SWEET transporters

SemiSWEET PQ-loop

Half Putative Sugar Transporter
Identifiers
Symbol PQ-loop
Pfam PF04193
Pfam clan PQ-loop
InterPro IPR006603
SMART SM00679
TCDB 2.A.123
OPM superfamily 501
OPM protein 5ctg

The SWEET family, also known as the PQ-loop, Saliva or MtN3 family (TC# 2.A.123), is a family of sugar transporters and a member of the TOG superfamily. The proteins of the SWEET family have been found in plants, animals, protozoans, and bacteria. Eukaryotic family members have 7 transmembrane segments (TMSs) in a 3+1+3 repeat arrangement.[1]

Function

Sugar efflux transporters are essential for the maintenance of animal blood glucose levels, plant nectar production, and plant seed and pollen development. Proteins of the SWEET family appear to catalyze facilitated diffusion (entry or export) of sugars across the plant plasma membrane or the endoplasmic reticulum membrane.[2]

Transport Reaction

The generalized reaction catalyzed by known proteins of this family is:[1]

sugars (in) ⇌ sugars (out)

Discovery

SWEETs were originally identified in Arabidopsis thaliana, in a screen for novel facilitators of transmembrane glucose transport. In this experiment, several previously uncharacterized membrane proteins were selected to be screened. These uncharacterized membrane proteins were assayed for glucose transport ability by expression in HEK293T (human embryonic kidney) cells, which have negligible glucose transport ability in the normal state. These membrane proteins were co-expressed with a fluorescent FRET (Förster resonance energy transfer) glucose sensor localized to the endoplasmic reticulum (ER).[3][4][5][6][7][8] Glucose movement from the cytoplasm to the ER of the HEK293T cells was monitored by quantifying changes in FRET ratio. By using this assay, the first member of the SWEET family, AtSWEET1, was identified. Other potential family members were identified by sequence homology.[9]

Homologues

Chen et al. (2010) reviewed evidence for a new class of sugar transporters, named SWEETs.[9] Those that mediate glucose transport include at least six out of seventeen sugar homologues in Arabidopsis (i.e., TC#s 2.A.123.1.3, 2.A.123.1.5, 2.A.123.1.9, 2.A.123.1.13), two out of over twenty porters in rice (TC#s 2.A.123.1.6 and 2.A.123.1.18), two out of seven homologues in Caenorhabditis elegans (i.e.,TC# 2.A.123.1.10) and the single copy human protein (SLC50A1 of Homo sapiens, TC# 2.A.123.1.4). Arabidopsis SWEET8 (TC# 2.A.123.1.5) is essential for pollen viability. The corn homolog ZmSWEET4c was shown to be involved in seed filling.[10] The rice homologues SWEET11 (TC# 2.A.123.1.13) and SWEET14 are specifically exploited by bacterial pathogens for virulence by means of direct binding of a bacterial effector to the SWEET promoter.[11][12] Bacterial symbionts and fungal and bacterial pathogens induce the expression of different SWEET genes, indicating that the sugar efflux function of SWEET transporters is targeted by pathogens and symbionts for nutritional gain.[13] The metazoan homologues may be involved in sugar efflux from intestinal, liver, epididymis and mammary cells.

Currently classified members of the SWEET transporter family can be found in the Transporter Classification Database.

SWEETs in plants

Plant SWEETs fall into four subclades.[9] The tomato genome encodes 29 SWEETs. Feng et al. (2015) analyzed the structures, conserved domains, and phylogenetic relationships of these proteins, and also analyzed the transcript levels of SWEET genes in various tissues, organs, and developmental stages in response to exogenous sugar and adverse environmental stress (high and low temperatures).[14]

Plant SWEETs play crucial roles in cellular sugar efflux processes: phloem loading, pollen nutrition and nectar secretion. Plants transport fixed carbon predominantly as sucrose, which is produced in mesophyll cells and imported into phloem cells for translocation throughout the plant. It had not been known how sucrose migrates from sites of synthesis in the mesophyll to the phloem, or which cells mediate efflux into the apoplasm as a prerequisite for phloem loading by the SUT (sucrose transporter family) sucrose-H+ cotransporters. Using optical sucrose sensors, Chen et al. (2012) identified a subfamily of SWEET sucrose efflux transporters. AtSWEET11 (TC# 2.A.123.1.13) and AtSWEET12 localize to the plasma membrane of the phloem. Mutant plants carrying insertions in AtSWEET11 and -12 are defective in phloem loading, thus revealing a two-step mechanism of SWEET-mediated export from parenchyma cells feeding H+-coupled import into the sieve element-companion cell complex. Restriction of intercellular transport to the interface of adjacent phloem cells may be an effective mechanism to limit the availability of photosynthetic carbon in the leaf apoplasm in order to prevent pathogen infections.[15]

SWEET9 in Nectar Secretion

Lin et al., 2014, examined the role of SWEET9 in nectaries. SWEET9 is a member of clade 3. A homologue in petunias had been shown to have an inverse correlation between expression and starch content in nectaries. Mutation and overexpression of SWEET9 in Arabidopsis led to corresponding loss of and increase in nectar secretion, respectively. After showing that SWEET9 is involved in nectar secretion, the next step was to determine at which phase of the process SWEET9 has its function. The 3 options were: phloem unloading, or uptake or efflux from nectary parenchyma. A combination of localization studies and starch accumulation assays showed that SWEET9 is involved in sucrose efflux from the nectary parenchyma.[16]

SWEETs 11, 12, and 15 in Embryo Nutrition

Chen et al., 2015, asked what SWEETs are involved in providing nutrition to an embryo. The team noticed that mRNA and protein for SWEETs 11, 12, and 15 are each expressed at high levels during some stage of embryo development. Each gene was subsequently mutated to generate a sweet11;12;15 triple mutant which lacked activity in each of the three genes. This triple mutant was shown to have delayed embryo development; that is, the seeds of the triple mutant were significantly smaller than that of the wild type at the same time during development. The starch content of the seed coat was higher than the wild-type, and the starch content of the embryo was lower than the wild-type. Additionally, protein levels were shown to be maternally controlled: in a sweet11;12;15 mutant crossed with a wild-type plant, the mutant phenotype was only seen when sweet11;12;15 was used as the maternal plant.[17]

Structure

Many bacterial homologues have only 3 TMSs and are half sized, but they nevertheless are members of the SWEET family with a single 3 TMS repeat unit. Other bacterial homologues have 7 TMSs as do most eukaryotic proteins in this family. The SWEET family is large and diverse. Based on 3-D structural analyses, it is likely that these paired 3 TMS SWEET family members function as carriers.

Bacterial SemiSWEETs, consist of a triple-helix bundle in a 1-3-2 conformation, with TM3 sandwiched between TM1 and TM2.[18] SemiSWEETs form semi-symmetrical, parallel dimers, thereby generating the translocation pathway. Two SemiSWEET isoforms have been crystallized, one in an apparently open state and one in an occluded state, indicating that SemiSWEETs and SWEETs are transporters that undergo rocking-type movements during the transport cycle.[18] The structures also show tryptophan and asparagine residues interacting with the sugar; point mutations of these residues to alanine destroys the hexose transport function of SemiSWEET. In SemiSWEETs and SWEETs with more than 3 TM domains, two triple-helix bundles are arranged in a parallel configuration to produce the 6- and (3 + 1 + 3)-transmembrane-helix pores, respectively. Given the similarity of SemiSWEETs and SWEETs to PQ-loop amino acid transporters and to mitochondrial pyruvate carriers (MPCs), the structures characterized by Xu et al., 2014 may also be relevant to other transporters in the SWEET clan.[18] The SWEET family is a member of the TOG superfamily which is believed to have arisen via the pathway:

2 TMSs --> 4 TMSs --> 8 TMSs --> 7 TMSs --> 3 + 3 TMSs.[19]

Several crystal structures are available on RCSB for members of the SWEET/SemiSWEET/PQ-loop/Saliva/MtN3 family.

3.1 A resolution structure of a eukaryotic SWEET transporter in a homotrimer (5CTG, OsSWEET2). Each different color represents one subunit.

Oligomerization

Arabidopsis SWEETs homo- and heterooligomerize. Xuan et al., (2013) examined mutant SWEET variants for negative dominance to test if oligomerization is necessary for function. Mutation of the conserved Y57 or G58 residues in SWEET1 (TC# 2.A.123.1.9) led to loss of activity. Coexpression of the defective mutants with functional A. thaliana SWEET1 inhibited glucose transport, indicating that homooligomerization is necessary for function. Collectively, these data imply that the basic unit of SWEETs is a 3-TM unit and that a functional transporter contains at least four such domains.[20] Tao et al., 2015, solved the structure of rice SWEET2 and showed that it forms a homotrimer.[21]

See also

Further reading

  • Ge, Y. X.; Angenent, G. C.; Wittich, P. E.; Peters, J.; Franken, J.; Busscher, M.; Zhang, L. M.; Dahlhaus, E.; Kater, M. M. (2000-12-01). "NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida". The Plant Journal: For Cell and Molecular Biology 24 (6): 725–734. ISSN 0960-7412. PMID 11135107.
  • Hamada, Mayuko; Wada, Shuichi; Kobayashi, Kenji; Satoh, Nori (2005-09-01). "Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis". Differentiation; Research in Biological Diversity 73 (7): 364–376. doi:10.1111/j.1432-0436.2005.00037.x. ISSN 0301-4681. PMID 16219040.
  • Hamada, Mayuko; Wada, Shuichi; Kobayashi, Kenji; Satoh, Nori (2007-07-01). "Novel genes involved in Ciona intestinalis embryogenesis: characterization of gene knockdown embryos". Developmental Dynamics: An Official Publication of the American Association of Anatomists 236 (7): 1820–1831. doi:10.1002/dvdy.21181. ISSN 1058-8388. PMID 17557306.
  • Tao, Yuyong; Cheung, Lily S.; Li, Shuo; Eom, Joon-Seob; Chen, Li-Qing; Xu, Yan; Perry, Kay; Frommer, Wolf B.; Feng, Liang (2015-11-12). "Structure of a eukaryotic SWEET transporter in a homotrimeric complex". Nature 527 (7577): 259–263. doi:10.1038/nature15391. ISSN 1476-4687. PMID 26479032.
  • Wu, Zhengdao; Soliman, Khairy M.; Bolton, James J.; Saha, Sukumar; Jenkins, Johnie N. (2008-05-01). "Identification of differentially expressed genes associated with cotton fiber development in a chromosomal substitution line (CS-B22sh)". Functional & Integrative Genomics 8 (2): 165–174. doi:10.1007/s10142-007-0064-5. ISSN 1438-793X. PMID 18043952.

References

  1. 1 2 Saier, MH Jr. "2.A.123 The Sweet; PQ-loop; Saliva; MtN3 (Sweet) Family". Transporter Classification Database. Saier Lab Bioinformatics Group / SDSC.
  2. ↑ Takanaga, Hitomi; Frommer, Wolf B. (2010-08-01). "Facilitative plasma membrane transporters function during ER transit". FASEB Journal 24 (8): 2849–2858. doi:10.1096/fj.09-146472. ISSN 1530-6860. PMC 3230527. PMID 20354141.
  3. ↑ "Nanosensors | Department of Plant Biology". dpb.carnegiescience.edu. Retrieved 2016-03-01.
  4. ↑ Bermejo, Clara; Ewald, Jennifer C.; Lanquar, Viviane; Jones, Alexander M.; Frommer, Wolf B. (2011-08-15). "In vivo biochemistry: quantifying ion and metabolite levels in individual cells or cultures of yeast". The Biochemical Journal 438 (1): 1–10. doi:10.1042/BJ20110428. ISSN 1470-8728. PMID 21793803.
  5. ↑ Jones, Alexander M.; Grossmann, Guido; Danielson, Jonas Åh; Sosso, Davide; Chen, Li-Qing; Ho, Cheng-Hsun; Frommer, Wolf B. (2013-06-01). "In vivo biochemistry: applications for small molecule biosensors in plant biology". Current Opinion in Plant Biology 16 (3): 389–395. doi:10.1016/j.pbi.2013.02.010. ISSN 1879-0356. PMC 3679211. PMID 23587939.
  6. ↑ Jones, Alexander M.; Ehrhardt, David W.; Frommer, Wolf B. (2012-01-01). "A never ending race for new and improved fluorescent proteins". BMC biology 10: 39. doi:10.1186/1741-7007-10-39. ISSN 1741-7007. PMC 3342923. PMID 22554191.
  7. ↑ Okumoto, Sakiko; Jones, Alexander; Frommer, Wolf B. (2012-01-01). "Quantitative imaging with fluorescent biosensors". Annual Review of Plant Biology 63: 663–706. doi:10.1146/annurev-arplant-042110-103745. ISSN 1545-2123. PMID 22404462.
  8. ↑ Hou, Bi-Huei; Takanaga, Hitomi; Grossmann, Guido; Chen, Li-Qing; Qu, Xiao-Qing; Jones, Alexander M.; Lalonde, Sylvie; Schweissgut, Oliver; Wiechert, Wolfgang (2011-11-01). "Optical sensors for monitoring dynamic changes of intracellular metabolite levels in mammalian cells". Nature Protocols 6 (11): 1818–1833. doi:10.1038/nprot.2011.392. ISSN 1750-2799. PMID 22036884.
  9. 1 2 3 Chen, Li-Qing; Hou, Bi-Huei; Lalonde, Sylvie; Takanaga, Hitomi; Hartung, Mara L.; Qu, Xiao-Qing; Guo, Woei-Jiun; Kim, Jung-Gun; Underwood, William (2010-11-25). "Sugar transporters for intercellular exchange and nutrition of pathogens". Nature 468 (7323): 527–532. doi:10.1038/nature09606. ISSN 1476-4687. PMC 3000469. PMID 21107422.
  10. ↑ Sosso, Davide; Luo, Dangping; Li, Qin-Bao; Sasse, Joelle; Yang, Jinliang; Gendrot, Ghislaine; Suzuki, Masaharu; Koch, Karen E.; McCarty, Donald R. (2015-12-01). "Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport". Nature Genetics 47 (12): 1489–1493. doi:10.1038/ng.3422. ISSN 1546-1718. PMID 26523777.
  11. ↑ Chu, Zhaohui; Fu, Binying; Yang, Hong; Xu, Caiguo; Li, Zhikang; Sanchez, A.; Park, Y. J.; Bennetzen, J. L.; Zhang, Qifa (2006-02-01). "Targeting xa13, a recessive gene for bacterial blight resistance in rice". TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik 112 (3): 455–461. doi:10.1007/s00122-005-0145-6. ISSN 0040-5752. PMID 16328230.
  12. ↑ Yang, Bing; Sugio, Akiko; White, Frank F. (2006-07-05). "Os8N3 is a host disease-susceptibility gene for bacterial blight of rice". Proceedings of the National Academy of Sciences of the United States of America 103 (27): 10503–10508. doi:10.1073/pnas.0604088103. ISSN 0027-8424. PMC 1502487. PMID 16798873.
  13. ↑ Chen, Li-Qing; Qu, Xiao-Qing; Hou, Bi-Huei; Sosso, Davide; Osorio, Sonia; Fernie, Alisdair R.; Frommer, Wolf B. (2012-01-13). "Sucrose efflux mediated by SWEET proteins as a key step for phloem transport". Science (New York, N.Y.) 335 (6065): 207–211. doi:10.1126/science.1213351. ISSN 1095-9203. PMID 22157085.
  14. ↑ Feng, Chao-Yang; Han, Jia-Xuan; Han, Xiao-Xue; Jiang, Jing (2015-12-01). "Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato". Gene 573 (2): 261–272. doi:10.1016/j.gene.2015.07.055. ISSN 1879-0038. PMID 26190159.
  15. ↑ Chen, Li-Qing; Qu, Xiao-Qing; Hou, Bi-Huei; Sosso, Davide; Osorio, Sonia; Fernie, Alisdair R.; Frommer, Wolf B. (2012-01-13). "Sucrose efflux mediated by SWEET proteins as a key step for phloem transport". Science (New York, N.Y.) 335 (6065): 207–211. doi:10.1126/science.1213351. ISSN 1095-9203. PMID 22157085.
  16. ↑ Lin, I. Winnie; Sosso, Davide; Chen, Li-Qing; Gase, Klaus; Kim, Sang-Gyu; Kessler, Danny; Klinkenberg, Peter M.; Gorder, Molly K.; Hou, Bi-Huei (2014-04-24). "Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9". Nature 508 (7497): 546–549. doi:10.1038/nature13082. ISSN 1476-4687. PMID 24670640.
  17. ↑ Chen, Li-Qing; Lin, I. Winnie; Qu, Xiao-Qing; Sosso, Davide; McFarlane, Heather E.; Londoño, Alejandra; Samuels, A. Lacey; Frommer, Wolf B. (2015-03-01). "A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo". The Plant Cell 27 (3): 607–619. doi:10.1105/tpc.114.134585. ISSN 1532-298X. PMC 4558658. PMID 25794936.
  18. 1 2 3 Xu, Yan; Tao, Yuyong; Cheung, Lily S.; Fan, Chao; Chen, Li-Qing; Xu, Sophia; Perry, Kay; Frommer, Wolf B.; Feng, Liang (2014-11-20). "Structures of bacterial homologues of SWEET transporters in two distinct conformations". Nature 515 (7527): 448–452. doi:10.1038/nature13670. ISSN 1476-4687. PMC 4300204. PMID 25186729.
  19. ↑ Yee, Daniel C.; Shlykov, Maksim A.; Västermark, Åke; Reddy, Vamsee S.; Arora, Sumit; Sun, Eric I.; Saier, Milton H. (2013-11-01). "The transporter–opsin–G protein-coupled receptor (TOG) superfamily". FEBS Journal 280 (22): 5780–5800. doi:10.1111/febs.12499. ISSN 1742-4658. PMC 3832197. PMID 23981446.
  20. ↑ Xuan, Yuan Hu; Hu, Yi Bing; Chen, Li-Qing; Sosso, Davide; Ducat, Daniel C.; Hou, Bi-Huei; Frommer, Wolf B. (2013-09-24). "Functional role of oligomerization for bacterial and plant SWEET sugar transporter family". Proceedings of the National Academy of Sciences of the United States of America 110 (39): E3685–3694. doi:10.1073/pnas.1311244110. ISSN 1091-6490. PMC 3785766. PMID 24027245.
  21. ↑ Tao, Yuyong; Cheung, Lily S.; Li, Shuo; Eom, Joon-Seob; Chen, Li-Qing; Xu, Yan; Perry, Kay; Frommer, Wolf B.; Feng, Liang (2015-11-12). "Structure of a eukaryotic SWEET transporter in a homotrimeric complex". Nature 527 (7577): 259–263. doi:10.1038/nature15391. ISSN 1476-4687. PMC 4734654. PMID 26479032.

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