help button home button Genetics Proc NAS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Genetics, Vol. 177, 2547-2551, December 2007, Copyright © 2007
doi:10.1534/genetics.107.082446

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kim, J. C.
Right arrow Articles by Dellaporta, S. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kim, J. C.
Right arrow Articles by Dellaporta, S. L.

Cell Cycle Arrest of Stamen Initials in Maize Sex Determination

Jong Cheol Kim*,{dagger}, Hélène Laparra*,1, Alejandro Calderón-Urrea*,2, John P. Mottinger{ddagger}, Maria A. Moreno* and Stephen L. Dellaporta*,3

* Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520-8104, {dagger} Environmental Biotechnology National Core Research Center, Gyeongsang National University, Jinju, 660-701, Korea and {ddagger} Department of Cell and Molecular Biology, University of Rhode Island, Kingston, Rhode Island 02881

3 Corresponding author: Yale University, Department of Molecular, Cellular and Developmental Biology, P.O. Box 208104, New Haven, CT 06520-8104.
E-mail: stephen.dellaporta{at}yale.edu

Manuscript received October 11, 2007. Accepted for publication October 17, 2007.


   ABSTRACT
TOP
 ABSTRACT
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
The maize sex determination pathway results in the arrest of stamen in ear spikelets and the abortion of pistils in both the tassel spikelets and in the secondary florets of ear spikelets. Arrested stamen cells showed no signs of DNA fragmentation, an absence of CYCLIN B expression, and an accumulation of the negative cell cycle regulator WEE1 RNA.

MAIZE plants produce unisexual flowers, called florets in grasses, which are spatially separated, with staminate florets on the terminal inflorescence and pistillate florets on the axillary inflorescences (Figure 1). These florets are arranged in pairs (upper and lower) within a spikelet, the basic unit of grass inflorescence. Each floret is initially bisexual with three stamen initials and a central pistil. Unisexuality is achieved through the selective elimination of floral organs. All pistil primordia are eliminated in tassel spikelets resulting in exclusively paired staminate florets. In most lines of maize, one or more axillary inflorescences (ears) contain spikelets with one pistillate floret and a sterile secondary floret through the elimination of all stamen primordia and the pistils in the secondary florets.


Figure 1
View larger version (13K):
[in this window]
[in a new window]
[Download PPT slide]
  		FIGURE 1.— Sex determination pathway in maize. Maize floral diagrams showing an immature spikelet (left) with two perfect (bisexual) floral meristems, each with a central pistil initial ({circ}), three stamen initials (•), a palea (–), lemma (Figure 1 or Figure 1), and subtending glumes (Figure 1 or Figure 1); lodicules are not shown. The transition to paired staminate spikelets in the tassel (top right) and to solitary pistillate spikelets in the ear (bottom right) is depicted. Secondary pistils also abort in ear florets (indicated by asterisk). The tasselseed (ts) genes 1, 2, 3, and 5 are required for pistil abortion in the tassel and in the secondary ear florets. The dwarf (d) 1, 3, 5, and 8 and anther ear 1 (an1) genes are required for stamen arrest in ear spikelets and in ts2 mutant tassel spikelets. The silkless 1 (sk1) gene protects primary ear pistils from tasselseed-mediated cell death. The pistillate (pi1, pi2) genes are required for E2 pistil abortion.

 
Maize sex determination is under the control of cell death, cell protection, and phytohormone-mediated processes (reviewed by IRISH and NELSON 1989; DELLAPORTA and CALDERON-URREA 1995; IRISH 1996). Mutations that affect sex include the tasselseed 1 (ts1) and ts2 mutations, which cause the failure of primary and secondary tassel pistils to abort with the subsequent arrest of all tassel stamen primordia. The abortion of pistils in the secondary ear florets is also blocked in these mutants resulting in paired pistillate ear spikelets. The ts2 gene encodes a short-chain alcohol dehydrogenase/reductase (SDR) that is required for the abortion of pistil cells in both tassel spikelets and the secondary pistils of ear spikelets (DELONG et al. 1993). TS2 is also expressed in the functional primary pistils of the ear spikelets even though these pistils do not undergo tasselseed-mediated cell death. Primary ear pistils survive through the action of the silkless 1 (sk1) gene; mutations in sk1 block pistil survival causing these pistils to abort by a tasselseed-mediated cell death process (VEIT et al. 1991; IRISH and NELSON 1993; CALDERON-URREA and DELLAPORTA 1999).

We examined the process of the formation of pistillate florets in both wild-type and in ts2 mutant plants. The nuclear integrity in arresting stamen initials was examined by staining paraffin-embedded tissue sections with DAPI (Figure 2). At the organ level, stamen arrest was evidenced in wild-type ear florets by the lack of enlargement of stamen initials soon after the bisexual stage of floral development. In these growth-arrested stamens, cells continued to show nuclear integrity, as judged by DAPI staining (Figure 2A). As the primary pistils continued to mature, stamen initials showed no loss of nuclear integrity even at the stage where tasselseed-mediated cell death had eliminated E2 pistils (Figure 2B). Unlike pistil abortion in tassel and secondary ear florets (CHENG et al. 1983; CALDERON-URREA and DELLAPORTA 1999), nuclear degeneration is not an indication of the stamen arrest process in ear florets.


Figure 2
View larger version (75K):
[in this window]
[in a new window]
[Download PPT slide]
  		FIGURE 2.— Nuclear integrity in arrested stamen initials. Paraffin-embedded sections of wild-type ear spikelets were analyzed by DAPI staining. (A) Early unisexual stage of ear spikelet development showing developing upper (E1) pistils and arrested stamens with intact nuclei. Lower (E2) pistils have not yet undergone tasselseed-mediated cell death. (B) Later unisexual stage of ear spikelet development showing arrested upper (E1) stamens with intact nuclei and complete elimination of the lower pistil (red arrow). Arrested lower stamen initials also show intact nuclei. (C) In ts2 mutant tassel spikelets, developing pistil and arrested upper (T1) stamen initials show intact nuclei. Bars, 100 µm. Inflorescences were fixed in 4% formaldehyde, embedded in paraffin, and sections were prepared for in situ hybridizations essentially as described (JACKSON 1992) except that Hemo-De (Fisher Scientific) was substituted for Histo-Clear (National Diagnostics, Atlanta). Nuclear integrity assays were performed by incubation of tissue sections in a 0.3 mM solution of 4',6-diamidine-2'-phenylindole dihydrochloride (DAPI; Roche Applied Sciences) in PBS followed by several washes in PBS and mounting in 70% glycerol in 30% PBS.

 
Mutations in ts2 cause pistillate florets to form in tassels instead of staminate florets. We examined the arrested stamens in the tassels of ts2 mutant plants. As with wild-type florets, the ts2 florets were initially bisexual (not shown) followed soon afterward by the arrest of stamen initials and the subsequent maturation of the pistil (Figure 2C). In arrested stamens, nuclear integrity was again evident with no indication of nuclear degeneration, and only at very late stages of inflorescence development (>50 mm length) did any signs of a loss of nuclear integrity in arrested stamens become apparent (not shown). The process of stamen arrest in ts2 tassel florets therefore appears to be similar to that observed in wild-type ears, whereby an arrest of stamens occurs without a loss of nuclear integrity.

To further characterize the process of stamen arrest, we performed TdT-mediated dUTP-biotin nick end labeling (TUNEL) assays (GAVRIELI et al. 1992) to detect signs of nuclear DNA fragmentation. In tassel and ear inflorescences up to 25 mm in length (bisexual stage), no DNA fragmentation was detected in the floral primordia in either pistil or stamen primordia (Figure 3, A and G). At later stages (inflorescences 30–50 mm length) as florets become unisexual, arrested stamens in ear florets showed no TUNEL signal (Figure 3, B and C) indicating a lack of detectable DNA fragmentation. As a positive control, we examined the process of elimination of pistil initials in wild-type tassel florets. As previously shown, pistil cells undergo a process of subepidermal tasselseed-mediated cell death detected by rapid loss of nuclei integrity (CALDERON-URREA and DELLAPORTA 1999). In aborting pistils, subepidermal cells were clearly positive in TUNEL assays (Figure 3, H and I) indicating extensive DNA fragmentation. TUNEL signals preceded the complete loss of nuclear integrity as judged by propidium iodide staining. Stamen arrest therefore was not a direct consequence of DNA fragmentation or cell death, unlike the process of pistil cell death, which is accompanied by a rapid loss of nuclear integrity and DNA fragmentation.


Figure 3
View larger version (85K):
[in this window]
[in a new window]
[Download PPT slide]
  		FIGURE 3.— CYCLIN B1 expression and DNA fragmentation in floral organs. TUNEL assays (green fluorescent signal) on paraffin-embedded section of wild-type ear (A–C), wild-type tassel (G–I), and ts2 mutant tassel (M–O) florets and counterstained with propidium iodide (red fluorescent signal). In situ hybridization with CYCLIN B1 antisense probes to serial sections of wild-type ear (D–F), wild-type tassel (J–L) and ts2 mutant tassel (P–R) florets. Note the absence of TUNEL signals (B and C) in wild-type stamen initials also showing no CYCLIN B1 expression (E and F). TUNEL signal is seen in wild-type pistils undergoing tasselseed-mediated cell death (H and I). Bars, 100 µm. Total RNA from maize tissues was purified by the guanidine thiocyanate method (CHIRGWIN et al. 1979). First strand cDNA was synthesized using SuperScript II (GIBCO BRL) and an oligod(T) primer according to the manufacturer's instructions. The cDNA clones were obtained by PCR amplification of first strand cDNA using CYCLIN B1 primers (P917 5'-CCTGGACTCTGAGAACAGCCTACCA-3' and P918 5'-CCGACTCTGAGAACAGCCTAGCAAA-3'). PCR amplification was performed using the expand long template PCR system (Boehringer Mannheim) using the manufacturer's instructions under the following cycling conditions: 94° for 2 min, then 10 cycles at 94° for 10 sec, 65° for 30 sec, and 68° for 2 min, followed by an additional 20 cycles of PCR at 94° for 10 sec, 65° for 30 sec, 68° for 2 min. Amplification products were cloned into the vector pCRII (Invitrogen), and sequenced to confirm their identity. For in situ riboprobes, plasmid DNA was linearized at a restriction site flanking the cDNA inserts by digestion with an appropriate enzyme that generates a 5' overhang. Linearized plasmid DNA was used as a template to synthesize digoxigenin-labeled RNA using T7 or T3 polymerase and 11-digoxigenin-dUTP according to manufacturer's instructions (Roche Diagnostics). The RNA probe was subject to mild alkaline hydrolysis for varying times in 0.1 N NaOH to yield products in the 100–200 nucleotide range. The final concentration of riboprobe was adjusted to 10 ng/µl/kb with overnight hybridization at 55°. Tissue fixation, nuclear staining, and sectioning were as described above (Figure 2). Washing and detection of RNA hybridization signals was as previously described (JACKSON 1992; CALDERON-URREA and DELLAPORTA 1999). TUNEL assay were performed on tissue sections using the DeadEnd Fluorometric TUNEL system according to manufacturer's instruction (Promega) followed by counterstaining in 10 µg/ml propidium iodide in PBS, several washes in PBS, and mounting in 70% glycerol in 30% PBS. All sections were examined using a Zeiss Axiophot microscope with the appropriate excitation and emission filters for epifluorescence imaging.

 
Next, we examined the possibility that a block in stamen development was the result of cell cycle arrest. The cyclin B gene acts as a positive regulator in the G2/M phase of the cell cycle and its RNA is short-lived and present only in dividing cells in the G2/M transition (FOBERT et al. 1994). In situ RNA hybridization with the maize B-type cyclin gene (RENAUDIN et al. 1994) is shown in Figure 3. The cyclin B gene was highly expressed in a subset of cells in all floral organs in the early bisexual stage of inflorescence development, an indication of prevalent cell division in these tissues. As ear florets matured, CYCLIN B expression continued to be detected throughout a subset of cells in developing pistils, but CYCLIN B expression was undetectable in any cells of the stamens (Figure 3, E and F), consistent with a cessation of cell division and arrested development of these stamens. Moreover, the lack of CYCLIN B expression occurred at the time that nuclei integrity remained high as judged by propidium iodide staining (Figure 3, B and C).

Likewise, in the tassel inflorescence, CYCLIN B expression was seen in a subset of cells throughout the floral meristem during early development (Figure 3J) and at later stages in the developing stamens (Figure 3K) but was absent from aborting pistils of wild-type tassels (Figure 3L). In mutant ts2 tassels, CYCLIN B was detected at all stages examined in a subset of cells of pistils (Figure 3, P–R), but not at later stages in stamens (Figure 3, Q and R), a result consistent with the arrest and cessation of cell division in these organs. Taken together, the data on nuclear integrity, TUNEL assays, and CYCLIN B expression suggest that the process of stamen arrest involves a cell cycle block rather than a cell death mechanism characteristic of tasselseed-mediated pistil elimination.

To further investigate the status of the cell cycle in the arrest of stamens, we examined the expression of several cell cycle regulators, including several other cyclins (RENAUDIN et al. 1994; GUTIERREZ et al. 2005), retinoblastoma-related protein (GRAFI et al. 1996), cyclin-dependent kinase (CDK) (DE LA PAZ SANCHEZ et al. 2002; SANCHEZ MDE et al. 2005), the spindle checkpoint protein MAD2 (YU et al. 1999), CDK inhibitor (COELHO et al. 2005), and WEE1 (XIE et al. 1996; SUN et al. 1999) genes (data not shown). Interestingly, expression of a negative cell cycle regulator, WEE1, showed a striking accumulation of its RNA in arrested stamen cells but not in other floral organs, including dying pistils (Figure 4, A and C). The maize WEE1 mRNA was well expressed in the arrested stamens of both wild-type ear florets (Figure 4A) and in mutant ts2 tassel florets (Figure 4C). This period in which WEE1 RNA accumulation was observed coincided with the period in which CYCLIN B was absent in the cells of the arrested stamens (Figure 4, D and F). Although CYCLIN B expression was absent (Figure 4C), WEE1 RNA did not accumulate during pistil abortion in ear florets (Figure 4B). This result implicates a cell cycle block, possibly mediated by negative cell cycle regulator WEE1, in the process of arresting stamen cells but apparently not in the process of pistil abortion.


Figure 4
View larger version (86K):
[in this window]
[in a new window]
[Download PPT slide]
  		FIGURE 4.— WEE1 and CYCLIN B1 expression in floral organs. In situ hybridization of serial sections using WEE1 (A–C) and CYCLIN B1 (D–F) antisense probes of wild-type ear (A and D), wild-type tassel (B and E), and ts2 mutant tassel (C and F) florets. Note accumulation of WEE1 (A and C) and absence of CYCLIN B1 (D and F) RNA in arrested stamen initials in the ear floret (A and D) and ts2 mutant tassel floret (C and F). Bars, 100 µm. The WEE1 cDNA clones were obtained by PCR amplification of first strand cDNA using primers WEE1 primers (P904 5'-TCACGCTATATGCCTCCGGAAATG-3' and P920 5'-CGCTGCCCAAATGCAACTGATAAC-3'). PCR amplification, probe preparation and in situ hybridization were performed as described above (Figures 2 and 3).

 
Previous studies have shown that the elimination of pistils in tassel florets and secondary ear florets is a cell death process (CHENG et al. 1983; CALDERON-URREA and DELLAPORTA 1999). Pistil cell death is associated with subepidermal TS2 expression and nuclear degeneration shortly after florets reach a bisexual stage of development (DELONG et al. 1993; CALDERON-URREA and DELLAPORTA 1999). In contrast to this process, the failure of stamens to mature in pistillate florets does not coincide with any early indications of cell death with growth of initials arrested shortly after the bisexual floret stage (CHENG et al. 1983; DELONG et al. 1993; CALDERON-URREA and DELLAPORTA 1999). At this stage of floral development there are no indications of a loss of nuclear integrity in arrested stamen cells as judged by DAPI (Figure 2, A and B) or propidium iodide (Figure 3, A–C) staining. The earliest cellular indications of stamen arrest was the cessation of cell division, as determined by the absence of detectable expression of the G2/M regulator CYCLIN B in the arrested stamens of wild-type ear florets (Figure 3, E and F) and in arrested stamens in the ts2 mutant tassel florets (Figure 3, Q and R). A second indication of cell cycle arrest was the accumulation of the negative cell cycle regulator WEE1 RNA only seen in arrested ear stamens (Figure 4, A and C) and arrested ts2 tassel stamens (Figure 4C). In contrast, the pistil abortion process was not associated with WEE1 RNA accumulation (Figure 4B), although CYCLIN B RNA was also not detected in aborting pistils (Figure 3, K and L). In aborting pistils, however, both signs of nuclear degeneration (Figure 2C) and DNA fragmentation (Figure 3, H and I) were evident.

In eukaryotic cells, cyclin B regulates the transition to mitosis and its transcription is cell-cycle regulated, peaking at the G2 -> M transition and repressed in G1 (reviewed by DE VEYLDER et al. 2003; FUNG and POON 2005). WEE1 is a known to be a negative regulator of mitosis, inhibiting cyclin B/Cdc2 activity and the progression of cells from G2 -> M in the cell cycle (NURSE and THURIAUX 1980; RUSSELL and NURSE 1986). WEE1 encodes a Thr/Tyr protein kinase that inhibits CDKs by phosphorylation (MUELLER et al. 1995a,b; MURAKAMI and VANDE WOUDE 1998). In light of our results, including the lack of DNA fragmentation, the absence of CYCLIN B expression, and the accumulation of WEE1, our data point to a cell cycle arrest rather than a cell death mechanism that is responsible for the production of pistillate florets in the maize sex determination pathway.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
This work was supported by grants from the National Institutes of Health (NIH) (R01 GM-38148) to S.L.D., from the United States Department of Agriculture (9935301-8048) to J.P.M., and from the Korean Science and Engineering Foundation (KOSEF) to the Environmental Biotechnology National Core Research Center (R15-2003-012-01001-0). J.C.K. was supported from a postdoctoral fellowship from the KOSEF and from the NIH (R01 GM-38148).


   FOOTNOTES
 
1 Present address: Meristem Therapeutics, 8 rue des Frères Lumière, 63100 Clermont-Ferrand, France. Back

2 Present address: Department of Biology, California State University, Fresno, CA 93740. Back


   LITERATURE CITED
TOP
 ABSTRACT
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

CALDERON-URREA, A., and S. L. DELLAPORTA, 1999 Cell death and cell protection genes determine the fate of pistils in maize. Development 126: 435–441.[Abstract]

CHENG, P. C., R. I. GRYSON and D. B. WALDEN, 1983 Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am. J. Bot. 70: 450–462.[CrossRef]

CHIRGWIN, J. M., A. E. PRZBYLA, R. J. MACDONALD and W. J. RUTTER, 1979 Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294.[CrossRef][Medline]

COELHO, C. M., R. A. DANTE, P. A. SABELLI, Y. SUN, B. P. DILKES et al., 2005 Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiol. 138: 2323–2336.[Abstract/Free Full Text]

DE LA PAZ SANCHEZ, M., A. TORRES, M. B. BONIOTTI, C. GUTIERREZ and J. M. VAZQUEZ-RAMO, 2002 PCNA protein associates to Cdk-A type protein kinases in germinating maize. Plant Mol. Biol. 50: 167–175.[CrossRef][Medline]

DE VEYLDER, L., J. JOUBES and D. INZE, 2003 Plant cell cycle transitions. Curr. Opin. Plant Biol. 6: 536–543.[CrossRef][Medline]

DELLAPORTA, S. L., and A. CALDERON-URREA, 1995 The sex determination process in maize. Science 266: 1501–1505.[CrossRef]

DELONG, A., A. CALDERON-URREA and S. L. DELLAPORTA, 1993 Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74: 757–768.[CrossRef][Medline]

FOBERT, P. R., E. S. COEN, G. J. MURPHY and J. H. DOONAN, 1994 Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. EMBO J. 13: 616–624.[Medline]

FUNG, T. K., and R. Y. POON, 2005 A roller coaster ride with the mitotic cyclins. Semin. Cell Dev. Biol. 16: 335–342.[CrossRef][Medline]

GAVRIELI, Y., Y. SHERMAN and S. A. BEN-SASSON, 1992 Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell. Biol. 119: 493–501.[Abstract/Free Full Text]

GRAFI, G., R. J. BURNETT, T. HELENTJARIS, B. A. LARKINS, J. A. DECAPRIO et al., 1996 A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc. Natl. Acad. Sci. USA 93: 8962–8967.[Abstract/Free Full Text]

GUTIERREZ, R., F. QUIROZ-FIGUEROA and J. M. VAZQUEZ-RAMOS, 2005 Maize cyclin D2 expression, associated kinase activity and effect of phytohormones during germination. Plant Cell Physiol. 46: 166–173.[Abstract/Free Full Text]

IRISH, E., 1996 Regulation of sex determination in maize. BioEssays 18: 363–369.[CrossRef]

IRISH, E. E., and T. NELSON, 1989 Sex determination in monoecious and dioecious plants. Plant Cell 1: 737–744.[Free Full Text]

IRISH, E. E., and T. M. NELSON, 1993 Development of tasselseed2 inflorescences in maize. Am. J. Bot. 80: 292–299.[CrossRef]

JACKSON, D., 1992 In situ hybridization in plants, pp. 163–174 in Plant Molecular Pathology: A Practical Approach, edited by S. J. GURR, M. J. MCPHERSON and D. J. BOWLES. Oxford University Press, Oxford.

MUELLER, P. R., T. R. COLEMAN and W. G. DUNPHY, 1995a Cell cycle regulation of a Xenopus Wee1-like kinase. Mol. Biol. Cell 6: 119–134.[Abstract]

MUELLER, P. R., T. R. COLEMAN, A. KUMAGAI and W. G. DUNPHY, 1995b Myt1: a membrane-associated inhibitory kinase that phosphorylates Cdc2 on both threonine-14 and tyrosine-15. Science 270: 86–90.[Abstract/Free Full Text]

MURAKAMI, M. S., and G. F. VANDE WOUDE, 1998 Analysis of the early embryonic cell cycles of Xenopus; regulation of cell cycle length by Xe-wee1 and Mos. Development 125: 237–248.[Abstract]

NURSE, P., and P. THURIAUX, 1980 Regulatory genes controlling mitosis in the fission yeast Schizosaccharomyces pombe. Genetics 96: 627–637.[Abstract/Free Full Text]

RENAUDIN, J. P., J. COLASANTI, H. RIME, Z. YUAN and V. SUNDARESAN, 1994 Cloning of four cyclins from maize indicates that higher plants have three structurally distinct groups of mitotic cyclins. Proc. Natl. Acad. Sci. USA 91: 7375–7379.[Abstract/Free Full Text]

RUSSELL, P., and P. NURSE, 1986 cdc25+ functions as an inducer in the mitotic control of fission yeast. Cell 45: 145–153.[CrossRef][Medline]

SANCHEZ MDE, L., S. H. GURUSINGHE, K. J. BRADFORD and J. M. VAZQUEZ-RAMOS, 2005 Differential response of PCNA and Cdk-A proteins and associated kinase activities to benzyladenine and abscisic acid during maize seed germination. J. Exp. Bot. 56: 515–523.[Abstract/Free Full Text]

SUN, Y., B. P. DILKES, C. ZHANG, R. A. DANTE, N. P. CARNEIRO et al., 1999 Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc. Natl. Acad. Sci. USA 96: 4180–4185.[Abstract/Free Full Text]

VEIT, B., B. GREENE, B. LOWE, J. MATHERN, N. SINHA et al., 1991 Genetic approaches to inflorescence and leaf development in maize. Dev. Suppl. 1: 105–111.

XIE, Q., A. P. SANZ-BURGOS, G. J. HANNON and C. GUTIERREZ, 1996 Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 15: 4900–4908.[Medline]

YU, H. G., M. G. MUSZYNSKI and R. KELLY DAWE, 1999 The maize homologue of the cell cycle checkpoint protein MAD2 reveals kinetochore substructure and contrasting mitotic and meiotic localization patterns. J. Cell. Biol. 145: 425–435.[Abstract/Free Full Text]

Communicating editor: A. J. BIRCHLER





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Kim, J. C.
Right arrow Articles by Dellaporta, S. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Kim, J. C.
Right arrow Articles by Dellaporta, S. L.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Copyright © 2007 by the Genetics Society of America.