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Gahlaut, V.; Gautam, T.; Dutta, M.; Jaiswal, V.; Zinta, G.; , . SWEET Sugar Transporters. Encyclopedia. Available online: https://encyclopedia.pub/entry/21911 (accessed on 21 December 2024).
Gahlaut V, Gautam T, Dutta M, Jaiswal V, Zinta G,  . SWEET Sugar Transporters. Encyclopedia. Available at: https://encyclopedia.pub/entry/21911. Accessed December 21, 2024.
Gahlaut, Vijay, Tinku Gautam, Madhushree Dutta, Vandana Jaiswal, Gaurav Zinta,  . "SWEET Sugar Transporters" Encyclopedia, https://encyclopedia.pub/entry/21911 (accessed December 21, 2024).
Gahlaut, V., Gautam, T., Dutta, M., Jaiswal, V., Zinta, G., & , . (2022, April 19). SWEET Sugar Transporters. In Encyclopedia. https://encyclopedia.pub/entry/21911
Gahlaut, Vijay, et al. "SWEET Sugar Transporters." Encyclopedia. Web. 19 April, 2022.
SWEET Sugar Transporters
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This entry is adapted from the peer-reviewed paper 10.3390/cells11081303

Sugars are the major source of energy in living organisms and play important roles in osmotic regulation, cell signaling and energy storage. SWEETs (Sugars Will Eventually be Exported Transporters) are the most recent family of sugar transporters that function as uniporters, facilitating the diffusion of sugar molecules across cell membranes. In plants, SWEETs play roles in multiple physiological processes including phloem loading, senescence, pollen nutrition, grain filling, nectar secretion, abiotic (drought, heat, cold, and salinity) and biotic stress regulation. 

Sugars Will Eventually be Exported Transporters Genes Abiotic Stress

1. Introduction

Photosynthetic organisms synthesize sugars during photosynthesis, a primary source of carbon and energy in cells [1]. Synthesized sugars are assimilated, transported, and distributed from source to sink tissues through the process of carbohydrate partitioning [1]. Sucrose is the main product of photosynthetic reactions, synthesized explicitly in the cytosol and transported to the sink organs [2]. Sucrose acts as a signaling molecule to control growth and differentiation [3]. Several research provide a detailed account of carbon partitioning, sugar metabolism, and signaling in plants [1][2][4][5][6][7][8]. Sugars are involved in various plant growth and developmental processes by acting as the source of carbon skeletons, the substrate of respiratory reactions, intermediate metabolites in biochemical reactions, storage substances, osmolyte, and signals in biotic and abiotic stresses [9][10][11][12][13][14]. The demand for sugar increases in the shoot/root apical meristem, flower buds, and seed/fruits organs [2][15][16]. Significant increases in sugar concentrations also occur under biotic and abiotic stresses such as cold, drought, phosphorus starvation, and pathogen attack [9][10][12][17]. In contrast, sugar levels decline under reduced oxygen conditions [9][13]. Additionally, sugars play a crucial role in regulating reproductive events such as pollen germination [18]. Thus, sugar metabolites form the core of the plant metabolism in response to developmental and environmental cues.
Sugar transporters across cell membranes mediate sugar translocation. These are evolutionally conserved genes present in bacteria, fungi, archaea, and plants [5][19][20][21]. Sugar transporters are classified into the following three types in plants: monosaccharide transporters (MSTs), sucrose transporters (SUTs), and the most recent type, SWEETs (Sugars Will Eventually be Exported Transporters) [5][19]. The major facilitator superfamily (MFS) transporters contain MSTs and SUTs and are primarily involved in sugar influx into the cytosol. However, some MSTs, namely tonoplast sugar transporter (TST), and the vacuolar glucose transporter (vGTs) are involved in transporting sugars from the cytosol to vacuoles and act as H+/sugar antiporters [22]. Both MSTs and SUTs contain 12 transmembrane α-helices and mediate membrane transport of different sugars [23][24]. MSTs are localized in plasma membranes and membranes of cell organelles such as chloroplast, Golgi, and vacuoles [25][26][27][28][29][30][31].

2. Role of SWEET Genes in Plant Development

2.1. Nectar Secretion

Nectar secretion is an essential and complex process to attract pollinators, which helps in pollination and maintaining genetic diversity in flowering plants. Nectar is produced in specialized organs called nectaries located inside or outside flowers. Furthermore, NEC1, an AtSWEET9 homolog, is predominantly expressed in the nectaries of Petunia hybrid and is assumed to play a role in nectar secretion [32]. A clade III member, SWEET9, is characterized as a nectary-specific sugar transporter in Arabidopsis, mustard and wild tobacco (Nicotiana attenuata) [33]. It functions in sucrose secretion from nectary parenchyma into apoplast, and mutation leads to a loss of nectar secretion. In other crops such as Hevea brasiliensis, Medicago truncatula, Pisum sativum orthologues of AtSWEET9 exhibited male flower-specific abundant expression, indicating a similar function to nectar production [34][35].

2.2. Leaf Senescence

Leaf senescence is an important trait that influences plant yield and nutritional quality. Carbohydrate offloading is mediated by SWEET (Clade II and III) and SUT (SUT1 and SUT2) in the senescing leaves [36]. The SWEET15, also called SAG29 (Senescence-Associated Gene 29), functions by remobilizing carbohydrates during senescence [37]. During senescence, SWEET15 is upregulated and can be used as a senescence marker. Overexpression of AtSWEET15 in Arabidopsis resulted in accelerated senescence that suggests its role in phloem loading during senescence [36]. The SAG gene (SAG101) encodes the membrane acyl hydrolase that regulates membrane hydrolysis in the early stages of senescence. The accumulation of hexose sugars (mainly glucose, fructose end galactose) in senescent leaves also leads to the speculation that clade II SWEETs may also function in carbon partitioning during senescence [37]. The OsSWEET5 belongs to clade II and is involved in the galactose transporter in rice. The overexpression of OsSWEET5 causes early leaf senescence, growth retardation, and change in auxin levels at the seedling stage in rice [38]. Increased clad II and III SWEET genes expression have been reported in senescing leaves of Pisum sativum and Brassica rapa [39][40]. In pear, the expression of PbSWEET4 (clade III member), a homolog of AtSWEET15, is localized in the cell membrane. The expression of the PbSWEET4 gene is potentially related to leaf development and is highly expressed in older leaves. The overexpression of PbSWEET4 in strawberry plants resulted in a reduced sugar and chlorophyll content and accelerated leaf senescence [41]. Overall, this suggests that SWEET genes can be modulated to alter leaf senescence traits in plants.

2.3. Fruit and Seed Development

Recent studies on gene expression in different plant species, including pineapple, apple, and pear, demonstrate the role of SWEETs in fruit development. For instance, in pineapple two genes, namely AnmSWEET-5 and 11 demonstrated up-regulation at the early phases of fruit development [42]. In apple, nine SWEET genes were abundantly expressed during apple fruit development. Two genes, MdSWEET9b and 15a, were associated with fruit sugar accumulation and likely to be implicated in fruit development [43]. Recently, in pear, histone acetylation-mediated regulation of SWEET genes was involved in fruit development [44]. Comparative transcriptomics of two pear varieties, ‘Nanguo’ (NG; low sucrose content) and its bud sport (BNG; high sucrose content) revealed that the PuSWEET15 gene is induced in BNG fruit. PuSWEET15 overexpression in NG fruit induced sucrose content, while silencing in BNG fruit reduced the sucrose level.
SWEET genes also play an essential role during seed development. An increase in transcript levels of several SWEET genes (ZmSWEET4c, 6b, 11, 13a, 13b, 14b and 15a) was observed during seed germination in maize [45]. These genes participate in the sucrose efflux from scutellum to embryo axis. In crops, yield is determined by the allocation of sugars from leaves to seed, which is carried out by specific SWEET transporters. In Arabidopsis, three SWEET genes (SWEET11, 12, and 15) of clad III showed spatiotemporal expression during seed development and might help to transport sucrose from seed coat to the developing embryo. Triple mutant lines of atsweet11:12:15 produce retarded embryos with reduced seed weight and low starch and lipid content, resulting in wrinkled seeds production [36]. In rice, the double knockout of ossweet11:15 accrued starch in the pericarp, whereas caryopses did not comprise a functional endosperm (Yang et al. 2018). However, the knockout of a single gene in rice (OsSWEET11) and soybean (GmSWEET15) also produces the same phenotype, i.e., decreased sucrose concentration in the embryo resulting in seed abortion [46][47]. This demonstrates that SWEET transports sucrose from seed coat to the developing embryo and plays a vital role in seed development. However, in some cases, clade II SWEET genes which transport mainly hexose, are also reported to play an essential role during seed development. In maize ZmSWEET4c, a clade II SWEET participates in the transport of hexoses across the basal endosperm transfer layer. Impaired seed filling was observed in the mutants of zmsweet4c and its rice ortholog ossweet4, suggesting that SWEET4 enhances sugar import into the endosperm in both maize and rice [48]. In Litchi chinensis, the temporal and spatial expression profiling indicated the role of LcSWEET2a and 3b in seed development [49].

2.4. Shoot Branching and Bud Outgrowth

Sugars are involved in shoot branching and bud outgrowth [50][51][52]. A SWEET gene (CmSWEET17) in Chrysanthemum morifolium displays axillary bud-specific expression after treatment with 20 mM sucrose, and the overexpression of CmSWEET17 promotes axillary bud growth [53]. Simultaneously, the CmSWEET17 overexpression lines revealed the induction of several auxin transporter genes [AUXIN RESISTANT 1 (AUX1), LIKE AUX1 2 (LAX2), PINFORMED1 (PIN1), PIN2 and PIN4], indicating that SWEET17 may be engaged in sucrose-mediated axillary bud outgrowth via the auxin transport pathway [53].

2.5. Development of Reproductive Organs

SWEET genes are expressed at different stages of pollen development. In Arabidopsis, AtSWEET8/RPG1 (Ruptured pollen grain 1) is expressed in microsporocyte and tapetum. Pollen grains of atsweet8 mutants are aborted and sterile, suggesting its involvement in anther and pollen development [54]. Furthermore, AtSWEET13/RPG2 partly restores the male fertility of atsweet8 at the late reproductive stages, which is also expressed in the anther during microsporogenesis, indicating functional redundancy among SWEETs. However, the double mutant of rpg1:rpg2 was fully sterile and was unable to restore [55]. Knockout mutants of AtSWEET11 and OsSWEET11/Os8N3/Xa13 also produced defective pollen grains and reduced male fertility in Arabidopsis and rice, respectively [56][57][58]. Some other SWEET genes such as AtSWEET1, PwSWEET1, and AtSWEET5/VEX1 are expressed at different stages of pollen development, which indicates their role in pollen development [19][59].

3. Role of SWEET Genes in Abiotic Stress

To cope with different abiotic constraints, plants tightly regulate the vacuolar storage and transport of sugars. For instance, sugar accumulation occurs in vacuoles to minimize freezing stress [60][61]. Additionally, SWEET genes are responsive to various abiotic stresses, suggesting their role in abiotic stress response.

3.1. Osmotic or Drought Stress

Prolonged drought increases the root to shoot ratio [1], which is affected by excess C assimilation in leaf that is transported to roots [62]. This suggests that sugar transporters may play a crucial role under drought stress conditions. Consistently, AtSWEET4, AtSWEET13, AtSWEET14 and AtSWEET15 were induced in Arabidopsis and OsSWEET12, OsSWEET15 and OsSWEET16 were induced in rice. Likewise, AtSWEET11, AtSWEET12, and AtSUC2 transcript levels were significantly induced in leaves, while AtSUC2 and AtSWEET11-15 were induced in roots of water-stressed Arabidopsis [63]. An increase in the expression of sugar transporters in both leaves and roots suggests that plants have to maintain an efficient root system under stress conditions, which is ensured by allocating more C to roots. In contrast, Durand et al. [64] reported the downregulation of AtSUC2, AtSWEET11, AtSWEET12, AtSWEET13, and AtSWEET15 and reduced sucrose transport between leaves and roots in response to poly-ethylene-glycol (PEG) treated Arabidopsis plants. This suggests that plants use distinct mechanisms to cope with drought and PEG-induced osmotic stress.
Several other examples demonstrate the role of SWEETs in drought tolerance. Arabidopsis seedlings overexpressing the Dianthus Spiculifolius gene DsSWEET12 have longer roots, high fructose, and glucose with a lower sucrose content and higher tolerance to osmotic and oxidative stresses compared to wild type plants [65]. Transgenic lines of tomato overexpressing Malus domestica SWEET gene MdSWEET17 showed a higher accumulation of fructose and enhanced drought tolerance [66]. It is well known that sugars act as osmoprotectants, and therefore participate in osmotic stress tolerance [67]. The total sugar content in embryos increased after PEG and NaCl treatment in sorghum, but the increase in fructose treatment was most apparent [68]. A significant reduction in the expression of SWEET10b under drought stress was also reported in potato [69].
In a recent study, another sugar transporter AtSWEET17, localized in the vacuolar membrane, was markedly upregulated during lateral root (LR) development under drought stress [70]. In another study, comparative root transcriptomics of chickpea under drought stress were carried out, and three SWEET genes (N3 (LOC101510607), SWEET1-like (LOC101515250), and SWEET4 (LOC101488443)) were reported to be upregulated in chickpea genotypes [71]. In soybean, drought stress increased leaf sucrose and soluble sugars but decreased root starch content. Consistent with this, the expression of sucrose transporters (GmSUC2, GmSWEET6, and 15) was upregulated in the leaves and roots [72]. In rice, OsSWEET13 and OsSWEET15 were induced in response to drought stress. The higher expression of these two genes was due to the binding of an ABA-responsive TF (OsbZIP72) to their promoter sequences. This modulates sucrose transport and distribution in response to drought stress, thus maintaining sugar homeostasis in response to drought stress [17]. In wheat, 13 SWEET genes showed differential expression after PEG treatment at the seedling stage. These genes include four members of clade I (TaSWEET2a1-6B, TaSWEET2a2-6D, and TaSWEET2b2-3A), four members of clade III (TaSWEET13c-6A, TaSWEET14h-6D, TaSWEET14g-1A, and TaSWEET15a-7D), and five members of clade IV (TaSWEET16c-4D, TaSWEET16a-4A, TaSWEET17a-5D, TaSWEET17c-5A, and TaSWEET17b-5B). However, these genes are expressed in a clade-specific manner, i.e., the members of clade I show downregulation, clade III show upregulation, and clade IV showed upregulation [73]. Similarly, in tea plants, seven genes (CsSWEET1a, 2a, 2c, 3a, 7a, 7b and 10a) were induced under drought stress [74]. However, further research is required to address the contrasting gene expression patterns of SWEET sugar transporters under drought and osmotic conditions.

3.2. Heat Stress

Heat stress inhibits carbon fixation while respiration increases, and heat tolerance involves the maintenance of leaf sugar content [75][76]. Heat reduces sugar export from source leaves to sink. For instance, in maize, the export rate of sugars from source leaves decreased after heat stress [77]. Heat stress caused a decline in the starch content of tomato mesophyll cells, but it increased significantly at a later time point [78]. Consistently, AtSWEET1, AtSWEET4, AtSWEET13 and AtSWEET15 were induced, and AtSWEET2, AtSWEET10 and AtSWEET17 were suppressed in Arabidopsis. In rice, OsSWEET14 and OsSWEET16 were induced, and OsSWEET3b, OsSWEET4 and OsSWEET5 were suppressed.
In wheat, 22 sugar transporters were up-regulated and 19 were suppressed under heat stress [79]. In Brassica napus, SWEET genes (BnSWEET9-2, 10-3, 12, 13-2 and 14) were up-regulated after heat stress [39]. In B. rapa, BrSWEET1 was expressed after 2 h of heat stress, while BrSWEET11 was expressed after 8 h of heat [80]. In cotton, GhSWEET4, 5, 10e, 49 and 55 showed induced expression under heat stress [81][82]. In wheat, 18 paralogues of nine SWEET genes (SWEET1, 2, 3, 4, 6, 14, 15, 16, and 17) showed a differential expression after 6 h of heat stress at the seedling stage. However, these genes expressed in a clade-specific manner, i.e., the members of clade II, III, and IV showed downregulation (except TaSWEET15a-7D), while the members of clade I showed both upregulation and downregulation [73]. Studies of different plant species under heat stress show that sugar levels of the source leaves decline due to decreased photosynthesis. However, functional gene studies are required to demonstrate the role of SWEET transporters in heat stress.

3.3. Cold Stress

Cold stress induces sugar accumulation in plants, and several SWEET genes such as AtSWEET15/SAG29 are up-regulated under cold stress [83]. The expression of AtSWEET1, AtSWEET2b, AtSWEET4, AtSWEET13 and AtSWEET15 was induced in Arabidopsis and OsSWEET7c and OsSWEET14 were induced in rice. Cold stress resulted in a higher accumulation of glucose and fructose than wild-type in Arabidopsis sweet11 and atsweet11/12 mutants, which resulted in cold stress tolerance. Enhanced tolerance observed in the double mutant may be due to the reduced number of xylem cells and smaller diameter vessels [84]. Additionally, it has been shown that the overexpression of AtSWEET16 shows freezing tolerance [85]. AtSWEET4 facilitates sugar transport in axial tissues during plant growth and development, and the transgenic plants overexpressing AtSWEET4 exhibits higher freezing tolerance [86]. In tea, CsSWEET16, a vacuolar membrane transporter, is downregulated after cold stress. The overexpression of the CsSWEET16 in Arabidopsis resulted in the compartmentation of sugars across the vacuole [60], while the overexpression of AtSWEET17 reduced the fructose content in leaves by 80% under cold stress conditions [87][88]. Furthermore, MaSWEET1, 4 and 14 expressions were upregulated in banana (Musa acuminata L.) under various stresses, indicating its role in stress tolerance to multiple stresses [89]. A genome-wide study carried out in Brassica oleracea reported the downregulation of BoSWEET11b, 11c, 12b, 16a, and 17 after chilling stress, possibly resulting in the accumulation of glucose and fructose and an enhanced chilling tolerance [90]. Similarly, several other genome-wide studies have been performed in different plants. They show differential expression of SWEET genes after cold stress, suggesting that SWEET genes mediate cold-induced sugar-signaling responses [60][74][82][89][90][91][92]. The above studies indicate the role of SWEET genes in providing cold stress tolerance in plants; however, functional validation of these genes is still needed.

3.4. Salinity Stress

Salinity stress affects various physiological and metabolic processes, ultimately inhibiting crop productivity [93]. There are two phases of salt stress in plants; the first phase is an osmotic phase in which leaf-growth inhibition occurs, followed by the second phase of ion toxicity in which accelerated leaf senescence occurs [94]. Instead, a phase zero is also suggested, known as the transient phase, and begins quickly after salt shock, resulting in a lower turgor pressure and growth rate [95]. Sucrose also behaves similarly to osmolyte and prevents salt stress-induced damages [96]. Additionally, SWEET15 (clade III member) is mainly involved in the sucrose transportation. AtSWEET1, AtSWEET2, AtSWEET4, AtSWEET14 and AtSWEET15 were induced in Arabidopsis and OsSWEET1b, OsSWEET7c and OsSWEET15 were induced in rice. Consistently, AtSWEET15 is induced under osmotic stress, and AtSWEET15 overexpression leads to accelerated senescence and hypersensitivity to salt stress [37]. The transcript level of SWEET15 was observed as 64-fold higher than the control in phase 1 after salt stress, and for this property, the expression of this gene can be used as a marker to differentiate between phase 0 and phase 1 in Arabidopsis and maize [97]. The expression of MtSWEET1a, MtSWEET2b, MtSWEET7, MtSWEET9b and MtSWEET13 were upregulated under salt, while MtSWEET2a and MtSWEET3c were down-regulated [91]. However, in Arabidopsis, a lower transcript level of SWEET2, 13, 16, and 17 was observed, while a higher transcript level was observed for SWEET14 [98]. Since SWEET2, 16 and 17 transport glucose, fructose and/or sucrose across the tonoplast along the concentration gradient, their downregulation supports the hypothesis of reducing the cytosolic sugar towards storage in the vacuole [36][85]. The heterologous expression of DsSWEET17, a tonoplast sugar transporters of Dianthus spiculifolius, in A. thaliana affects sugar metabolism and tolerance to salinity, osmotic, and oxidative stresses [65].

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Vijay Gahlaut
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Tinku Gautam
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Madhushree Dutta
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Vandana Jaiswal
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Gaurav Zinta
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