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Journal of Experimental Botany, Vol. 54, No. 385, pp. 1125±1126, April 2003
DOI: 10.1093/jxb/erg138
PLANT CULTURE: SEARCHING QUESTIONS
Why should we study the plant cell cycle?
Dirk InzeÂ1
Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, KL Ledeganckstraat 35, B-9000 Gent,
Belgium
Received 14 January 2003; Accepted 20 January 2003
ABSTRACT
Description of the molecular biology of plant and animal cell cycles highlights similarities and critical differences. The cell cycle is a point of control in both
growth and development and deepening understanding
of underlying processes and mechanisms may have
many practical applications.
Key words: Animal cell cycle, cell cycle genes, cell proliferation,
cell walls, development, growth, plant cell cycle.
Introduction
Ten years of molecular cell cycle research in plants has given a
picture of how plant cells divide that has still to be re®ned. Most
interesting was the discovery that many of the fundamental control
mechanisms that govern cell division in animals are also conserved
in higher plants. Like animals, plants use cyclin-dependent kinases
(CDKs), cyclins, CDK inhibitors, retinoblastoma, E2F/DP transcription factors, and WEE kinases to control the progression
through the various cell cycle phases (Stals and InzeÂ, 2001).
Whereas, in some cases, genes (such as those coding for the A-type
CDK, the docking factor CKS, and some cyclins) are functionally
interchangeable between organisms, in other cases the conservation
is more structural rather than functional. Examples of the latter are
the plant CDK inhibitors, now designated Kip-related proteins
(KRPs; De Veylder et al., 2001), which share very little sequence
homology with their mammalian counterparts, but nevertheless most
probably exert similar functions. What does all this mean? Can the
plant cell cycle teach anything about the animal cell cycle? How
crucial is the plant cell cycle as a point of control in plant
development? Below are listed a few thoughts that I feel are worthy
of consideration.
Cell walls
The rigid cell walls of plants prevent division by constriction,
therefore plants have developed an intriguing and novel mechanism
to construct new cell walls. Early in prophase, a microtubular array,
called the preprophase band, positions the future cell wall and,
during telophase, another microtubular array, the phragmoplast,
ensures the formation of the so-called cell plate that grows from the
centre of the cell toward the parental cell walls. Remarkably little is
1
known about the mechanisms that position new cell walls in plants,
and the molecular processes that lead to the formation of a
phragmoplast and cell plate are currently being discovered.
Because the process of cell wall formation in plants and animals is
so different, it is not surprising that, already, several new cell cycle
regulators without functional homologues in other organisms have
been detected in plants. A good example is the existence of a novel,
plant-speci®c class of CDKs that control the G2-to-M transition
(Porceddu et al., 2001; Sorrell et al., 2001).
Cell cycle genes
Since the entire genome sequence of Arabidopsis thaliana has
become available, it has become clear that the complement of cell
cycle genes is even more complex in plants than in mammals. For
instance, the number of CDKs, cyclins, and CDK inhibitors (KRPs)
exceed those found in humans (Vandepoele et al., 2002). One rather
attractive explanation for this remarkable observation is that this
high complexity re¯ects the plant's sessile lifestyle. Plants cannot
escape adverse conditions and are, therefore, well-adapted to adjust
their development in response to changing environmental conditions. Possibly, the high number of cell cycle genes allows ®netuning of development with the probable result that land plants are so
successful in colonizing different habitats. More and more data seem
to support this view. For example, several cyclins have been shown
to be differentially affected by plant growth regulators, such as
cytokinins, brassinosteroids, and sucrose (De Veylder et al., 1999;
Riou-Khamlichi et al., 2000). An alternative explanation for the
reduced number of cell cycle genes in mammals when compared to
that in plants is the frequent occurrence of splice variants in
mammalian genes, a process that has been rarely reported in plant
genes.
Cell proliferation
The amazingly long lifespan of some plant cells is possibly of far
reaching importance. Cells in the meristems of some trees continue,
year after year, to produce faithful copies of themselves, without the
appearance of cancerous growths. Some scientists will argue that
plants cannot form cancers because of the strictly rigid constraints of
the tissues in which the cells are embedded. However, many
proliferative diseases of plants, such as crown galls formed by
Agrobacterium tumefaciens, show that cancerous tissues can easily
proliferate. It will be of the utmost interest to understand how plant
cells avoid the cell cycle running out of control and this in the
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Journal of Experimental Botany, Vol. 54, No. 385, ã Society for Experimental Biology 2003; all rights reserved
1126
InzeÂ
absence of known anti-proliferative mechanisms, such as p53 in
animals. Obviously, understanding such basic mechanisms might
have consequences for the control of cell proliferation in animals.
Presumably, in connection with this consideration is that speci®c
cells in the meristems of plants have the ability to produce new
daughter cells over very long periods. Such `stem' cells might be
very interesting to study in greater detail in the future.
The cell cycle and development
Plants offer a unique possibility to study the integration of cell
division, growth, and development of multicellular organisms.
Because plants develop mainly post-embryonically, they have an
enormous plasticity and seem to tolerate many more changes in
numbers and sizes of cells than most other organisms. As such,
plants will still be able to reproduce with many fewer cells or with
cells that are several times larger than those of control plants. We are
just starting to use this plasticity to elucidate the long-standing
question as to whether cell division is the driver for growth (cellular
theory) or whether cell division just follows a developmental master
plan (organismal theory). Most intriguing is that the issue is still
unresolved and that experimental data sometimes support the
cellular theory and sometimes the organismal theory. For example,
overproduction of the transcription factor E2F results in extra cells,
thereby creating larger structures (De Veylder et al., 2002). On the
other hand, overproduction of KRPs reduces the number of cells in
the leaves by a factor of ten; but, this effect is compensated by
greatly enhanced cell sizes (Wang et al., 2000; De Veylder et al.,
2001). Yet another serious experiment indicates that overexpression
of the cyclin genes CYCB1;1, CYCD2;1, and CYCD3;1 just speeds
up the cell cycle and, consequently, organ development (Doerner
et al., 1996; Cockcroft et al., 2000; Dewitte et al., 2003). How to
consolidate all these observations is certainly a major challenge for
the near future. Neither the cellular nor the organismal theories are
correct and presumably new and more complex concepts will
emerge. It is my ®rm belief that understanding how cell division is
co-ordinated and integrated into the development of higher plants
can help scientists to address similar questions in other organisms.
An advantage of working with plants is that they have a very ¯exible
development with determinate and indeterminate growing organs
and a large reservoir of natural variation. Furthermore, combining a
well-developed technology to analyse growth processes (division
and expansion) at high spatio/temporal resolution (Beemster and
Baskin, 1998) with the emerging genomics tools will yield
unprecedented possibilities to anchor the cell cycle into developmental networks.
Practical applications
A thorough understanding of the plant cell cycle will probably be of
major practical importance in enhancing biomass production and
yield in major crops. Indeed, augmenting the number of cells in
concert with cell growth is expected to increase biomass. In addition,
acceleration of the cell cycle has been shown to reduce the lifespan
of plants (seed to seed). The systematic functional analysis of cell
cycle genes in crops is currently underway.
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