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Li, J.;  Kim, Y.;  Zhang, D. Source-To-Sink Transport of Sugar During Male Reproductive Development. Encyclopedia. Available online: https://encyclopedia.pub/entry/26015 (accessed on 16 September 2024).
Li J,  Kim Y,  Zhang D. Source-To-Sink Transport of Sugar During Male Reproductive Development. Encyclopedia. Available at: https://encyclopedia.pub/entry/26015. Accessed September 16, 2024.
Li, Jingbin, Yu-Jin Kim, Dabing Zhang. "Source-To-Sink Transport of Sugar During Male Reproductive Development" Encyclopedia, https://encyclopedia.pub/entry/26015 (accessed September 16, 2024).
Li, J.,  Kim, Y., & Zhang, D. (2022, August 10). Source-To-Sink Transport of Sugar During Male Reproductive Development. In Encyclopedia. https://encyclopedia.pub/entry/26015
Li, Jingbin, et al. "Source-To-Sink Transport of Sugar During Male Reproductive Development." Encyclopedia. Web. 10 August, 2022.
Source-To-Sink Transport of Sugar During Male Reproductive Development
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This entry is adapted from the peer-reviewed paper 10.3390/genes13081323

Sucrose is produced in leaf mesophyll cells via photosynthesis and exported to non-photosynthetic sink tissues through the phloem. The molecular basis of source-to-sink long-distance transport in cereal crop plants is of importance due to its direct influence on grain yield—pollen grains, essential for male fertility, are filled with sugary starch, and rely on long-distance sugar transport from source leaves. 

sugar partitioning phloem sink source sugar signaling

1. Introduction

Rice (Oryza sativa), the monocot model plant, is a major crop, meeting the food demands of more than 50% of the global population [1][2]. Reproductive development, which connects the dominant diploid sporophytic and short haploid gametophytic stages, is a critical element in grain production [3]. The male reproductive organ, the stamen, consists of a filament and an anther containing multiple specialized tissues that generate mature male gametophytes, the pollen grains, via a series of developmental events such as meristem specification, cell differentiation, meiosis, mitosis, and starch accumulation [4][5].
Sugars are the constituents of main anther, and play essential roles in cell structure formation, energy supply, and male fertility in response to environmental conditions [6]. In rice, the expression of Cell Wall Invertase 3 (OsCWIN3/OsINV4) correlates with sucrose accumulation and pollen sterility depending on temperature [7], while two MYB domain proteins, Carbon Starved Anther (CSA) and CSA2, regulate sugar partitioning and male fertility in response to photoperiod [8][9][10][11]. The sugar transporter OsXa13/OsSWEET11 plays essential roles in pollen development and disease resistance against bacterial blight [12][13].

2. Strategies of Source-to-Sink Sugar Partitioning

Carbon is fixed from carbon dioxide into carbohydrate in chloroplasts of leaf tissues, primarily mesophyll cells, and accumulated in the cytosol of the same cells. The energy demands of sink tissues, such as roots, flowers, and seeds, drive the export of sugars from the leaf, mainly in the form of sucrose, via long-distance transport in plant vasculature, the phloem [14]. Over half of the photo-assimilates (50–80%) are exported from source leaves to maintain non-photosynthetic sink tissues [15]. Carbohydrate partitioning from source-to-sink tissues comprises three elements [16]: phloem loading of sugars from source tissues; transportation in the sieve element of the phloem; phloem unloading of sugars to sink tissues [17].
Phloem is composed of several cell types, including parenchyma cells, sieve elements (SEs), and companion cells (CCs) [18][19]. Phloem loading is the first vital step in sugar’s long-distance transport—transferring the sugars from mesophyll cells to the SEs and CCs of the phloem [20][21][22]. Three different strategies are used for phloem loading by different plants according to the abundance of plasmodesmata, SUT activity, and the concentration gradient of photosynthates (Figure 1) [23].
Figure 1. Three strategies for phloem loading. (A) Symplastic pathway: sucrose accumulates in mesophyll cells and is passively translocated to the phloem through plasmodesmata (PD) along the concentration gradient. (B) Apoplastic pathway: sucrose is exported to the apoplast by SWEETs and, after diffusion, imported into the phloem by SUTs. (C) Polymer trapping: sucrose is passively exported to phloem companion cells and synthesized into RFOs that can only move into sieve element cells due to their larger molecular mass.
The symplastic pathway is a passive loading process, driven by concentration gradients between mesophyll cells and phloem tissue (Figure 1A) [21][24], whereby the sucrose accumulated in mesophyll cells diffuses through plasmodesmata to reach phloem CCs [21][24]. Most tree species employ passive loading in the mesophyll cells, which meets the anatomical feature with high plasmodesmatal frequencies in the phloem of minor veins [23][25][26]. In most herbaceous plants, the apoplastic pathway is the main strategy for phloem loading [19]. Sucrose from mesophyll cells is actively exported to the apoplast by SWEET proteins (consuming energy), diffuses within the apoplast, and is actively loaded to phloem CCs via SUTs against a concentration gradient (Figure 1B) [19][25]. Polymer trapping, the third phloem-loading strategy, is an energy-consuming symplastic process adopted by a small number of specific plants (Figure 1C) [26].

3. Proteins Involved in Sugar Partitioning

3.1. Sucrose Transporters (SUTs)

Sucrose transporters (SUTs) act as symporters to import the sucrose from the apoplasm into phloem CCs against the concentration gradient, driven by the motive force generated by H+-ATPases (Figure 1B) [25][27]. The 12 transmembrane domains of the SUT protein forms a pore to transport sucrose across the plasma membrane [28].
The first sucrose transporter (SoSUT) was found in spinach (Spinacea oleracea) by an elegant yeast complementation strategy [29]. Nine and five SUTs have been found in Arabidopsis and rice, respectively [30][31]. Based on sequence, sub-cellular location, and activity, SUTs have been classified into three types: type I (specific to eudicots, plasma membrane–localized); type II (present in all plants, plasma membrane–localized); and type III (present in all plants, vacuolar membrane–localized) [32]. In rice, OsSUT1, OsSUT3, OsSUT4, and OsSUT5 are type II SUTs, and OsSUT2 is a type III tonoplast SUT (Table 1) [32].
Table 1. Proteins involved in sugar metabolism in rice.
Gene Family Number of Genes Reported Genes/Reference
SUT 5 SUT1 [33][34];
SUT2 [35];
SUT3 [36];
SUT4, SUT5 [30]
SWEET 21 SWEET5 [37];
SWEET6a [38][39];
SWEET6b [39];
SWEET11 [12];
SWEET14 [13];
SWEET15 [40]
MST 64  
AZT subfamily 6 AZT3 [10]
ERD subfamily 6  
pGlcT subfamily 4  
Xylose subfamily 2  
STP subfamily 15 MST1, MST2, MST3 [41];
MST5 [42];
MST6 [43];
MST8 [8];
SPT17, SPT27 [38][39]
PLT subfamily 28  
INT subfamily 3  
Invertases 18  
VIN 2 VIN2 [44]
CIN 8 CIN8/Cyt-INV1 [45]
CWIN 8 GIF1 [46];
INV4 [7];
CWIN6 [39]
The shaded areas represent subfamilies of these proteins.

3.2. Sugars Will Eventually Be Exported Transporters (SWEETs)

SWEETs are a group of evolutionally conserved genes expressed in eukaryotes, prokaryotes, and archaea [47][48]. These genes, encoding MtN3/saliva domain proteins, were initially found to encode glucose transporters [49], and have since been found to be capable of transporting a variety of mono- and di-saccharides [37][50][51][52]. According to their protein structures, SWEET proteins encode either one or two MtN3/saliva domains [53].
Rice encodes 21 SWEET proteins that are involved in multiple biological processes (Table 1) [53]. OsSWEET11, containing two MtN3/saliva domains, acts as a glucose uniporter in panicles and anthers [12]. Its knockdown mutant reveals defects in microspore development, suggesting a function in male development [12]. OsSWEET11 is also upregulated in response to bacterial infection by Xanthomonas oryzae pv. oryzae [12]. OsSWEET14 has a similar disease response, and its knockout mutant showed growth retardation, reduced plant size, and insensitivity to bacterial infection [13].

3.3. Invertases (INVs)

Invertases (INVs) encode proteins that hydrolyze sucrose into glucose and fructose [54], classified according to sub-cellular location into vacuolar (VIN), cell wall (CWIN), or cytoplasmic (CIN) invertases (Table 1) [55][56]. CINs prefer a neutral pH of 7.0–7.8 in the cytosol, while VINs and CWINs have an optimal pH of 4.5–5.5 [55]. Rice has 19 invertase genes, including nine CWINs, two VINs, and eight VINs (Table 1) [57]. CWIN proteins bind to the cell wall and play essential roles in sugar transmembrane transport during phloem unloading [55].

3.4. Monosaccharide Transporters (MSTs)

Monosaccharide transporters (MSTs) are membrane proteins involved in the transmembrane transport of hexoses, hydrolyzed from sucrose by INVs, in sink tissues in the apoplastic pathway (Figure 1B) [58]. An Arabidopsis phylogeny of 53 MST proteins suggests seven subfamilies—AZT, XTPH, ERD, pGlcT, PLT, INT, and STP (Table 1)—many of whose expression patterns or function have not yet been characterized [59]. Among the seven subfamilies of MST proteins, AZT and XTPH proteins localize on the tonoplast and play essential roles in sugar transport to the tonoplast [60][61][62]. AtERD6, a member of ERD proteins, was proved to be involved in the transport of monosaccharides, whose expression was induced by abiotic stress [63]. pGlcT proteins are transporters of glucose, and PLT proteins are symporters of polyols and monosaccharides [64][65]. AtINT4, the first identified member of the INT proteins, exhibits H+ symporter activities for myoinositol in yeast (Saccharomyces cerevisiae) and Xenopus laevis oocytes [66]. MST members of the STP sub-family are H+/hexose cotransporters locating on plasma membranes, which transport a series of hexoses, including glucose, fructose, galactose, xylose, mannose, pentose, and ribose [58].

4. Roles of Sugar Transporters in Phloem Loading and Unloading

Photosynthesis—“source activity”—and sink energy utilization—“sink strength”—combine to raise plant productivity [17][67]. Understanding the processes of phloem loading in source leaves and unloading in sink tissues can improve source activity and sink strength, leading to higher grain yields (Figure 2). After long-distance phloem transport from source tissues, sugar (mainly sucrose) is unloaded in sink organs; however, this process will lead to sucrose accumulation in sink tissues (reduced sink strength), resulting in reduced efficiency in sugar transport and source activity (Figure 2) [68].
Figure 2. Schematic diagrams of sugar source-to-sink transport in rice. (A) High source activity in source leaves promotes phloem transport. (B) High sink strength results in high sugar demand, increasing the sugar transport.
In Arabidopsis, AtSUC2 is expressed in phloem CCs of minor leaf veins, which are supposed to be involved in the source-to-sink transition [69][70]. An AtSUT2 T-DNA insertion mutant line exhibits decreased sucrose exports from leaves, resulting in sucrose accumulation in leaves, and delayed root growth and flowering [71]. OsSUT1, a type II SUT like AtSUC2, is highly expressed in leaves, stems, and grains; however, knockdown lines of OsSUT1 do not show sucrose accumulation in source leaves [33][34]. OsSUT3, another type II SUT, is preferentially expressed in pollen, suggesting a function in pollen development and maturity rather than phloem loading in source leaves [36]. OsSUT2, a type III SUT, is involved in sucrose transfer across the tonoplast from the vacuole lumen to the cytosol in rice [35].
SWEETs transport mono- or di-saccharides across membranes for phloem transport [72]. In Arabidopsis, AtSWEET11/12 localizes in the plasma membrane of vascular tissues and participates in phloem transport [50]. Maize ZmSWEET4c functions in hexose transport during seed development, and its mutation demonstrates a lack of hexose transport and defect in seed filling [73]. In rice, OsSWEET11 and OsSWEET14, two response factors to bacterial infection, also show essential roles in grain filling, whose mutants reveal defective in grain filling, resulting in increased starch accumulation in the pericarp [13][74][75]. OsSWEET15, another symporter highly expressed in rice caryopses, is necessary for sucrose efflux from caryopses to grains during seed filling [40]. OsSWEET5 encodes a galactose transporter, whose overexpression causes growth retardation and precocious senescence in rice seedlings [37]. These SWEET proteins showed important roles in grain filling, demonstrating their biological function of sucrose transfer from caryopses (source) to grains (sink).
Cell wall invertases (CWINs) play important roles in apoplasmic unloading, decreasing the concentration of sucrose in sink tissues to improve sink strength [55][76]. In rice, grain yield significantly decreased when the expression of OsCWIN2 (GIF1) was suppressed [77], and a similar phenotype is observed in ZmCWIN2 (Incw2) mutants in maize (Zea mays) [74]. VfCWIN1 in Vicia faba, a dicot species, is also reported to impact seed size [75]. Moreover, OsCWIN3 (INV4) has high expression in rice anthers, and affects male fertility in response to temperature variations [7].

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Subjects: Developmental Biology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Jingbin Li
,
Yu-Jin Kim
,
Dabing Zhang
View Times: 612
Revisions: 2 times (View History)
Update Date: 15 Aug 2022
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