Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-15T09:19:27.319Z Has data issue: false hasContentIssue false
  • English
  • Français

Expression analysis of seed-specific genes in four angiosperm species with an emphasis on the unconserved expression patterns of homologous genes

Published online by Cambridge University Press:  24 September 2013

Lichao Ma ,
Yanrong Wang ,
Wenxian Liu  and
Zhipeng Liu
Lichao Ma
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, School of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou730020, China
Yanrong Wang
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, School of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou730020, China
Wenxian Liu
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, School of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou730020, China
Zhipeng Liu*
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, School of Pastoral Agricultural Science and Technology, Lanzhou University, Lanzhou730020, China
*
*Correspondence E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Medicago truncatula, soybean (Glycine max), Arabidopsis thaliana and rice (Oryza sativa) all belong to the core angiosperm group of plants. Seed-specific genes are important for seed formation and development in these angiosperms. The identification of genes specifically expressed in angiosperm seeds and the comparison of the expression patterns of homologous genes among different angiosperm species can provide novel insights into the functions of genes that control seed development and the evolution of angiosperms. We downloaded the sequences and expression data from the relevant databases, and the seed-specific expression of genes was identified with cut-offs of a gene expression level ratio ≥ 5 and a Z-score ≥ 6. The genes were analysed using local BLAST software with an E-value ≤ 1.0E − 505. A total of 605, 581, 778 and 722 genes showed specific expression in the seeds of Medicago, soybean, Arabidopsis and rice, respectively. Additionally, we compared the expression patterns of seed-specific genes from each species with their homologues in the other three species, and found that the degree of variation in the expression patterns of homologous genes was low among closely related species but higher among more distantly related ones. The discrepancy between the homologous gene expression patterns may be caused by the different characteristics of the cis-elements in the promoter regions of the homologous genes.

Keywords

angiospermsgene expressionhomologous geneseeds
Type
Research Papers
Information
Seed Science Research , Volume 23 , Issue 4 , December 2013 , pp. 223 - 231
Copyright
Copyright © Cambridge University Press 2013 

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.)

References

Allen, R.D., Bernier, F., Lessard, P.A. and Beachy, R.N. (1989) Nuclear factors interact with a soybean beta-conglycinin enhancer. Plant Cell 1, 623–631.Google ScholarPubMed
Baskin, C.C. and Baskin, J.M. (1998) Seeds: ecology, biogeography and evolution of dormancy and germination. San Diego, Academic Press.Google Scholar
Baumlein, H., Boerjan, W., Nagy, I., Bassuner, R., Van Montague, M., Inze, D. and Wobus, U. (1991) A novel seed protein gene from Vicia faba is developmentally regulated in transgenic tobacco and Arabidopsis plants. Molecular Genetics and Genomics 225, 459–467.CrossRefGoogle ScholarPubMed
Benedito, V.A., Torres-Jerez, I., Murray, J., Andriankaja, A., Allen, S., Kakar, K., Wandrey, M., Verdier, J., Zuber, H., Ott, T., Moreau, S., Niebel, A., Frickey, T., Weiller, G., He, J., Dai, X., Zhao, P., Tang, Y. and Udvardi, M. (2008) A gene expression atlas of the model legume Medicago truncatula. Plant Journal 55, 504–513.CrossRefGoogle ScholarPubMed
Boulter, D., Evans, I.M., Ellis, J.R., Shirsat, A., Gatehouse, J.A. and Croy, R.R.D. (1987) Differential gene expression in the development of Pisum sativum. Plant Physiology and Biochemistry 25, 283–289.Google Scholar
Chanderbali, A.S., Yoo, M.J., Zahn, L.M., Brockington, S.F. and Wall, P.K. (2010) Conservation and canalization of gene expression during angiosperm diversification accompany the origin and evolution of the flower. Proceedings of the National Academy of Sciences USA 107, 22570–22575.CrossRefGoogle ScholarPubMed
Chandrasekharan, M.B., Blshop, K.J. and Hall, T.C. (2003) Module-specific regulation of the beta-phaseolin promoter during embryogenesis. Plant Journal 33, 853–866.CrossRefGoogle ScholarPubMed
Chuck, G., Meeley, R.B. and Hake, S. (1998) The control of maize spikelet meristem fate by the APETALA2-like gene INDETERMINATE SPIKELET1. Genes and Development 12, 1145–1154.CrossRefGoogle Scholar
Clark, R.M., Schweikert, G., Toomajian, C., Ossowski, S., Zeller, G., Shinn, P., Warthmann, N., Hu, T.T., Fu, G., Hinds, D.A., Chen, H., Frazer, K.A., Huson, D.H., Schölkopf, B., Nordborg, M., Rätsch, G., Ecker, J.R. and Weigel, D. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317, 338–342.CrossRefGoogle ScholarPubMed
Conrad, U., Fiedler, U., Artsaenko, O. and Phillips, J. (1998) High-level and stable accumulation of single-chain Fv antibodies in plant storage organs. Journal of Plant Physiology 152, 708–711.CrossRefGoogle Scholar
Crane, P.R., Friis, E.M. and Pedersen, K.R. (1995) The origin and early diversification of angiosperms. Nature 374, 27–33.CrossRefGoogle Scholar
Czihal, A., Conrad, U., Buchner, P., Brevis, R., Farouk, A.A., Manteuffel, R. and Adler, K. (1999) Gene farming in plants: expression of a heat-stable bacillus amylase in transgenic legume seeds. Journal of Plant Physiology 155, 183–189.CrossRefGoogle Scholar
Dong, Q., Schlueter, S.D. and Brendel, V. (2004) PlantGDB, plant genome database and analysis tools. Nucleic Acids Research 32, 354–359.CrossRefGoogle ScholarPubMed
Doyle, J.J. and Luckow, M.A. (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiology 131, 900–910.CrossRefGoogle Scholar
Ellerstrom, M., Stalberg, K., Ezcurra, I. and Rask, L. (1996) Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Molecular Biology 32, 1019–1027.CrossRefGoogle ScholarPubMed
Ezcurra, I., Ellerstrom, M., Wycliffe, P., Stalberg, K. and Rask, L. (1999) Interaction between composite elements in the napA promoter: both the B-box ABA-responsive complex and the RY/G complex are necessary for seed-specific expression. Plant Molecular Biology 40, 499–709.CrossRefGoogle ScholarPubMed
Fiedler, U. and Conrad, U. (1995) High-level production and long-term storage of engineered antibodies in transgenic tobacco seeds. Biotechnology 13, 1090–1093.CrossRefGoogle ScholarPubMed
Finkelstein, R.R. and Lynch, T.J. (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599–609.CrossRefGoogle ScholarPubMed
Higo, K., Ugawa, Y., Iwamoto, M. and Korenaga, T. (1999) Plant cis-acting regulatory DNA elements (PLACE) database:1999. Nucleic Acids Research 27, 297–300.CrossRefGoogle ScholarPubMed
Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J. and dePamphilis, C.W. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100.CrossRefGoogle ScholarPubMed
Jofuku, K.D., Omidyar, P.K., Gee, Z. and Okamuro, J.K. (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proceedings of the National Academy of Sciences USA 102, 3117–3122.CrossRefGoogle ScholarPubMed
Kim, S., Soltis, P.S., Wall, K. and Soltis, D.E. (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Molecular Biology and Evolution 23, 107–120.CrossRefGoogle ScholarPubMed
Li, G. and Hall, T.C. (1999) Footprinting in vivo reveals changing profiles of multiple factor interactions with the β-phaseolin promoter during embryogenesis. Plant Journal 18, 633–641.CrossRefGoogle ScholarPubMed
Li, M.N., Xu, W.Y., Yang, W.Q., Kong, Z.S. and Xue, Y.B. (2007) Genome-wide gene expression profiling reveals conserved and novel molecular functions of the stigma in rice. Plant Physiology 144, 1797–1812.CrossRefGoogle ScholarPubMed
Liu, Z.P., Ma, L.C., Na, Z.B. and Wang, Y.R. (2013) Comparative transcriptional profiling provides insights into the evolution and development of the zygomorphic flower of Vicia sativa (Papilionoideae). PLoS One 8, e57338.CrossRefGoogle ScholarPubMed
Maes, T., van de Steene, N., Zethof, J., Karimi, M., D'Hauw, M., Mares, G., van Montagu, M. and Gerats, T. (2001) Petunia AP2-like genes and their role in flower and seed development. Plant Cell 13, 229–244.CrossRefGoogle ScholarPubMed
Ohto, M.A., Fischer, R.L., Goldberg, R.B., Nakamura, K. and Harada, J.J. (2005) Control of seed mass by APETALA2. Proceedings of the National Academy of Sciences USA 102, 3123–3128.CrossRefGoogle ScholarPubMed
Phillips, J., Artsaenko, O., Fiedler, U., Horstmann, C., Mock, H.P., Muntz, K. and Conrad, U. (1997) Seed-specific immunomodulation of abscisic acid activity induces a developmental switch. EMBO Journal 16, 4489–4496.CrossRefGoogle ScholarPubMed
Qu, L.Q., Xing, Y.P., Liu, W.X., Xu, X.P. and Song, Y.R. (2008) Expression pattern and activity of six glutelin gene promoters in transgenic rice. Journal of Experimental Botany 59, 2417–2424.CrossRefGoogle ScholarPubMed
Reidt, W., Wohlfarth, T., Elierstrom, M., Czlhai, A., Tewes, A., Ezcurra, I., Rask, L. and Baumlein, H. (2000) Gene regulation during late embryogenesis: the RY motif maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant Journal 21, 401–408.CrossRefGoogle ScholarPubMed
Saalbach, I., Giersberg, M. and Conrad, U. (2001) High-level expression of a single chain Fv fragment (scFv) antibody in transgenic pea seeds. Journal of Plant Physiology 158, 529–533.CrossRefGoogle Scholar
Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K.N., Hsu, Y.C., Lee, P.Y., Truong, M.T., Beals, T.P. and Goldberg, R.B. (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11, 297–322.CrossRefGoogle Scholar
Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D. and Lohmann, J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501–506.CrossRefGoogle ScholarPubMed
Severin, A.J., Woody, J.L., Bolon, Y.T., Joseph, B., Diers, B.W., Farmer, A.D., Muehlbauer, G.J., Nelson, R.T., Grant, D., Specht, J.E., Graham, M.A., Cannon, S.B., May, G.D., Vance, C.P. and Shoemaker, R.C. (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biology 10, 160.CrossRefGoogle Scholar
Shirsat, A.H., Meakin, P.J. and Gatehouse, J.A. (1990) Sequences 5′ to the conserved 28 bp Leg box element regulate the expression of pea seed storage protein gene legA. Plant Molecular Biology 15, 685–693.CrossRefGoogle Scholar
Sonnhammer, E.L.L. and Koonin, E.V. (2002) Orthology, paralogy and proposed classification for paralog subtypes. Trends in Genetics 18, 619–620.CrossRefGoogle ScholarPubMed
Stalberg, K., Ellerstom, M., Ezcurra, I., Ablov, S. and Rask, L. (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199, 515–519.CrossRefGoogle ScholarPubMed
Sutoh, K. and Yamauchi, D. (2003) Two cis-acting elements necessary and sufficient for gibberellin-upregulated proteinase expression in rice seeds. Plant Journal 34, 635–645.CrossRefGoogle ScholarPubMed
Tang, M.F., Li, G.S. and Chen, M.S. (2007) The phylogeny and expression pattern of APETALA2-like genes in rice. Journal of Genetics and Genomics 34, 930–938.CrossRefGoogle ScholarPubMed
Thomas, M.S. and Flavell, R.B. (1990) Identification of an enhancer element for the endosperm-specific expression of high molecular weight glutenin. Plant Cell 2, 1171–1180.Google ScholarPubMed
Thompson, A.J., Evans, I.M., Boulter, D., Croy, R.R.D. and Gatehouse, J.A. (1989) Transcriptional and post-transcriptional regulation of seed storage-protein gene expression in pea (Pisum sativum). Planta 179, 279–287.CrossRefGoogle Scholar
Wei, L.Q., Xu, W.Y., Deng, Z.Y., Su, Z., Xue, Y.B. and Wang, T. (2010) Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11, 338.CrossRefGoogle ScholarPubMed
Wendel, F. (2000) Genome evolution in polyploids. Plant Molecular Biology 42, 225–249.CrossRefGoogle ScholarPubMed
Wikstrom, N., Savolainen, V. and Chase, M.W. (2001) Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society of London, series B 268, 2211–2220.CrossRefGoogle ScholarPubMed
Wu, C., Washida, H., Onodera, Y., Harada, K. and Takaiwa, F. (2000) Quantitative nature of the Prolamin-box, ACGT and AACA motifs in a rice glutelin gene promoter: minimal cis-element requirements for endosperm-specific gene expression. Plant Journal 23, 415–421.CrossRefGoogle Scholar
Yoo, M.J., Altman, N., Soltis, D., Soltis, P. and Soltis, D. (2010) Evolutionary trends in the floral transcriptome: insights from one of the basalmost angiosperms, the water lily Nuphar advena (Nymphaeaceae). Plant Journal 64, 687–698.CrossRefGoogle ScholarPubMed
Young, N.D. and Udvardi, M. (2009) Translating Medicago truncatula genomics to crop legumes. Current Opinion in Plant Biology 12, 193–201.CrossRefGoogle ScholarPubMed
Zakharov, A., Giersberg, M., Hosein, F., Melzer, M., Muntz, K. and Saalbach, I. (2004) Seed-specific promoters direct gene expression in non-seed tissue. Journal of Experimental Botany 55, 1463–1471.CrossRefGoogle ScholarPubMed
Zhang, X.M., Odom, D.T., Koo, S.H., Conkright, M.D., Canettieri, G., Best, J., Chen, H.M., Jenner, R., Herbolsheimer, E., Jacobsen, E., Kadam, S., Ecker, J.R., Emerson, B., Hogenesch, J.B., Unterman, T., Young, R.A. and Montminy, M. (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proceedings of the National Academy of Sciences USA 102, 4459–4464.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 329 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 326 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 325 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 324.9 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 324.4 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 323.6 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 323.4 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 318.2 KB
Supplementary material: Image

Ma Supplementary Material

Image

Download Ma Supplementary Material(Image)
Image 388.8 KB
Supplementary material: File

Ma Supplementary Material

Table

Download Ma Supplementary Material(File)
File 23 KB