Mannose Inhibits Arabidopsis Germination via a Hexokinase-Mediated Step1

Abstract

Low concentrations of the glucose (Glc) analog mannose (Man) inhibit germination of Arabidopsis seeds. Man is phosphorylated by hexokinase (HXK), but the absence of germination was not due to ATP or phosphate depletion. The addition of metabolizable sugars reversed the Man-mediated inhibition of germination. Carbohydrate-mediated regulation of gene expression involving a HXK-mediated pathway is known to be activated by Glc, Man, and other monosaccharides. Therefore, we investigated whether Man blocks germination through this system. By testing other Glc analogs, we found that 2-deoxyglucose, which, like Man, is phosphorylated by HXK, also blocked germination; no inhibition was observed with 6-deoxyglucose or 3-O-methylglucose, which are not substrates for HXK. Since these latter two sugars are taken up at a rate similar to that of Man, uptake is unlikely to be involved in the inhibition of germination. Furthermore, we show that mannoheptulose, a specific HXK inhibitor, restores germination of seeds grown in the presence of Man. We conclude that HXK is involved in the Man-mediated repression of germination of Arabidopsis seeds, possibly via energy depletion.Among the many regulatory systems and signals in plants, carbon-metabolite-mediated gene regulation has been receiving growing attention in the past few years (for reviews, see

Sugar Coordinately and Differentially Regulates Growth- and Stress-Related Gene Expression via a Complex Signal Transduction Network and Multiple Control Mechanisms

“…Upon entry into the plant cell, Man is phosphorylated by hexokinase, yielding Man-6-P. Man-6-P is then slowly processed by plant cells, since the enzymes required for this process are either absent or exist in very low concentrations (Walder and Sivak, 1986). Man has been shown to inhibit germination of Arabidopsis seeds due to phosphorylation by hexokinase and not due to ATP or P depletion (Peto et al, 1999). As shown in Figure 6, the effect of Glc on mRNA accumulation of SU and SD genes was similar as in Figure 5.…”

Glucose delays seed germination in Arabidopsis thaliana

“…The finding that even low concentrations (1%) of glucose are able to delay seed germination (Fig. 1a) was unexpected, since low concentrations of metabolizable sugars are effective in relieving the inhibitory action of ABA and mannose during germination (Garciarrubio et al 1997;Pego et al 1999;Finkelstein and Lynch 2000). As expected, elevated levels of glucose (up to 5%) restricted germination more severely.…”

“…This is shown by the reduced seed dormancy of aba and several abi mutants (Koornneef et al 1982(Koornneef et al , 1984, while the GA-deficient mutants (ga1, ga2 and ga3) are incapable of germination (Debeaujon and Koornneef 2000;Bentsink and Koornneef 2002). Previous studies showed that mannose and 2-deoxyglucose, both of which are substrates for HXK, are potent inhibitors of Arabidopsis seed germination (Pego et al 1999). Sugar uptake is probably not involved since the non-metabolizable sugars 6-DG and 3-OMG do not affect germination in this assay.…”

“…Most of these screens revealed a central role for the plant hormones abscisic acid (ABA; Arenas-Huertero et al 2000;Huijser et al 2000;Laby et al 2000;Rook et al 2001) and ethylene (Zhou et al 1998;Gibson et al 2001) in sugar-induced signalling during early seedling development (for review, see Gazzarrini and McCourt 2001;Rolland et al 2002). Many other processes are affected by sugars as well, including germination (Garciarrubio et al 1997;Pego et al 1999;Finkelstein and Lynch 2000).…”

Monosaccharide Absorption Activity of Arabidopsis Roots Depends on Expression Profiles of Transporter Genes under High Salinity Conditions

“…4C). In addition, mannose strongly inhibits seed germination and postgermination growth (27). It has been previously reported that the stp1 mutant exhibits insensitivity to galactose and mannose (11).…”