biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 62:24-32, 2018 | DOI: 10.1007/s10535-017-0750-7

Identification, characterization, and expression of the SWEET gene family in Phalaenopsis equestris and Dendrobium officinale

T. Wang1, Z. Song1, W. L. Meng2, L. B. Li1,*
1 State Key Laboratory of Forest Genetics and Tree Breeding, Key Laboratory of Silviculture of the State Forestry Administration, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, P.R. China
2 Environmental Protection Research Institute of Handan, Handan, P.R. China

Sugars are important molecules that function not only as primary metabolites, but also as nutrients and signal molecules in plants. The sugar transport protein genes family SWEET has been recently identified. The availability of the Dendrobium officinale and Phalaenopsis equestris genome sequences offered the opportunity to study the SWEET gene family in this two orchid species. We identified 22 and 16 putative SWEET genes, respectively, in the genomes of D. officinale and P. equestris using comprehensive bioinformatics analysis. Based on phylogenetic comparisons with SWEET proteins from Arabidopsis and rice, the DoSWEET and PeSWEET proteins could be divided into four clades; among these, clade II specifically lacked PeSWEETs and clade IV specifically lacked DoSWEETs, and there were orthologs present between D. officinale and P. equestris. Protein sequence alignments suggest that there is a predicted serine phosphorylation site in each of the highly conserved MtN3/saliva domain regions. Gene expression analysis in four tissues showed that three PeSWEET genes were most highly expressed in the flower, leaf, stem, and root, suggesting that these genes might play important roles in growth and development in P. equestris. Analysis of gene expression in different floral organs showed that five PeSWEET genes were highly expressed in the column (gynostemium), implying their possible involvement in reproductive development in this species. The expression patterns of seven PeSWEETs in response to different abiotic stresses showed that three genes were upregulated significantly in response to high temperature and two genes were differently expressed at low temperature. The results of this study lay the foundation for further functional analysis of SWEET genes in orchids.

Keywords: floral organs; high or low temperature; orchids; phylogenetic trees; sugar transporters
Subjects: transport proteins; SWEET gene family; phylogenetic tree; gene expression; floral organs; salinity; drought; cold stress; heat stress; sugars; orchids

Received: August 23, 2016; Revised: April 8, 2017; Accepted: April 18, 2017; Published: January 1, 2018  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Wang, T., Song, Z., Meng, W.L., & Li, L.B. (2018). Identification, characterization, and expression of the SWEET gene family in Phalaenopsis equestris and Dendrobium officinale. Biologia plantarum, 62(1), 24-32. doi: 10.1007/s10535-017-0750-7
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201801-0003_S1.pdf

    File size: 2.85 MB

    References

    1. Afoufa-Bastien, D., Medici, A., Jeauffre, J., Coutos-Thévenot, P., Lemoine, R., Atanassova, R., Laloi, M.: The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. - BMC Plant Biol. 10: 245, 2010. Go to original source...
    2. Antony, G., Zhou, J., Huang, S., Li, T., Liu, B., White, F., Yang, B.: Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility Gene Os-11N3. - Plant Cell 22: 3864-3876, 2010. Go to original source...
    3. Bock, K.W., Honys, D., Ward, J.M., Padmanaban, S., Eric P. Nawrocki, Hirschi, K.D., Twell, D., Sze, H.: Integrating membrane transport with male gametophyte development and function through transcriptomics. - Plant Physiol. 140: 1151-1168, 2006. Go to original source...
    4. Cai, J., Liu, X., Vanneste, K., Proost, S., Tsai, W., Liu, K., Chen, L., He, Y., Xu, Q., Bian, C., Zheng, Z., Sun, F., Liu, W., Hsiao, Y.: The genome sequence of the orchid Phalaenopsis equestris. - Nat. Genet. 47: 304, 2014. Go to original source...
    5. Chen, L., Qu, X., Hou, B., Sosso, D., Osorio, S., Fernie, A.R., Frommer, W.B.: Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. - Science 335: 207-211, 2012. Go to original source...
    6. Chen, L.Q., Hou, B.H., Lalonde, S., Takanaga, H., Hartung, M.L., Qu, X.Q., Guo, W.J., Kim, J.G., Underwood, W., Chaudhuri, B., Chermak, D., Antony, G., White, F.F., Somerville, S.C., Mudgett, M.B., Frommer. W.B.: Sugar transporters for intercellular exchange and nutrition of pathogens. - Nature 468: 527-532, 2010. Go to original source...
    7. Chong, J., Piron, M., Meyer, S., Merdinoglu, D., Bertsch, C., Mestre, P.: The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. - J. exp. Bot. 65: 6589-6601, 2014. Go to original source...
    8. Chu, Z., Yuan, M., Yao, J., Ge, X., Yuan, B., Xu, C., Li, X., Fu, B., Li, Z., Jeffrey, Bennetzen, L., Zhang, Q., Wang, S.: Promoter mutations of an essential gene for pollen development result in disease resistance in rice. - Gene Dev. 20: 1250-1255, 2006. Go to original source...
    9. Deng, W., Wang, Y., Liu, Z., Cheng, H., Xue, Y.: HemI: a toolkit for illustrating heatmaps. - PLoS ONE 11: e111988, 2014. Go to original source...
    10. Feng, C., Han, J., Han, X., Jiang, J.: Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. - Gene 573: 261-72, 2015. Go to original source...
    11. Graham, D., Patterson, B.D.: Responses of plants to low, nonfreezing temperatures: proteins, metabolism, and acclimation. - Annu. Rev. Plant Physiol. 33: 347-372, 1982. Go to original source...
    12. Guan, Y., Huang, X., Zhu, J., Gao, J., Zhang, H., Yang, Z.: 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, 2008. Go to original source...
    13. Guo, W., Nagy, R., Chen, H., Pfrunder, S., Yu, Y., Santelia, D., Frommer, W.B., Martinoia, E.: SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. - Plant Physiol. 164: 777-789, 2014. Go to original source...
    14. Hamada, M., Wada, S., Kobayashi, K., Satoh, N.: 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, 2005. Go to original source...
    15. Han, J., Jiang, J.: Genome-wide analysis of SWEET gene family in Arabidopsis thaliana, Oryza sativa and Lycopersicum esculentum. - Chin. mol. Plant Breed. 13: 581-588, 2015.
    16. He, F., Kang, J., Zhou, X., Su, Z., Qu, L., Gu, H.: Variation at the transcriptional level among Chinese natural populations of Arabidopsis thaliana in response to cold stress. - Chin. Sci. Bull. 53: 2989-2999, 2008. Go to original source...
    17. He, J., Huang, X.Y., Guan, Y.F., Sun, M.X., Zhu, J., Yang, Z.N.: Genome-wide analysis of MtN3/saliva protein family in Arabidopsis thaliana. - Chin. J. Shanghai Normal Univ. (Natur. Sci.) 39: 290-298, 2010.
    18. Hu, B., Jin, J., Guo, A.Y., Zhang, H., Luo, J.C., Gao, G.: GSDS 2.0: an upgraded gene feature visualization server. - Bioinformatics 31: 1296-1297, 2015a. Go to original source...
    19. Hu, X., Guo, Y., Xiang, J., Du, Y.: Research advances in polysaccharides of Dendrobium officinale. - Chin. Anhui agr. Sci. 43: 78-80, 2015b.
    20. Klemens, P.A.W., Patzke, K., Deitmer, J., Spinner, L., Le Hir, R., Bellini, C., Bedu, M., Chardon, F., Krapp, A., Neuhaus, H.E.: Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. - Plant Physiol. 163: 1338-1352, 2013. Go to original source...
    21. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. - Bioinformatics 23: 2947-2948, 2007. Go to original source...
    22. Liu, X., Wang, X.F., Piao, Y.J.: A study on cold resistance of different Phalaenopsis cultivars. - Chin. Acta hort. sin. 34: 425-430, 2007.
    23. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. - Methods 25: 402-408, 2001. Go to original source...
    24. Manck-Götzenberger, J., Requena, N.: Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. - Front. Plant Sci. 7: 487, 2016. Go to original source...
    25. Milton H. Saier, J., Tran, C.V., Barabote, R.D.: TCDB: the transporter classification database for membrane transport protein analyses and information. - Nucl. Acids Res. 34: 181-186, 2006. Go to original source...
    26. Patil, G., Valliyodan, B., Deshmukh, R., Prince, S., Nicander, B., Zhao, M., Sonah, H., Song, L., Lin, L., Chaudhary, J., Liu, Y., Joshi, T., Xu, D., Nguyen, H.T.: Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. - BMC Genomics 16: 520, 2015. Go to original source...
    27. Perotto, S., Rodda, M., Benetti, A., Sillo, F., Ercole, E., Rodda, M., Girlanda, M., Murat, C., Balestrini, R.: Gene expression in mycorrhizal orchid protocorms suggests a friendly plant-fungus relationship. - Planta 239: 1337-1349, 2014. Go to original source...
    28. Quiapim, A.A.C., Michael, S.B., Luciano, A.S.B.I., Malavazi, I., DePaoli, H.C., Molfetta-Machado, J.B., Giuliatti, S., Goldman, G.H., Goldman, M.H.S.: Analysis of the Nicotiana tabacum stigma/style transcriptome reveals gene expression differences between wet and dry stigma species. - Plant Physiol. 149: 1211-1230, 2009. Go to original source...
    29. Salts, Y., Sobolev, I., Chmelnitsky, I., Shabtai, S., Barg, R.: Genomic structure and expression of Lestd1, a seventransmembrane-domain protein-encoding gene specifically expressed in tomato pollen. - Israel J. Plant Sci. 53: 79-88, 2005. Go to original source...
    30. Seo, P.J., Park, J., Kang, S.K., Kim, S., Park, C.: An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. - Planta 233: 189-200, 2011. Go to original source...
    31. Seonga, E.S., Baeka, K., Oha, S., Joa, S.H., Yia, S.Y., Parka, J.M., Joungb, Y.H., Leea, S., Choa, H.S., Choi, D.: Induction of enhanced tolerance to cold stress and disease by overexpression of the pepper CaPIF1 gene in tomato. - Physiol. Plant. 129: 555-566, 2007. Go to original source...
    32. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S.: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony. - Mol. Biol. Evol. 11: 2731-2739, 2011. Go to original source...
    33. Wang, L., Xie, W., Chen, Y., Tang, W., Yang, J., Ye, R., Liu, L., Lin, Y., Xu, C., Xiao, J., Zhang, Q.: A dynamic gene expression atlas covering the entire life cycle of rice. - Plant J. 61: 752-766, 2010. Go to original source...
    34. Yamada, K., Osakabe, Y., Mizoi, J., Nakashima, K., Fujita, Y., Shinozaki, K., Yamaguchi-Shinozaki, K.: Functional analysis of an Arabidopsis thaliana abiotic stress-inducible facilitated diffusion transporter for monosaccharides. - J. biol. Chem. 285: 1138-1146, 2010. Go to original source...
    35. Yan, L., Wang, X., Liu, H., Tian, Y., Lian, J., Yang, R., Hao, S., Wang, X., Yang, S., Li, Q., Qi, S., Kui, L., Okpekum, M., Ma, X., Zhang, J., Ding, Z., Zhang, G., Wang, W., Dong, Y., Sheng, J.: The Genome of Dendrobium officinale illuminates the biology of the important traditional Chinese orchid herb. - Mol. Plant 8: 922-934, 2015. Go to original source...
    36. Yang, H., Chen, H.: Effect of high temperature stress on morphological and physiological characteristics in Phalaenopsis seedlings. - Chin. agr. Sci. Bull. 25: 123-127, 2009.
    37. Yang, J., Meng, H., Yang, S., Zhang, W., Zha, Y., Wen, G.: Correlation between soluble polysaacharide and sucrose metabolic enzymes in Dendrobium officinale. - J. West China Forest Sci. 41: 62-67, 2012.
    38. Yuan, M., Wang, S.: Rice MtN3/Saliva/SWEET family genes and their homologs in cellular organisms. - Mol. Plant 6: 665-674, 2013. Go to original source...
    39. Yuan, M., Zhao, J., Huang, R., Li, X., Xiao, J., Wang, S.: Rice MtN3/saliva/SWEET gene family: evolution, expression profiling, and sugar transport. - J. integr. Plant Biol. 56: 559-570, 2014a. Go to original source...
    40. Yuan, X., Jiang, S., Wang, M., Ma, J., Zhang, X., Cui, B.: Evaluation of internal control for gene expression in Phalaenopsis by quantitative real-time PCR. - Appl. Biochem. Biotechnol. 173: 1431-1445, 2014b. Go to original source...

    Return to the content