We show here that a cell-wall invertase encoded by the Incw1 gene is regulated at both the transcriptional and posttranscriptional levels by sugars in a heterotrophic cell suspension culture of maize. The Incw1 gene encoded two transcripts: Incw1-S (small) and Incw1-L (large); the size variation was attributable to different lengths in the 3 untranslated region. Both metabolizable and nonmetabolizable sugars induced Incw1-L RNA apparently by default. However, only the metabolizable sugars, sucrose and D-glucose, were associated with the increased steady-state abundance of Incw1-S RNA, the concomitant increased levels of INCW1 protein and enzyme activity, and the downstream metabolic repression of the sucrose synthase gene, Sh1. Conversely, nonmetabolizable sugars, including the two glucose analogs 3-O-methylglucose and 2-deoxyglucose, induced greater steady-state levels of the Incw1-L RNA, but this increase did not lead to either an increase in the levels of the INCW1 protein͞enzyme activity or the repression of the Sh1 gene. We conclude that sugar sensing and the induction of the Incw1 gene is independent of the hexokinase pathway. More importantly, our results also suggest that the 3 untranslated region of the Incw1 gene acts as a regulatory sensor of carbon starvation and may constitute a link between sink metabolism and cellular translation in plants.The enzyme invertase (EC 3.2.1.26), also known as -fructofuranosidase, is known to catalyze sucrose (suc) cleavage to its monosaccharide constituents, glucose (glc) and fructose, in an irreversible manner. At least two forms of the enzyme, soluble and particulate, are features common to all invertases, and recent molecular analyses indicate that each belongs to two distinct class of small gene families (ref. 1 and references therein). The physiological role of the invertases is believed to be in suc partitioning between source and sink regions of the plant. In general, the vacuolar invertases are believed to be important in the regulation of hexose levels in certain specific tissues and in the use of stored suc in vacuoles. The cell-wall forms (extracellular or secreted) are associated with rapidly growing tissues and have been implicated in phloem unloading and source͞sink regulation (2).Although the experimental evidence is largely correlative in nature, a lot of insight regarding the roles of invertases is now emerging from studies of transgenic or mutant plants. Among several studies on transgenic plants, the most detailed analyses are reported in potato where yeast invertase has been expressed in both the cytosol and apoplast (3). Tissue-specific elevated expression of invertase in both cellular locations leads to substantial reductions in tuber suc content and a corresponding large increase in glc content. More importantly, the apoplastic and cytosolic increases in enzyme activities are associated with different phenotypic responses: an increased tuber size but reduced tuber number in the former and a reversed pattern in the latter. In contrast, w...