482 Plant cell division occurs mainly in developing tissues and appears to be highly regulated in both space and time. Recently, genetic and molecular analyses have been able to dissect the function of cell proliferation in the processes of growth and development. Mutant studies have shown that plants have a compensatory mechanism whereby increased cell expansion can partially cover for defects in proliferation. Ectopic expression of developmental and cell-cycle regulators has indicated how growth rate is controlled at the molecular level in meristems and lateral organs. Addresses John Innes Centre, Colney, Norwich NR4 7UH, UK; e-mail: john.doonan@bbsrc.ac.uk Current Opinion in Plant Biology 2000, 3:482–487 1369-5266/00/$ - see front matter © 2000 Elsevier Science Ltd. All rights reserved. Abbreviations ABA abscisic acid ANT AINTEGUMENTA CDK cyclin-dependent protein kinase CYC CYCLOIDEA M Mitosis S Synthesis SHR SHORT ROOT sin2 short integuments 2 Introduction Flowering plants are multicellular organisms whose mode of growth and development appears, at least superficially, to be distinct from that of animals. Whereas animal devel- opment has a defined and early embryonic phase during which all of the major organ systems are put in place, plant growth continues throughout the lifespan and is modular. Moreover, the modules (known as phytomers) are formed as the result of two distinct types of growth: determinate growth, producing organs of limited maximum size, and indeterminate growth, producing tissues of no defined maximum size. The shoot and root meristems have the potential for unlimited growth along the longitudinal (i.e. shoot to root) axis and are indeterminate, whereas leaves, most other lateral organs and some meristems (e.g. floral meristems) have determined growth patterns for all three developmental axes. How plant cell proliferation is regu- lated within the context of development has been a subject of debate for many years. Mutations in many developmental genes affect the pattern and the extent of cell proliferation and, formally, these genes can be argued to regulate division [1]. The molecular mechanism(s) by which developmental genes influence cell division and proliferation have remained, until recently, largely obscure. The central controls of the cell cycle in plants are largely similar to those in other eukaryotes and have been reviewed extensively in recent years [2 •• ]. Briefly, entry into and progress through the cycle is regulated at a set of key transitions (minimally considered to include at least G 0 →G 1 , G 1 →Synthesis [S] phase and G 2 →Mitosis [M]). Each transition is unidirectional and controlled by the activity of one or more cyclin-dependent protein kinases (CDKs). The CDKs are typically activated by the synthesis of cyclins or other interacting proteins and by the reversible phosphorylation of key amino-acid residues. Inactivation of the kinase complex typically involves the destruction of cyclin protein by a ubiquitin-proteosome pathway and phosphorylation. Checkpoint pathways couple different processes within the cycle, ensuring its orderly progression. The cell cycle also responds to developmental cues, but a mechanistic understanding of how developmental processes modulate and interact with the plant cell cycle is only just beginning to emerge. This review focuses on our present understanding of that interaction. Mutual compensation: cell proliferation and cell expansion can cover for each other’s mistakes There are at least two models to explain how cells behave within the context of a growing plant. One model proposes that cell growth and proliferation are part of a regulatory cascade that is controlled by developmental genes. In this model, the spatial and temporal control of cell proliferation is defined in terms of patterns established by those genes. The second view is that cells fill in a ‘developmental space’ that is defined at a higher level by genes specifying size and shape. According to this model, the boundaries and size of an organ could be defined by mechanisms that do not directly affect cell-cycle parameters. Although these models are not mutually exclusive, they have led to different ways of thinking about the role of cell proliferation in plant development. The ‘space filling’ view arose as a result of classical experiments in which developmental processes continued relatively normally even when cell proliferation was compromised. For exam- ple, when cell division in cereals was arrested using high dose gamma irradiation, increased cell enlargement com- pensated to the extent that morphologically normal leaves were produced. The leaves contained many fewer but larger cells [3]. Mosaic plants, in which different tissues contain cells of radically different sizes or growth rates, also develop normally, suggesting that growth controls operate globally within tissues. Finally, over the past decade many mutants have been found in which either cell division or cell expan- sion is perturbed but, surprisingly, the mutant plants develop more or less normally. Defects in either cell divi- sion or cell expansion are compensated for by enhancement of the other process. For example, the tangled mutant of maize has misaligned cell divisions but its overall leaf shape is almost normal [4]; the short integuments 2 (sin2) Social controls on cell proliferation in plants John Doonan