Development of the plant shoot is dependent on the shoot apical meristem. Interactions between KNOX homeodomain transcription factors and the myb domain transcription factor AS1 (ASYMMETRIC LEAVES1) regulate both meristem function as well as leaf patterning. This review summarizes these interactions.
There are many obvious differences between plants and animals, but from a developmental point of view one key difference relates to how the adult body is formed. In animals, all organs are formed during development of the embryo and post-embryonic development primarily involves growth in size. In plants, on the other hand, most organs are specified post-embryonically. This developmental habit is the result of establishment and maintenance of stem cell populations within organized structures called meristems. Stem cells in the centre of the meristem are undifferentiated and divide to give rise to daughter cells, some of which maintain the pool of stem cells and others contribute to the peripheral region of the meristem. Peripheral region cells undergo many divisions. The products of these cell divisions differentiate and so contribute to mature organs of the plant body.
Two primary meristems and their corresponding stem cells are established in the embryo, one at the apex and another at the base of the embryo. Throughout the plant life cycle, the meristem at the apex of the plant, the shoot apical mersitem, gives rise to all aerial portions of the plant including leaves and stems, as well as secondary meristems that form branches and flowers (Figure 1). The meristem at the base of the plant establishes the root system.
The plant shoot apex
KNOX gene interactions in the shoot apical meristem
One gene required to maintain the shoot apical meristem is the class 1 KNOX gene STM (SHOOT MERISTEMLESS). STM is expressed in the shoot apical meristem and down-regulated in cells that are recruited to form terminally differentiated lateral organs such as leaves [1,2]. STM maintains meristem function, in part, by repressing the differentiation gene AS1 (ASYMMETRIC LEAVES1) . Loss of function of STM results in loss of the shoot meristem. However, meristem function is recovered when AS1 is also removed. In this case, meristem maintenance is assumed by BP (BREVIPEDICELLUS), the Arabidopsis class 1 KNOX gene most closely related to STM . Interestingly, in plants lacking STM and AS1, BP can support vegetative and inflorescence meristem function but not floral meristems. Unlike STM, loss of BP function alone does not radically affect meristem function [4–6]. STM and BP are therefore redundant, but STM has additional roles that are not shared by BP. Both STM and BP proteins interact directly with one another and with a more distantly related homoeodomain transcription factor, BLR (BELLRINGER) [7–9]. BLR is expressed in a domain overlapping that of STM and BP and enhances meristem defects of both but BLR itself is not essential for meristem function. This again appears to be due to redundancy .
Repression of KNOX genes in the leaf
While the KNOX gene STM functions to repress AS1 in the shoot meristem, AS1 and orthologues in other species with simple leaves act to repress KNOX gene expression in differentiating lateral organs [3,11–16]. KNOX genes are expressed in leaves of compound leaf species, indicating that temporal and spatial regulation of these meristem genes have influenced the evolution of leaf form . Partial reduction of KNOX gene misexpression in Arabidopsis plants lacking AS1 has no great suppression effect on the leaf defect. However, at least three KNOX genes are misexpressed in these plants, so eliminating all ectopic KNOX gene expression will potentially repress the as1 mutant leaf development defect. The role of KNOX genes in modulating simple leaf developments is suggested by interactions with the hormone GA (gibberellic acid). KNOX genes directly repress expression of the GA biosynthesis enzyme, GA20 oxidase [18,19]. Increasing GA suppresses leaf development defects resulting from ectopic KNOX expression including leaf defects of as1, thereby implicating GA and KNOX genes in the as1 phenotype [11,18].
Role of AS1 and KNOX genes in leaf patterning
As lateral organs, such as leaves, are initiated on the flanks of the shoot apical meristem, three principal axes of development are specified. Development along proximodistal (base-to-tip), dorsoventral (adaxial-to-abaxial) and mediolateral axes establishes leaf polarity (Figure 1). The current model for leaf development postulates that a signal from the meristem to the initiating leaf primordium promotes adaxial identity in cells closest to the meristem. Cells further from the meristem apex assume abaxial identity. Subsequently, mutual negative interactions between genes specifying adaxial and abaxial leaf domains establish a boundary that is essential for outgrowth of the leaf lamina. The mature leaf lamina in many species is characterized by cell type differences in the adaxial and abaxial domains of the leaf. Loss of either adaxial or abaxial domains results in a radial leaf. Consistent with this model, a number of mutations have defined genes required for dorsoventral patterning and lamina outgrowth (reviewed in ).
The first leaf dorsoventral patterning gene to be described was the myb domain transcription factor gene PHAN (PHANTASTICA) in Antirrhinum. Plants lacking PHAN have leaves with sectors of abaxial tissue on the adaxial leaf surface surrounded by ectopic lamina. More severely affected leaves are fully radial and only have abaxial features. [21,22]. PHAN-related genes have been isolated from diverse land plant species. The PHAN orthologue in Arabidopsis is AS1 . In contrast with PHAN in Antirrhinum, loss of AS1 in Arabidopsis does not significantly affect leaf dorsoventral polarity. Typically leaves of plants lacking AS1 are shorter and broader and can be lobed, although occasionally the base of the leaf is radial [3,12,13,23,24].
Interestingly loss-of-function in the PHAN orthologue in other species, including tobacco, pea and tomato, results in variable degrees of abaxialization [11,14,25]. In both tobacco and pea, phenotypes are reminiscent of that in Antirrhinum. Some leaves form ectopic lamina outgrowths on the adaxial side of the leaf, whereas other leaves are completely radial and abaxial. The lack of similar phenotypes in Arabidopsis suggests novel genetic redundancies specifying adaxial fate in this species. Identifying such genetic components and comparing functions in diverse species will build a picture of complexities in the evolution of simple leaves.
Stem Cells and Development: A Focus Topic at BioScience2005, held at SECC Glasgow, U.K., 17–21 July 2005. Edited by T. Kouzarides (Cambridge, U.K.), S. Newbury (Newcastle upon Tyne, U.K.), B. Richardson (University College London, U.K.), R. Sablowski (John Innes Centre, Norwich, U.K.), D. Tosh (Bath, U.K.), M. Welham (Bath, U.K.) and A. Willis (Nottingham, U.K.).