Regulation and roles for alternative pathways of hexose metabolism in plants

Abstract

Plant cells have two cytoplasmic pathways of glycolysis and gluconeogenesis for the reversible interconversion of fructose 6‐phosphate (F‐6‐P) and fructose 1,6‐bisphosphate (F‐1,6‐P2). One pathway is described as a maintenance pathway that is catalyzed by a nucleotide triphosphate‐dependent phosphofructokinase (EC 2.7.1.11; ATP‐PFK) glycolytically and a F‐1,6 bisphosphatase (EC 3.1.3.11) gluconeogenically. These are non‐equilibrium reactions that are energy consuming. The second pathway, described as an adaptive pathway, is catalyzed by a readily reversible pyrophosphate‐dependent phosphofructokinase (EC 2.7.1.90; PP‐PFK) in an equilibrium reaction that conserves energy through the utilization and the synthesis of pyrophosphate. A constitutive regulator cycle is also present for the synthesis and hydrolysis of fructose 2,6‐bisphosphate (F‐2,6‐P2) via a 2‐kinase and a 2‐phosphatase, respectively. The pathway catalyzed by the ATP‐PFK and F‐1,6‐bisphosphatase, the maintenance pathway, is fairly constant in maximum activity in various plant tissues and shows less regulation by F‐2,6‐P2. Plants use F‐2,6‐P2 initially to regulate the adaptive pathway at the reversible PPi‐PFK step. The adaptive pathway, catalyzed by PPi‐PFK, varies in maximum activity with a variety of phenomena such as plant development or changing biological and physical environments. Plants can change F‐2,6‐P2 levels rapidly, in less than 1 min when subjected to rapid environmental change, or change levels slowly over periods of hours and days as tissues develop. Both types of change enable plants to cope with the environmental and developmental changes that occur during their lifetimes. The two pathways of sugar metabolism can be efficiently linked by the cycling of uridylates and pyrophosphate required for sucrose breakdown via a proposed sucrose synthase pathway. The breakdown of sucrose via the sucrose synthase pathway requires half the net energy of breakdown via the invertase pathway. Pyrophosphate occurs in plant tissues as a substrate pool for biosynthetic reactions such as the PPi‐PFK or uridine diphosphate glucose pyrophosphorylase (EC 2.7.7.9; UDPG pyrophosphorylase) that function in the breakdown of imported sucrose. Also, pyrophosphate links the two glycolytic/gluco‐neogenic pathways; and in a reciprocal manner pyrophosphate is produced as an energy source during gluconeogenic carbon flow from F‐1,6‐P2 toward sucrose synthesis.

Product Inhibition of Potato Tuber Pyrophosphate:Fructose-6-Phosphate Phosphotransferase by Phosphate and Pyrophosphate

“…Rather, it may provide a way of modifying fluxes in response to external factors, or when large amounts of carbon are being moved between starch, sucrose and organic acids. This resembles the idea that plants may have 'maintenance' and 'adaptive' pathways for carbohydrate metabolism (5 Fru6P could allow a considerable flexibility in the response of primary metabolism to these contrasting demands.…”

“…It has been suggested that PFP could operate in a cycle with the phosphofructokinase or fructose-1,6-bisphosphatase to generate or consume PPi, respectively (1,5). The properties of PFP would suit it for a role in controlling the PPi concentration.…”

“…In this case, PFP might equally well operate in the gluconeogenic direction. Indeed, several studies of Fru2,6P2 levels and PFP activities in contrasting tissues have been interpreted as evidence that the reverse reaction provides carbon for synthesis of sugars, or PPi for sucrose mobilization via sucrose synthase (1,4,5,9,12,17 13,14,32). It is also known that Fru6P increases the affinity for Fru2,6P2, while Pi acts in the opposite manner as do a range of other anions (13,14,32).…”

Sucrose Synthase, Starch Accumulation, and Tomato Fruit Sink Strength

“…Acid invertase and sucrose synthase are both involved in the breakdown of sucrose. However, sucrose synthase requires half the net energy of the sucrose metabolic pathway catalyzed by invertase (Black et al, 1987). Studies of the distribution of these two enzymes suggest that high sucrose synthase activity is present in starch and sucrose storage sinks, whereas high acid invertase activity occurs in tissues in which active cell elongation is occurring (Sung et al, 1988).…”

Crassulacean acid metabolism photosynthesis: ‘working the night shift’

“…This discovery in CAM plants led the recognition of a new pathway of glycolysis in plants; led us to realize that pyrophosphate was a new and useful energy source in plants; led to the discovery of fructose 2,6-bisphosphate as our most potent regulator of plant carbohydrate metabolism; and led us to new aspects of sucrose metabolism (Carnal and Black 1983;Smyth and Black 1984;Black et al 1987Black et al , 1995. These follow-up discoveries were an extraordinary outcome in plant biochemistry, gained from studying the daily carbohydrate metabolism of CAM photosynthesis!…”