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. Here, we overview sugar partitioning via phloem transport in rice, especially where relevant for male reproductive development.
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][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][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
[9][6]. In rice, the expression of
Cell Wall Invertase 3 (
OsCWIN3/OsINV4) correlates with sucrose accumulation and pollen sterility depending on temperature
[10][7], while two MYB domain proteins, Carbon Starved Anther (CSA) and CSA2, regulate sugar partitioning and male fertility in response to photoperiod
[11,12,13,14][8][9][10][11]. The sugar transporter OsXa13/OsSWEET11 plays essential roles in pollen development and disease resistance against bacterial blight
[15,16][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 [17][14]. Over half of the photo-assimilates (50–80%) are exported from source leaves to maintain non-photosynthetic sink tissues
[18][15]. Carbohydrate partitioning from source-to-sink tissues comprises three elements
[19][16]: phloem loading of sugars from source tissues; transportation in the sieve element of the phloem; phloem unloading of sugars to sink tissues
[20][17].
Phloem is composed of several cell types, including parenchyma cells, sieve elements (SEs), and companion cells (CCs)
[21,22][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
[23,24,25][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)
[26][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)
[24[21][24],
27], whereby the sucrose accumulated in mesophyll cells diffuses through plasmodesmata to reach phloem CCs
[24,27][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
[26,28,29][23][25][26]. In most herbaceous plants, the apoplastic pathway is the main strategy for phloem loading
[22][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)
[22,28][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)
[29][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)
[28,32][25][27]. The 12 transmembrane domains of the SUT protein forms a pore to transport sucrose across the plasma membrane
[33][28].
The first sucrose transporter (
SoSUT) was found in spinach (
Spinacea oleracea) by an elegant yeast complementation strategy
[34][29]. Nine and five SUTs have been found in
Arabidopsis and rice, respectively
[35,36][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)
[37][32]. In rice, OsSUT1, OsSUT3, OsSUT4, and OsSUT5 are type II SUTs, and OsSUT2 is a type III tonoplast SUT (
Table 1)
[37][32].
Table 1.
Proteins involved in sugar metabolism in rice.