (NADPH) for several "reducing" biosynthetic reactions. Although it is involved in multiple physiological processes, current knowledge on its exact role and regulation is still piecemeal. The present review provides a concise and comprehensive picture of the diversity of plant G6PDHs and their role in seed germination, nitrogen assimilation, plant branching, and plant response to abiotic stress. This work will help define future research directions to improve our knowledge of G6PDHs in plant physiology and to integrate this hidden player in plant performance.

Keywords: ROS; abiotic stress; apical dominance; glucose-6-phosphate dehydrogenase; seed germination; sugar signaling.

Figure 1

Overview of the reactions of the pentose phosphate pathway (PPP) and its connection to glycolysis. The glycolytic pathway is colored in green. The oxidative part of the PPP is colored in orange, the non-oxidative part in purple; one-headed arrows designate physiologically irreversible reactions, two-headed arrows reversible ones; abbreviation meanings: G6PDH, glucose-6-phosphate dehydrogenase (EC 1.1.1.49); 6PGL, 6-phosphogluconolactonase (EC 3.1.1.31); 6PGDH, 6-phosphogluconate dehydrogenase (EC 1.1.1.44); RPI, ribose-5-phosphate isomerase (EC 5.3.1.6); RuPE, ribulose-5-phosphate 3-epimerase (EC 5.1.3.1); TKT, transketolase (EC 2.2.1.1); TAL, transaldolase (EC 2.2.1.2); PHI, hexose-6-phosphate isomerase (EC 5.3.1.9); SBPase, sedoheptulose-1,7-bisphosphatase (EC 3.1.3.37); other details in the text.

Figure 2

Comparison of different G6PDH isoforms from 8 higher plants; (A), phylogenetic tree showing the relative positions of 39 different gene encoding isoforms from higher plants, inferring by the maximum likelihood method of complete protein sequences; 10 sequences are P1-G6PDH, 10 sequences are P2-G6PDH, 8 sequences are P0-G6PDH; and 11 sequences are Cy-G6PDH. Legend for plant species: At, Arabidopsis thaliana; Os, Oryza sativa Japonica Group; Zm, Zea mays; Rc, Rosa chinensis; Vit, Vitis vinifera; Pp, Prunus persica; Solyc, Solanum lycopersicum; St, Solanum tuberosum. (B), List of G6PDH isoforms and their relative gene symbol from different higher plants, summarizing from the phylogenetic tree constructed in (A). The complete list of sequences using for tree construction is showed in Table S1.

Figure 3

Cytosolic G6PDH in radicle of imbibed seed modulates ROS homeostasis and hormonal signaling in the control of seed germination. The NADPH provided by cytosolic G6PDH activity is required both for ROS production by NADPH oxidase and for ROS scavenging by activation of GSH ascorbate cycle; the working model based on genetic evidence proposed that G6PDH modulates ROS to a steady state level controlling ABA and GA activities and dormancy release; GSH, reduced glutathione; ROS, reactive oxygen species; ABA, abscisic acid; GA, gibberellic acid.

Figure 4

Regulatory network of G6PDH in the context of plant responses to abiotic stress. The NADPH provided by cytosolic G6PDH activity is required both for ROS production by NADPH oxidase and for ROS scavenging by activation of GSH ascorbate cycle. The working model proposed that G6PDH plays a pivotal role in redox homeostasis, ROS signaling and NO cascade signaling. ASKα, Arabidopsis thaliana glycogen synthase kinase3 (GSK3)/SHAGGY-like kinase; ABA, abscisic acid; APX, ascorbate peroxidase; POD, peroxidase; SOD, superoxide dismutase; GSH, reduced glutathione; ROS, reactive oxygen species.