See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/11158717

Cell Cycle Regulation in Plants

Article in Plant Physiology · December 1994

DOI: 10.1104/pp.106.3.823 · Source: PubMed

CITATIONS READS

63 1,041

1 author:

Peter Doerner
The University of Edinburgh
94 PUBLICATIONS 7,802 CITATIONS

SEE PROFILE

All content following this page was uploaded by Peter Doerner on 30 May 2014.

The user has requested enhancement of the downloaded file.

Plant Physiol. (1994)106:823-827

Cell Cycle Regulation in Plants

Peter W. Doerner*
Plant Biology Laboratory’, The Salk lnstitute for Biological Studies, 10100 North Torrey Pines Road,
La Jolla, California 92037

Cell division plays a crucial role during a11 phases of plant neither protein alone, has protein kinase activity. Stepwise
development. Continuing organogenesis and plastic growth changes of its activity and substrate specificity regulate pro-
responses to a changing environment require precise spatial, gression through the cycle. To ensure that the reactions
temporal, and developmental regulation of cell division activ- controlled by the engine are camed out to completion with
ity in meristems. The molecular analysis of cell division and sufficient accuracy and in the proper order, its activity is
its regulation in plants lags far behind such studies in yeast feedback regulated at checkpoints (Hartwell and Weinert,
and animals. Since the cell theory was proposed by Schleiden 1989). At such checkpoints its kinase activity becomes limit-
and Schwann in 1838, many approaches have been taken to ing for further progress until the feedback control network
elucidate how cells divide, but insight into the molecular signals the completion of the dependent reactions, which
basis of division control developed only after the genetic then activates the kinase for passage through to the next
analysis of cell division was initiated in yeast 25 years ago checkpoint. These quanta1 changes of activity are mechanist-
(Hartwell et al., 1970). Cell division cycle mutants in the ically regulated by reversible phosphorylation of the engine
yeasts Schizosaccharomyces pombe and Saccharomyces cerevis- components, by changes in subcellular localization of
iae continue to provide a conceptual framework for analyzing the complex, and by the rates of synthesis of liiting
gene interactions controlling the cellular processes leading to components.
division. The convergence of genetic, biochemical, and mo-
lecular lines of inquiry during the last decade has shown that CDKs
key cell-cycle regulators are universally conserved and has
triggered the explosive growth of the field. The proteins encoded by the S. cerevisiae CDC28 and the
The complex network controlling growth in eukaryotes is S. pombe cdc2+ genes are the prototypic CDKs required at
hierarchically organized (Fig. 1). Regulatory pathways that both the GI/S and the G2/M transitions. In animals, CDKl
communicate environmental constraints, such as nutrient (=cdc2) is essential for the G2/M transition, whereas CDK2
availability, signals such as growth factors or hormones, as and CDK3 are required for the Gl/S transition (Heuvel and
well as developmental cues control when and in which cells Harlow, 1993). These three CDKs share a short amino acid
division occurs. In animals, genes such as ras and p53 are sequence, PSTAIRE. Severa1 related kinases with homology
players in these pathways that activate the cell-cycle engine. but incomplete sequence identity to the PSTAIRE domain
This engine coordinates the various biochemical processes have been identified (Meyerson et al., 1992). Notwithstand-
required for division. Although much is known about the ing a function for CDKs in other processes not directly
biochemistry of these events, e.g. DNA synthesis, in most involved in cell-cycle regulation (Kaffman et al., 1994), one
cases the question of how these metabolic pathways are explanation for the evolution of the extensive CDK gene
activated remains unanswered. Cell-cycle regulation in ani- family in metazoans is increased opportunities for cell-cycle
mals and yeast has been extensively reviewed (Nurse, 1990; regulation during development.
Forsburg and Nurse, 1991; Murray, 1992; Norbury and
Nurse, 1992). This update will introduce the components of CY CLlNS
the eukaryotic cell-cycle machinery and their regulation, and
then focus on progress in molecular dissection of cell-cycle Cyclins were first identified in marine invertebrates as
regulation in plants. proteins whose levels oscillated during the cell cycle and that,
when injected into frog oocytes, could induce meiosis. The
observation that the S. pombe cdcl3 gene, which encodes a
THE CELL-CYCLE ENCINE AND ITS CONTROL cyclin, genetically interacts with cdc2 established a tight func-
In a11 eukaryotes, the biochemical machine that controls tional link between the components of the cell-cycle engine.
progress through the cell cycle consists of a catalytic protein Since then, an increasing number of cyclins have been iden-
kinase and an activating cyclin subunit. This complex, but tified in a11 eukaryotes studied (Lew and Reed, 1992). In S.
cerevisiae, three cyclins (CLNI, CLNZ, and CLN3) are ex-
The Plant Biology Laboratory is supported by a grant from the pressed and presumably function in G1, two are expressed in
Samuel Roberts Noble Foundation.
* Fax 1-619-558-6379. Abbreviation: CDK, cyclin-dependent kinase.
823
824 Doerner Plant Physiol. Vol. 106, 1994

signaling growth putative cell-cycle regulators has not yet been examined in
pathways factors
that control planta. Therefore, at present it is unknown wh.it function
cell division -/7 any of the genes described below has during plarit cell-cycle
progression.

PLANT CDKs
Putative CDK homologs have been cloned from pea (Feiler
and Jacobs, 1990), alfalfa (Hirt et al., 1991), maize (Colasanti
et al., 1991), Arabidopsis (Ferreira et al., 1991; Hirayama et
al., 1991), soybean (Miao et al., 1993), and rice 1:Hashimoto
et al., 1992). More than one gene was cloned from each of
these plants and expressed in cdc2 or cdc28 conclitional mu-
tants to examine whether it could rescue these yeitst mutants.
One alfalfa gene, cdc2MsA, passed this test. A scxond hom-
olog, cdcZMsB, rescued only a S. cerevisiae cdc28 mutant that
arrests at the GI/S transition (Hirt et al., 1993). It is not
apparent what the molecular basis for this is, bxause con-
served amino acid motifs, including the PSTAIRE domain,
are present in the cdc2MsB gene. Although botli rice genes
Figure 1. The eukaryotic cell cycle is divided into four phases: GI, preserve the PSTAIRE motif, only one was able to rescue a
during which the cell grows; S, during which the nuclear genetic cdc28 allele that arrests at the G1/S transition (Hashimoto et
information is replicated; C2,when further growth in preparation al., 1992). Only one maize gene was tested, which was able
for division occurs; and M, in which the cellular contents are to complement a cdc28 mutation (Colasanti et al. 1991). The
partitioned between two daughter cells. In animals and yeast, two maize genes differ by seven amino acids, none of which
signaling pathways that control cell division, key players of which represents a highly conserved residue. Both soybean genes
include ras, mitogen-activated protein kinases, and p53, function were able to rescue a cdc28 mutant (Miao et al., 1993). Only
in G, to activate C1cyclins. Many of these crucial molecules have one Arabidopsis gene, A t c d c M , was able to rescue a cdc28
not yet been identified in plants. In animals, these G, cyclins mutant, but in the second gene, AtcdcZB, the hallmark
associate with CDK2 and CDK3. This results in a transient, rapid
PSTAIRE motif occurred as PPTALRE (Imajuku c?tal., 1992).
increase in protein kinase activity, indicated here by the width of
the shaded area, which propels the cell through the START point Likewise, in one of the PCR products amplified from pea,
and commits the cell to division. C1 cyclins are then inactivated this motif appeared as PITAIRE (Feiler and Jacobs, 1991).
but other cyclins, first A and then 6,take over the role of activating Similar variations were observed in animal proíeins related
CDKs. After completion of D N A synthesis in plants, the transient to the cdc2 kinase (Meyerson et al., 1992).
formation of a preprophase band is observed, which anticipates the These results suggest that at least some of thesc plant genes
position of the future cell wall. The cell cycle arrests at t h e G2/M can function as CDKs. However, it is not clear why severa1
boundary due to limiting kinase activity of the cdc2/cyclin B com- cdc2-related genes with conserved PSTAIRE inotifs were
plex. After the feedback control system, which monitors cell divi- unable to rescue yeast mutants. The recent disowery that a
sion, signals the faithful completion of GZ biosynthetic reactions,
cyclin-CDK complex in yeast, PH080-PHO85, functions in a
this complex is activated to initiate t h e visible cellular events ulti-
mately leading to cytokinesis. The duration of cell-cycle phases is regulatory pathway other than the control of cmel division,
not drawn to scale. yet P H 0 8 5 contains a bona fide PSTAIRE motif (Kaffman et
al., 1994), highlights the necessity of establishin4 the role of
the above-mentioned genes during cell division in plants.
S phase (CLBS and CLB6), and four are expressed in mitosis
(CLBI, CLB2, CLB3, and CLB4). In animals, the C-, D-, and E- PLANT CYCLINS
class cyclins are expressed in G1, cyclin A is expressed in the
S and Gz phases, and the B cyclins are expressed in the Gz Putative cyclins have been cloned from carrot, soybean,
and early M phases. In most cells, the decision of whether to alfalfa, and Arabidopsis (Hata et al., 1991; Heinerly et al.,
commit to division is made during G1, and this was recently 1992; Hirt et al., 1992). The soybean and Arabidopsis gene
shown to be mediated by G1 cyclins (Quelle et al., 1993). It products promote nuclear envelope breakdow n when the
is not understood how cyclins activate CDKs mechanistically. corresponding mRNAs are injected into X e n o , m oocytes,
Cyclins are involved in determining the substrate specificity indicating their functionality as mitotic cyclins. All plant
of CDKs (Peeper et al., 1993) as well in targeting CDK activity cyclins described to date share homology to both A- and B-
to specific subcellular compartments during the cell cycle type cyclins within the cyclin box, an approximately 120-
(Pines and Hunter, 1991). amino acid domain thought to mediate the protein-protein
interaction with CDKs. It is unclear whether these plant
cyclins play roles during the S phase, as reported for animal
CELL DlVlSlON IN PLANTS
A-type cyclins, as well as during the GZ and b A phases, as
Plant genes homologous to components of the cell-cycle shown for B-type cyclins. A-type cyclins have been found
engine have been cloned recently, but the function of these only in animals. Therefore, plant AB-cyclins niay be early
 Cell Cycle Regulation in Plants 825

members of an evolutionarily more divergent cyclin gene iae. The specialized kinases and phosphatases responsible for
family. No G1 cyclin has yet been reported from plants. these modifications in animals and yeast have not yet been
detected in plants. Recently, severa1 homologs of mitogen-
RECULATION OF CELL DlVlSlON IN PLANTS activated protein kinases were cloned from alfalfa, pea, and
Arabidopsis (Duerr et al., 1993; Jonak et al., 1993; Mizoguchi
It is a safe assumption that the regulatory pathways that et al., 1994). Mitogen-activated protein kinases function in
control meristem function ultimately target components of growth-factor signal transduction upstream of the cell-cycle
the crll-cycle engine. Therefore, the dissection of cell-cycle engine during G1, as well as downstream of it, in the M
regulation in meristems was initiated with the analysis of the phase, to phosphorylate microtubule-associatedproteins. Ar-
accumulation of cell-cycle engine components during devel- abidopsis mitogen-activated protein kinase is activated in
opment and changes thereof by environmental and hormonal extracts from auxin-treated plants, suggesting that this class
signals. The expression of cdc2 homologs is higher in mitot- of kinase transduces mitogenic signals in plants.
ically active tissues, such as floral buds, and low or unde- Several aspects of cell division are unique to plants, but
tectable in mature, nonproliferating organs, such as leaves arguably the most important of these is how the plant deals
(Colasanti et al., 1991; Ferreira et al., 1991; Hirt et al., 1991; with the constraints on morphogenesis imposed by the rigid
Hashimoto et al., 1992; Mia0 et al., 1993). This analysis was cell wall. The rates and planes of cell division in a11 meristem
taken to the cellular leve1 in Arabidopsis (Martinezet al., 1992; cell layers are exquisitely coordinated to enable organogen-
Hemerly et al., 1993). Atcdc2A expression in a11 mitotically esis. The signals and mechanisms by which the spatial coor-
active meristems, but also in nonproliferating tissues such as dinates of a cell’s environment and its developmental com-
the pericycle, from which lateral roots originate, or vascular petence are translated into the selection of the correct plane
cells responsible for secondary growth, indicates that cdc2 of division are unknown at present. The earliest cytological
expression is a marker for the developmental competence to indication of the position of the future cell wall appears
divide. When roots are treated with auxin, which stimulates transiently during late interphase with the preprophase band,
cell division in a subset of pericycle cells that subsequently a dense ring of cortical microtubules. A ~34‘~‘’ gene product
form lateral roots, normalized cdc2 mRNA levels in Arabidop- associates with the preprophase band in maize and onion,
sis do not increase, suggesting that RNA levels of the Atcdc2A suggesting one interface where the cell-cycle engine and the
kinase subunit of tlie cell-cycle engine are not limiting for pathways specifying the spatial execution of cytokinesis in-
meristem activity in this tissue. The developmental compe- teract (Mineyuki et al., 1991; Colasanti et al., 1993). An
tente for division is not to be confused with totipotency, exciting possibility is that a specific cyclin recruits p34 to the
which is not developmentally programmed but is rather the preprophase band.
capacity to reenter a proliferative state under artificial circum-
stances. CENETIC APPROACHES TO DISSECT
Whereas cdc2 mRNA expression correlates with the com- CROWTH CONTROL
petence to divide, AB-type mitotic cyclin mRNA accumulates
only in actively dividing cells. AB-type cyclin mRNA is The paucity of conditional mutants makes genetic analysis
expressed only in those cells of the floral meristem in Antir- of essential cell-cycle engine components in plants less fea-
rhinum that are approaching mitosis, but is not observed in sible than in yeast, but a wealth of developmental and signal-
nonproliferating tissue (Fobert et al., 1994). However, accu- transduction mutants, here restricted to a few from Arubidop-
mulation of cyclin RNA only during this cell-cycle phase does sis, affected in the control of cell division remains to be
not indicate that its abundance controls commitment to a exploited. Collectively, these mutants define the network of
new round of cell division, at least in the floral meristem, functions that, directly or indirectly, control cell-cycle engine
because this decision is made much earlier in the cycle, in activity. Altematively, their gene products could be substrates
G1.The temporal pattem of AB-type cyclin expression in of the cell-cycle kinase differentially expressed during
plants parallels earlier observations of periodic cyclin accu- development.
mulation (Evans et al., 1983). In animals and yeast, the Several mutations identify genes that function as negative
observation of feed-forward and feed-back regulation of regulators of cell division activity. For example, cell division
cyclin expression by cyclins has led to a model in which in apical meristems does not arrest in the dark, as it does in
successive cyclin oscillations “help the cell cycle clock tick” the wild type, after germination of de-etiolated (Chory et al.,
(Amon et al., 1993; Edgar et al., 1994). This indicates that 1989) and constitutiue photomorphogenic mutant seedlings
cyclin abundance limits progression in many types of cell (Deng et al., 1991). Vegetative, inflorescence, and floral mer-
cycle and that therefore control of cyclin expression is critica1 istems are enlarged in the clauutal mutant due to increased
for the activation of the cell-cycle engine. cell numbers (Clark et al., 1993). In addition to other phe-
Regulation of the cell-cycle engine at other levels, such as notypic changes, the loss of agamous function, a floral hom-
by phosphorylation or differential subcellular localization, eotic gene, results in indeterminate growth of the inner floral
has not yet been reported in plants. The amino acid residues whorl (Bowman et al., 1989). Three other mutants define
that are phosphorylated in yeast or animal CDKs are con- pathways involved in cytokinesis. In gnom, the asymmetry of
served in a11 cloned plant cdc2 homologs. Phosphorylation the first zygotic division is affected in such a way that the
of Thr16’is essential for the activation of ~34‘~‘’in yeast and apical and basal daughter cells appear equal in size (Mayer
animals, and Tyr phosphorylation of Tyr” is inhibitory for et al., 1993). The lesion in monopteros becomes apparent at
kinase activity in S. pombe and humans, but not in S. cereuis- the octant stage of embryonic development, at which time
826 Doerner Plant Physiol. Vol. 106, 1994

stereotypic divisions in the wild type that generate the cells Ferreira PCG, Hemerly AS, Villarroel R, Van Montagu M, Inze
D (1991) The Arabidopsis functional homolog of the ~ 3 4 ' " protein
~
that organize into the embryonic root do not occur (Berleth kinase. Plant C e l l 3 531-540
and Jiirgens, 1993). The short-root mutant (Benfey et al., Fobert PR, Coen ES, Murphy GJP, Doonan JH (1994) Pattems of
1993) lacks a formative cell division that leads to the loss of cell division revealed by transcriptional regulation of genes during
the endodermal cell layer in the root. the cell cycle in plants. EMBO J 1 3 616-624
Forsburg SL, Nurse P (1991) Cell cycle regulation in the yeasts
Saccharomyces cerevisiae and Schizosaccharomyces pom be. Annu Rev
PERSPECTIVES Cell Biol7: 227-256
Hartwell LH, Culotti J, Reid B (1970) Genetic control cf cell division
In the next few years genetic analysis of a11 aspects of cell- in yeast. I. Detection of mutants. Proc Natl Acad Sci USA 66:
cycle control in plants, the network controlling the activity 352-359
of the cell division machinery, the cell-cycle engine itself, as Hartwell LH, Weinert TA (1989) Checkpoints: controls that ensure
well as the cellular functions controlled by it, will reveal the the order of cell cycle events. Science 246 629-634
Hashimoto J, Hirabayashi T, Hayano Y, Hata S,Ohashi Y, Suzuka
causal relationships goveming growth. Complementing mo- I, Utsugi T,Toh-E A, Kikuchi Y (1992) Isolation and character-
lecular, biochemical, and cytological analysis will begin to ization of cDNA clones encoding cdc2 homologues from Oryza
reveal the mechanisms, both general and species-specific, of sativa: a functional homologue and cognate variants. MOI Gen
cell division control in plants. Genet 233 10-16
Hata S, Kouchi H, Suzuka I, Ishii T (1991) lsolation 2nd character-
ization of cDNA clones for plant cyclins. EMBO J 10: 2681-2688
ACKNOWLEDCMENTS Hemerly A, Bergouniow C, Van Montagu M, Inze D, Ferreira P
I thank A. Colon, J. Reed, and V. Vitart for reading the manuscript. (1992) Genes regulating the plant cell cycle: isolatioii of a mitotic-
like cyclin from Arabidopsis thaliana. Proc Natl Aca(l Sci USA 8 9
3295-3299
Received May 2, 1994; accepted June 28, 1994. Hemerly AS, Ferreira P, Engler JDA, Montagu MV, Engler G,
Copyright Clearance Center: 0032-0889/94/106/0823/05. Inze D (1993) cdc2A expression in Arabidopsis h j linked with
competence for cell division. Plant Cell 5 1711-1723
Heuvel SVD, Harlow E (1993) Distinct roles for cyclin-dependent
kinases in cell cycle control. Science 262 2050-2054
LITERATURE ClTED Hirayama T, Imajuku Y, Anai T, Matsui M, Oka A (1991) Identi-
Amon A, Tyers M, Futcher B, Nasmyth K (1993) Mechanisms that fication of two cell cycle controlling cdc2 gene homologs in Arabi-
help the yeast cell cycle clock tick: G2 cyclins transcriptionally dopsis thaliana. Gene 105 159-165
activate G2 cyclins and repress G1 cyclins. Cell74 993-1007 Hirt H, Mink M, Pfosser M, Bogre L, Gyorgyey J, Jonak C, Gartner
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser M-T, A, Dudits D, Heberle-Bors E (1992) Alfalfa cychis: differential
Aeschbacher RA (1993) Root development in Arabidopsis: four expression during the cell cycle and in plant organ:;. Plant Cell 4
mutants with dramatically altered root morphogenesis. Develop- 1531-1538
ment 119 57-70 Hirt H, Pay A, Bogre L, Meskiene I, Heberle-Bors E (1993) cdcMsB,
Berleth T, Jiirgens G (1993) The role of the monopteros gene in a cognate cdc2 gene from alfalfa, complements the Gl/S but not
organisiig the basal body region of the Arabidopsis embryo. De- the G2/M transition of budding yeast cdc28 mutants. Plant J 4
velopment 118: 575-587 61-69
Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing Hirt H, Pay A, Gyorgyey J, BadÓ L, Mémeth K, Bogri! L, Schweyen
flower development in Arabidopsis. Plant Cell 1: 37-52 RJ, Heberle-Bors E, Dudits D (1991) Complement2:tionof a yeast
Chory J, Peto C, Feinbaum R, Pratt L, Ausubel F (1989)Arabidopsis ceI1 cycle mutant by an alfalfa cDNA encoding a protein kinase
thaliana mutant that develops as a light-grown plant in the absence homologous to p34'd'Z. Proc Natl Acad Sci USA 88: 1636-1640
of light. Cell58: 991-999 Imajuku Y, Hirayama T, Endoh H, Oka A (199:!) Exon-intron
Clark SE, Running MP, Meyerowitz EM (1993) CLAVATAI, a organization of the Arabidopsis thaliana protein kinase genes CDC2a
regulator of meristem and flower development in Arabidopsis. and CDCZb. FEBS Lett 304 73-77
Development 119 397-418 Jonak C, Páy A, Bogre L, Hirt H, Heberle-Bors E ("3) The plant
Colasanti J, Cho S-O, Wick S, Sundaresan V (1993) Localization of homologue of MAP kinase is expressed in a cell qde-dependent
the functionalp34'd" homolog of maize in root tip and stomatal and organ-specific manner. Plant J 3 611-617
complex cells: association with the predicted division sites. Plant Kaffman A, Herskowitz I, Tjian R, O'Shea EK (1994) Phosphoryl-
C e l l 5 1101-1111 ation of the transcription factor PH04 by a cyclin-CDK complex,
Colasanti J, Tyers M, Sundaresan V (1991) Isolation and character- PHO8O-PH085. Science 263 1153-1156
ization of cDNA clones encoding a functionalp3PdC2homologue Lew DJ, Reed SI (1992) A proliferation of cyclins. Trends Cell Biol
from Zea mays. Proc Natl Acad Sci USA 8 8 3377-3381 2 77-81
Deng XW, Caspar T, Quail PH (1991) copl: a regulatory locus Martinez MC, J~rgensenJ-E, Lawton MA, Lamb CJ, Doerner PW
involved in light-controlled development and gene expression in (1992) Spatial pattem of cdc2 expression in relation to meristem
Arabidopsis. Genes Dev 5 1172-1182 activity and cell proliferation during plant developrnent. Proc Natl
Duerr 8, Gawienowski M, Ropp T, Jacobs T (1993) MsERKl: A Acad Sci USA 8 9 7360-7364
mitogen-activated protein kinase from a flowering plant. Plant Mayer U, Büttner G, Jürgens G (1993) Apical-basal pattem forma-
C e l l 5 87-96 tion in the Arabidopsis embryo: studies on the role of the gnom
Edgar BA, Sprenger F, Duronio RJ, Leopold P, OFarrell PH (1994) gene. Development 117: 149-162
Distinct molecular mechanisms regulate cell cycle timing at suc- Meyerson M, Enders GH, Wu C-L, Su L-K, Gorka C, Nelson C,
cessive stages of Drosophila embryogenesis. Genes Dev 8: 440-452 Harlow E,TsaiL-H (1992) A family of human cdc2-relatedprotein
Evans T, Rosenthal ET, Youngblom J, Diste1 D, Hunt T (1983) kinases. EMBO J 11: 2909-2917
Cyclin: a protein specified by matemal mRNA in sea urchin eggs Miao GH, Hong Z, Verma DP (1993) Two functional soybean genes
, that is destroyed at each cleavage division. Cell33 389-396 encoding ~ 3 4 ' ~protein
'~ kinases are regulated by different plant
Feiler HS, Jacobs TW (1990) Cell division in higher plants: A cdc2 developmental pathways. Proc Natl Acad Sci USA 9 0 943-947
gene, its 34-kDa product, and histone H1 kinase activity in pea. Mineyuki Y, Yamashita M, Nagahama Y (1991) ~34'~'' kinase
Proc Natl Acad Sci USA 87: 5397-5401 homologue in the preprophase band. Protoplasma 162: 182-186
Feiler HS, Jacobs TW (1991) Cloning of the pea cdc2 homologue by Mizoguchi T, Gotoh Y, Nishida E, Yamaguchi-Shinozaki K, Hay-
efficient immunological screening of PCR products. Plant Mo1 Biol ashida N, Iwasaki T, Kamada H, Shinozaki K (1!)94) Character-
17: 321-333 ization of two cDNAs that encode MAP kinase homologues in
 Cell Cycle Regulation in Plants 827

ashida N, Iwasaki T, Kamada H, Shinozaki K (1994) Character- Peeper DS, Parker LL, Ewen ME, Toebes M, Hall FL, Xu M,
ization of two cDNAs that encode MAP kinase homologues in Zantema A, van der Eb AJ, Piwnica-Worms H (1993) A- and B-
Arabidopsis thaliana and analysis of the possible role of auxin in type cyclins differentially modulate substrate specificity of cyclin-
activating such kinase activities in cultured cells. Plant J 5 cdk complexes. EMBO J 1 2 1947-1954
111-122 Pines J, Hunter T (1991) Human cyclins A and B1 are differentially
Murray AW (1992) Creative blocks: cell-cycle checkpoints and feed- located in the cell and undergo cell cycle-dependent nuclear trans-
back controls. Nature 359 599-604 port. J Cell Biol 115: 1-17
Norbury C, Nurse P (1992) Animal cell cycles and their control. Quelle DE, Ashmun RA, Shurtleff SA, Kato J-Y,Bar-Sagi D,
Annu Rev Biochem 61: 441-470 Roussel MF, Sherr CJ (1993) Overexpression of mouse D-type
Nurse P (1990) Universal control mechanism regulating onset of M- cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev 7:
phase. Nature 344 503-508 1559-1571

View publication stats