Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-25T08:16:17.891Z Has data issue: false hasContentIssue false

Identification, characterization and expression analysis of the chalcone synthase family in the Antarctic moss Pohlia nutans

Published online by Cambridge University Press:  11 January 2019

Xinghao Yao
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Jinan 250100, China
Tailin Wang
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Tianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin 300308, China
Huijuan Wang
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Jinan 250100, China
Hongwei Liu
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Jinan 250100, China
Shenghao Liu
Affiliation:
Marine Ecology Research Center, The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
Qingang Zhao
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China
Kaoshan Chen
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Jinan 250100, China
Pengying Zhang*
Affiliation:
National Glycoengineering Research Center and School of Life Science, Shandong University, Jinan 250100, China Shandong Provincial Key Laboratory of Carbohydrate Chemistry and Glycobiology, Jinan 250100, China

Abstract

Mosses have adapted to the Antarctic environment and are an ideal medium for studying plant resistance to abiotic stress. Chalcone synthase is the first committed enzyme in the flavonoid metabolic pathway, which plays an indispensable role in plant resistance to adversity. In this study, six genes (Pn021, PnCHS088, Pn270, PnCHS444, PnCHS768 and Pn847) were identified in the Antarctic moss Pohlia nutans Lindberg transcriptome by reverse transcription polymerase chain reaction (RT-PCR) and rapid amplification of cDNA ends (RACE). Sequence alignment and three-dimensional structure analysis revealed the conserved amino acid residues of the enzymes of the chalcone synthase family, including three catalytic residues (Cys164, His303 and Asn336) and two substrate recognition residues (Phe215 and Phe265). Phylogenetic analysis indicated that PnCHS088, PnCHS444 and PnCHS768 might be chalcone synthase but that Pn021 is more like stilbenecarboxylate synthase. These genes were located at the transition between fungi and advanced plants in the phylogenetic tree. In addition, real-time PCR analysis revealed that the expression profiles of the six P. nutans genes were influenced by diverse abiotic stresses as well as by abscisic acid and methyl jasmonate. The results presented here contribute to the study of the CHS gene family in polar mosses and further reveal the mechanisms underlying the adaptation of mosses to extreme environments.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

joint lead authorship

References

Baharum, H., Morita, H., Tomitsuka, A., Lee, F.C., Ng, K.Y., Rahim, R.A., et al. 2011. Molecular cloning, modeling, and site-directed mutagenesis of type III polyketide synthase from Sargassum binderi (Phaeophyta). Marine Biotechnology, 13, 845856.Google Scholar
Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., et al. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(Web Server issue), W252W258.Google Scholar
Castellarin, S.D., Matthews, M.A., Gaspero, G.D. & Gambetta, G.A. 2007. Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta, 227, 101112.Google Scholar
Chen, L.J., Guo, H.M., Lin, Y. & Cheng, H.M. 2015. Chalcone synthase EaCHS1 from Eupatorium adenophorum functions in salt stress tolerance in tobacco. Plant Cell Reports, 34, 885894.Google Scholar
Chen, S., Pan, X.H., Li, Y.T., Cui, L.J., Zhang, Y.C., Zhang, Z.M. et al. 2017. Identification and characterization of chalcone synthase gene family members in Nicotiana tabacum. Journal of Plant Growth Regulation, 36, 374384.Google Scholar
Choi, S., Kwon, Y.R., Hossain, M.A., Hong, S.W., Lee, B.H. & Lee, H. 2009. A mutation in ELA1, an age-dependent negative regulator of PAP1/MYB75, causes UV- and cold stress-tolerance in Arabidopsis thaliana seedlings. Plant Science, 176, 678686.Google Scholar
Convey, P. & Stevens, M.I. 2007. Antarctic biodiversity. Science, 317, 18771878.Google Scholar
Dale, T.M., Skotnicki, M.L., Adam, K.D. & Selkirk, P.M. 1999. Genetic diversity in the moss Hennediella heimii in Miers Valley, Southern Victoria Land, Antarctica. Polar Biology, 21, 228233.Google Scholar
Dao, T.T.H., Linthorst, H.J.M. & Verpoorte, R. 2011. Chalcone synthase and its functions in plant resistance. Phytochemistry Reviews, 10, 397412.Google Scholar
Feinbaum, R.L. & Ausubel, F.M. 1988. Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Molecular and Cellular Biology, 8, 19851992.Google Scholar
Gambino, G., Perrone, I. & Gribaudo, I. 2008. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochemical Analysis, 19, 520525.Google Scholar
Goiris, K., Muylaert, K., Voorspoels, S., Noten, B., Paepe, D.D., Baart, G.J.E. & Cooman, L.D. 2014. Detection of flavonoids in microalgae from different evolutionary lineages. Journal of Phycology, 50, 483492.Google Scholar
Han, Y.H., Cao, Y.P., Jiang, H.Y. & Ding, T. 2017. Genome-wide dissection of the chalcone synthase gene family in Oryza sativa. Molecular Breeding, 37, 119.Google Scholar
Han, Y.H, Ding, T., Su, B. & Jiang, H.Y. 2016. Genome-wide identification, characterization and expression analysis of the chalcone synthase family in maize. International Journal of Molecular Sciences, 17, 161.Google Scholar
Hrazdina, G., Zobel, A.M. & Hoch, H.C. 1987. Biochemical, immunological, and immunocytochemical evidence for the association of chalcone synthase with endoplasmic reticulum membranes. Proceedings of the National Academy of Sciences of the United States of America, 84, 89668970.Google Scholar
Jez, J.M., Bowman, M.E. & Noel, J.P. 2002. Expanding the biosynthetic repertoire of plant type III polyketide synthases by altering starter molecule specificity. Proceedings of the National Academy of Sciences of the United States of America, 99, 53195324.Google Scholar
Jez, J.M., Ferrer, J.L., Bowman, M.E., Dixon, R.A. & Noel, J.P. 2000. Dissection of malonyl-coenzyme A decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry, 39, 890902.Google Scholar
Jiang, C.G., Schommer, C.K., Kim, S.Y. & Suh, D.Y. 2006. Cloning and characterization of chalcone synthase from the moss, Physcomitrella patens. Phytochemistry, 67, 25312540.Google Scholar
Jiang, J.J., Shao, Y.L., Li, A.M., Lu, C.L., Zhang, Y.T. & Wang, Y.P. 2013. Phenolic composition analysis and gene expression in developing seeds of yellow- and black-seeded Brassica napus. Journal of Integrative Plant Biology, 55, 537551.Google Scholar
Kim, S.Y., Che, C.C., Wiedemann, G., Jepson, C., Rahimi, M., Rothwell, J.R., et al. 2013. Physcomitrella PpORS, basal to plant type III polyketide synthases in phylogenetic trees, is a very long chain 2’-oxoalkylresorcinol synthase. Journal of Biological Chemistry, 288, 27672777.Google Scholar
Koduri, P.K.H., Gordon, G.S., Barker, E.I., Colpitts, C.C., Ashton, N.W. & Suh, D.Y. 2010. Genome-wide analysis of the chalcone synthase superfamily genes of Physcomitrella patens. Plant Molecular Biology, 72, 247263.Google Scholar
Landrey, L.G., Chapple, C.C.S. & Last, R.L. 1995. Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiology, 109, 11591166.Google Scholar
Leyva, A., Jarillo, J.A., Salinas, J. & Martinez-Zapater, J.M. 1995. Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiology, 108, 3946.Google Scholar
Li, L., Aslam, M., Rabbi, F., Vanderwel, C., Ashton, N.W. & Suh, D.Y. 2018. PpORS, an ancient type III polyketide synthase, is required for integrity of leaf cuticle and resistance to dehydration in the moss, Physcomitrella patens. Planta, 247, 527541.Google Scholar
Li, J., Ou-Lee, T.M., Raba, R., Amundson, R.G. & Last, R.L. 1993. Arabidopsis flavonoid mutants are hypersensitive to UV-B irradiation. Plant Cell, 5, 171179.Google Scholar
Liu, S.H., Ju, J.F. & Xia, G.M. 2014. Identification of the flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase genes from Antarctic moss and their regulation during abiotic stress. Gene, 543, 145152.Google Scholar
Oh, J.E., Kim, Y.H., Kim, J.H., Kwon, Y.R. & Lee, H.J. 2011. Enhanced level of anthocyanin leads to increased salt tolerance in Arabidopsis PAP1-D plants upon sucrose treatment. Journal of the Korean Society for Applied Biological Chemistry, 54, 7988.Google Scholar
Roads, E., Longton, R.E. & Convey, P. 2014. Millennial timescale regeneration in a moss from Antarctica. Current Biology, 24, 222223.Google Scholar
Saslowsky, D. & Winkel-Shirley, B. 2001. Localization of flavonoid enzymes in Arabidopsis roots. Plant Journal, 27, 3748.Google Scholar
Schmelzer, E., Jahnen, W. & Hahlbrock, K. 1988. In situ localization of light-induced chalcone synthase mRNA, chalcone synthase, and flavonoid end products in epidermal cells of parsley leaves. Proceedings of the National Academy of Sciences of the United States of America, 85, 29892993.Google Scholar
Seppelt, R.D., Green, T.G.A., Schwartz, A.M.J. & Frost, A. 1992. Extreme southern locations for moss sporophytes in Antarctica. Antarctic Science, 4, 3739.Google Scholar
Shvarts, M., Borochov, A. & Weiss, D. 1997. Low temperature enhances petunia flower pigmentation and induces chalcone synthase gene expression. Physiologia Plantarum, 99, 6772.Google Scholar
Skotnicki, M.L., Mackenzie, A.M., Clements, M.A. & Selkirk, P.M. 2005. DNA sequencing and genetic diversity of the 18S–26S nuclear ribosomal internal transcribed spacers (ITS) in nine Antarctic moss species. Antarctic Science, 17, 377384.Google Scholar
Tian, L., Wan, S.B., Pan, Q.H., Zheng, Y.J. & Huang, W.D. 2008. A novel plastid localization of chalcone synthase in developing grape berry. Plant Science, 175, 431436.Google Scholar
Wang, S.S., Xie, X.D., Zhang, L., Lin, F.C., Luo, Z.P., Li, F., et al. 2017. Comparative analysis of chalcone synthase gene family among Nicotiana tabacum L. and its diploid progenitors. Tobacco Science & Technology, 13, 114.Google Scholar
Xu, W.J., Dubos, C. & Lepiniec, L. 2015. Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends in Plant Science, 20, 176185.Google Scholar
Zhang, J.Z. 2003. Evolution by gene duplication: an update. Trends in Ecology & Evolution, 18, 292298.Google Scholar
Zhang, X.B., Abrahan, C., Colquhoun, T.A., Liu, C.J. 2017. A proteolytic regulator controlling chalcone synthase stability and flavonoid biosynthesis in Arabidopsis. Plant Cell, 29, 11571174.Google Scholar
Zhang, Y.M., Muyrers, J.P., Testa, G. & Stewart, A.F. 2000. DNA cloning by homologous recombination in Escherichia coli. Nature Biotechnology, 18, 13141317.Google Scholar
Zhu, J.K. 2002. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology, 53, 247273.Google Scholar
Supplementary material: PDF

Yao et al. supplementary material

Yao et al. supplementary material 1

Download Yao et al. supplementary material(PDF)
PDF 12.8 KB