Floret-specific differences in gene expression and support for the hypothesis that tapetal degeneration of Zea mays L. occurs via programmed cell death

David S. Skibbe; Xiujuan Wang; Lisa A. Borsuk; Daniel A. Ashlock; Dan Nettleton; Patrick S. Schnable

doi:10.1016/S1673-8527(08)60081-8

Volume 35 Issue 10

Oct. 2008

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Floret-specific differences in gene expression and support for the hypothesis that tapetal degeneration of Zea mays L. occurs via programmed cell death

doi: 10.1016/S1673-8527(08)60081-8

a
Department of Genetics, Iowa State University, Ames, Iowa 50011 USA
b
Department of Mathematics, Iowa State University, Ames, Iowa 50011 USA
c
Department of Statistics, Iowa State University, Ames, Iowa 50011 USA
d
Center for Plant Genomics, Iowa State University, Ames, Iowa 50011 USA
e
Department of Agronomy, Iowa State University, Ames, Iowa 50011 USA

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Corresponding author: E-mail address: schnable@iastate.edu (Patrick S. Schnable)
Received Date: 2007-07-25
Accepted Date: 2008-07-10
Rev Recd Date: 2008-06-25

Available Online: 2008-10-18

Publish Date: 2008-10-20

Abstract

Abstract

The maize (Zea mays) spikelet consists of two florets, each of which contains three developmentally synchronized anthers. Morphologically, the anthers in the upper and lower florets proceed through apparently similar developmental programs. To test for global differences in gene expression and to identify genes that are coordinately regulated during maize anther development, RNA samples isolated from upper and lower floret anthers at six developmental stages were hybridized to cDNA microarrays. Approximately 9% of the tested genes exhibited statistically significant differences in expression between anthers in the upper and lower florets. This finding indicates that several basic biological processes are differentially regulated between upper and lower floret anthers, including metabolism, protein synthesis and signal transduction. Genes that are coordinately regulated across anther development were identified via cluster analysis. Analysis of these results identified stage-specific, early in development, late in development and bi-phasic expression profiles. Quantitative RT-PCR analysis revealed that four genes whose homologs in other plant species are involved in programmed cell death are up-regulated just prior to the time the tapetum begins to visibly degenerate (i.e., the mid-microspore stage). This finding supports the hypothesis that developmentally normal tapetal degeneration occurs via programmed cell death.
- anther development,
- programmed cell death,
- microarray,
- maize

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References(59)

References

[1]	Altschul, S.F., Gish, W., Miller, W. et al. Basic local alignment search tool J. Mol. Biol., 215 (1990),pp. 403-410
[2]	Altschul, S.F., Madden, T.L., Schaffer, A.A. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res., 25 (1997),pp. 3389-3402
[3]	Aouali, N., Laporte, P., Clement, C. Planta, 213 (2001),pp. 71-79
[4]	Baldi, P., Brunak, S.
[5]	Bedinger, P., Edgerton, M.D. Developmental staging of maize microspores reveals a transition in developing microspore proteins Plant Physiol., 92 (1990),pp. 474-479
[6]	Bedinger, P., Russell, S.D.
[7]	Bevan, M., Bancroft, I., Mewes, H.W. et al. Bioessays, 21 (1999),pp. 110-120
[8]	Bevan, M., Bancroft, I., Bent, E. et al. Nature, 391 (1998),pp. 485-488
[9]	Buchanan, B.B., Gruissem, W., Jones, R.L.
[10]	Cacharrón, J., Saedler, H., Theissen, G. Dev. Genes Evol., 209 (1999),pp. 411-420
[11]	Chitnis, P.R. PHOTOSYSTEM I: Function and physiology Annu. Rev. Plant Physiol. Plant Mol. Biol., 52 (2001),pp. 593-626
[12]	Coe, E.H., McCormick, S., Modena, S. White pollen in maize J. Hered., 72 (1981),pp. 318-320
[13]	DeGuzman, R., Riggs, C.D. A survey of proteinases active during meiotic development Planta, 210 (2000),pp. 921-924
[14]	Dudoit, S., Fridlyand, J. A prediction-based resampling method for estimating the number of clusters in a dataset Genome Boil., 3 (2002)
[15]	Grotewold, E. The genetics and biochemistry of floral pigments Annu. Rev. Plant. Biol., 57 (2006),pp. 761-780
[16]	Helentjaris, T., Weber, D., Wright, S. Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms Genetics, 118 (1988),pp. 353-363
[17]	Hellmann, H., Estelle, M. Plant development: Regulation by protein degradation Science, 297 (2002),pp. 793-797
[18]	Horner, H.T., Palmer, R.G. Mechanisms of genic male sterility Crop Sci., 35 (1995),pp. 1527-1535
[19]	Hsu, S.-Y., Peterson, P.A. The upper and lower florets of spikelets in maize J. Genet. Breeding, 45 (1991),pp. 215-222
[20]	Hsu, S.-Y., Huang, Y.-C., Peterson, P.A. Maydica, XXXIII (1988),pp. 77-98
[21]	Kapoor, S., Kobayashi, A., Takatsuji, H. Plant Cell, 14 (2002),pp. 2353-2367
[22]	Kobayashi, A., Sakamoto, A., Kubo, K. et al. Seven zinc-finger transcription factors are expressed sequentially during the development of anthers in petunia Plant J., 13 (1998),pp. 571-576
[23]	Lee, S.-L.J., Warmke, H.E. Organelle size and number in fertile and T-cytoplasmic male-sterile corn Am. J. Bot., 66 (1979),pp. 141-148
[24]	Li, N., Zhang, D.S., Liu, H.S. et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development Plant Cell, 18 (2006),pp. 2999-3014
[25]	Liu, F., Cui, X., Horner, H.T. et al. Mitochondrial aldehyde dehydrogenase activity is required for male fertility in maize Plant Cell, 13 (2001),pp. 1063-1078
[26]	Liu, F., Schnable, P.S. Functional specialization of maize mitochondrial aldehyde dehydrogenases Plant Physiol., 130 (2002),pp. 1657-1674
[27]	Ma, H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants Annu. Rev. Plant. Biol., 56 (2005),pp. 393-434
[28]	Mandaron, P.M., Niogret, F., Mache, R. et al. Theor. Appl. Genet., 80 (1990),pp. 134-138
[29]	Mewes, H.W., Albermann, K., Bahr, M. et al. Overview of the yeast genome Nature, 387 (1997),pp. 7-65
[30]	Mo, Y., Nagel, C., Taylor, L.P. Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen Proc. Natl. Acad. Sci. USA, 89 (1992),pp. 7213-7217
[31]	Nair, R.B., Bastress, K.L., Ruegger, M.O. et al. Plant Cell, 16 (2004),pp. 544-554
[32]	Nakazono, M., Qiu, F., Borsuk, L.A. et al. Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: Identification of genes expressed differentially in epidermal cells or vascular tissues of maize Plant Cell, 15 (2003),pp. 583-596
[33]	op den Camp, R.G., Kuhlemeier, C. Aldehyde dehydrogenase in tobacco pollen Plant Mol., 35 (1997),pp. 355-365
[34]	Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res., 29 (2001),p. e45
[35]	Poovaiah, B.W., Xia, M., Liu, Z. et al. Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers Planta, 209 (1999),pp. 161-171
[36]	Reed, J.C. Mechanisms of apoptosis J. Pathol., 157 (2000),pp. 1415-1430
[37]	Riley, M. Microbiol Rev., 57 (1993),pp. 862-952
[38]	Samach, A., Klenz, J.E., Kohalmi, S.E. et al. Plant J., 20 (1999),pp. 433-445
[39]	Scheller, H.V., Jensen, P.E., Haldrup, A. et al. Role of subunits in eukaryotic Photosystem I Biochim. Biophys. Acta, 1507 (2001),pp. 41-60
[40]	Skibbe, D.S., Schnable, P.S. Male sterility in maize Maydica, 50 (2005),pp. 367-376
[41]	Skibbe, D.S., Wang, X., Zhao, X. et al. Scanning microarrays at multiple intensities enhances discovery of differentially expressed genes Bioinformatics, 22 (2006),pp. 1863-1870
[42]	Skibbe, D.S., Liu, F., Wen, T.J. et al. Plant Mol. Biol., 48 (2002),pp. 751-764
[43]	Steiglitz, H. Role of beta-1,3 glucanase in post-meiotic microspore release Dev. Biol., 57 (1977),pp. 87-97
[44]	Storey, J.D., Tibshirani, R. Statistical significance for genomewide studies Proc. Natl. Acad. Sci. USA, 100 (2003),pp. 9440-9445
[45]	Sullivan, J.A., Shirasu, K., Deng, X.W. The diverse roles of ubiquitin and the 26S proteasome in the life of plants Nat. Rev. Genet., 4 (2003),pp. 948-958
[46]	Swidzinski, J.A., Leaver, C.J., Sweetlove, L.J. A proteomic analysis of plant programmed cell death Phytochemistry, 65 (2004),pp. 1829-1838
[47]	Tadege, M., Kuhlemeier, C. Aerobic fermentation during tobacco pollen development Plant Mol. Biol., 35 (1997),pp. 343-354
[48]	Tadege, M., Dupuis, I.I., Kuhlemeier, C. Ethanolic fermentation: New functions for an old pathway Trends Plant Sci., 4 (1999),pp. 320-325
[49]	Taylor, A.A., Horsch, A., Rzepczyk, A. et al. Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis Plant J., 12 (1997),pp. 1261-1271
[50]	Tsuji, H., Meguro, N., Suzuki, Y. et al. Induction of mitochondrial aldehyde dehydrogenase by submergence facilitates oxidation of acetaldehyde during re-aeration in rice FEBS Lett., 546 (2003),pp. 369-373
[51]	Vierstra, R.D. Proteolysis in plants: Mechanisms and functions Plant Mol. Biol., 32 (1996),pp. 275-302
[52]	Vierstra, R.D. The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins Trends Plant Sci., 8 (2003),pp. 135-142
[53]	Vizcay-Barrena, G., Wilson, Z.A. J. Exp. Bot., 57 (2006),pp. 2709-2717
[54]	Wang, M., Hoekstra, S., van Bergen, S. et al. Plant Mol. Biol., 39 (1999),pp. 489-501
[55]	Warmke, H.E., Lee, S.-L. Mitochondrial degeneration in Texas cytoplasmic male-sterile corn anthers J. Hered., 68 (1977),pp. 213-222
[56]	Wilson, Z.A., Morroll, S.M., Dawson, J. et al. Plant J., 28 (2001),pp. 27-39
[57]	Wise, R.P., Bronson, C.R., Schnable, P.S. et al. The genetics, pathology, and molecular biology of T-cytoplasm male sterility in maize Advance in Agronomy, 65 (1999),pp. 79-130
[58]	Wolfinger, R.D., Gibson, G., Wolfinger, E.D. et al. Assessing gene significance from cDNA microarray expression data via mixed models J. Comput. Biol., 8 (2001),pp. 625-637
[59]	Zhao, D., Yu, Q., Chen, M. et al. Development, 128 (2001),pp. 2735-2746