Abstract
MEZ1 (MEiosis-associated Zinc-finger protein 1) was first isolated as an anther-specific cDNA from Petunia hybrida. In the present study, we report its functional characterization, including its spatial and temporal expression profiles and phenotypes in MEZ1-silenced plants. MEZ1 transcripts were specifically localized in pollen mother cells during early stages of anther development, and were later distributed in vegetative tissues in anthers. Silencing of MEZ1 by cosuppression resulted in several anomalies during male meiosis that included inability of chromosomes to condense, loss of meiotic synchrony, and premature and apparently uncontrolled cytokinetic events. Consequently, by the end of meiosis 8–10 cells, instead of the normal 4, with varying DNA contents were formed in the MEZ1-silenced meiocytes. Most of these aborted prematurely, and those that matured had a distinctive morphology. MEZ1-silenced plants were female sterile when pollinated with wild-type pollen but they infrequently produced a few seeds upon self-pollination. Resulting T1 plants had increased ploidy levels and exhibited severe anomalies during male meiosis, rendering them completely sterile. We discuss possible role of MEZ1 in the proper progression of plant meiosis.
Similar content being viewed by others
Abbreviations
- am1 :
-
ameiotic1
- Bl:
-
bud length
- CaMV:
-
cauliflower mosaic virus
- DAP:
-
days after pollination
- DAPI:
-
4′,6-diamidino-2-phenylindole
- MEZ1 :
-
MEiosis-associated Zinc-finger protein 1
- cMEZ1 :
-
MEZ1 cDNA
- NLS:
-
nuclear localization signal
- PMC:
-
pollen mother cell
- SAP :
-
STERILE APETALA
- SPL/NZZ :
-
SPOROCYTELESS/NOZZLE
- SWI1 :
-
Switch1
References
R.C. Brown B.E. Lemmon (1988) ArticleTitleMicrotubules associated with simultaneous cytokinesis of coenocytic microsporocytes Am. J. Bot. 75 1848–1856 Occurrence Handle10.2307/2444739
R.C. Brown B.E. Lemmon (2001) ArticleTitleThe cytoskeleton and spatial control of cytokinesis in the plant life cycle Protoplasma 215 35–49 Occurrence Handle11732063 Occurrence Handle1:STN:280:DC%2BD3Mnos1Onsw%3D%3D Occurrence Handle10.1007/BF01280302
C. Bushell M. Spielman R.J. Scott (2003) ArticleTitleThe basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species Plant Cell 15 1430–1442 Occurrence Handle12782734 Occurrence Handle1:CAS:528:DC%2BD3sXkvVektrg%3D Occurrence Handle10.1105/tpc.010496
M.V. Byzova J. Franken M.G. Aarts J. Almeida-Engler Particlede G. Engler C. Mariani M.M. Lookeren Campagne ParticleVan G.C. Angenent (1999) ArticleTitle Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development Genes Dev. 13 1002–1014 Occurrence Handle10215627 Occurrence Handle1:CAS:528:DyaK1MXivFGkurk%3D
C. Canales A.M. Bhatt R. Scott H. Dickinson (2002) ArticleTitleEXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis Curr. Biol. 12 1718–1727 Occurrence Handle12401166 Occurrence Handle1:CAS:528:DC%2BD38Xot1ags7w%3D Occurrence Handle10.1016/S0960-9822(02)01151-X
L. Comai A.P. Tyagi K. Winter R. Holmes-Davis S.H. Reynolds Y. Stevens B. Byers (2000) ArticleTitlePhenotypic instability and rapid gene silencing in newly formed arabidopsis allotetraploids Plant Cell 12 1551–1568 Occurrence Handle11006331 Occurrence Handle1:CAS:528:DC%2BD3cXnsVylsbc%3D Occurrence Handle10.1105/tpc.12.9.1551
P. Echlin H. Godwin (1968) ArticleTitleThe ultrastructure and ontogeny of pollen in Helleborus foetidus L. II. Pollen grain development through the callose special wall stage J Cell Sci 3 175–186 Occurrence Handle5661995 Occurrence Handle1:STN:280:CCeA38ngsFI%3D
M. Foiani R. Capone E. Nadjar-Boger S. Sagee T. Hashimshoni Y. Kassir (1996) ArticleTitleA meiosis-specific protein kinase, Ime2, is required for the correct timing of DNA replication and for spore formation in yeast meiosis Mol. Gen. Genet. 293 278–288 Occurrence Handle10.1007/s004380050323
I. Golubovskaya N. Avalkina W.F. Sheridan (1997) ArticleTitleNew insights into the role of the maize ameiotic1 locus Genetics 147 1339–1350 Occurrence Handle9383075 Occurrence Handle1:STN:280:DyaK1c%2FktlChsQ%3D%3D
T. Hirano (2002) ArticleTitleThe ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair Genes Dev. 16 399–414 Occurrence Handle11850403 Occurrence Handle1:CAS:528:DC%2BD38XhvFKgs74%3D Occurrence Handle10.1101/gad.955102
T. Hirano R. Kobayashi M. Hirano (1997) ArticleTitleCondensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein Cell 89 511–521 Occurrence Handle9160743 Occurrence Handle1:CAS:528:DyaK2sXjsVShsb4%3D Occurrence Handle10.1016/S0092-8674(00)80233-0
C.J. Jiang K. Shoji R. Matsuki A. Baba N. Inagaki H. Ban T. Iwasaki N. Imamoto Y. Yoneda X.W. Deng N. Yamamoto (2001) ArticleTitleMolecular cloning of a␣novel importin alpha homologue from rice, by which constitutive photomorphogenic 1 (COP1) nuclear localization signal (NLS)-protein is preferentially nuclear imported J. Biol. Chem. 276 9322–9329 Occurrence Handle11124253 Occurrence Handle1:CAS:528:DC%2BD3MXisVCms7g%3D Occurrence Handle10.1074/jbc.M006430200
S.A. Johnston T.P.M. Nijs Particleden S.J. Peloquin J.R.E. Hanneman (1980) ArticleTitleThe significance of genic balance to endosperm development in interspecific crosses Theor. Appl. Genet. 57 5–9
S.A. Johnston R.E. Hanneman (1982) ArticleTitleManipulations of endosperm balance number overcome crossing barriers between diploid Solanum species Science 217 446–448
R.A. Jorgensen P.D. Cluster J. English Q. Que C.A. Napoli (1996) ArticleTitle Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single-copy vs. complex T-DNA sequences Plant Mol. Biol. 31 957–973 Occurrence Handle8843939 Occurrence Handle1:CAS:528:DyaK28XmtFGju7c%3D Occurrence Handle10.1007/BF00040715
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 Handle12368491 Occurrence Handle1:CAS:528:DC%2BD38XotFels7o%3D Occurrence Handle10.1105/tpc.003061
K. Kimura T. Hirano (2000) ArticleTitleDual roles of the 11S regulatory subcomplex in condensin functions Proc. Natl. Acad. Sci. USA 97 11972–11977 Occurrence Handle11027308 Occurrence Handle1:CAS:528:DC%2BD3cXnvVSgtrw%3D Occurrence Handle10.1073/pnas.220326097
A. Kobayashi A. Sakamoto K. Kubo Z. Rybka Y. Kanno H. Takatsuji (1998) ArticleTitleSeven zinc-finger transcription factors are expressed sequentially during the development of anthers in petunia Plant J. 13 571–576 Occurrence Handle9680999 Occurrence Handle1:CAS:528:DyaK1cXitFyrs7k%3D Occurrence Handle10.1046/j.1365-313X.1998.00043.x
K. Kubo Y. Kanno T. Nishino H. Takatsuji (2000) ArticleTitleZinc-finger genes that specifically express in pistil secretory tissues of petunia Plant Cell Physiol. 41 377–382 Occurrence Handle10805603 Occurrence Handle1:CAS:528:DC%2BD3cXitFegtbo%3D
J. Logemann J. Schell L. Willmitzer (1987) ArticleTitleImproved method for the isolation of RNA from plant tissues Anal. Biochem. 163 16–20 Occurrence Handle2441623 Occurrence Handle1:CAS:528:DyaL2sXktlKitr0%3D Occurrence Handle10.1016/0003-2697(87)90086-8
J.P. Mackay M. Crossley (1998) ArticleTitleZinc fingers are sticking together Trends Biochem. Sci. 23 1–4 Occurrence Handle9478126 Occurrence Handle1:CAS:528:DyaK1cXptFOksQ%3D%3D Occurrence Handle10.1016/S0968-0004(97)01168-7
R. Mercier S.J. Armstrong C. Horlow N.P. Jackson C.A. Makaroff D. Vezon G. Pelletier G.H. Jones F.C. Franklin (2003) ArticleTitleThe meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis Development 130 3309–3318 Occurrence Handle12783800 Occurrence Handle1:CAS:528:DC%2BD3sXlvF2gtbo%3D Occurrence Handle10.1242/dev.00550
R. Mercier D. Vezon E. Bullier J.C. Motamayor A. Sellier F. Lefevre G. Pelletier C. Horlow (2001) ArticleTitleSWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis Genes Dev. 15 1859–1871 Occurrence Handle11459834 Occurrence Handle1:CAS:528:DC%2BD3MXlsFanu7Y%3D Occurrence Handle10.1101/gad.203201
A.P. Mitchell S.E. Driscoll H.E. Smith (1990) ArticleTitlePositive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae Mol. Cell. Biol. 10 2104–2110 Occurrence Handle2183020 Occurrence Handle1:CAS:528:DyaK3cXktlGltbc%3D
M. Otegui L.A. Staehelin (2000) ArticleTitleCytokinesis in flowering plants: more than one way to divide a cell Curr. Opin. Plant Biol. 3 493–502 Occurrence Handle11074381 Occurrence Handle1:CAS:528:DC%2BD3cXovVShsrw%3D Occurrence Handle10.1016/S1369-5266(00)00119-9
S.L. Page R.S. Hawley (2003) ArticleTitleChromosome choreography: the meiotic ballet Science 301 785–789 Occurrence Handle12907787 Occurrence Handle1:CAS:528:DC%2BD3sXmtVGqsLo%3D Occurrence Handle10.1126/science.1086605
K.J. Ross P. Fransz G.H. Jones (1996) ArticleTitleA light microscopic atlas of meiosis in Arabidopsis thaliana Chromosome Res. 4 507–516 Occurrence Handle8939362 Occurrence Handle1:CAS:528:DyaK28XntlSktrw%3D Occurrence Handle10.1007/BF02261778
S.E. Ruzin (1999) Plant Microtechnique and Microscopy Oxford University Press New York
R.J. Scott M. Spielman J. Bailey H.G. Dickinson (1998) ArticleTitleParent-of-origin effects on seed development in Arabidopsis thaliana Development 125 3329–3341 Occurrence Handle9693137 Occurrence Handle1:CAS:528:DyaK1cXmtlyhsLo%3D
N.U. Siddiqui P.E. Stronghill R.E. Dengler C.A. Hasenkampf C.D. Riggs (2003) ArticleTitleMutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis Development 130 3283–3295 Occurrence Handle12783798 Occurrence Handle1:CAS:528:DC%2BD3sXlvF2gtbw%3D Occurrence Handle10.1242/dev.00542
H. Stieglitz (1977) ArticleTitleRole of beta-1,3-glucanase in postmeiotic microspore release Dev. Biol. 57 87–97 Occurrence Handle863114 Occurrence Handle1:CAS:528:DyaE2sXhvVKitrg%3D Occurrence Handle10.1016/0012-1606(77)90356-6
H. Takatsuji (1999) ArticleTitleZinc-finger proteins: the classical zinc finger emerges in contemporary plant science Plant Mol. Biol. 39 1073–1078 Occurrence Handle10380795 Occurrence Handle1:CAS:528:DyaK1MXktFCgu7w%3D Occurrence Handle10.1023/A:1006184519697
H. Takatsuji N. Nakamura Y. Katsumoto (1994) ArticleTitleA new family of zinc finger proteins in Petunia: structure, DNA sequence recognition, and floral organ-specific expression Plant Cell 6 947–958 Occurrence Handle8069106 Occurrence Handle1:CAS:528:DyaK2MXjtFOrtw%3D%3D Occurrence Handle10.1105/tpc.6.7.947
F.A. Engelen Particlevan J.W. Molthoff A.J. Conner J.P. Nap A. Pereira W.J. Stiekema (1995) ArticleTitlepBINPLUS: an improved plant transformation vector based on pBIN19 Transgenic Res. 4 288–290 Occurrence Handle7655517 Occurrence Handle10.1007/BF01969123
W.C. Yang V. Sundaresan (2000) ArticleTitleGenetics of gametophyte biogenesis in Arabidopsis Curr. Opin. Plant Biol. 3 53–57 Occurrence Handle10679449 Occurrence Handle1:CAS:528:DC%2BD3cXhs1artLY%3D Occurrence Handle10.1016/S1369-5266(99)00037-0
S.-L. Yang L.-F. Xie H.-Z. Mao C.S. Puah W.-C. Yang L. Jiang V. Sundaresan D. Ye (2003) ArticleTitle TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther Plant Cell 15 2792–2804 Occurrence Handle14615601 Occurrence Handle1:CAS:528:DC%2BD2cXhtVSitw%3D%3D Occurrence Handle10.1105/tpc.016618
W.C. Yang D. Ye J. Xu V. Sundaresan (1999) ArticleTitleThe SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein Genes Dev. 13 2108–2117 Occurrence Handle10465788 Occurrence Handle1:CAS:528:DyaK1MXmtValsb8%3D
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 Genes Dev. 16 2021–2031 Occurrence Handle12154130 Occurrence Handle1:CAS:528:DC%2BD38XmtFaksro%3D Occurrence Handle10.1101/gad.997902
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kapoor, S., Takatsuji, H. Silencing of an Anther-specific Zinc-finger Gene, MEZ1, Causes Aberrant Meiosis and Pollen Abortion in Petunia. Plant Mol Biol 61, 415–430 (2006). https://doi.org/10.1007/s11103-006-0020-0
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11103-006-0020-0