Abstract
Both sorbitol and sucrose are imported into apple fruit from leaves. The metabolism of sorbitol and sucrose fuels fruit growth and development, and accumulation of sugars in fruit is central to the edible quality of apple. However, our understanding of the mechanisms controlling sugar metabolism and accumulation in apple remains quite limited. We identified members of various gene families encoding key enzymes or transporters involved in sugar metabolism and accumulation in apple fruit using homology searches and comparison of their expression patterns in different tissues, and analyzed the relationship of their transcripts with enzyme activities and sugar accumulation during fruit development. At the early stage of fruit development, the transcript levels of sorbitol dehydrogenase, cell wall invertase, neutral invertase, sucrose synthase, fructokinase and hexokinase are high, and the resulting high enzyme activities are responsible for the rapid utilization of the imported sorbitol and sucrose for fruit growth, with low levels of sugar accumulation. As the fruit continues to grow due to cell expansion, the transcript levels and activities of these enzymes are down-regulated, with concomitant accumulation of fructose and elevated transcript levels of tonoplast monosaccharide transporters (TMTs), MdTMT1 and MdTMT2; the excess carbon is converted into starch. At the late stage of fruit development, sucrose accumulation is enhanced, consistent with the elevated expression of sucrose-phosphate synthase (SPS), MdSPS5 and MdSPS6, and an increase in its total activity. Our data indicate that sugar metabolism and accumulation in apple fruit is developmentally regulated. This represents a comprehensive analysis of the genes involved in sugar metabolism and accumulation in apple, which will serve as a platform for further studies on the functions of these genes and subsequent manipulation of sugar metabolism and fruit quality traits related to carbohydrates.
Highlights
Carbohydrates provide energy and building blocks for plant growth and development
Blastp searches of the Malus Genome Database, using A. thaliana invertase, SUSY, HK, sucrose-phosphate synthase (SPS), SUT, tonoplast monosaccharide transporters (TMTs) and vacuolar glucose transporter (vGT) sequences as query, allowed the identification of candidate genes in Malus, and these genes are expressed in Malus transcriptome based on their ESTs in Genbank
Sugar metabolism in apple fruit is developmentally regulated to match the high requirements for energy and intermediates during the early stage of fruit development and sugar accumulation from the beginning of cell expansion to fruit maturity
Summary
Carbohydrates provide energy and building blocks for plant growth and development. In addition, soluble sugars, including sucrose (Suc), glucose (Glc) [1,2] and fructose (Fru) [3,4], are known to act as signal molecules to regulate the expression of many key genes involved in plant metabolic processes and defense responses, regulating plant growth and development [1,5]. Plants have evolved an elaborate system for sugar metabolism and accumulation in sink cells (Figure 1) We name this system as Suc-Suc cycle (previously called ‘futile recycles’ [6]). In this system, once Suc is transported into sink cells (e.g. fruit, root or shoot tips), it is converted to Fru and Glc by neutral invertase (NINV, EC 3.2.1.26), or to Fru and UDP-glucose (UDPG) by sucrose synthase (SUSY, EC 2.4.1.13). Suc can be converted to Glc and Fru by vacuolar acid invertase (vAINV) [1] This system operates in such a way that it allows carbon to be allocated into different pathways to satisfy sink growth and development, and coordinates sugar metabolism and accumulation and maintains the balance in osmotic potential and turgor between cytosol and other subcellular compartments
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