vascular tissue differentiation and pattern …

5 Apr 2002 10:21 AR AR156-08.tex AR156-08.SGM LaTeX2e(2001/05/10)P1: ILV10.1146/annurev.arplant.53.100301.135245

Annu. Rev. Plant Biol. 2002. 53:183–202DOI: 10.1146/annurev.arplant.53.100301.135245

Copyright c© 2002 by Annual Reviews. All rights reserved

VASCULAR TISSUE DIFFERENTIATION AND

PATTERN FORMATION IN PLANTS

Zheng-Hua YeDepartment of Botany, University of Georgia, Athens, Georgia 30602;e-mail: [email protected]

Key Words auxin, procambium, positional information, venation, xylem

■ Abstract Vascular tissues, xylem and phloem, are differentiated from meristem-atic cells, procambium, and vascular cambium. Auxin and cytokinin have been consid-ered essential for vascular tissue differentiation; this is supported by recent molecularand genetic analyses. Xylogenesis has long been used as a model for study of celldifferentiation, and many genes involved in late stages of tracheary element formationhave been characterized. A number of mutants affecting vascular differentiation andpattern formation have been isolated inArabidopsis. Studies of some of these mutantshave suggested that vascular tissue organization within the bundles and vascular patternformation at the organ level are regulated by positional information.

CONTENTS

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184VASCULAR PATTERNS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

Vascular Tissue Organization Within a Vascular Bundle. . . . . . . . . . . . . . . . . . . . . 185Vascular Tissue Organization at the Organ Level. . . . . . . . . . . . . . . . . . . . . . . . . . . 185

MODEL SYSTEMS FOR STUDYING VASCULAR DEVELOPMENT. . . . . . . . . . 186Coleus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186Zinnia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 186Arabidopsis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

APPROACHES USED FOR STUDYINGVASCULAR DEVELOPMENT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

VISUALIZATION OF VASCULAR TISSUES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 188PROCESSES OF VASCULAR DIFFERENTIATION. . . . . . . . . . . . . . . . . . . . . . . . . 188

Formation of Procambium and Vascular Cambium. . . . . . . . . . . . . . . . . . . . . . . . . 188Initiation of Xylem Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 190Cell Elongation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192Secondary Wall Thickening. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 192Cell Death . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

VASCULAR PATTERN FORMATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193Vascular Bundles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

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Vascular Patterning at the Organ Level. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 195CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 197

INTRODUCTION

Plant vascular tissues, xylem and phloem, evolved as early as the Silurian periodsome 430 million years ago. Evolution of vascular tissues solved the problem oflong-distance transport of water and food, thus enabling early vascular plants togradually colonize the land (71). In primitive vascular plants, vascular tissues areorganized in a simple pattern such that xylem is located at the center and phloemsurrounds xylem. With the evolution of diverse vascular plants, vascular tissues alsoevolved to have a variety of organizations (28). In a given cross section of primarystems and roots, the most prominent variation of anatomical structures amongdifferent species is the organization of vascular tissues. In the stems of woodyplants, the vascular tissue, secondary xylem or wood, provides both mechanicalstrength and long-distance transport of water and nutrients, which enables shootsof some woody plants to grow up to 100 m tall. Vascular tissues have long beenchosen as a model for study of cell differentiation (48, 73, 79). In this review,I first briefly describe the general anatomical features of vascular tissues thatwill be useful to readers who are not familiar with this subject, and then devotemy discussion mainly to the latest progress and current status of the study ofvascular differentiation and pattern formation. For additional information, readersare referred to several recent excellent reviews that cover additional aspects ofvascular differentiation and pattern formation (9, 11–13, 23, 34, 35, 64, 74, 78).

VASCULAR TISSUES

Vascular tissues are composed of two basic units, xylem and phloem. Xylem trans-ports and stores water and nutrients, transports plant hormones such as abscisic acidand cytokinin, and provides mechanical support to the plant body. Phloem providespaths for distribution of the photosynthetic product sucrose and for translocationof proteins and mRNAs involved in plant growth and development. Xylem iscomposed of conducting tracheary elements and nonconducting elements such asxylary parenchyma cells and xylary fibers. Tracheary elements in angiospermstypically are vessel elements that are perforated at both ends to form continuoushollow columns called vessels (Figure 1a). Tracheary elements in gymnospermsare tracheids that are connected through bordered pits to form continuous columns.Phloem is composed of conducting sieve elements and nonconducting cells suchas parenchyma cells and fibers. Sieve elements of nonflowering plants are sievecells that are connected with each other through sieve areas. Sieve elements ofmost flowering plants are sieve tube members that are connected through sieveplates to form continuous columns (28, 58).

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VASCULAR TISSUE DIFFERENTIATION 185

Vascular tissues can be formed from two different meristematic tissues, pro-cambium and vascular cambium. During the primary growth of stems and roots,procambial initials derived from apical meristems produce primary xylem andprimary phloem. Vascular cambium initials, which are originated from procam-bium and other parenchyma cells when plants undergo secondary growth, giverise to secondary xylem, commonly called wood, and secondary phloem. Vascularcambium is typically composed of two types of initials: fusiform initials that pro-duce tracheary elements and xylary fibers in the longitudinal system of wood andray initials that produce ray parenchyma cells in the transverse system of wood(28, 58).

VASCULAR PATTERNS

Vascular Tissue Organization Within a Vascular Bundle

There is great plasticity in the organization of vascular tissues within a vascularbundle as long as vascular tissues are functional for transport. The common vas-cular organization within a bundle is a parallel placement of xylem and phloem,a pattern called collateral vascular bundles (Figure 1c). In some families such asCucurbitaceae and Solanaceae, xylem is placed in parallel with external phloemand internal phloem, a pattern called bicollateral vascular bundles. Several less-common vascular tissue organizations were also evolved in vascular plants. In somemonocot plants such asAcorusandDracaena, phloem is surrounded by a con-tinuous ring of xylem, a pattern called amphivasal vascular bundles (Figure 1d ).In contrast, amphicribral vascular bundles, which are found in some angiospermsand ferns, have xylem surrounded by a ring of phloem (58).

Vascular Tissue Organization at the Organ Level

Conducting elements of xylem and phloem form continuous columns, a vascularsystem throughout the plant body for transport of water, nutrients, and food. Sim-ilar to the diverse organizations of vascular tissues seen within vascular bundles,vascular plants have also evolved a diversity of patterns for placement of vascularbundles in the stele. In primary stems and roots, two major patterns for placementof vascular bundles are recognized. One is the protostele in which xylem forms asolid mass at the center of the stele and phloem surrounds xylem. This is consid-ered to be a primitive type of vascular pattern that is commonly seen in shoots ofmany nonseed vascular plants and in the primary roots of many dicot plants. Theother is the siphonostele in which individual vascular bundles are arranged in thestele. Based on the arrangement of vascular bundles in the stele, siphonostele isgenerally grouped into two major patterns. In one, vascular bundles are organizedas a ring in the stele, a pattern called eustele, which is mainly seen in stems of dicotsand in roots of monocots. In the other, vascular bundles are scattered throughoutthe ground tissue, a pattern called atactostele, which is commonly seen in stems

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of monocot plants. Siphonostele may have evolved from the protostele by gradualreplacement of the solid mass of xylem at the center with parenchyma cells (58).

In leaves, vascular bundles, commonly called veins, are organized in distinctpatterns among different species. Leaves of most dicot plants have a midvein and anetwork of minor veins. Leaves of most monocot plants typically have veins run inparallel. Ginkgo leaves have an open dichotomous venation pattern. Many subtlevariations of leaf venation patterns among different species have been recorded(76).

MODEL SYSTEMS FOR STUDYING VASCULARDEVELOPMENT

Coleus

It is apparent that the complexity of vascular tissues and their organizations presentsa big challenge for studying the molecular mechanisms underlying vascular dif-ferentiation and pattern formation. At the same time, vascular tissues represent amodel for understanding many aspects of fundamental biological questions regard-ing cell specification, cell elongation, cell wall biosynthesis, and pattern formation.To study the different aspects of vascular development, it is ideal to choose simpleor genetically manipulable systems. One of the early systems used for vascularstudy is Coleus in which the stems were used to study roles of auxin and cytokininin the induction of xylem and phloem formation (3, 4). The advantage of Coleus isthat the stems are big enough for easy excision of vascular tissues and subsequentanalysis of effects of external factors on vascular differentiation. However, thissystem has been limited to physiological studies.

Zinnia

Tissue culture has long been used to study the effects of hormones on xylem andphloem differentiation (3). The most remarkable in vitro system developed so faris the zinnia in vitro tracheary element induction system (34). In this system, iso-lated mesophyll cells from young zinnia leaves can be induced to transdifferentiateinto tracheary elements in the presence of auxin and cytokinin (Figure 1b). Theadvantage of this system is that isolated mesophyll cells are nearly homogeneous,and the induction rate of tracheary elements can reach up to 60%. Thus the bio-chemical and molecular changes associated with the differentiation of a single celltype, tracheary elements, can be monitored. A number of genes associated withtracheary element formation have been isolated and characterized by using thissystem (34, 61). The zinnia in vitro tracheary element induction system presentsan excellent source for isolation of genes essential for different aspects of tra-cheary element differentiation, including cell specification, patterned secondarywall thickening, and programmed cell death.

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Arabidopsis

With the introduction of the model plantArabidopsisas a genetic system for study-ing plant growth and development,Arabidopsishas been adopted as a powerfulsystem for genetic dissection of vascular differentiation and pattern formation. Un-like the zinnia system, which is limited to the study of one cell-type differentiation,Arabidopsiscan be used to study not only the differentiation of multiple cell typesin the vascular tissues but also vascular differentiation and pattern formation atthe organ level. Recent studies ofArabidopsismutants have opened new avenuesfor understanding the molecular mechanisms regulating various aspects of vas-cular development, such as alignment of vascular strands (17, 69), formation of anetwork of veins in leaves (16, 18, 19, 24, 43, 52, 69), division of procambial cells(55, 81), differentiation of primary and secondary xylem (36, 105), and organiza-tion of vascular tissues within the bundles in leaves (59, 60, 95, 96, 104) and stems(104). It is apparent that theArabidopsissystem is still not fully exploited, andnovel mutant-screening approaches should be employed to isolate more mutantsaffecting various aspects of vascular differentiation and pattern formation.

APPROACHES USED FOR STUDYINGVASCULAR DEVELOPMENT

Vascular development has traditionally been studied using physiological, biochem-ical, and molecular approaches. Early physiological studies have established thatthe plant hormones auxin and cytokinin are important for vascular differentiation(3, 77). A number of proteins and genes involved in different stages of trachearyelement formation such as secondary wall thickening and cell death have beencharacterized using biochemical and subtractive hybridization approaches (34).

With the recent advance of molecular tools and the introduction of theAra-bidopsisgenetic system, many new approaches have been applied to the researchof vascular differentiation. One powerful approach that goes beyondArabidopsisis the large-scale sequencing of the expressed sequences from cambium and sec-ondary xylem of pine (2) and poplar (86). Categorization of the genes expressed inthe vascular cambium and secondary xylem by microarray technology (42a) willprovide invaluable tools for further study of proteins involved in the differentiationof different cell types in wood. A similar approach using PCR-amplified fragmentlength polymorphisms has been applied to the zinnia system for isolation of genesinvolved in the differentiation of tracheary elements (61).

Another powerful approach is to isolate mutants with defects in vascular de-velopment. Isolation of genes that regulate vascular differentiation and patternformation is essential for the study of vascular development because these genescan be used as tools for isolation of upstream and downstream genes by molecularand genomic approaches such as direct target screening, microarray, and yeast two-hybrid analysis. ManyArabidopsismutants affect vascular patterning or normalformation of vascular strands (Tables 1–4), but none completely block the vascular

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cell differentiation, presumably because of the potential lethality to plants. Newmutant-screening approaches such as temperature-sensitive mutants and T-DNAenhancer trap lines should be exploited.

VISUALIZATION OF VASCULAR TISSUES

The most prominent feature of vascular tissues is the presence of tracheary elementswith thickened secondary wall and lignin deposition. Tracheary elements can beeasily visualized by histological staining with dyes such as toluidine blue andphloroglucinol-HCl (66). For large organs such as stems ofArabidopsis, free-handsections stained with the dyes often give satisfactory anatomical images (92). Forhigh resolution, thin or ultrathin sections should be sought (66). For observation ofleaf venation pattern, leaves can be cleared with chloral hydrate and then observedunder light microscope (16, 57). Recently, confocal microscopy, which can givehigh-quality images, has been applied to visualize vascular tissues in leaves androots. After staining with basic Fuchsin, the lignified tracheary elements in leavesand roots can be readily seen under a confocal microscope (17, 25).

Molecular markers can be used to visualize the differentiation of vascular tis-sues. For example, the promoters ofATHB8(6) and phosphoinositol kinase (27)genes, which are expressed in procambial cells, can be used as early markers of vas-cular differentiation. The promoter ofTED3gene, which is specifically expressedin xylem cells (44), can be used as a marker of xylogenesis.

PROCESSES OF VASCULAR DIFFERENTIATION

Owing to the existence of multiple cell types and various organizations of vasculartissues, one can imagine that the molecular mechanisms controlling the vas-cular differentiation are also complicated, and many genes may be involved invascular development. Because most of the research on vascular differentiationhas been focused on xylem differentiation and very few studies have been doneon phloem differentiation (90), I focus my discussion on the processes of xylemformation as follows: formation of procambium and vascular cambium, initiationof xylem differentiation, cell elongation, secondary wall thickening, and cell death.

Formation of Procambium and Vascular Cambium

Vascular tissues are differentiated from meristematic cells: procambial cells duringprimary growth and vascular cambium cells during secondary growth. Procambialcells in roots and stems are derived from apical meristems. Procambial cells inleaves are formed during very early stages of leaf development. It is clear that thesites for procambial cell initiation determine the pattern of vascular organizationand that the activity of procambial cells controls the differentiation of vasculartissues. The central question is how molecular signals mediate the initiation of

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procambial cells and promote their division, which continuously provides precur-sor cells for differentiation of xylem and phloem.

It has long been proposed that auxin, which is polarly transported from shootapical meristem and young leaves, induces formation of procambial cells. Earlyphysiological studies have clearly demonstrated that the signals for induction ofprocambial cell formation are derived from apex and that exogenous auxin couldreplace the function of apex in the induction of procambial cell formation (3, 77).Roles of auxin in the induction of procambial cell formation have been supported bygenetic studies inArabidopsismutants. Mutation of theMPgene, which encodes anauxin-response factor, disrupts the normal formation of continuous vascular strands(10, 41, 69). Mutants such aspin1(36, 67) andgnom(52, 85) with defects in auxinpolar transport show dramatic alterations in vascular differentiation. ThePIN1geneencodes an auxin efflux carrier (36), and theGNOMgene encodes a membrane-associated guanine-nucleotide exchange factor for an ADP-ribosylation factor Gprotein that is required for the coordinated polar location of PIN1 protein (85).Further studies on the roles of additional auxin polar transport carriers and auxinresponse factors will help us understand the roles of auxin in procambial cellformation.

Cytokinin is essential for promoting the division of procambial cells (3). Mu-tation of theWOL/CRE1gene, which encodes a cytokinin receptor (47, 55), leadsto differentiation of all procambial cells into protoxylem (55, 81). Crossing ofwolwith fass, a mutant with supernumerary cell layers, shows that WOL is not essentialfor phloem and metaxylem formation, indicating that WOL is involved in promo-tion of procambial cell division. WOL is localized in procambial cells in roots andembryos (55). Because there are several other WOL-like cytokinin receptors intheArabidopsisgenome (82), it will be interesting to investigate whether they arealso involved in promoting procambial cell division.

Little is known at the molecular level about how auxin and cytokinin induceprocambial cell formation. Because procambial cells are dividing cells, auxin andcytokinin are likely to stimulate cell proliferation by regulating the cell cycle pro-gression (22a,b). Recently, investigators have shown that an inositol phospholipidkinase, which is involved in the synthesis of phosphoinositide signaling molecules,is predominantly expressed in procambial cells (27). Because auxin induces theformation of phosphoinositides that may be involved in cell proliferation (29),phosphoinositides might be involved in the auxin and cytokinin signal transduc-tion pathways, leading to procambial cell formation. The auxin response factorssuch as MP are obvious candidates for involvement in auxin signaling, and furthercharacterization of their functions will be essential for understanding how auxininitiates procambial cell formation. A number of other genes such asATHB8(6) andOshox1(80) are expressed in procambial cells, but their precise roles in procambialcell formation are not known. Overexpression ofATHB8leads to overproductionof vascular tissues, suggesting that ATHB8 might be involved in stimulation ofprocambial cell activity (7).

Vascular cambium, a lateral meristem, is derived from procambial cells andother parenchyma cells, such as interfascicular cells in stems and pericycle cells

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in roots, when organs initiate secondary growth. Auxin may regulate cambiumactivity (3). Recently, auxin has been shown to be distributed in a gradient acrossthe cambial zone of pine stems (93, 94). In addition, reduction in auxin polartransport in the inflorescence stems of theifl1 mutants leads to a block of vascularcambium activity at the basal parts of stems (103, 105). The block of vascular cam-bium activity in theifl1 mutants is associated with reduced expression of auxinefflux carriers PIN3 and PIN4 (106), suggesting important roles of polar auxinflow in vascular cambium activity. Because many auxin efflux carrier homologueshave been identified in theArabidopsisgenome, it will be important to investi-gate which carriers play central roles in the formation of vascular cambial cells.Induction of vascular cambial cell formation by auxin is likely mediated throughthe protein kinase PINOID (21) because mutation of thePINOID gene completelyabolishes the vascular cambium formation (R. Zhong & Z-H. Ye, unpublished ob-servations). Cytokinin is considered essential for the continuous division of vas-cular cambium cells, which supply precursor cells for differentiation into xylemand phloem (3). BecauseArabidopsisstems and roots undergo secondary growth(7, 26, 102), it will be interesting to investigate whether WOL or other cytokininreceptor homologs are involved in the regulation of vascular cambium cell divisionin Arabidopsis. Dissection of the signaling transduction pathways of auxin and cy-tokinin that lead to vascular cambium formation is essential for our understandingof vascular cambium development.

Initiation of Xylem Differentiation

Procambium and vascular cambium are polar in terms of the final fates of theirdaughter cells. The daughter cells may become either xylem precursor cells orphloem precursor cells, depending on their positions. This suggests that the cam-bial cells at different positions receive different signals that specify different cellfates. Auxin may act as a patterning agent for differentiation of vascular tissues.Auxin is distributed in a gradient across the cambial region (93, 94), indicating thatdifferent levels of auxin together with other signaling molecules such as cytokininare important for vascular cell differentiation (3, 4, 77, 78). Transgenic studies haveshown that alterations of endogenous auxin level dramatically affect xylem for-mation (50, 75). Although the phenotype of thewol mutant suggests that cytokininis not directly involved in xylem differentiation, in vitro studies in zinnia indicatethat both auxin and cytokinin are required for induction of xylem cell formation.It is possible that other WOL-like genes play roles in xylem cell differentiation. Inaddition to auxin and cytokinin, other factors such as brassinosteroid (49, 98, 99)and phytosulfokine, a peptide growth factor (56), might play important roles in thestimulation of xylogenesis.

Little is known about the signal transduction pathways of auxin and cytokinin,which lead to xylem cell formation. MP, an auxin response factor, is likely in-volved in this process because mutation of theMP gene results in misalignedxylem strands (41, 69). Many other auxin response factors have been identified(39), and studies of their functions will likely help us to further understand vascularcell differentiation. Several other transcription factors such asArabidopsisATHB8

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(6, 7), rice Oshox1 (80), and aspen PttHB1 (42) might also play roles in xylemcell differentiation. Auxin-insensitive mutantsaxr6 (43) andbodenlos(40) aredefective in venation pattern, and their corresponding genes are likely involvedin auxin signaling pathways important for vascular differentiation. In addition,the maizewilted mutant causes a partial block of metaxylem cell formation (68)(Figures 2a,b), and theArabidopsis eli1mutant shows discontinuous xylem strands(17). Isolation and functional characterization of these genes will be important forfurther dissection of the molecular mechanisms underlying xylem cell differenti-ation (Table 1).

So far, no mutants with a complete block of xylem cell differentiation have beenisolated presumably because these kinds of mutants are lethal. This greatly hindersthe utilization of the genetic approach to study xylogenesis. One complementaryapproach is to use the zinnia in vitro tracheary element induction system to isolategenes associated with xylogenesis. Because isolated zinnia mesophyll cells canbe induced to transdifferentiate into tracheary elements, this system has long beenexploited to isolate genes involved in different stages of xylogenesis (34). Manygenes that are induced within hours after hormonal treatment have been isolatedin the zinnia system using PCR-amplified fragment length polymorphisms (61).Researchers anticipate that homologous genes will be found inArabidopsisandtheir functions in xylogenesis studied by using T-DNA or transposon knock-outmutants.

TABLE 1 Mutants affecting vascular differentiation

Mutant Species Vascular phenotype Gene product Reference

wilted Maize Disrupted metaxylem differentiation Unknown 68

wilty-dwarf Tomato Compound perforation plate in Unknown 1, 72vessels instead of wild-type simpleperforation plate

wol Arabidopsis Block of procambial cell division Cytokinin receptor 47, 55, 81

mp Arabidopsis Misaligned vessel elements Auxin response factor 10, 41

pin1 Arabidopsis Increased size of vascular bundles Auxin efflux carrier 36, 67in stems

ifl1 Arabidopsis Reduced secondary xylem Homeodomain leucine 105differentiation in stems zipper protein

eli1 Arabidopsis Discontinuous xylem strands Unknown 17

irx1 Arabidopsis Reduced secondary wall formation Cellulose synthase 87, 92in xylem cells catalytic subunit

irx2 Arabidopsis Reduced secondary wall formation Unknown 92in xylem cells

irx3 Arabidopsis Reduced secondary wall formation Cellulose synthase 88, 92in xylem cells catalytic subunit

gpx Arabidopsis Gapped xylem Unknown 91

fra2 Arabidopsis Reduced length of vascular cells Katanin-like microtubule 15severing protein

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Cell Elongation

After initiation of vascular cell differentiation, the conducting cells, tracheary ele-ments in the xylem and sieve elements in the phloem, undergo significant elonga-tion before the tubular conducting system is formed. Because developing conduct-ing cells cease to elongate when the secondary cell wall starts to be laid down (1),which is typical of diffuse cell elongation, the molecular mechanisms regulatingthe elongation of conducting cells are likely similar to those for other nonvascularcells. A katanin-like microtubule-severing protein AtKTN1 is important for thenormal elongation of both xylem and phloem cells (15), indicating that micro-tubules regulate cell elongation in vascular tissues. Microtubules are thought todirect the orientation of cellulose microfibril deposition, which in turn determinesthe axis of cell elongation. Cell elonagtion requires the loosening of the exist-ing cellulose-hemicellulose network, a process mediated by cell wall looseningenzymes such as expansins (22). Expansin mRNA is preferentially localized atthe ends of differentiating tracheary elements in zinnia, suggesting that expansinsare important in the elongation of vessel cells (46). Plant hormones are clearlyinvolved in regulation of vascular cell elongation. Mutation of genes involved inbrassinosteroid biosynthesis results in a dramatic reduction in length of all cellsincluding vascular cells (20).

Secondary Wall Thickening

After elongation, tracheary elements undergo secondary wall thickening withannular, helical, reticulate, scalariform, and pitted patterns (58). The thickenedsecondary wall provides mechanical strength to the vessels for withstanding thenegative pressure generated through transpiration. The patterned secondary wallthickening is regulated through controlled deposition of cellulose microfibrils, aprocess that is apparently regulated by the patterns of cortical microtubules lo-cated underneath the plasma membrane. Pharmacological studies have shown thatdisruption of the cortical microtubule organization completely alters the patternsof secondary wall thickening (30–32). Little is known about how the cortical mi-crotubules form different patterns and how they regulate the patterns of secondarywall thickening. In addition to cortical microtubules, microfilaments also appearto be important for the normal patterning of secondary wall in tracheary elements(51).

There has been a significant progress in the characterization of genes involvedin the synthesis of secondary wall, including synthesis of cellulose and lignin. Sev-eral Arabidopsismutants affecting secondary wall formation have been isolated(91, 92); two of which encode cellulose synthase catalytic subunits that are specif-ically involved in cellulose synthesis in the secondary wall (87, 88). Isolation ofthese genes will further expand our understanding of secondary wall biosynthesis.

Lignin impregnated in the cellulose and hemicellulose network provides addi-tional mechanical strength to the secondary wall and also renders the secondarywall waterproof owing to its hydrophobic nature. Monolignols are synthesized

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through the phenylpropanoid pathway and are exported into the secondary wallwhere they are polymerized into lignin polymers. Most genes involved in mono-lignol biosynthesis have been isolated and characterized, and readers are referredto a recent review on this topic (97).

Cell Death

After fulfilling cellular activities necessary for building up a secondary wall, devel-oping tracheary elements undergo cell death to remove their cellular contents, andin the case of vessel elements, their ends are perforated to form tubular columnscalled vessels. The ends of vessel elements can be perforated with a single hole,a pattern called simple perforation plate, or with more than one hole, a patterncalled complex perforation plate (28). Perforation sites contain only the primarywall that is digested by cellulase during autolysis, whereas the secondary wallimpregnated with lignin is resistant to cellulase attack. However, to date, no cel-lulase genes have been shown to be specifically expressed at the late stages ofxylogenesis. Perforation plate patterns, whether simple or complex, are controlledby the patterned deposition of secondary wall on both ends of vessel elements. Itis extremely interesting to note that mutation of a gene in the tomatowilty-dwarfmutant (1a, 72) converts the wild-type simple perforation plate in vessels into acompound perforation plate (Figures 2c,d ). Isolation of the corresponding geneshould shed new insight into the mechanisms controlling the patterned secondarywall deposition.

Hydrolytic enzymes including cysteine proteases (8, 45, 65, 101, 102), serineproteases (8, 38, 101, 102), and nucleases (5, 89, 100) are highly induced duringxylogenesis, and they are stored in vacuoles before autolysis occurs (35). Cell deathis initiated by disruption of the vacuole membrane, resulting in release of hydrolyticenzymes into the cytosol (37, 38, 53, 65). One of the biochemical markers forthe cell death of tracheary elements is the degradation of nuclear DNA that canbe detected by terminal deoxynucleotidyl transferase-mediated dUTP nick-endlabeling (37, 63). Little is known about what signals trigger the biosynthesis of abattery of hydrolytic enzymes and the final disruption of vacuoles, except for apossible involvement of calcium influx and an extracellular serine protease in theinitiation of cell death of tracheary elements (38).

VASCULAR PATTERN FORMATION

Vascular Bundles

Vascular tissues, xylem and phloem, within a vascular bundle can be organizedinto distinctive patterns, such as collateral, amphivasal, and amphicribral bundles.Recent genetic analysis has begun to unravel the molecular mechanisms under-lying vascular pattern formation. Studies from three mutants have revealed thatthe vascular tissue organization within the bundles is controlled by positional

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TABLE 2 Mutants affecting vascular tissue organization within vascular bundles


phan Antirrhinum Amphicribral vascular bundles MYB transcription factor 95, 96in leaves instead of wild-typecollateral vascular bundles

phb-1d Arabidopsis Amphivasal vascular bundles Homeodomain leucine 59, 60in leaves instead of wild-type zipper proteincollateral vascular bundles

avb1 Arabidopsis Amphivasal vascular bundles Homeodomain leucine 104in leaves and stems instead of zipper proteinwild-type collateral vascular bundles

information (Table 2). InArabidopsisleaves, vascular tissues within a bundle areorganized as collateral, i.e., xylem is parallel to phloem. In the bundle, xylem ispositioned next to the adaxial side of leaves, and phloem is positioned next to theabaxial side of leaves. The leaves ofArabidopsis phb-1dmutant, which exhibits aloss of abaxial characters, have amphivasal vascular bundles, i.e., xylem surroundsphloem (59). Similarly, in the leaves of theArabidopsis avb1mutant, which showsa partial loss of leaf polarity (R. Zhong & Z-H. Ye, unpublished observations),the collateral vascular bundles are transformed into amphivasal bundles (104). Incontrast, in the leaves of theAntirrhinum phanmutant, which causes a loss ofadaxial cell fate, the collateral vascular bundles are transformed into amphicribralbundles, i.e., phloem surrounds xylem (95). This suggests that, when the positionalinformation that determines the normal placement of xylem is disrupted, xylemforms a circle around phloem by default, as seen in thephb-1dandavb1mutants.Similarly, when the positional information that determines the normal placementof phloem is disrupted, phloem forms a circle around xylem by default, as seenin thephanmutant. This also indicates that similar positional information is uti-lized by plants to control leaf polarity and vascular tissue organization in leaves.ThePHB (60) andAVB1(R. Zhong & Z-H. Ye, unpublished observations) geneshave been cloned, and they encode proteins belonging to a family of homeodomainleucine-zipper transcription factors. ThePHANgene encodes a MYB transcriptionfactor (96). With the availability of these molecular tools, it will be possible to fur-ther investigate how these transcription factors regulate the positional signals thatdirect various organizations of vascular tissues. Because auxin and cytokinin areinducers of vascular differentiation, it is reasonable to propose that the positionalinformation might regulate the positions of the hormonal flow that determine theformation of various vascular tissue organizations.

In Arabidopsisinflorescence stems, the vascular tissues within a bundle arealso organized as collateral. In the bundle, xylem is positioned next to the cen-ter of stems, and phloem is positioned next to the periphery (Figure 1c). In thestems of theavb1mutant, the normal collateral placement of xylem and phloemis disrupted, leading to formation of amphivasal vascular bundles with xylem

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surrounding phloem (104) (Figure 1d ). This suggests that leaves and stems mightshare the same molecular mechanisms in controlling the organization of vasculartissues.

Vascular Patterning at the Organ Level

At the organ level, vascular tissues can be arranged in a variety of patterns. Inprimary stems and roots, vascular bundles can be organized as a single ring or ina scattered pattern. In stems and roots with secondary growth, vasculature can beorganized as a single ring, multiple concentric rings, multiple separated rings, ormultiple scattered bands (58). In leaves, vascular bundles, often called veins, formdiverse patterns such as parallel and networked arrangements. The positions of thepolar auxin flow may determine the pattern of vascular tissues at the organ level(77, 78). This proposal has been supported by both pharmacological and geneticstudies inArabidopsis. Alteration of auxin polar transport by auxin polar trans-port inhibitors (57, 83) and by mutation of genes affecting auxin polar transport(12, 57) dramatically alters the venation pattern inArabidopsisleaves. With theidentification of all putative auxin efflux carriers in theArabidopsisgenome, it isnow possible to further investigate the roles of these carriers in determining thevascular patterns in different organs.

Genetic analysis has indicated that vascular patterns at the organ level are alsoregulated by positional information (Tables 3 and 4). Mutation of theArabidopsisAVB1gene not only transforms the collateral vascular bundles into amphivasalbundles, but also disrupts the ring-like organization of vascular bundles in stems(104). In theavb1mutant, multiple bundles are branched into the pith, a patternreminiscent of those seen in the monocot stems. This suggests that, when the posi-tional information that determines the ring-like vascular organization is disrupted,additional vascular bundles are formed in pith by default, as seen in theavb1mu-tant. It will be interesting to investigate the distribution patterns of auxin effluxcarriers in theavb1mutant. The importance of positional information in regulatingvascular patterning is also demonstrated by several organ polarity mutants suchas theyabby(84) andago1(14) mutants. These mutants exhibit altered venationpatterns in leaves. TheYABBYgenes encode putative transcription factors (84),and theAGOgene encodes a protein with unknown functions (14).

A number of other mutants affecting vascular patterning have been isolated(Tables 3 and 4). Most of these mutants were isolated based on alterations of the

TABLE 3 Mutants affecting vascular patterns in stems and roots


avb1 Arabidopsis Disruption of the ring-like vascular Homeodomain leucine 104bundle organization in stems zipper protein

lsn1 Maize Disorganization of vascular Unknown 54bundles in roots and scutellar nodes

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TABLE 4 Mutants affecting leaf venation patterns


midribless Pearl millet Lack of midrib Unknown 70

mbl Panicum maximumLack of midrib Unknown 33

lop1 Arabidopsis Midvein bifurcation, Unknown 19discontinuous and reducednumber of veins

mp Arabidopsis Discontinuous and reduced Auxin response factor 10, 41number of veins

bdl Arabidopsis Discontinuous and reduced Unknown 40number of veins

ago Arabidopsis Reduced number of veins Protein with unknown 14identity

fil-5 yab3-1 Arabidopsis Reduced number of veins Transcription factors 84

cvp1, cvp2 Arabidopsis Discontinuous and reduced Unknown 18number of veins

van1, van2 Arabidopsis Discontinuous and reduced Unknown 52van3, van4 number of veinsvan5, van6

gnom/van7 Arabidopsis Discontinuous and reduced Guanine-nucleotide 52, 85number of veins exchange factor

sfc Arabidopsis Discontinuous and reduced Unknown 24number of veins

axr6 Arabidopsis Discontinuous and reduced Unknown 43number of veins

hve Arabidopsis Reduced number of veins Unknown 16

ixa Arabidopsis Reduced number of veins Unknown 16and free-ending vascularstrands

ehy Arabidopsis Exess of hydathodes Unknown 16

pin1 Arabidopsis Reduced number of veins Auxin efflux carrier 12

ifl1 Arabidopsis Reduced number of veins Homeodomain leucine 105zipper protein

venation pattern in cotyledons or leaves. These mutations cause discontinuous,random, or reduced numbers of veins (16, 18, 24, 33, 52, 70). Recently, a maizemutant with an alteration of vascular patterns in roots and scutellar nodes has beendescribed (54). All these vascular pattern mutants also display defects in otheraspects of plant growth and development, indicating that the genes affected areinvolved in multiple processes important for normal plant development. Isolationof the corresponding genes in these mutants and further characterization of theirfunctions will undoubtedly contribute to the dissection of pathways involved invascular pattern formation.

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CONCLUSIONS

Significant progress has been made in our understanding of vascular differentia-tion and pattern formation, which lays a foundation for further dissecting thesecomplicated processes at the molecular level. The isolation of genes involved inauxin polar transport and signaling of auxin and cytokinin will help us to inves-tigate how auxin polar flow is spatially regulated and how auxin and cytokininsignals are transduced to induce vascular differentiation. With the availability ofmany vascular pattern mutants and further characterization of their correspond-ing genes, it will soon be possible to investigate how positional signals determinethe organization of vascular tissues. Although the zinnia system will still be animportant player in the search for genes specifically involved in tracheary ele-ment formation, the model plantArabidopsisis undoubtedly a powerful geneticsystem for investigating the molecular mechanisms regulating different aspectsof vascular differentiation and pattern formation. Because the inflorescence stemsand roots ofArabidopsisundergo secondary growth,Arabidopsisis also a usefulgenetic tool for studying wood formation. It is anticipated that a combined appli-cation of molecular, genetic, genomic, cellular, and physiological tools will soonlead to many exciting discoveries regarding the molecular mechanisms underlyingvascular tissue differentiation and vascular tissue patterning.

ACKNOWLEDGMENTS

Work in the author’s laboratory was supported by a grant from the Cooperative StateResearch, Education, and Extension Service, U.S. Department of Agriculture.

Visit the Annual Reviews home page at www.annualreviews.org

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Figure 1 Anatomy of vascular tissues. (a) Longitudinal section of anArabidopsisstem showing vessels (arrow). (b) Tracheary elements differentiated from isolatedzinnia mesophyll cells. (c) Cross section of the wild-typeArabidopsisstem showinga collateral vascular bundle. (d) Cross section of theArabidopsis avb1mutant stemshowing an amphivasal vascular bundle. ph, phloem; x, xylem. Figures 1c andd werereproduced with permission from (104).

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Figure 2 Anatomical phenotypes of two vascular mutants. (a) Cross section of thewild-type maize stem showing two prominent metaxylem cells (arrows) in a vascularbundle. x, protoxylem. (b) Cross section of the maizewiltedmutant stem showing theabsence of metaxylem cells in a vascular bundle. (c) Cross section of the wild-typetomato stem showing the simple perforation plate (arrow) in a vessel. (d) Cross sectionof the tomatowilty-dwarf mutant showing a compound perforation plate (arrow) in avessel. Figures 2a andb were reproduced with permission from (68). Figures 2c anddwere reproduced with permission from (1).

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March 14, 2002 11:24 Annual Reviews AR156-FM

Annual Review of Plant BiologyVolume 53, 2002

CONTENTS

Frontispiece—A. A. Benson xii

PAVING THE PATH, A. A. Benson 1

NEW INSIGHTS INTO THE REGULATION AND FUNCTIONALSIGNIFICANCE OF LYSINE METABOLISM IN PLANTS, Gad Galili 27

SHOOT AND FLORAL MERISTEM MAINTENANCE IN ARABIDOPSIS,Jennifer C. Fletcher 45

NONSELECTIVE CATION CHANNELS IN PLANTS, Vadim Demidchik,Romola Jane Davenport, and Mark Tester 67

REVEALING THE MOLECULAR SECRETS OF MARINE DIATOMS,Angela Falciatore and Chris Bowler 109

ABSCISSION, DEHISCENCE, AND OTHER CELL SEPARATION PROCESSES,Jeremy A. Roberts, Katherine A. Elliott, and Zinnia H. Gonzalez-Carranza 131

PHYTOCHELATINS AND METALLOTHIONEINS: ROLES IN HEAVY METALDETOXIFICATION AND HOMEOSTASIS, Christopher Cobbettand Peter Goldsbrough 159

VASCULAR TISSUE DIFFERENTIATION AND PATTERN FORMATIONIN PLANTS, Zheng-Hua Ye 183

LOCAL AND LONG-RANGE SIGNALING PATHWAYS REGULATINGPLANT RESPONSES TO NITRATE, Brian G. Forde 203

ACCLIMATIVE RESPONSE TO TEMPERATURE STRESS IN HIGHERPLANTS: APPROACHES OF GENE ENGINEERING FOR TEMPERATURETOLERANCE, Koh Iba 225

SALT AND DROUGHT STRESS SIGNAL TRANDUCTION IN PLANTS,Jian-Kang Zhu 247

THE LIPOXYGENASE PATHWAY, Ivo Feussner and Claus Wasternack 275

PLANT RESPONSES TO INSECT HERBIVORY: THE EMERGINGMOLECULAR ANALYSIS, Andre Kessler and Ian T. Baldwin 299

PHYTOCHROMES CONTROL PHOTOMORPHOGENESIS BYDIFFERENTIALLY REGULATED, INTERACTING SIGNALINGPATHWAYS IN HIGHER PLANTS, Ferenc Nagy and Eberhard Schafer 329

vi

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March 14, 2002 11:24 Annual Reviews AR156-FM

CONTENTS vii

THE COMPLEX FATE OF α-KETOACIDS, Brian P. Mooney, Jan A. Miernyk,and Douglas D. Randall 357

MOLECULAR GENETICS OF AUXIN SIGNALING, Ottoline Leyser 377

RICE AS A MODEL FOR COMPARATIVE GENOMICS OF PLANTS,Ko Shimamoto and Junko Kyozuka 399

ROOT GRAVITROPISM: AN EXPERIMENTAL TOOL TO INVESTIGATEBASIC CELLULAR AND MOLECULAR PROCESSES UNDERLYINGMECHANOSENSING AND SIGNAL TRANSMISSION IN PLANTS,K. Boonsirichai, C. Guan, R. Chen, and P. H. Masson 421

RUBISCO: STRUCTURE, REGULATORY INTERACTIONS, ANDPOSSIBILITIES FOR A BETTER ENZYME, Robert J. Spreitzerand Michael E. Salvucci 449

A NEW MOSS GENETICS: TARGETED MUTAGENESIS INPHYSCOMITRELLA PATENS, Didier G. Schaefer 477

COMPLEX EVOLUTION OF PHOTOSYNTHESIS, Jin Xiong and Carl E. Bauer 503

CHLORORESPIRATION, Gilles Peltier and Laurent Cournac 523

STRUCTURE, DYNAMICS, AND ENERGETICS OF THE PRIMARYPHOTOCHEMISTRY OF PHOTOSYSTEM II OF OXYGENICPHOTOSYNTHESIS, Bruce A. Diner and Fabrice Rappaport 551

INDEXESSubject Index 581Cumulative Index of Contributing Authors, Volumes 43–53 611Cumulative Index of Chapter Titles, Volumes 43–53 616

ERRATAAn online log of corrections to Annual Review of PlantBiology chapters (if any, 1997 to the present) may befound at http://plant.annualreviews.org/

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