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The Shoot Apical Meristem and Development of Vascular Architecture1

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The Shoot Apical Meristem and Development of Vascular Architecture1 1660 REVIEW / SYNTHE` SE The shoot apical meristem and development of vascular architecture1 Nancy G. Dengler Abstract: The shoot apical meristem (SAM) functions to generate external architecture and internal tissue pattern as well as to maintain a self-perpetuating population of stem-cell-like cells. The internal three-dimensional architecture of the vas- cular system corresponds closely to the external arrangement of lateral organs, or phyllotaxis. This paper reviews this cor- respondence for dicotyledonous plants in general and in Arabidopsis thaliana (L.) Heynh., specifically. Analysis is partly based on the expression patterns of the class III homeodomain-leucine zipper transcription factor ARABIDOPSIS THALI- ANA HOMEOBOX GENE 8 (ATHB8), a marker of the procambial and preprocambial stages of vascular development, and on the anatomical criteria for recognizing vascular tissue pattern. The close correspondence between phyllotaxis and vascu- lar pattern present in mature tissues arises at early stages of development, at least by the first plastochron of leaf primor- dium outgrowth. Current literature provides an integrative model in which local variation in auxin concentration regulates both primordium formation on the SAM and the first indications of a procambial prepattern in the position of primordium leaf trace as well as in the elaboration of leaf vein pattern. The prospects for extending this model to the development of the complex three-dimensional vascular architecture of the shoot are promising. Key words: ATHB8, auxin, phyllotaxis, ATPIN1, procambium, vascular development. Re´sume´ : La fonction du me´riste`me apical de la tige est de ge´ne´rer l’architecture externe et le patron histologique interne, ainsi que de maintenir une population de cellules de nature caulinaire par auto-perpe´tuation. L’architecture interne tridi- mensionnelle du syste`me vasculaire correspond e´troitement a` l’arrangement externe des organes late´raux, ou phyllotaxie. L’auteur passe en revue cette correspondance chez les plantes dicotyles en ge´ne´ral, et plus particulie`rement chez l’Arabi- dopsis thaliana. L’analyse est partiellement base´e sur l’expression des patrons de classe III du facteur de transcription de l’home´odomaine-leucine-zipper, ARABIDOPSIS THALIANA HOMEOBOX GENE 8 (ATHB8), un marqueur des stades cambial et procambial du de´veloppement vasculaire, ainsi que sur des crite`res anatomiques pour reconnaıˆtre le patron des tissus vasculaires. L’e´troite correspondance entre la phyllotaxie et le patron des tissus vasculaires, dans les tissus matures, apparaıˆta` un stade pre´coce du de´veloppement, au moins au premier plastochron de l’apparition du primordium foliaire. La litte´rature courante pre´sente un mode`le inte´grateur dans lequel la variation locale des teneurs en auxines re`gle a` la fois la formation du primordium sur le me´riste`me apical de la tige et les premie`res indications d’un pre´-patron procambial, dans la position de la trace foliaire du primordium, ainsi que dans l’e´laboration du patron vasculaire foliaire. La perspective d’e´tendre ce mode`le de de´veloppement de l’architecture vasculaire tridimensionnelle complexe de la tige apparaıˆt promet- teuse. Mots cle´s : ATHB8, auxine, phyllotaxie, ATP1N1, procambium, de´veloppement vasculaire. [Traduit par la Re´daction] Introduction prerequisite for understanding plant development as well as the special properties of plants as organisms with an indeter- The shoot apical meristem (SAM) functions to generate minate body plan. Recently, attention has focused on the external architecture and internal tissue pattern as well as to generation of external architecture, specifically the place- maintain a self-perpetuating population of cells. Knowledge ment of lateral organs (e.g., Fleming 2005; Reinhardt 2005), of the development and behavior of the apical meristems is and on the formation and maintenance of the population of stem-cell-like cells at the core of the SAM (e.g., Baurle and Received 22 February 2006. Published on the NRC Research Press Web site at http://canjbot.nrc.ca on 6 February 2007. Laux 2003; Carles and Fletcher 2003). Less attention has been given to the generation of the pattern of dermal, N.G. Dengler. Department of Botany, University of Toronto, ground, and vascular tissues within the shoot. While the pro- Toronto, ON M5S 1A1, Canada (e-mail: toderm (precursor of the dermal tissue system) is derived [email protected]). from the surface layer (L1) of the SAM simply by a restric- 1This review is one of a selection of papers published on the tion of division plane to anticlinal, the gradual emergence of Special Theme of Shoot Apical Meristems. vascular pattern from more homogeneous-appearing precur- Can. J. Bot. 84: 1660–1671 (2006) doi:10.1139/B06-126 # 2006 NRC Canada Dengler 1661 sors derived from the L2 and deeper layers of the SAM is RONA) are expressed in the SAM, adaxial domains of less well understood (Steeves and Sussex 1989). The pro- lateral organs, and developing vascular tissues, while ex- cambium (vascular tissue precursor) becomes distinct from pression of ATHB8 is restricted to developing vascular tis- surrounding ground meristem (ground tissue precursor) by sues (Baima et al. 1995; McConnell et al. 2001; Emery et differential patterns of cellular vacuolation, division, and en- al. 2003; Prigge et al. 2005; Williams et al. 2005). During largement (Esau 1965a, 1965b). Procambial pattern can be the development of leaf venation pattern, ATHB8-GUS is recognized because the component cells are elongate in expressed at very early stages in positions where veins are shape and less vacuolated than adjacent ground meristem predicted to appear, but before the diagnostic anatomical and form continuous strands (Esau 1965a, 1965b; Nelson features of procambium are expressed (Kang and Dengler and Dengler 1997). As it emerges, the procambial system 2004; Scarpella et al. 2004). In developing leaves, linearly can be seen to form a complex, three-dimensional architec- adjacent ground tissue cells initiate ATHB8 expression, and ture within the shoot that is continuous with more mature development is continuous and polar in the sense that the parts of the vascular system. Moreover, the complex internal first cells to express ATHB8-GUS are adjacent to pre- architecture of the vascular system corresponds closely to existing procambial strands and that ground cells at the the external architecture of lateral organ arrangement, or terminus of a developing file are recruited to the ATHB8- phyllotaxis. GUS-expressing file, extending it across a panel of ground The purpose of this review is to examine the close corre- tissue (Kang and Dengler 2004; Scarpella et al. 2004). This spondence between phyllotaxis and primary vascular archi- expression pattern within the ground meristem presages the tecture. The literature on this subject extends back for anatomical emergence of procambium and has been termed almost 150 years, since botanists such as Na¨geli (1858) and ‘‘preprocambium’’ (Mattsson et al. 2003). Following the DeBary (1884) noted that the geometric array of developing preprocambial stage of development, cells in the file ac- and mature leaves gives an external clue to the internal ar- quire the distinctive anatomical features of procambium, rangement of vascular bundles. In past decades, the causality and ATHB8-GUS expression increases (Kang and Dengler of this correspondence has been hotly debated, but as em- 2004; Scarpella et al. 2004). In contrast with the progres- phasized by Esau (1965a, 1965b), the opposing views that sive appearance of the preprocambial phase, the emer- either (i) new primordia induce the formation of the vascular gence of procambium anatomy appears to occur bundles that supply them or (ii) acropetal development of simultaneously along the file of cells (Scarpella et al. vascular bundles induces the formation of primordia are 2004). As xylem and phloem cells gradually differentiate oversimplifications, and it is more likely that both phyllo- from procambial tissue, ATHB8-GUS expression becomes taxis and vascular architecture are determined by a common restricted to the residual procambium between the vascular mechanism. Recent experimental and modeling studies have tissues and undifferentiated cells on the adaxial (xylem) provided strong evidence for such a common mechanism side of procambial strands; expression ceases in fully dif- (Fleming 2005; Reinhardt and Kuhlemeier 2002; Reinhardt ferentiated veins (Kang and Dengler 2002). Similarly, in et al. 2003; Reinhardt 2005; Smith et al. 2006; Jo¨nsson et stem vascular bundles, ATHB8 expression becomes re- al. 2006). In this paper, I first review the expression pattern stricted to a narrow zone of procambium between the dif- of ARABIDOPSIS THALIANA HOMEOBOX GENE8 ferentiating xylem and phloem tissues (Baima et al. 1995). (ATHB8), a putative marker of procambium, and its precur- Thus, ATHB8 expression provides a uniquely suitable sors within the SAM region. Second, I review primary vascu- marker for analysis of vascular architecture, as it defines lar architecture of dicotyledonous shoots and its both an early prepattern and procambium itself throughout correspondence to phyllotaxis and then describe this corre- its development. spondence for A. thaliana based on an analysis of pro- Despite this distinctive expression pattern, the specific cambium anatomy and the expression pattern of ATHB8 developmental function of ATHB8 is unknown (Emery et (based on the results
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