Abstract

The extent to which vacuolar sugar transport activity affects molecular, cellular, and developmental processes in Arabidopsis (Arabidopsis thaliana) is unknown. Electrophysiological analysis revealed that overexpression of the tonoplast monosaccharide transporter TMT1 in a tmt1-2::tDNA mutant led to increased proton-coupled monosaccharide import into isolated mesophyll vacuoles in comparison with wild-type vacuoles. TMT1 overexpressor mutants grew faster than wild-type plants on soil and in high-glucose (Glc)-containing liquid medium. These effects were correlated with increased vacuolar monosaccharide compartmentation, as revealed by nonaqueous fractionation and by chlorophyll(ab)-binding protein1 and nitrate reductase1 gene expression studies. Soil-grown TMT1 overexpressor plants respired less Glc than wild-type plants and only about half the amount of Glc respired by tmt1-2::tDNA mutants. In sum, these data show that TMT activity in wild-type plants limits vacuolar monosaccharide loading. Remarkably, TMT1 overexpressor mutants produced larger seeds and greater total seed yield, which was associated with increased lipid and protein content. These changes in seed properties were correlated with slightly decreased nocturnal CO(2) release and increased sugar export rates from detached source leaves. The SUC2 gene, which codes for a sucrose transporter that may be critical for phloem loading in leaves, has been identified as Glc repressed. Thus, the observation that SUC2 mRNA increased slightly in TMT1 overexpressor leaves, characterized by lowered cytosolic Glc levels than wild-type leaves, provided further evidence of a stimulated source capacity. In summary, increased TMT activity in Arabidopsis induced modified subcellular sugar compartmentation, altered cellular sugar sensing, affected assimilate allocation, increased the biomass of Arabidopsis seeds, and accelerated early plant development.

Highlights

  • The extent to which vacuolar sugar transport activity affects molecular, cellular, and developmental processes in Arabidopsis (Arabidopsis thaliana) is unknown

  • Respiration of Newly Imported Glc, and Expression of chlorophyllab-binding protein1 (CAB1) and nitrate reductase1 gene (NR1) in Soil-Grown Arabidopsis In Figure 4B, we reported altered subcellular sugar compartmentation in TMT1 overexpressor plants

  • It has been demonstrated that sugar deposition in vacuoles in the form of fructans greatly enhances leaf storage capacity (Pollock, 1986), the extent to which sugar transport across the vacuolar membrane limits plant performance has not been determined

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Summary

Introduction

The extent to which vacuolar sugar transport activity affects molecular, cellular, and developmental processes in Arabidopsis (Arabidopsis thaliana) is unknown. TMT1 overexpressor mutants grew faster than wild-type plants on soil and in high-glucose (Glc)-containing liquid medium. These effects were correlated with increased vacuolar monosaccharide compartmentation, as revealed by nonaqueous fractionation and by chlorophyllab-binding protein and nitrate reductase gene expression studies. TMT1 overexpressor mutants produced larger seeds and greater total seed yield, which was associated with increased lipid and protein content These changes in seed properties were correlated with slightly decreased nocturnal CO2 release and increased sugar export rates from detached source leaves. Sugars are required for the synthesis of cell walls and carbohydrate polymers They are necessary for starch accumulation and serve as precursors for a range of primary and secondary plant intermediates. Both facilitated diffusion and proton-driven antiport mechanisms have been described for monosaccharide and Suc transport across the vacuolar membrane (Thom and Komor, 1984; Daie and Wilusz, 1987; Martinoia et al, 1987; Shiratake et al, 1997; Neuhaus, 2007)

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