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Networks in leaf development Mary E Byrne Shoots are characterized by indeterminate growth resulting from divisions of undifferentiated cells in the central region of the shoot apical meristem. These cells give rise to peripheral derivatives from which lateral organ initials are recruited. During initial stages of cell recruitment, the three-dimensional form of lateral organs is specified. Lateral organs such as leaves develop and differentiate along proximodistal (base-to-tip), dorsoventral (top-to bottom) and mediolateral (middle-to-margin) planes. Current findings are refining our knowledge of the genes and genetic interactions that regulate these early processes and are providing a picture of how these pathways may contribute to variation in leaf form. Addresses Department of Crop Genetics, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK Corresponding author: Byrne, Mary E ([email protected]) Current Opinion in Plant Biology 2005, 8:59–66 This review comes from a themed issue on Growth and development Edited by Liam Dolan and Michael Freeling Available online 25th November 2004 1369-5266/$ – see front matter # 2005 Elsevier Ltd. All rights reserved. cells from the peripheral region of the shoot apical meristem (SAM). The extent of founder-cell recruitment from the flanks of the SAM varies between species, with Arabidopsis and maize representing two developmental extremes (Figure 1). Development along adaxial–abaxial (dorsoventral), proximal–distal, and midvein–margin (mediolateral) planes establishes leaf polarity (Figures 1 and 2). After this ground plan is set, continued cell division and expansion further contribute to leaf shape and form. At the same time, there is differentiation of specific cell and tissue types, such as outer layer epidermal cells, inner photosynthetic mesophyll and vasculature. Together, these processes establish the specialized function of the leaf as the main light-harvesting organ of the plant. Leaf initiation and patterning has long been the subject of experimental and theoretical work. Recent studies are building on results of classic work and are now defining molecular networks that are involved in many different aspects of leaf development. This review aims only to spotlight several of the more recent studies that have contributed to our understanding of the mechanisms that regulate leaf initiation, ground-plan patterning and specification of final form. Several recent reviews provide further reading [1–3]. Cell recruitment Introduction Leaf development initiates by recruitment of cells from the peripheral region of the SAM. Although the extent of founder-cell recruitment from the flanks of the SAM varies between species (Figure 1; [4–6]), genetic programs that control this early stage of leaf development appear to be conserved. For example, founder-cell recruitment in both Arabidopsis and maize is intimately linked with downregulation of KNOX homeobox transcription factors [3]. Auxin could be one regulator of this early event as chemical inhibition of polar auxin transport results in failure to downregulate KNOX expression in founder cells [7]. However, in Arabidopsis, PIN-FORMED1, a gene necessary for polar auxin transport in the SAM, is not required for downregulation of KNOX genes in founder cells [8,9]. Furthermore, in maize, ectopic expression of KNOX genes disrupts polar auxin transport and inhibition of polar auxin transport mimics the effects of KNOX gene overexpression [7,10]. Potentially, there are mutual inhibitory interactions between KNOX genes and auxin transport in the SAM. Leaves are the fundamental lateral appendage of land plants. The initiation and ground-plan patterning of leaves is a multistage process of interdependent events. Leaf primordia are initiated by recruitment of founder Recent work on the maize narrow sheath (ns) mutants has added to this picture. ns1 and ns2 are duplicate genes that are required for KNOX downregulation specifically in DOI 10.1016/j.pbi.2004.11.009 Abbreviations AGO1 ARGONAUTE1 AS1 ASYMMETRIC LEAVES1 CIN CINCINNATA FIL FILAMENTOUS FLOWER GA gibberellic acid GRAM GRAMINAFOLIA JAG JAGGED KAN KANADI ns narrow sheath PHAN PHANTASTICA PHB PHABULOSA PHV PHAVOLUTA PRS PRESSED FLOWER REV REVOLUTA rs2 rough sheath2 SAM shoot apical meristem yab3 yabby3 www.sciencedirect.com Current Opinion in Plant Biology 2005, 8:59–66 60 Growth and development Figure 1 tions primarily affect floral organ development, but prs mutants also lack stipules that are normally found at the margins and base of the Arabidopsis leaf (Figure 1a; [12,13]). Therefore, like ns mutants in maize, prs mutants are disrupted in the specification of lateral and proximal features of the leaf. Consistent with a requirement for regional specific founder cell recruitment, ns and PRS are both expressed in two lateral foci in the peripheral region of the SAM (Figure 3). Dorsoventrality and lamina outgrowth Development at the plant shoot apex. (a) Arabidopsis and (b) maize SAM and developing leaf primordia. In Arabidopsis, primordia are established by recruitment of cells from a limited region on the flanks of the SAM. In maize, cells from around the circumference of the SAM are recruited into the developing primordia. Young primordia grow out from the SAM establishing proximodistal (base-to-tip) polarity. Differential development of the side of the leaf closest to the SAM (adaxial) compared with the side away from the SAM (abaxial) establishes dorsoventral polarity. Mediolateral polarity is evident by the formation of lateral stipules in Arabidopsis and midvein-margin regions in maize. founder cells that specify the lateral domain of the leaf [11]. Leaves that are mutant for ns1 and ns2 are narrower than wildtype leaves but only in the proximal region of the leaf. The ns genes encode WUSCHEL-related homeobox transcription factors and are related to PRESSED FLOWER (PRS) in Arabidopsis [12]. prs muta- It is now well established that a dorsoventrally flattened lamina requires adjacent adaxial and abaxial leaf domains [1,14]. Loss of either the adaxial or abaxial domain results in partial or complete radialisation of the leaf. Adaxial identity in Arabidopsis is specified by the class III HD-ZIP family genes PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV) [15,16,17,18,19]. Dominant gain-of-function mutants have adaxial leaves. Loss of function of any one gene in this family has little effect on leaf development. When combined, however, mutations in all three genes results in radial abaxial leaves, a phenotype that is complementary to the dominant mutant phenotypes [15]. Conservation of the function of this gene family is reflected in mutations in other species. Thus, dominant mutations in rolled leaf1, the maize orthologue of REV, and in NSPHAVOLUTA, a tobacco orthologue of PHV, also result in leaf polarity defects with gain of adaxial features on the abaxial side of the leaf [20,21]. Consistent with a role in determining leaf polarity, the expression of this gene family is confined Figure 2 Leaf polarity. The adaxial side of the leaves of (a) Arabidopsis and (b) maize, indicating the proximal and distal ends, which define the proximodistal plane, and the midvein and margin, which define the mediolateral plane. In Arabidopsis, the proximal region of the vegetative rosette leaf forms a petiole and the lamina or leaf blade develops more distally. In maize, a sheath develops in the proximal region of the leaf, and the blade develops in the distal region of the leaf. The sheath and blade are separated by the auricle and ligule. Current Opinion in Plant Biology 2005, 8:59–66 www.sciencedirect.com Networks in leaf development Byrne 61 Figure 3 Adaxial–abaxial polarity. Gene expression patterns in the shoot apex of (a) Arabidopsis and (b) maize. PHB/PHV/REV genes (red) are expressed in the SAM. In Arabidopsis, these genes are expressed throughout the initiating primordium and their expression becomes confined to the adaxial domain upon further development of the primordium. In maize, the expression of the REV-related gene rolled leaf1 is adaxial in initiating and young primordia, and becomes confined to the margins later in development. Regulatory microRNAs, miRNA165/166 (yellow), are expressed on the abaxial side of the leaf in a domain that is complementary to the expression zone of target PHB/PHV/REV genes. The expression pattern of PRS in Arabidopsis and ns in maize is confined to a lateral region of the SAM (purple) and to the margins of leaf primordia (not indicated). The expression domain of the KNOX gene SHOOT MERISTEMLESS (blue) in Arabidopsis is also indicated. P1 to P5 indicate successive leaf primordia. M, meristem. to the adaxial domain of the leaf (Figure 3). Exclusion from the abaxial domain is mediated, at least in part, by miRNA-mediated posttranscriptional cleavage. All PHB, PHV, and REV genes have a sequence that is complementary to miR165 and miR166 [22,23]. Dominant mutations in PHB/PHV/REV genes all disrupt the miRNA-binding site [15,19,20,21]. Furthermore, in Arabidopsis and maize, miR165 and miR166 are expressed on the abaxial side of the leaf, a domain opposite that of PHB/PHV/REV target genes [20,24]. Spatial regulation of these target genes is necessary for the establishment of leaf polarity, but regulation of miR165 function also appears to be crucial for leaf patterning [24]. Mutations in ARGONAUTE1 (AGO1), a key component in RNA interference (RNAi)-mediated posttranscriptional gene regulation (see Kidner and Martienssen, this issue), result in ectopic expression of PHB and adaxialisation of the leaf. Abaxial cell fate is specified by the KANADI (KAN) genes [15,25,26,27,28]. Members of this family are expressed in the abaxial domain of the leaf. KAN genes are members of the GARP family of transcription factors, which includes four closely related genes in Arabidopsis. Mutations in individual family members only have subtle effects on leaf polarity, whereas combined mutations reveal a role for KAN genes in abaxial specification [26,27,29]. The leaves of kan1 kan2 mutants are partially adaxialised, and kan1 kan2 kan3 mutants display more complete adaxialisation. KAN and PHB/PHV/REV genes appear to establish an abaxial–adaxial leaf by mutual suppression [29]. These two gene families also show polar www.sciencedirect.com expression in vasculature [15,20]. KAN genes are expressed in the abaxial phloem and PHB genes are expressed in the adaxial xylem, and both gene families are required for the polar development of vasculature. It is possible that genes that are required for polar vascular development have been co-opted during evolution of the leaf [1]. Another class of leaf patterning genes are members of the YABBY family. Of the five YABBY genes in Arabidopsis, three are expressed in leaves [28,30,31]. Deletion analysis of the promoter of one YABBY gene, FILAMENTOUS FLOWER (FIL), has revealed independent cis-acting sequences that promote the expression of FIL throughout the leaf primordium and repress FIL expression on the adaxial side of the leaf primordium. This demonstrates that FIL is actively excluded from the adaxial domain [32]. The role of YABBY genes in abaxial specification is not clear, however, because loss-of-function mutants do not have obvious dorsoventral defects. This may be due, in part, to redundancy within the YABBY gene family and also with KAN genes. For instance, there are no obvious polarity defects in the fil and yabby3 (yab3) double mutant, but abaxial fate is compromised in this double mutant when KAN activity is reduced [26,30]. These two YABBY genes have further interactions with KAN genes. Double kan1 kan2 mutants have ectopic lamina outgrowths on the abaxial side of the leaf. It is not clear what preconditions lamina outgrowth as this phenotype is not always evident in backgrounds in which abaxial fate is disrupted. However, ectopic outgrowths are dependent on FIL and YAB3, supporting a role for YABBY genes in lamina outgrowth. GRAMINAFOLIA (GRAM) in Antirrhinum is Current Opinion in Plant Biology 2005, 8:59–66 62 Growth and development closely related to FIL and YAB3 [33]. As with YABBY genes in Arabidopsis, GRAM is expressed in the abaxial domain of the leaf. However, genetic interactions indicate that GRAM may regulate leaf polarity by repressing adaxial fate in the abaxial domain of the leaf. Furthermore, GRAM appears to promote adaxial fate in a noncell-autonomous manner. This suggests that the role of YABBY genes in dorsoventral polarity differs between species, although it is also possible that differences in loss-of-function phenotypes of different species reflect divergent levels of redundancy. PHANTASTICA genes and leaf patterning Leaf patterning can be altered by the ectopic expression of class I KNOX genes (reviewed in [3,34]). Typically, these genes are expressed in the SAM and downregulated in leaf primordia. The myb domain transcription factors PHANTASTICA (PHAN) in Antirrhinum, rough sheath2 (rs2) in maize and ASYMMETRIC LEAVES1 (AS1) in Arabidopsis are key negative regulators of KNOX gene expression in leaves [35–38]. The sequence identities and expression patterns of these genes clearly indicate that they form an orthologous gene family. The mutant phenotype in each species is not immediately comparable, however, leading to disparate interpretations of the defect. In phan mutants, early leaves have patches of abaxial tissue associated with ectopic lamina outgrowth on their adaxial leaf surface. The lamina of later leaves becomes progressively restricted to the distal tip of the leaf. In the most extreme form, the leaf is radial and abaxial [14]. PHAN is therefore required for leaf dorsoventral patterning. In comparison, as1 leaves are shorter and rounder than wildtype leaves, have occasional lobes and show no obvious dorsoventral defects [35,39,40], although under some conditions the base of the petiole may be radial [41,42]. Despite these differences, the maize gene rs2 rescues as1, indicating that function is conserved within this gene family. Overexpression of either AS1 or rs2 in Arabidopsis does not result in dorsoventral defects [42,43]. This is in contrast to overexpression of the LOB domain gene AS2, which is a protein partner of AS1 [42,44]. Mutations in AS2 result in leaf patterning defects that are comparable to those of as1, and in growth-condition-dependant radialisation of the petiole base [39,40,42,45]. However, overexpression of AS2 results in dorsoventral defects that are consistent with adaxialisation of the leaf [42,46]. Lamina outgrowths, similar to those of kan1 kan2 mutants, occur on the abaxial side of leaf of AS2-overexpressing lines. This phenotype is dependant on AS1. Together, the data indicate that AS1 and AS2 have at least retained the potential to pattern dorsoventral development and act by repression of abaxial fate in the adaxial domain of the leaf [46]. If this is the case, adaxial specification in Arabidopsis is determined by pathways that are redundant with AS1. Current Opinion in Plant Biology 2005, 8:59–66 The phenotype of the maize rs2 mutant sheds a different light on the role of PHAN genes in leaf development. In rs2 mutants, proximal features of the sheath, ligule and auricle (Figure 2) are displaced distally into the leaf blade [47]. rs2, therefore, is defective in proximodistal patterning. On the basis of the maize phenotype, an alternative interpretation of the phan phenotype proposed that radialisation of the Antirrhinum leaf is due to transformation of distal lamina into tissue that has petiole or stem features [37]. A recent report describing the effects of reduced NSPHAN in tobacco revisits this interpretation [48]. The upper leaves of plants with reduced NSPHAN expression are similar to those of phan mutants, with leaf lamina being confined to the distal tip of the leaf. More proximal regions develop dorsoventrality but, as in the petiole, there is no leaf lamina. The tobacco leaves are radial only at the base of the leaf. Surprisingly, the radial region has phloem surrounding xylem, a morphology that is indicative of abaxialisation, but the expression of NSPHB, a marker for adaxial fate, remains on the adaxial side of the leaf. This suggests that the radial leaves maintain some adaxial features. Thus, reducing NSPHAN levels potentially disrupts proximodistal development, with proximal features of stem and petiole being displaced distally along the leaf base-to-tip axis. The lower leaves of antisense NSPHAN plants have adaxial ectopic lamina outgrowths. Unlike those of phan mutants, these outgrowths are not associated with obvious dorsoventral defects. Instead, the lamina outgrowths of antisense NSPHAN plants may be associated with delayed maturation or indeterminacy in the leaf caused by misexpression of KNOX genes. Consistent with this idea, ectopic lamina is suppressed by application of gibberellic acid (GA), a hormone whose function is negatively regulated by KNOX genes [48,49,50]. Misregulation of KNOX genes in simple leaved species is typically associated with ectopic shoots. However, reducing GA levels in a background in which KNOX genes are ectopically expressed can generate ectopic callus, lamina or shoots on the leaf [49]. Thus, the formation of shoot as opposed to leaf may be determined by the relative temporal and spatial levels of KNOX genes and GA. Interestingly the tomato PHAN orthologue, LePHAN, is expressed in the SAM and on the adaxial side of leaf primordia [51,52]. Decreased LePHAN expression results in leaves that have various degrees of reduced lamina development. The proximal region may be radialised and the distal lamina can develop as a trumpet or as leaflets at the tip of the radial petiole. Leaflets may be confined to the abaxial side of the petiole or be arranged around the entire petiole circumference, phenotypes that are comparable to non-peltate and peltate palmate leaves, respectively. LePHAN antisense phenotypes are correlated with the expression of LePHAN being progressively confined to the distal tip of the leaf. Furthermore, the www.sciencedirect.com Networks in leaf development Byrne 63 expression domain of PHAN in a range of species that have compound leaves correlates with the type of compound leaf, whether pinnate, palmate or peltate-palmate. Convergent evolutionary changes in the expression of PHAN may be responsible for phenotypic variation in compound leaf species. Equally likely, PHAN expression could be a consequence of developmental variation mediated by one or more alternative regulators. Elaboration of the leaf lamina Subsequent to events that direct leaf polarity, the control of final leaf shape and size continues by coordinated regulation of cell division and expansion along the length and width of the leaf [53]. Cessation of cell division and differentiation proceeds along the proximodistal plane from leaf tip to base (Figure 2). In the dorsoventral plane, continued divisions in the adaxial mesophyll differentiate the adaxial pallisade from the abaxial spongy mesophyll [54,55,56]. Another dimension of control is provided by the relative rates of cell division across the mediolateral plane of the developing leaf. Cell divisions cease in the mid-region of the leaf slightly ahead of divisions at the margins. Maintaining this pattern of cell division is crucial for the development of a flat leaf surface, as highlighted by mutations in CINCINNATA (CIN) in Antirrhinum [55,57]. In cin mutants, the leaf margin is rumpled as a result of the slower arrest of cell divisions at the leaf margins relative to the middle of the leaf. A comparable phenotype is seen in jaw-D mutants in Arabidopsis [58]. In this case, overexpression of a miRNA results in the downregulation of target genes belonging to the TCP family of transcription factors, which are closely related to CIN in Antirrhinum [58,59]. Ubiquitous expression of TCPs partially suppresses the jaw-D mutant phenotype, and the degree of rescue is dependent on the level of target gene expression. This suggests a dose-dependent interaction between the miRNA and its direct target. Interactions such as these may serve to fine-tune development. Another gene that is involved in specifying final leaf shape is JAGGED (JAG) [60,61]. In jag mutants, the leaves are more predominantly serrated than those in the wildtype and the distal tips of floral organs are jagged, absent or reduced. Misexpression of JAG results in ectopic leaf-like lamina outgrowths in proximal leaf regions and on the stem. The development of blade on the petiole is reminiscent of the phenotypes of recessive blade on petiole (bop) mutants and of dominant mutations that affect the LEAFY PETIOLE gene [62–64]. In one sense, these mutations may represent the disruption of proximodistal specification, with transformation of proximal features to a more distal fate. The expression of a cell division marker is decreased in jag mutant leaves, however, indicating that JAG is required to prevent premature cell differentiation. In this respect, JAG and JAW may specify opposing but complementary functions in lamina outgrowth. www.sciencedirect.com Conclusions Early surgical experiments demonstrated that the separation of an initiating primordium from the SAM resulted in a radial leaf that has abaxial features [65,66]. Subsequently, the notion of interdependence of SAM function and leaf patterning has been reinforced by studies defining genes and genetic interactions that are essential to these processes. In simple leaves, this involves turning off the KNOX genes that maintain meristem indeterminacy. KNOX repression is maintained during leaf development by several different gene classes, including PHAN, BOP, and YABBY genes, all apparently acting in distinct pathways. As cells are recruited into the initiating leaf primordia, adaxial PHB family class III HD-ZIP genes repress abaxial KAN genes. Abaxial fate is either established or reinforced by KAN and miRNA-mediated repression of PHB family genes. Layered onto this information, YABBY genes contribute to abaxial fate as well as to mediolateral outgrowth of the leaf lamina. In addition to specification of dorsoventral fate, PHB and KAN family genes are required for correct patterning of polar vascular development. Furthermore, PHB family genes and regulation of the corresponding miRNA are required for SAM function, potentially reflecting polar centralperipheral development along the main axis of the shoot ([65,66]; see del Mar Castellano and Sablowski, this issue). Thus, this shared genetic pathway can be seen as a reflection of a common developmental theme. Although positional information in the developing primordium depends on contact with or signalling from the SAM, the nature of this signal is still to be determined. Suggested candidates are regulators of adaxial fate and may be either a miRNA or a sterol ligand that targets the PHB gene family [15,16,20,24]. Although some genes that specify dorsoventrality also affect other planes of leaf development, our understanding of the mechanisms that regulate proximodistal outgrowth and bilateral symmetry is limited. Flexibility in these pathways is likely to contribute to the diversity of leaf form. Acknowledgements I thank Cathie Martin and Robert Sablowski for comments on the manuscript. I apologise to those whose work I failed to address in this review because of lack of space. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest 1. Engstrom EM, Izhaki A, Bowman JL: Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiol 2004, 135:685-694. 2. Kidner CA, Timmermans MCP, Byrne ME, Martienssen RA: Developmental Genetics of the Angiosperm Leaf, vol 38. Edited by Callow JA. London: Academic Press; 2002. 3. Tsiantis M, Hay A: Comparative plant development: the time of the leaf? Nat Rev Genet 2003, 4:169-180. Current Opinion in Plant Biology 2005, 8:59–66 64 Growth and development 4. Furner IJ, Pumfrey JE: Cell fate in the shoot apical meristem of Arabidopsis thaliana. Development 1992, 115:755-764. 5. Irish VF, Sussex IM: A fate map of the Arabidopsis embryonic shoot apical meristem. Development 1992, 115:745-753. 6. Poethig RS, Szymkowiak EJ: Clonal analysis of leaf development in maize. Maydica 1995, 40:67-76. 7. Scanlon MJ: The polar auxin transport inhibitor N-1naphthylphthalamic acid disrupts leaf initiation, KNOX protein regulation, and formation of leaf margins in maize. Plant Physiol 2003, 133:597-605. 8. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C: Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426:255-260. This paper examines the regional and cellular expression pattern of two genes, PIN-FORMED1 and PINOID, that are involved in polar auxin transport in the shoot apical meristem. Evidence is presented to support a role for these genes and for polar auxin transport in establishing the site of organ initiation and maintaining the regular phyllotactic pattern of organ initiation. 9. Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J: PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 2000, 127:5157-5165. 10. Tsiantis M, Brown MI, Skibinski G, Langdale JA: Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiol 1999, 121:1163-1168. 11. Scanlon MJ, Schneeberger RG, Freeling M: The maize mutant narrow sheath fails to establish leaf margin identity in a meristematic domain. Development 1996, 122:1683-1691. 12. Nardmann J, Ji J, Werr W, Scanlon MJ: The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 2004, 131:2827-2839. The ns mutations are duplicate genes that are required for the recruitment of a specific group of founder cells comprising those in the lateral regions of the initiating leaf primordium. The cloning of these genes demonstrates their close relationship to PRS in Arabidopsis. Mutations in prs principally affect floral organ development but this work shows that stipules at the base of the leaf are absent from the prs mutant. Two points of interest result from this work. First, the expression patterns of PRS/ns and the phenotypes of prs/ns mutants correlate with domain-specific founder-cell recruitment. Second, a comparison of the maize and Arabidopsis phenotypes can be interpreted in terms of classical ideas on dicot and monocot leaf morphology. 13. Matsumoto N, Okada K: A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers. Genes Dev 2001, 15:3355-3364. 14. Waites R, Hudson A: phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 1995, 121:2143-2154. 15. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL: Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 2003, 13:1768-1774. The authors of this paper build on previous work on the role of PHB/PHV/ REV class III HD-ZIP genes and KANADI genes in patterning dorsoventrality. Specifically, they address the role of these genes in vascular patterning. They demonstrate a correlation between the phenotype of dominant mutations in REV and disruption of the miRNA-binding site. Analysis of loss-of-function mutants in the class III HD-ZIP genes supports a model whereby these genes pattern adaxial–abaxial vascular polarity in the leaf and radial vascular polarity in the stem. 16. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK: Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411:709-713. 17. Talbert PB, Adler HT, Parks DW, Comai L: The REVOLUTA gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 1995, 121:2723-2735. 18. Zhong R, Ye ZH: IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomainleucine zipper protein. Plant Cell 1999, 11:2139-2152. Current Opinion in Plant Biology 2005, 8:59–66 19. Zhong R, Ye ZH: Amphivasal vascular bundle 1, a gain-of function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 2004, 45:369-385. The authors demonstrate that a dominant mutation in the REV gene is due to disruption of the regulatory miRNA binding site. Unlike the work reported in [15], the work described here shows that the gain-offunction mutant has dramatic effects on organ polarity and SAM function. 20. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC: microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 2004, 428:84-88. This paper describes the cloning of a classical dominant mutation in maize. rolled leaf1 (rld1) is the maize orthologue of REV in Arabidopsis. The Rld1 phenotype is due to a sequence change in the miRNA-binding site of the gene, as found for dominant mutations in this gene class in Arabidopsis. Expression of the regulatory miRNA occurs in the abaxial leaf and abaxial phloem, in a pattern that complements the expression of the target gene. 21. McHale NA, Koning RE: MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell 2004, 16:1730-1740. Analysis of a dominant mutant that affects the tobacco orthologue of the Arabidopsis gene PHV reveals a role for this orthologue in adaxial fate and SAM function, as well as in vascular cambium patterning. Dominant mutations affect the gene’s miRNA-binding site. 22. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP: Prediction of plant microRNA targets. Cell 2002, 110:513-520. 23. Tang G, Reinhart BJ, Bartel DP, Zamore PD: A biochemical framework for RNA silencing in plants. Genes Dev 2003, 17:49-63. 24. Kidner CA, Martienssen RA: Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 2004, 428:81-84. An important paper that describes the effects of the AGO1 gene on leaf and flower development. In contrast to work described in previous reports, phenotypic analysis of an allelic series and misexpression of downstream targets of AGO1 demonstrate that disruptions of this gene cause a defect in abaxial-fate specification. Consistent with this phenotype, the adaxial gene PHB and its miRNA regulator are misregulated in ago1 mutants, demonstrating regulation of the miR165, and consequently the corresponding target, by AGO1. 25. Eshed Y, Baum SF, Bowman JL: Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 1999, 99:199-209. 26. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL: Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 2004, 131:2997-3006. Complementary to [15], this paper describes the shoot phenotype of combinatorial mutations in KAN and YABBY family genes. 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Genes Dev 1999, 13:1079-1088. www.sciencedirect.com Networks in leaf development Byrne 65 32. Watanabe K, Okada K: Two discrete cis elements control the abaxial side-specific expression of the FILAMENTOUS FLOWER gene in Arabidopsis. Plant Cell 2003, 15:2592-2602. 33. Golz JF, Roccaro M, Kuzoff R, Hudson A: GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 2004, 131:3661-3670. The authors report the cloning of the Antirrhinum gene GRAM, which is found to be a member of the YABBY gene class, closely related to FIL and YAB3. The phenotype of gram mutants, their expression pattern, their genetic interactions with phan and clonal analysis are used to derive a model for GRAM function. The authors conclude that GRAM has two functions that are specific to adaxial fate: repression of adaxial fate in the abaxial domain and non-cell-autonomous positive regulation of adaxial fate in the adaxial domain. 34. 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