Abstract
In flowering plants, anthers bear male gametophytes whose development is regulated by the elaborate coordination of many genes. In addition, both gibberellic acid (GA3) and jasmonic acid (JA) play important roles in anther development and pollen fertility. To facilitate the analysis of anther development genes and how GA3 and JA regulate anther development, we performed microarray experiments using a 10-K cDNA microarray with probes derived from seedlings, meiotic anthers, mature anthers and GA3- or JA-treated suspension cells of rice. The expression level change of 2155 genes was significantly (by 2-fold or greater) detected in anthers compared with seedlings. Forty-seven genes, representing genes with potential function in cell cycle and cell structure regulation, hormone response, photosynthesis, stress resistance and metabolism, were differentially expressed in meiotic and mature anthers. Moreover, 314 genes responded to either GA3 or JA treatment, and 24 GA3- and 82 JA-responsive genes showed significant changes in expression between meiosis and the mature anther stages. RT-PCR demonstrated that gene y656d05 was not only highly expressed in meiotic anthers but also induced by GA3. Strong RNA signals of y656d05 were detected in pollen mother cells and tapetum in in situ hybridization. Further characterization of these candidate genes can contribute to the understanding of the molecular mechanism of anther development and the involvement of JA and GA3 signals in the control of anther development in rice.
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Abbreviations
- EST:
-
expressed sequence tag
- GA3:
-
gibberellic acid
- JA:
-
jasmonic acid
- RT-PCR:
-
reverse transcription-polymerase chain reaction
References
S.J. Armstrong G.H. Jones (2003) ArticleTitleMeiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana J. Exp. Bot. 54 1–10 Occurrence Handle10.1093/jxb/54.380.1 Occurrence Handle12456750
D. Aubert M. Chevillard A.M. Dorne G. Arlaud M. Herzog (1998) ArticleTitleExpression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions Plant Mol. Biol. 36 871–883 Occurrence Handle10.1023/A:1005938624418 Occurrence Handle9520278
G. Ben-Nissan J.Y. Lee A. Borohov D. Weiss (2004) ArticleTitleGIP, a Petunia hybrida GA-induced cysteine-rich protein: a possible role in shoot elongation and transition to flowering Plant J. 37 229–238 Occurrence Handle14690507
V. Cecchetti M. Pomponi M.M. Altamura M. Pezzotti S. Marsilio S. D’Angeli G.B. Tornielli P. Costantino M. Cardarelli (2004) ArticleTitleExpression of rolB in tobacco flowers affects the coordinated processes of anther dehiscence and style elongation Plant J. 38 512–525 Occurrence Handle10.1111/j.0960-7412.2004.02064.x Occurrence Handle15086797
C.B. Chen Y.Y. Xu K. Chong H. Ma Z.H. Xu (2005) ArticleTitleCell biological characterization of male meiosis and microspore development in rice (Oryza sativa L.) J. Integr. Plant Biol. 47 734–744
H. Cheng L. Qin S. Lee X. Fu D.E. Richards D. Cao D. Luo N.P. Harberd J. Peng (2004) ArticleTitleGibberellin regulates Arabidopsis floral development via suppression of DELLA protein function Development 131 1055–1064 Occurrence Handle10.1242/dev.00992 Occurrence Handle14973286
C.C. Chu C.C. Wang C.S. Sun (1975) ArticleTitleEstablishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources Sci. Sinica 18 659–668
D.J. Cosgrove L.C. Li H.T. Cho S. Hoffmann-Benning R.C. Moore D. Blecker (2002) ArticleTitleThe growing world of expansins Plant Cell Physiol. 43 1436–1444 Occurrence Handle10.1093/pcp/pcf180 Occurrence Handle12514240
P. Groot Particlede K. Weterings M. Been Particlede F. Wittink R. Hulzink J. Custers M. Herpen Particlevan G. Wullems (2004) ArticleTitleSilencing of the pollen-specific gene NTP303 and its family members in tobacco affects in vivo pollen tube growth and results in male sterile plants Plant Mol. Biol. 55 715–726 Occurrence Handle15604712
A. Devoto M. Nieto-Rostro D. Xie C. Ellis R. Harmston E. Patrick J. Davis L. Sherratt M. Coleman J.G. Turner (2002) ArticleTitleCOI1 links jasmonate signalling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis Plant J. 32 457–466 Occurrence Handle10.1046/j.1365-313X.2002.01432.x Occurrence Handle12445118
D.J. Dix J.W. Allen B.W. Collins C. Mori N. Nakamura P. Poorman-Allen E.H. Goulding E.M. Eddy (1996) ArticleTitleTargeted gene disruption of Hsp70-2 results in failed meiosis, germ cell apoptosis, and male infertility Proc. Natl. Acad. Sci. USA 93 3264–3268 Occurrence Handle10.1073/pnas.93.8.3264 Occurrence Handle8622925
R.B. Goldberg T.P. Beals P.M. Sanders (1993) ArticleTitleAnther development: basic principles and practical applications Plant Cell 5 1217–1229 Occurrence Handle10.1105/tpc.5.10.1217 Occurrence Handle8281038
J. Gomez-Maldonado F.M. Canovas C. Avila (2004) ArticleTitleMolecular analysis of the 5′-upstream region of a gibberellin-inducible cytosolic glutamine synthetase gene (GS1b) expressed in pine vascular tissue Planta 218 1036–1045 Occurrence Handle10.1007/s00425-003-1185-2 Occurrence Handle14735362
N. Goto R.P. Pharis (1999) ArticleTitleRole of gibberellins in the development of floral organs of gibberellin-deficient mutant, ga1-1, of Abrabidopsis thaliana Can. J. Bot. 77 944–954
L. Hennig W. Gruissem U. Grossniklaus C. Kohler (2004) ArticleTitleTranscriptional programs of early reproductive stages in Arabidopsis Plant Physiol. 135 1765–1775 Occurrence Handle10.1104/pp.104.043182 Occurrence Handle15247381
J.D. Higgins S.J. Armstrong F.C. Franklin G.H. Jones (2004) ArticleTitleThe Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis Gene. Dev. 18 2557–2570 Occurrence Handle10.1101/gad.317504 Occurrence Handle15489296
S. Huang R.E. Cerny Y. Qi D. Bhat C.M. Aydt D.D. Hanson K.P. Malloy L.A. Ness (2003) ArticleTitleTransgenic studies on the involvement of cytokinin and gibberellin in male development Plant Physiol. 131 1270–1282 Occurrence Handle10.1104/pp.102.018598 Occurrence Handle12644677
S. Ikeda J.B. Nasrallah R. Dixit S. Preiss M.E. Nasrallah (1997) ArticleTitleAn aquaporin-like gene required for the Brassica self-incompatibility response Science 276 1564–1566 Occurrence Handle10.1126/science.276.5318.1564 Occurrence Handle9171060
A. Izhaki A. Borochov E. Zamski D. Weiss (2002) ArticleTitleGibberellin regulates post-microsporogenesis processes in petunia anthers Physiol. Plant 115 442–447 Occurrence Handle10.1034/j.1399-3054.2002.1150314.x Occurrence Handle12081537
M. Kaneko Y. Inukai M. Ueguchi-Tanaka H. Itoh T. Izawa Y. Kobayashi T. Hattori A. Miyao H. Hirochika M. Ashikari M. Matsuoka (2004) ArticleTitleLoss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development Plant Cell 16 33–44 Occurrence Handle14688295
S. Kapoor A. Kobayashi H. Takatsuji (2002) ArticleTitleSilencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia Plant Cell 14 2353–2367 Occurrence Handle10.1105/tpc.003061 Occurrence Handle12368491
V.I. Klimyuk J.D. Jones (1997) ArticleTitleAtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression Plant J. 11 1–14 Occurrence Handle10.1046/j.1365-313X.1997.11010001.x Occurrence Handle9025299
L.F. Lan W. Chen Y. Lai J. Suo Z. Kong C. Li Y. Lu Y. Zhang X. Zhao X. Zhang B. Han J. Cheng Y.B. Xue (2004) ArticleTitleMonitoring of gene expression profiles and isolation of candidate genes involved in pollination and fertilization in rice (Oryza sativa L.) with a 10 K cDNA microarray Plant Mol. Biol. 54 471–487 Occurrence Handle10.1023/B:PLAN.0000038254.58491.c7 Occurrence Handle15316284
B. Lauga L. Charbonnel-Campaa D. Combes (2000) ArticleTitleCharacterization of MZm3-3, a Zea mays tapetum-specific transcript Plant Sci. 157 65–75 Occurrence Handle10.1016/S0168-9452(00)00267-3 Occurrence Handle10940470
A. Mandaokar V.D. Kumar M. Amway J. Browse (2003) ArticleTitleMicroarray and differential display identify genes involved in jasmonate-dependent anther development Plant Mol. Biol. 52 775–786 Occurrence Handle13677466
J.P. Mascarenhas (1990) ArticleTitleGene activity during pollen development Annu. Rev. Plant Dev. 41 317–318 Occurrence Handle10.1146/annurev.pp.41.060190.001533
H.S. Mason D.B. DeWald J.E. Mullet (1993) ArticleTitleIdentification of a methyl jasmonate-responsive domain in the soybean vspB promoter Plant Cell 5 241–251 Occurrence Handle8467221
K. Nonomura K. Miyoshi M. Eiguchi T. Suzuki A. Miyao H. Hirochika N. Kurata (2003) ArticleTitleThe MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice Plant Cell 15 1728–1739 Occurrence Handle10.1105/tpc.012401 Occurrence Handle12897248
S.Y. Park E.M. Lord (2003) ArticleTitleExpression studies of SCA in lily and confirmation of its role in pollen tube adhesion Plant Mol. Biol. 51 183–189 Occurrence Handle10.1023/A:1021139502947 Occurrence Handle12602877
S.K. Park R. Howden D. Twell (1998) ArticleTitleThe Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate Development 125 3789–3799 Occurrence Handle9729487
S.V. Pavlova S.M. Zakiian (2003) ArticleTitleSMC (structural maintenance of chromosomes) structural protein family and their role in chromatin reorganization Genetika 39 1301–1316 Occurrence Handle14658334
C. Prigent S. Dimitrov (2003) ArticleTitlePhosphorylation of serine 10 in histone H3, what for? J. Cell Sci. 116 3677–3685 Occurrence Handle10.1242/jcs.00735 Occurrence Handle12917355
M.R. Roberts F. Robson G.D. Foster J. Draper R.J. Scott (1991) ArticleTitleA Brassica napus mRNA expressed specifically in developing microspores Plant Mol. Biol. 17 295–299 Occurrence Handle10.1007/BF00039509 Occurrence Handle1863784
N. Rotman A. Durbarry A. Wardle W.C. Yang A. Chaboud J.E. Faure F. Berger D. Twell (2005) ArticleTitleA novel class of MYB factors controls sperm-cell formation in plants Curr. Biol. 15 244–248 Occurrence Handle10.1016/j.cub.2005.01.013 Occurrence Handle15694308
A.V. Strunnikov (2003) ArticleTitleCondensin and biological role of chromosome condensation Prog. Cell Cycle Res. 5 361–367 Occurrence Handle14593730
A.V. Strunnikov R. Jessberger (1999) ArticleTitleStructural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions Eur. J. Biochem. 263 6–13 Occurrence Handle10.1046/j.1432-1327.1999.00509.x Occurrence Handle10429180
S.M. Swain A.J. Muller D.P. Singh (2004) ArticleTitleThe gar2 and rga alleles increase the growth of gibberellin-deficient pollen tubes in Arabidopsis Plant Physiol. 134 694–705 Occurrence Handle10.1104/pp.103.031666 Occurrence Handle14764903
P. Theerakulpist H. Xu M.B. Singh J.M. Pettitt R.B. Knox (1991) ArticleTitleIsolation and developmental expression of Bcpl, an anther specific cDNA clone in Brassica campestris Plant Cell 3 1073–1084 Occurrence Handle10.1105/tpc.3.10.1073 Occurrence Handle1821760
V. Walbot M.M. Evans (2003) ArticleTitleUnique features of the plant life cycle and their consequences Nat. Rev. Genet. 4 369–79 Occurrence Handle10.1038/nrg1064 Occurrence Handle12728279
Z. Wang C.B. Chen Y.Y. Xu R.X. Jiang Y. Han Z.H. Xu K. Chong (2004) ArticleTitleA practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.) Plant Mol. Biol. Rep. 22 409–417
M. Weingartner H.R. Pelayo P. Binarova K. Zwerger B. Melikant C. la Torre Particlede E. Heberle-Bors L. Bogre (2003) ArticleTitleA plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint J. Cell Sci. 116 487–498 Occurrence Handle10.1242/jcs.00250 Occurrence Handle12508110
F. Wellmer J.L. Riechmann M. Alves-Ferreira E.M. Meyerowitz (2004) ArticleTitleGenome-wide analysis of spatial gene expression in Arabidopsis flowers Plant Cell 16 1314–1326 Occurrence Handle10.1105/tpc.021741 Occurrence Handle15100403
K. Weterings W. Reijnen R. Aarssen Particlevan A. Kortstee J. Spijkers M. Herpen Particlevan J. Schrauwen G. Wullems (1992) ArticleTitleCharacterization of a pollen-specific cDNA clone from Nicotiana tabacum expressed during microgametogenesis and germination Plant Mol. Biol. 18 1101–1111 Occurrence Handle10.1007/BF00047713 Occurrence Handle1600146
L. Xu F. Liu E. Lechner P. Genschik W.L. Crosby H. Ma W. Peng D. Huang D. Xie (2002a) ArticleTitleThe SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis Plant Cell 14 1919–1935 Occurrence Handle10.1105/tpc.003368
Y.Y. Xu K. Chong Z.H. Xu K.H. Tan (2002b) ArticleTitleThe practical technique of in situ hybridization with RNA probe Chinese Bull. Bot. 19 234–238
M. Yang Y. Hu M. Lodhi W.R. McCombie H. Ma (1999) ArticleTitleThe Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation Proc. Natl. Acad. Sci. USA 96 11416–11421 Occurrence Handle10.1073/pnas.96.20.11416 Occurrence Handle10500191
X. Yang C.A. Makaroff H. Ma (2003) ArticleTitleThe Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis Plant Cell 15 1281–1295 Occurrence Handle10.1105/tpc.010447 Occurrence Handle12782723
J. Yazaki N. Kishimoto Y. Nagata M. Ishikawa F. Fujii A. Hashimoto K. Shimbo Z. Shimatani K. Kojima K. Suzuki M. Yamamoto S. Honda A. Endo Y. Yoshida Y. Sato K. Takeuchi K. Toyoshima C. Miyamoto J. Wu T. Sasaki K. Sakata K. Yamamoto K. Iba T. Oda Y. Otomo K. Murakami K. Matsubara J. Kawai P. Carninci Y. Hayashizaki S. Kikuchi (2003) ArticleTitleGenomics approach to abscisic acid- and gibberellin-responsive genes in rice DNA Res. 10 249–261 Occurrence Handle15029956
D.Z. Zhao H. Ma (2000) ArticleTitleMale fertility: a case of enzyme identity Curr. Biol. 10 R904–R907 Occurrence Handle10.1016/S0960-9822(00)00848-4 Occurrence Handle11137026
D.Z. Zhao G.F. Wang B. Speal H. Ma (2002) ArticleTitleThe excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther Gene. Dev. 16 2021–2031 Occurrence Handle10.1101/gad.997902 Occurrence Handle12154130
D.Z. Zhao T. Han E. Risseeuw W.L. Crosby H. Ma (2003) ArticleTitleConservation and divergence of ASK1 and ASK2 gene functions during male meiosis in Arabidopsis thaliana Plant Mol. Biol. 53 163–173 Occurrence Handle10.1023/B:PLAN.0000009273.81702.b5 Occurrence Handle14756314
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Wang, Z., Liang, Y., Li, C. et al. Microarray Analysis of Gene Expression Involved in Anther Development in rice (Oryza sativa L.). Plant Mol Biol 58, 721–737 (2005). https://doi.org/10.1007/s11103-005-8267-4
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DOI: https://doi.org/10.1007/s11103-005-8267-4