Current perspectives on the regulatory mechanisms of sucrose accumulation in sugarcane

Abstract

Sugars transported from leaves (source) to stems (sink) energize cell growth, elongation, and maintenance. which are regulated by a variety of genes. This review reflects progress and prospects in the regulatory mechanism for maximum sucrose accumulation, including the role of sucrose metabolizing enzymes, sugar transporters and the elucidation of post-transcriptional control of sucrose-induced regulation of translation (SIRT) in the accumulation of sucrose. The current review suggests that SIRT is emerging as a significant mechanism controlling Scbzip44 activities in response to endogenous sugar signals (via the negative feedback mechanism). Sucrose-controlled upstream open reading frame (SC-uORF) exists at the 5' leader region of Scbzip44's main ORF, which inhibits sucrose accumulation through post-transcriptional regulatory mechanisms. Sucrose transporters (SWEET1a/4a/4b/13c, TST, SUT1, SUT4 and SUT5) are crucial for sucrose translocation from source to sink. Particularly, SWEET13c was found to be a major contributor to the efflux in the transportation of stems. Tonoplast sugar transporters (TSTs), which import sucrose into the vacuole, suggest their tissue-specific role from source to sink. Sucrose cleavage has generally been linked with invertase isozymes, whereas sucrose synthase (SuSy)-catalyzed metabolism has been associated with biosynthetic processes such as UDP-Glc, cellulose, hemicellulose and other polymers. However, other two key sucrose-metabolizing enzymes, such as sucrose-6-phosphate phosphohydrolase (S6PP) and sucrose phosphate synthase (SPS) isoforms, have been linked with sucrose biosynthesis. These findings suggest that manipulation of genes, such as overexpression of SPS genes and sucrose transporter genes, silencing of the SC-uORF of Scbzip44 (removing the 5' leader region of the main ORF that is called SIRT-Insensitive) and downregulation of the invertase genes, may lead to maximum sucrose accumulation. This review provides an overview of sugarcane sucrose-regulating systems and baseline information for the development of cultivars with higher sucrose accumulation.

Keywords: Post-transcriptional factors; Source-sink communication; Sucrose accumulation; Sucrose metabolizing enzymes; Sugarcane genetic engineering.

Fig. 1

A potential pathway for sucrose transportation in a sugarcane. Sucrose synthesizes in sugarcane leaf mesophyll cells and is temporarily stored in leaf vacuoles. Further, the sucrose is transported by the transporter gene through either the symplastic pathway or the apoplastic pathway. During transportation, sucrose is hydrolyzed into hexose (fructose and glucose) at different locations by invertases like the cell wall, cytoplasmic, and vacuolar invertases. In the cytoplasm, sucrose is resynthesized by SPS and SPP. Finally stored in vacuoles. Abbreviations: Cytoplasmic invertase (CyIN), vacuolar invertase (VIN), cell wall invertase (CWIN), sucrose synthase (SuS), sucrose phosphate synthase (SPS), sucrose phosphate phosphatase (SPP), sucrose transporters (SUTs), Fructose (Fru), uridine diphosphate glucose (UDP-Glc). Note: The green circle indicates sucrose transporters and the black circle indicates hexose transporters, while the arrow indicates sucrose flow from source to sink.

Fig. 2

(A) Basic metabolic supply-demand system model adapted from Ref. [26]. The feedback inhibition of the supply process (red line), which is exerted through the concentration of the intermediate (P), is what regulates how much product is formed. This equilibrium between supply and demand, in turn, determines the concentration of the intermediate (P). (B) Demand in plants is probably the result of metabolic processes such as growth and development, respiration and storage, especially in species with high sucrose storage levels like sugarcane. As a result of the supply's sensitivity to intermediate concentrations in this example, sucrose feedback inhibition is suggested.

Fig. 3

Hypothetical model of phloem loading mechanisms in plants: (A) apoplastic loading, symplastic loading, and polymer entrapment. Apoplastic loading involves sucrose entering the cytoplasm via the cell wall via the proton motive force, requiring transmembrane protein transporters. (B) Symplastic loading involves sucrose transporting cells to cells via plasmodesmata, allowing carbon to move into the phloem or companion cell complex without being transported against a concentration gradient. (C) Polymer entrapment involves an energy-intensive step where sucrose enters specialized partner cells that interact symbiotically with photosynthetic cells. Raffinose and stachyose produced from sucrose are too large to disperse back via plasmodesmata. Abbreviations: Photosynthetic cell (PC), companion cell (CC), intermediary cell (IC) and sieve element (SE). Arrows point out the directional flow of sugars via cells.

Fig. 4

A hypothetical model of the mechanism known as sucrose-induced repression of translation (SIRT) is intended to elucidate how expression of the “Scbzip44″ gene in sugarcane plant cells accumulates maximum sucrose (A) In normal cells, the Scbzip44 gene works as a transactivator for the ASN gene, and the ASN gene activates the metabolic reprogramming pathways. However, after a certain level of sucrose accumulates in sugarcane stems due to the negative feedback inhibition signaled by sucrose to Sc-uORF, which inhibits the Scbzip44 gene translation, sucrose is limited in this cell. (B) On the other hand, in SIRT-insensitive or deregulated cells with overexpression of the ox-Scbzip44 gene, sucrose accumulates continuously without disruption, so maximum sucrose is obtained. Abbreviations: Asparagine synthase (ASN), Sucrose phosphate phosphatase (SPP), Sucrose phosphate synthase (SPS), Sucrose-controlled upstream open reading frame (SC-uORF), Overexpression of sugarcane zip transcription factor gene (Ox-Scbzip44).