Sugar Repression of Mannitol Dehydrogenase Activity in Celery Cells

Abstract

We present evidence that the activity of the mannitolcatabolizing enzyme mannitol dehydrogenase (MTD) is repressed by sugars in cultured celery (Apium graveolens L.) cells. Furthermore, this sugar repression appears to be mediated by hexokinases (HKs) in a manner comparable to the reported sugar repression of photosynthetic genes. Glucose (Glc)-grown cell cultures expressed little MTD activity during active growth, but underwent a marked increase in MTD activity, protein, and RNA upon Clc starvation. Replenishment of Glc in the medium resulted in decreased MTD activity, protein, and RNA within 12 h. Addition of mannoheptulose, a competitive inhibitor of HK, derepressed MTD activity in Glc-grown cultures. In contrast, the addition of the sugar analog 2-deoxyglucose, which is phosphorylated by HK but not further metabolized, repressed MTD activity in mannitol-grown cultures. Collectively, these data suggest that HK and sugar phosphorylation are involved in signaling MTD repression. In vivo repression of MTD activity by galactose (Cal), which is not a substrate of HK, appeared to be an exception to this hypothesis. Further analyses, however, showed that the products of Cal catabolism, Glc and fructose, rather than Cal itself, were correlated with MTD repression.

Overexpression of Arabidopsis Hexokinase in Tomato Plants Inhibits Growth, Reduces Photosynthesis, and Induces Rapid Senescence

“…Hexokinase may be involved in the regulation of additional pathways affected by sugars in addition to photosynthesis, growth, and senescence (Graham et al, 1994;Perata et al, 1997;Prata et al, 1997;Smeekens and Rook, 1997). Photosynthesis, growth, and senescence are also regulated by light and by hormones, such as auxin, cytokinin, gibberellic acid, brassinosteroids, and ethylene.…”

“…Furthermore, sugars affect developmental and metabolic processes throughout the life cycle of the plant. These processes include germination, growth, flowering, senescence, sugar metabolism, and photosynthesis (von Schaewen et al, 1990;Dickinson et al, 1991;Stitt et al, 1991; Goldschmidt and Huber, 1992; Huber and Hanson, 1992; Bernier et al, 1993; Ding et al, 1993; Yang et al, 1993;Thomas and Rodriguez, 1994; Dangl et al, 1995; Kovtun and Daie, 1995; Jang and Sheen, 1997;Perata et al, 1997;Prata et al, 1997;Smeekens and Rook, 1997; Wingler et al, 1998).…”

“…Recently, it was demonstrated that hexokinase, which catalyzes sugar phosphorylation, the first step of hexose metabolism, is involved in glucose sensing (Jang and Sheen, 1994; Jang et al, 1997;Perata et al, 1997;Prata et al, 1997). Sugar-repressible, photosynthetic, and metabolic genes have been used to show that phosphorylation of sugars by hexokinase is critical for sugar signaling.…”

“…Furthermore, sugars affect developmental and metabolic processes throughout the life cycle of the plant. These processes include germination, growth, flowering, senescence, sugar metabolism, and photosynthesis (von Schaewen et al, 1990;Dickinson et al, 1991;Stitt et al, 1991; Goldschmidt and Huber, 1992; Huber and Hanson, 1992; Bernier et al, 1993; Ding et al, 1993; Yang et al, 1993;Thomas and Rodriguez, 1994; Dangl et al, 1995; Kovtun and Daie, 1995; Jang and Sheen, 1997;Perata et al, 1997;Prata et al, 1997;Smeekens and Rook, 1997; Wingler et al, 1998).Photosynthesis is regulated by sugar levels, and this regulation overrides that of light, tissue type, and developmental stage (Sheen, 1990;von Schaewen et al, 1990; Krapp et al, 1993). Increased concentrations of externally supplemented sugar or internal modification of sugar content inhibits photosynthesis and causes stunted growth of various plants (von Schaewen et al, 1990;Dickinson et al, 1991;Sonnewald et al, 1991Sonnewald et al, , 1993 Goldschmidt and Huber, 1992; Jones et al, 1996; Jang et al, 1997).…”

Dissecting the roles of osmolyte accumulation during stress

“…Synthesis of Mtl via Man-6-P occurs naturally in a limited number of plant species (Stoop et al 1996). Sugar repression of MTD is apparently mediated by active HK (Prata et al 1997). Pathways of choline and DMSP synthesis are discussed by Rhodes & Hanson (1993).…”