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of Plant ResearchJ
Plant ResLife Sciences25410.1007/s10265-005-0254-y
J Plant Res (2006) 119:1–4 Digital Object Identiﬁer (DOI) 10.1007/s10265-005-0254-y
© The Botanical Society of Japan and Springer-Verlag Tokyo 2005
Hirokazu Tsukaya • Gerrit T. S. Beemster
Genetics, cell cycle and cell expansion in organogenesis in plants
Published online: December 20, 2005
The Botanical Society of Japan and Springer-Verlag 2005
Key words Cell cycle · Cell expansion · Compensation · Genetics · Organogenesis · Systems biology
Growth has been of primary interest since the early days of plant research, both because of its implications for crop production and in order to understand evolutionary divergence in plant size and shape. At the cellular level, the growth of an organ is controlled by two processes: cell division and cell expansion. Many of the molecular mechanisms that regulate the plant cell cycle have been uncovered, and it has been established that regulation of cell expansion occurs primarily at the level of cell wall synthesis and the loosening of cross-links between cell wall polymers by speciﬁc enzymes. It is clear that in the context of a growing organ these two mechanisms must somehow be coordinated. In fact, recent work on mutants of leaf shape/size has yielded important clues regarding such coordinating systems. The nature of the link between these processes has been the subject of longstanding, mainly theoretical, discussions, and is crucial to understanding regulation of growth. It has become clear that unraveling this interrelationship requires multidisciplinary research, and the availability of new tools, such as inducible promoter systems, mutant and transgenic collections for genes involved in the cell cycle as well as in cell wall regulation and leaf morphology, micro arrays and image analysis systems, now enables the complex
H. Tsukaya (*) Graduate School of Science, University of Tokyo, Science Building #2, 7-3-1 Hongo, Tokyo 113-0033, Japan Tel. +81-3-58414047; Fax +81-3-58414047 e-mail: firstname.lastname@example.org H. Tsukaya National Institute for Basic Biology, Myodaiji-cho, Okazaki 444-8585, Japan G.T.S. Beemster Department of Plant Systems Biology, Ghent University, VIB, Technologie Park 927, 9052 Zwijnaarde, Belgium
interactions between molecular regulation, cellular processes and whole organ development to be mapped. On the occasion of the XVII International Botanical Congress (IBC), held 17–23 July 2005 in the Austria Center Vienna, Austria, we organized a symposium on this topic by inviting leading scientists from various disciplines within this research ﬁeld to discuss recent progress, in particular from the viewpoint of the integration of studies of genetics, cell cycle and cell expansion. This special JPR Symposium issue presents articles from six speakers from the IBC symposium describing exciting recent advances in this research ﬁeld. As an introduction, we will brieﬂy introduce here current issues concerning the topics discussed at the symposium.
Control of cell shape
Although there is some debate whether cells make an organ or an organ makes cells (cell theory vs organismal theory: see Tsukaya 2002a) organogenesis is highly dependent on the number and size of cells. In plants, cell size and shape is strictly regulated through the physical nature of the cell wall of expanding cells. The longstanding dogma entails that polarity of cell enlargement is controlled by polarity of the arrangement of cellulose microﬁbrils. Polarity of the cellulose microﬁbrils in turn would be regulated by a polar arrangement of cortical microtubules (MTs), a plantspeciﬁc form of cytoskeleton that is affected by plant hormones (e.g., Shibaoka 1994). Morphological defects in plant organs have been basically interpreted from this viewpoint. For example, Kim et al. (2002) interpreted the role of the ANGUSTIFOLIA (AN) gene as a regulator of the arrangement of cortical MTs because the mutant shows an altered arrangement of cortical MTs and altered polar growth of leaf cells. This approach to understanding cell shape control has been quite successful to date. However, a relationship between MT orientation and the direction of cellulose deposition is not always observed (Baskin et al. 2004; Wasteneys 2004). Recently, evidence has accumulated for the idea that cell shape may depend not only on the
have identiﬁed basic components of cell-cycle regulation in plants (Vandepoele et al. In the course of genome-wide collection of such gene families. This “microﬁbril length regulation model” (Wasteneys 2004). Genome-wide transcriptome analysis will help us obtain new clues to understanding how cell wall biosynthesis and restructuring are involved in cell division. and marginal and plate meristems in leaf primordia. this activity can continue for up to centuries. Uncovering such components will no doubt constitute a major breakthrough in this research ﬁeld. which turns out to be remarkably conserved across all eukaryotes. to a large extent. to pursue their analysis of cell-wall-related enzymes in cell wall dynamics. Wu et al. Therefore. (2001) analyzed diversity in the maize expansin family that is implicated in cell wall loosening. clues from studies of cell cycle regulation in single-celled organisms such as yeasts. 2005a). recent application of genomic approaches in this research ﬁeld has supplied new viewpoints. However. When plant cells enlarge their volume. For example. root apical meristem (RAM). in which embryonic stems are also still active. These meristems continuously supply new cells that differentiate into the various tissues of leaves. Yokoyama et al. cell shape can be thought of as being regulated both by arrangement and length of cortical MTs. Organ-wide regulation As mentioned above. it is clear that understanding what determines the transition of cells from proliferation to differentiation is crucial to understanding growth at the organ level. stems and roots. 2005). cell expansion and cell differentiation. 2006). and early frog embryos undergoing “cleavage” divisions. These meristems are believed to contain stem cells in the strict sense (Laux 2003) and appear to correspond to early embryonic stages of vertebrates. (2004) found unexpected diversiﬁcation of the xyloglucan endotransglucosylase/ hydrolase family. considering that most cell-wall-related enzymes (and putative enzymes) are highly multiplied and diversiﬁed in a genome. because it is mainly postembryonic and continues throughout the life of the plants. Recently. At some point. the detailed molecular and biochemical mechanisms have remained unknown. is presented in this issue (Wasteneys and Fujita 2006). Redundancy and inter-homolog differentiation of roles are expected in gene families and thus we should analyze all members of such families in conjunction in order to elucidate the precise role of these genes in cell wall regulation. The most typical example of such organogenesis occurs in the two apical meristems: the shoot apical meristem (SAM) and . Imoto et al. Moreover. These meristems do not appear to have stem cells. several key steps should be executed harmoniously: increasing of turgor pressure based on vacuole enlargement via water uptake. Similarly.2 arrangement but also on the length of cellulose microﬁbrils during axis establishment and growth. which is believed to play an important role in cell wall loosening and restructuring in the process of cell elongation in rice genome. Alternatively. Although the importance of these steps in cell enlargement has been well established. plant organogenesis cannot be fully understood if plant organs are viewed as a mere collection of single cells. At the molecular level. all meristematic activity shares some common characteristics: initial cells produce progeny that initially goes through a series of division resulting in an exponentially increasing population of proliferating cells. From a cellular perspective. (2005) established a microarray speciﬁcally designed for 765 genes encoding cell-wall-related enzymes of Arabidopsis. Further detailed analyses of these multigene families are needed to understand how cell wall construction is regulated. Tsukaya 1997). no genes that connect the cell cycle machinery and multicellular organogenesis have been identiﬁed to date (Gutierrez 2005. However. 2002). and how various members of gene families can compensate for alterations in each others’ activity. Powerful kinematic methods that facilitate the study of cell division and cell expansion in the context of growing organs have been developed and are reviewed in this issue by Silk (2006). 1999. It is clear that the timing of this transition largely determines the output of the meristem and thereby. In the case of cambium. the growth rate of the organ as a whole (Beemster et al. which could provide a novel clue to understanding the linkage between developmental genes and cell and organ shape control. This is an important strategy. marginal and plate meristems in leaf primordia are usually short-lived. and de novo synthesis and rearrangement of cell wall components. which expresses some SAM-related genes and supports thickening of tree trunks (Groover 2005). 2003). loosening of cell wall. Since cellulose microﬁbril length is believed to be correlated with the length of cortical MTs. cells exit the cell cycle and start to differentiate. These studies have provided important information about the molecular components that regulate the progression of the cell cycle. the plant has various other types of meristem: cambium. although some exceptional cases are known (Donnelly et al. Inzé 2005). they have presented us with the question of how this mechanism is coordinated between cells in a multi-cellular Cell cycle control Organogenesis in plants differs from the process in vertebrates such as humans. but they may be found among a large set of genes that are speciﬁcally expressed in proliferating tissues in multiple organs (Beemster et al. but nevertheless have the capacity to supply new cells for growth. Molecular biologists studying cell cycle regulation initially studied primarily single-celled organisms such as bacteria and yeasts. it was only very recently conﬁrmed that separation of parallel microﬁbrils takes place in the process of cell wall extension (Marga et al. One excellent example of such a study on the expansin family is presented in this issue (Sampedro et al. thereby typically increasing their size many-fold. intercalary meristem. However.
fewer but larger leaf cells in leaves. Leaf cells in the ﬂank region of leaf primordia appear to behave particularly cell autonomously (Marcotrigiano 2001). it has been reported that local and direct acceleration of cell cycling in the ﬂank of tobacco-leaf lamina caused local suppression of lamina growth. at the same time the volume of each cell is increased and. 2006). computational plant models or “virtual plants” have recently interested many researchers as a useful tool and many trials have been published (e.g. a loss-of-function mutant of the putative transcription factor AtGRF5. Fortunately.3 context. 2003. For example. suggesting one-way co-ordination from pathways of cell proliferation to those of cell enlargement. Since the size of mature leaf cells is highly dependent on the volume of the vacuole. Most mutants and transgenics exhibiting compensation have smaller and abnormally shaped leaves. Perspective This special issue presents seven articles that focus on recent progress in understanding the mechanisms of plant organogenesis. how can we pursue the unraveling of these complicated regulatory mechanisms of multicellular organogenesis in plants? One strategy might involve well-established genetic studies using mutants. cell-cell communication that coordinates and integrates the processes of cell proliferation and cell enlargement in plant organs. What could cause such a difference? An article by Horiguchi et al. b. Horiguchi et al. namely. Taken together. However. dynamic simulation models crucial to the understanding of such complex processes are constructed by connecting the genetic network that results in organogenesis (Vercruysse and Kuiper 2005). but over-expression of ANT only increases the number of leaf cells without resulting in any defect in cell size (Mizukami and Fischer 2000). loss-of-function of AINTEGUMENTA (ANT) causes compensation. although theoretical explanations have been proposed. did not show compensation. So. Recently. Early results towards unraveling the links between cell cycle and growth are presented in this issue (Beemster et al. 2002). In this case. the decrease in total area of the leaf blade is smaller than expected from the decrease in the number of cells. but only when cells of one type are in contact with cells of another (Marcotrigiano 2001). mathematical analysis suggested that increases in gene number might not contribute signiﬁcantly to the evolution of a variety of different cell types within organisms. For example. To date. For example. when cell proliferation is inhibited in leaves. as does AN3/GIF1. (2006) in this issue proposes a strategy to solve the enigma of this interesting compensation syndrome by using leaf-shape/size mutants. in which interactions of many different layers and levels of control (from intracellular. whereas local suppression of cyclin-dependent kinase activity in the ﬂank of tobacco-leaf lamina caused local expansion of the lamina (Wyrzykowska et al. which has ten times or more the volume of the cytoplasm. although a smaller decrease in the number of leaf cells was observed (Horiguchi et al. Beemster et al. which do not always agree with our intuition. On the other hand. as a result. Other kinds of studies also suggest that growth of cells in an organ is coordinated by some unknown positional signal(s). In this approach. Systems biology Another strategy to unravel complex regulatory networks of developmental processes might be the newly emerging systems biology approach. its basis is currently not well understood (Tsukaya 2002a. compensation partially reduces the effect of the decreased number of cells on the total area of leaves. and since enlargement of the vacuole occurs after completion of cell cycling. mechanisms of con- trol of organogenesis appear to be far more complex than expected from our knowledge of the behavior of singlecelled organisms. as is known to occur in single-celled organisms. This coordination differs from mechanisms of totalmass control known for animal organs (Potter and Xu 2001). 2005). the observed abnormal enlargement of leaf cells is not due to simple uncoupling of cell cycling and cell enlargement. This curious phenomenon is often referred to as “compensation” and. if they are not completely surrounded with cells of the other genotype. the compensation phenomenon suggests the importance of. providing us with new viewpoints for understanding of networks. which interacts with AN3/GIF1 and positively regulates cell proliferation in leaf primordia. For example. As mentioned . the number of cells in a growing organ is decreased signiﬁcantly as expected. Interestingly. an increase in cell number does not cause abnormality in cell size. as illustrated in this issue (Fleming 2006). Further development of systems biology will greatly help our understanding of the mechanisms of organogenesis of plants. several mutants and transgenic plants have been found to exhibit compensation syndrome (reviewed in Tsukaya 2003) but no detailed genetic analysis has been carried out. Mundermann et al.. as yet unknown. In addition. Thus. 2005). Rather. (2005) found that loss-of-function of the transcription co-activator ANGUSTIFOLIA3/GRF-INTERACTING FACTOR1 (AN3/GIF1) gene results in typical compensation. analysis of organogenesis of chimeras between two genotypes with different leaf size clearly showed that positional signal(s) for the coordinated organogenesis of leaf primordia might be supplied from all neighboring cells to cells in a primordium. as introduced brieﬂy above. local perturbations in the expression of regulatory components proves a very powerful approach with which to unravel coordination between cells. organ-wide. while the number of self-regulatory genes may signiﬁcantly increase cellular diversity (Mochizuki 2005). cells in an organ could pursue their developmental program even if their neighbors were genetically programmed to make a differently shaped organ. Experimental observations have shown that this question is not easily solved (Beemster et al. intercellular to intertissue levels) are essential. 2003). 2005b).
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