Abstract
Background
The sugar will eventually be exported transporter (SWEET) family is a novel type of membrane-embedded sugar transporter that contains seven transmembrane helices with two MtN3/saliva domains. The SWEET family plays crucial roles in multiple processes, including carbohydrate transportation, development, environmental adaptability and host–pathogen interactions. Although SWEET genes, especially those involved in response to biotic stresses, have been extensively characterized in many plants, they have not yet been studied in potato.
Objective
The identification of StSWEET genes provides important candidates for further functional analysis and lays the foundation for the production of good quality and high yield potatoes through molecular breeding.
Methods
In this study, StSWEET genes were identified using a genome-wide search method. A comprehensive analysis of StSWEET family through bioinformatics methods, such as phylogenetic tree, gene structure and promoter prediction analysis. The expression profiles of StSWEET genes in different potato tissues and under P. infestans attack and sugar stress were studied using quantitative real-time polymerase chain reaction (qRT-PCR).
Results
Phylogenetic analysis classified 33 StSWEET genes into four groups containing 12, 5, 12 and 4 genes. Furthermore, the gene structures and conserved motifs found that the StSWEET genes are very conservative during evolution. The chromosomal localization pattern showed that the distribution and density of the StSWEETs on 10 potato chromosomes were uneven and basically clustered. Predictive promoter analysis indicated that StSWEET proteins are associated with cell growth, development, secondary metabolism, and response to biotic and abiotic stresses. Finally, the expression patterns of the StSWEET genes in different tissues and the induction of P. infestans and the process of the sugar stress were investigated to obtain the tissue-specific and stress-responsive candidates.
Conclusion
This study systematically identifies the SWEET gene family in potato at the genome-wide level, providing important candidates for further functional analysis and contributing to a better understanding of the molecular basis of development and tolerance in potato.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Artero RD, Terol-Alcayde J, Paricio N, Ring J, Bargues M, Torres A, Perez-Alonso M (1998) Saliva, a new Drosophila gene expressed in the embryonic salivary glands with homologues in plants and vertebrates. Mech Dev 75:159–162. https://doi.org/10.1016/S0925-4773(98)00087-2
Ayre BG (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 4:377–394. https://doi.org/10.1093/mp/ssr014
Bing Y, Akiko S, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A 103:10503–10508. https://doi.org/10.1073/pnas.0604088103
Bourke PMA (1964) Emergence of potato blight, 1843–46. Nature 203:805–808. https://doi.org/10.1038/203805a0
Braun DM (2012) SWEET! the pathway is complete. Science 335:173–174. https://doi.org/10.1126/science.1216828
Braun DM, Slewinski TL (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol 149:71–81. https://doi.org/10.1104/pp.108.129049
Chardon F, Bedu M, Calenge F et al (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23:697–702. https://doi.org/10.1016/j.cub.2013.03.021
Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155. https://doi.org/10.1111/nph.12445
Chen LQ, Hou BH, Lalonde S et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532. https://doi.org/10.1038/nature09606
Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211. https://doi.org/10.1126/science.1213351
Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlane HE, Londono A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619. https://doi.org/10.1105/tpc.114.134585
Chong J, Piron MC, Meyer S, Merdinoglu D, Bertsch C, Mestre P (2014) The SWEET family of sugar transporters in grapevine: vvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot 65:6589–6601. https://doi.org/10.1093/jxb/eru375
Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang Q, Wang S (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255. https://doi.org/10.1101/gad.1416306
Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138:2124–2133. https://doi.org/10.1104/pp.104.054213
Feng L, Frommer WB (2015) Structure and function of SemiSWEET and SWEET sugar transporters. Trends Biochem Sci 40:480–486. https://doi.org/10.1016/j.tibs.2015.05.005
Feng CY, Han JX, Han XX, Jiang J (2015) Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene 573:261–272. https://doi.org/10.1016/j.gene.2015.07.055
Finn RD, Mistry J, Schuster-Bockler B et al (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251. https://doi.org/10.1093/nar/gkj149
Gao Y, Wang ZY, Kumar V, Xu XF, Yuan P, Zhu XF, Li TY, Jia B, Xuan YH (2018) Genome-wide identification of the SWEET gene family in wheat. Gene 642:284–292. https://doi.org/10.1016/j.gene.2017.11.044
Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147:852–863. https://doi.org/10.1104/pp.108.118026
Guo WJ, Nagy R, Chen HY, Pfrunder S, Yu YC, Santelia D, Frommer WB, Martinoia E (2014) SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol 164:777–789. https://doi.org/10.1104/pp.113.232751
Han J, Jiang J (2015) Genome-wide analysis of SWEET gene family in Arabidopsis thaliana, Oryza sativa and Lycopersicum esculentum. Mol Plant Breed 13:581–588
Haverkort AJ, Boonekamp PM, Hutten R, Jacobsen E, Lotz LAP, Kessel GJT, Vossen JH, Visser RGF (2016) Durable late blight resistance in potato through dynamic varieties obtained by cisgenesis: scientific and societal advances in the DuRPh project. Potato Res 59:35–66. https://doi.org/10.1007/s11540-015-9312-6
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Hu L-P, Zhang F, Song S-H, Tang X-W, Xu H, Liu G-M, Wang Y, He H-J (2017) Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. J Integr Agric 16:1486–1501. https://doi.org/10.1016/s2095-3119(16)61501-0
Jaehme M, Guskov A, Slotboom DJ (2014) Crystal structure of the vitamin B3 transporter PnuC, a full-length SWEET homolog. Nat Struct Mol Biol 21:1013–1015. https://doi.org/10.1038/nsmb.2909
Jaehme M, Guskov A, Slotboom DJ (2015) The twisted relation between Pnu and SWEET transporters. Trends Biochem Sci 40:183–188. https://doi.org/10.1016/j.tibs.2015.02.002
Kersey PJ, Allen JE, Armean I et al (2016) Ensembl genomes 2016: more genomes, more complexity. Nucleic Acids Res 44:D574–D580. https://doi.org/10.1093/nar/gkv1209
Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol 163:1338–1352. https://doi.org/10.1104/pp.113.224972
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lemoine R, La Camera S, Atanassova R et al (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272. https://doi.org/10.3389/fpls.2013.00272
Li J, Qin M, Qiao X, Cheng Y, Li X, Zhang H, Wu J (2017a) A new insight into the evolution and functional divergence of SWEET transporters in Chinese white pear (Pyrus bretschneideri). Plant Cell Physiol 58:839–850. https://doi.org/10.1093/pcp/pcx025
Li Y, Wang Y, Zhang H, Zhang Q, Zhai H, Liu Q, He S (2017b) The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. Front Plant Sci 8:197. https://doi.org/10.3389/fpls.2017.00197
Li W, Ren Z, Wang Z et al (2018) Evolution and stress responses of Gossypium hirsutum SWEET genes. Int J Mol Sci 19:769. https://doi.org/10.3390/ijms19030769
Ludewig F, Flugge UI (2013) Role of metabolite transporters in source-sink carbon allocation. Front Plant Sci 4:231. https://doi.org/10.3389/fpls.2013.00231
Manck-Gotzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487. https://doi.org/10.3389/fpls.2016.00487
Mayuko H, Shuichi W, Kenji K, Nori S (2010) Ci-Rga, a gene encoding an MtN3/saliva family transmembrane protein, is essential for tissue differentiation during embryogenesis of the ascidian Ciona intestinalis. Differentiation 73:364–376. https://doi.org/10.1111/j.1432-0436.2005.00037.x
Miao H, Sun P, Liu Q et al (2017) Genome-wide analyses of SWEET family proteins reveal involvement in fruit development and abiotic/biotic stress responses in banana. Sci Rep 7:3536. https://doi.org/10.1038/s41598-017-03872-w
Miao L, Lv Y, Kong L, Chen Q, Chen C, Li J, Zeng F, Wang S, Li J, Huang L, Cao J, Yu X (2018) Genome-wide identification, phylogeny, evolution, and expression patterns of MtN3/saliva/SWEET genes and functional analysis of BcNS in Brassica rapa. BMC Genom 19:174. https://doi.org/10.1186/s12864-018-4554-8
Mizuno H, Kasuga S, Kawahigashi H (2016) The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling. Biotechnol Biofuels 9:127. https://doi.org/10.1186/s13068-016-0546-6
Navathe S, Singh S, Singh V, Chand R, Mishra V, Joshi A (2019) Genome-wide mining of respiratory burst homologs and its expression in response to biotic stresses in Triticum aestivum. Genes Genom 41:1027–1043. https://doi.org/10.1007/s13258-019-00821-x
Patil G, Valliyodan B, Deshmukh R et al (2015) Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genom 16:520. https://doi.org/10.1186/s12864-015-1730-y
Roitsch T, Gonzalez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613. https://doi.org/10.1016/j.tplants.2004.10.009
van der Vossen EA, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S (2005) The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J 44:208–222. https://doi.org/10.1111/j.1365-313X.2005.02527.x
Vision TJ, Brown DG, Tanksley SD (2000) The origins of genomic duplications in Arabidopsis. Science 290:2114–2117. https://doi.org/10.1126/science.290.5499.2114
Wang L, Yao L, Hao X, Li N, Qian W, Yue C, Ding C, Zeng J, Yang Y, Wang X (2018) Tea plant SWEET transporters: expression profiling, sugar transport, and the involvement of CsSWEET16 in modifying cold tolerance in Arabidopsis. Plant Mol Biol 96:577–592. https://doi.org/10.1007/s11103-018-0716-y
Waqas M, Azhar M, Rana I, Azeem F, Ali M, Nawaz M, Chung G, Atif R (2019) Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea (Cicer arietinum L.) reveal their role in abiotic stress-responses. Gene Genom 41:467–481. https://doi.org/10.1007/s13258-018-00780-9
Wei X, Liu F, Chen C, Ma F, Li M (2014) The Malus domestica sugar transporter gene family: identifications based on genome and expression profiling related to the accumulation of fruit sugars. Front Plant Sci 5:569. https://doi.org/10.3389/fpls.2014.00569
Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117. https://doi.org/10.1371/journal.pgen.0020117.eor
Weschke W, Panitz R, Gubatz S, Wangy Q, Radchuk R (2010) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:399–411. https://doi.org/10.1046/j.1365-313X.2003.01633.x
Wheeler TJ, Eddy SR (2013) nhmmer: dna homology search with profile HMMs. Bioinformatics 29:2487–2489. https://doi.org/10.1093/bioinformatics/btt403
Xu X, Pan S, Cheng S et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195. https://doi.org/10.1038/nature10158
Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. Proc Natl Acad Sci USA 109:1187–1192. https://doi.org/10.1073/pnas.1109047109
Yang L, Wang D, Xu Y, Zhao H, Wang L, Cao X, Chen Y, Chen Q (2017) A new resistance gene against potato late blight originating from Solanum pinnatisectum located on potato chromosome 7. Front Plant Sci 8:1729. https://doi.org/10.3389/fpls.2017.01729
Yoshida K, Schuenemann VJ, Cano LM et al (2013) The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. Elife 2:e00731. https://doi.org/10.7554/eLife.00731
Yuan M, Wang S (2013) Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. Mol Plant 6:665–674. https://doi.org/10.1093/mp/sst035
Yuan M, Zhao J, Huang R, Li X, Xiao J, Wang S (2014) Rice MtN3/saliva/SWEET gene family: evolution, expression profiling, and sugar transport. J Integr Plant Biol 56:559–570. https://doi.org/10.1111/jipb.12173
Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Cruz CV, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643. https://doi.org/10.1111/tpj.12838
Acknowledgements
This work was supported by the Modern Agricultural Industry Technology System (No. CARS-9), the R&D and Demonstration of Key Technologies for High-Quality Development of Specialized Potato Industry (No. 2019-NK-A1), the Qinghai Science and Technology Department Science and Technology Cooperation Special (No. 2018-HZ-802) and CAS “Light of West China” Program (No. 1_8).
Author information
Authors and Affiliations
Contributions
ML, GY, and YZ designed the experiments; ML, HX, MH, WS, and YY carried out the experiments; ML, HX, WS, and JW analyzed the experimental results. ML, HX, and MH analyzed the data and developed the analytical tools. ML and GY wrote the manuscript; ML, WS, GY, and YZ revised the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, M., Xie, H., He, M. et al. Genome-wide identification and expression analysis of the StSWEET family genes in potato (Solanum tuberosum L.). Genes Genom 42, 135–153 (2020). https://doi.org/10.1007/s13258-019-00890-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-019-00890-y