Subcellular compartmentation of sugar signaling: links among carbon cellular status, route of sucrolysis, sink-source allocation, and metabolic partitioning

Abstract

Recent findings suggest that both subcellular compartmentation and route of sucrolysis are important for plant development, growth, and yield. Signaling effects are dependent on the tissue, cell type, and stage of development. Downstream effects also depend on the amount and localization of hexoses and disaccharides. All enzymes of sucrose metabolism (e.g., invertase, hexokinase, fructokinase, sucrose synthase, and sucrose 6-phosphate synthase) are not produced from single genes, but from paralog families in plant genomes. Each paralog has unique expression across plant organs and developmental stages. Multiple isoforms can be targeted to different cellular compartments (e.g., plastids, mitochondria, nuclei, and cytosol). Many of the key enzymes are regulated by post-transcriptional modifications and associate in multimeric protein complexes. Some isoforms have regulatory functions, either in addition to or in replacement of their catalytic activity. This explains why some isozymes are not redundant, but also complicates elucidation of their specific involvement in sugar signaling. The subcellular compartmentation of sucrose metabolism forces refinement of some of the paradigms of sugar signaling during physiological processes. For example, the catalytic and signaling functions of diverse paralogs needs to be more carefully analyzed in the context of post-genomic biology. It is important to note that it is the differential localization of both the sugars themselves as well as the sugar-metabolizing enzymes that ultimately led to sugar signaling. We conclude that a combination of subcellular complexity and gene duplication/subfunctionalization gave rise to sugar signaling as a regulatory mechanism in plant cells.

Keywords: AGPase; cell organelles; hexokinase; signal transduction; sucrose synthase; sucrose/hexose ratio; sugar signaling.

FIGURE 1

Central metabolism in photosynthetic cells. Carbon is converted into starch in the plastid and sucrose (Suc), in the cytosol. Suc is partitioned into different pathways by multiple isozymes in the different subcellular compartments. Signaling metabolites (Pi, T6P) coordinate fluxes within the cytosol and the plastids. BE, branching enzyme; cBAM, pBAM, cytosolic and plastidial beta-amylase; CBB; Calvin–Benson–Bassham; CS, cellulose synthase; DB, debranching enzyme; DHAP; dihydroxyacetone phosphate; Fru, fructose; cFBPase, pFBPase, cytosolic and plastidial Fructose-1,6-bisphosphate phosphatase; FK, fructokinase; FT, fructosyl-transferase; Glu, glucose; G6P, glucose-6P; G1P, glucose-1P; GT, glucose transporter; GWD, glucan water dikinase; cHxk, mHxk, nHxk, pHxk, cytosolic, mitochondrial, nuclear, and plastidial hexokinase; cInv, cwInv, pInv, vInv, cytosolic, cell wall, plastidial, and vacuolar invertase; Malt, maltose; Mex1, maltose exporter; Pi, inorganic phosphate; PPi, pyrophosphate; Pyr, pyruvate; S6P, sucrose-6-P; SBPase, sedoheptulose-1,7-bisphosphate phosphatase; SPP, sucrose-6-P phosphatase; SPS, sucrose-6-P synthase; SS, starch synthase; SUS, sucrose synthase; SUT, sucrose transporter; Tre, trehalose; T6P, trehalose-6-phosphate; TCA, tricarboxylic acid cycle; TPP, trehalose-6-P phosphatase; TPT, triose-P translocator; VDAC, voltage-dependent anion channel.