Comparative Transcriptomics of Early Meiosis in Arabidopsis and Maize

Stefanie Dukowic-Schulze; Anthony Harris; Junhua Li; Anitha Sundararajan; Joann Mudge; Ernest F. Retzel; Wojciech P. Pawlowski; Changbin Chen

doi:10.1016/j.jgg.2013.11.007

Volume 41 Issue 3

Mar. 2014

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2014 > 41(3): 139-152

PDF( 3852 KB)

Comparative Transcriptomics of Early Meiosis in Arabidopsis and Maize

doi: 10.1016/j.jgg.2013.11.007

a
Department of Horticultural Science, University of Minnesota, St. Paul, MN 55108, USA
b
College of Life Sciences, Henan Normal University, Xinxiang, Henan 453007, China
c
National Center for Genome Resources, Santa Fe, NM 87505, USA
d
Department of Plant Breeding and Genetics, Cornell University, Ithaca, NY 14853, USA

More Information

Corresponding author: E-mail address: chenx481@umn.edu (Changbin Chen)
Received Date: 2013-06-29
Accepted Date: 2013-11-07
Rev Recd Date: 2013-10-31

Available Online: 2013-12-14

Publish Date: 2014-03-20

Abstract

Abstract

Though sexually reproductive plants share the same principle and most processes in meiosis, there are distinct features detectable. To address the similarities and differences of early meiosis transcriptomes from the dicot model system Arabidopsis and monocot model system maize, we performed comparative analyses of RNA-seq data of isolated meiocytes, anthers and seedlings from both species separately and via orthologous genes. Overall gene expression showed similarities, such as an increased number of reads mapping to unannotated features, and differences, such as the amount of differentially expressed genes. We detected major similarities and differences in functional annotations of genes up-regulated in meiocytes, which point to conserved features as well as unique features. Transcriptional regulation seems to be quite similar in Arabidopsis and maize, and we could reveal known and novel transcription factors and cis-regulatory elements acting in early meiosis. Taken together, meiosis between Arabidopsis and maize is conserved in many ways, but displays key distinctions that lie in the patterns of gene expression.
- Meiosis,
- Transcriptome,
- RNA-seq,
- Meiocytes,
- Maize

FullText(HTML)

References(57)

References

[1]	Adamo, A., Pinney, J.W., Kunova, A. et al. PloS ONE, 3 (2008),p. e2889
[2]	Anders, S., Huber, W.
[3]	Arabidopsis Genome Initiative Nature, 408 (2000),pp. 796-815
[4]	Armstrong, S.J., Franklin, F.C.H., Jones, G.H. Sex. Plant Reprod., 16 (2003),pp. 141-149
[5]	Armstrong, S.J., Jones, G.H. J. Exp. Bot., 54 (2003),pp. 1-10
[6]	Ayadi, M., Delaporte, V., Li, Y.-F. et al. FEBS Lett., 562 (2004),pp. 147-154
[7]	Azumi, Y., Liu, D., Zhao, D. et al. EMBO J., 21 (2002),pp. 3081-3095
[8]	Bowman, J.L., Smyth, D.R. Development (Cambridge, England), 126 (1999),pp. 2387-2396
[9]	Bowman, J.L., Smyth, D.R., Meyerowitz, E.M. Development, 112 (1991),pp. 1-20
[10]	Chen, C., Farmer, A.D., Langley, R.J. et al. BMC Plant Biol., 10 (2010),p. 280
[11]	Chen, C., Retzel, E.F.
[12]	Clifton, S.W., Minx, P., Fauron, C.M.-R. et al. Sequence and comparative analysis of the maize NB mitochondrial genome Plant Physiol., 136 (2004),pp. 3486-3503
[13]	Couteau, F., Belzile, F., Horlow, C. et al. Plant Cell, 11 (1999),pp. 1623-1634
[14]	Du, Z., Zhou, X., Ling, Y. et al. agriGO: a GO analysis toolkit for the agricultural community Nucleic Acids Res., 38 (2010),pp. W64-70
[15]	Duval, M., Hsieh, T.-F., Kim, S.Y. et al. Plant Mol. Biol., 50 (2002),pp. 237-248
[16]	Engel, M.L., Holmes-Davis, R., McCormick, S. Plant Physiol., 138 (2005),pp. 2124-2133
[17]	Galuschka, C., Schindler, M., Bülow, L. et al. AthaMap web tools for the analysis and identification of co-regulated genes Nucleic Acids Res., 35 (2007),pp. D857-862
[18]	Gaut, B. Nat. Genet., 44 (2012),pp. 115-116
[19]	Giegé, P., Brennicke, A. Proc. Natl. Acad. Sci. USA, 96 (1999),pp. 15324-15329
[20]	Haberer, G., Young, S., Bharti, A.K. et al. Structure and architecture of the maize genome Plant Physiol., 139 (2005),pp. 1612-1624
[21]	Hochberg, Y., Benjamini, Y. More powerful procedures for multiple significance testing Stat. Med., 9 (1990),pp. 811-818
[22]	Hsu, S.Y., Huang, Y.C., Peterson, P.A. Maydica, 33 (1988),pp. 77-98
[23]	Kubo, T., Fujita, M., Takahashi, H. et al. Transcriptome analysis of developing ovules in rice isolated by laser microdissection Plant Cell Physiol., 54 (2013),pp. 750-765
[24]	Kurzbauer, M.-T., Uanschou, C., Chen, D. et al. Plant Cell, 24 (2012),pp. 2058-2070
[25]	Li, J., Farmer, A.D., Lindquist, I.E. et al. BMC Plant Biol., 12 (2012),p. 104
[26]	Libeau, P., Durandet, M., Granier, F. et al. Plant Biol. (Stuttg), 13 (2011),pp. 784-793
[27]	Lin, X., Kaul, S., Rounsley, S. et al. Nature, 402 (1999),pp. 761-768
[28]	Liseron-Monfils, C., Lewis, T., Ashlock, D. et al. Promzea: a pipeline for discovery of co-regulatory motifs in maize and other plant species and its application to the anthocyanin and phlobaphene biosynthetic pathways and the Maize Development Atlas BMC Plant Biol., 13 (2013),p. 42
[29]	Lough, A.N., Roark, L.M., Kato, A. et al. Mitochondrial DNA transfer to the nucleus generates extensive insertion site variation in maize Genetics, 178 (2008),pp. 47-55
[30]	Mahony, S., Benos, P.V. STAMP: a web tool for exploring DNA-binding motif similarities Nucleic Acids Res., 35 (2007),pp. W253-258
[31]	Mata, J., Lyne, R., Burns, G. et al. The transcriptional program of meiosis and sporulation in fission yeast Nat. Genet., 32 (2002),pp. 143-147
[32]	Milne, I., Stephen, G., Bayer, M. et al. Using Tablet for visual exploration of second-generation sequencing data Brief Bioinform., 14 (2012),pp. 193-202
[33]	Mizukami, Y., Huang, H., Tudor, M. et al. Functional domains of the floral regulator AGAMOUS: characterization of the DNA binding domain and analysis of dominant negative mutations Plant Cell, 8 (1996),pp. 831-845
[34]	Okamoto, H., Hirochika, H. Silencing of transposable elements in plants Trends Plant Sci., 6 (2001),pp. 527-534
[35]	Padmore, R., Cao, L., Kleckner, N. Cell, 66 (1991),pp. 1239-1256
[36]	Peirson, B.N., Bowling, S.E., Makaroff, C.A. Plant J., 11 (1997),pp. 659-669
[37]	Riaño-Pachón, D.M., Ruzicic, S., Dreyer, I. et al. PlnTFDB: an integrative plant transcription factor database BMC Bioinform., 8 (2007),p. 42
[38]	Riechmann, J.L., Meyerowitz, E.M. The AP2/EREBP family of plant transcription factors Biol. Chem., 379 (1998),pp. 633-646
[39]	Rounsley, S.D., Ditta, G.S., Yanofsky, M.F. Plant Cell, 7 (1995),pp. 1259-1269
[40]	Schmidt, A., Schmid, M.W., Grossniklaus, U. Analysis of plant germline development by high-throughput RNA profiling: technical advances and new insights Plant J., 70 (2012),pp. 18-29
[41]	Schnable, P.S., Ware, D., Fulton, R.S. et al. The B73 maize genome: complexity, diversity, and dynamics Science, 326 (2009),pp. 1112-1115
[42]	Sharma, N., Russell, S.D., Bhalla, P.L. et al. Putative cis-regulatory elements in genes highly expressed in rice sperm cells BMC Res. Notes, 4 (2011),p. 319
[43]	Sheehan, M.J., Pawlowski, W.P. Imaging chromosome dynamics in meiosis in plants Methods Enzymol., 505 (2012),pp. 125-143
[44]	Sorensen, A.-M., Kröber, S., Unte, U.S. et al. Plant J., 33 (2003),pp. 413-423
[45]	Staiger, C.J., Cande, W.Z. Microfilament distribution in maize meiotic mutants correlates with microtubule organization Plant Cell, 3 (1991),pp. 637-644
[46]	Steffens, N.O., Galuschka, C., Schindler, M. et al. Nucleic Acids Res., 32 (2004),pp. D368-D372
[47]	Stupar, R.M., Lilly, J.W., Town, C.D. et al. Proc. Natl. Acad. Sci. USA, 98 (2001),pp. 5099-5103
[48]	Sundaresan, V., Springer, P., Volpe, T. et al. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements Genes Dev., 9 (1995),pp. 1797-1810
[49]	Supek, F., Bošnjak, M., Škunca, N. et al. REVIGO summarizes and visualizes long lists of gene ontology terms PLoS ONE, 6 (2011),p. e21800
[50]	Suwabe, K., Suzuki, G., Takahashi, H. et al. Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray Plant Cell Physiol., 49 (2008),pp. 1407-1416
[51]	Tang, X., Zhang, Z.-Y., Zhang, W.-J. et al. Global gene profiling of laser-captured pollen mother cells indicates molecular pathways and gene subfamilies involved in rice meiosis Plant Physiol., 154 (2010),pp. 1855-1870
[52]	Unte, U.S., Sorensen, A.-M., Pesaresi, P. et al. Plant Cell, 15 (2003),pp. 1009-1019
[53]	Wang, Y., Magnard, J.-L., McCormick, S. et al. Plant Physiol., 136 (2004),pp. 4127-4135
[54]	Xing, S., Salinas, M., Höhmann, S. et al. Plant Cell, 22 (2010),pp. 3935-3950
[55]	Yamasaki, M., Wright, S.I., McMullen, M.D. Genomic screening for artificial selection during domestication and improvement in maize Ann. Bot., 100 (2007),pp. 967-973
[56]	Yang, H., Lu, P., Wang, Y. et al. Plant J., 65 (2011),pp. 503-516
[57]	Yang, X., Makaroff, C.A., Ma, H. Plant Cell, 15 (2003),pp. 1281-1295