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Plant Physiol. (1999) 120: 53-64 Transformation of the Collateral Vascular Bundles into Amphivasal Vascular Bundles in an Arabidopsis Mutant1
Department of Botany, University of Georgia, Athens, Georgia 30602
Arabidopsis inflorescence stems develop a vascular pattern similar to that found in most dicots. The arrangement of vascular tissues within the bundle is collateral, and vascular bundles in the stele are arranged in a ring. Although auxin has been shown to be an inducer of vascular differentiation, little is known about the molecular mechanisms controlling vascular pattern formation. By screening ethyl methanesufonate-mutagenized populations of Arabidopsis, we have isolated an avb1 (amphivasal vascular bundle) mutant with a novel vascular pattern. Unlike the collateral vascular bundles seen in the wild-type stems, the vascular bundles in the avb1 stems were similar to amphivasal bundles, i.e. the xylem completely surrounded the phloem. Furthermore, branching vascular bundles in the avb1 stems abnormally penetrated into the pith, which resulted in a disruption in the ring-like arrangement of vascular bundles in the stele. The avb1 mutation did not affect leaf venation pattern and root vascular organization. Auxin polar transport assay indicated that the avb1 mutation did not disrupt the auxin polar transport activity in inflorescence stems. The avb1 mutation also exhibited pleiotropic phenotypes, including curled stems and extra cauline branches. Genetic analysis indicated that the avb1 mutation was monogenic and partially dominant. The avb1 locus was mapped to a region between markers mi69 and ASB2, which is covered by a yeast artificial chromosome clone, CIC9E2, on chromosome 5. Isolation of the avb1 mutant provides a novel means to study the evolutionary mechanisms controlling the arrangement of vascular tissues within the bundle, as well as the mechanisms controlling the arrangement of vascular bundles in the stele.
Vascular plants appeared on the land in the Silurian period
(438-408 million years ago) and they are dominant on the earth. One of
the key events for their successful emergence from aquatic environments
was the evolution of vascular tissues, which solved the problem of
water and food transport on the land (Raven et al., 1992 In primary stems vascular patterns are organized at two levels (Esau,
1977 Second, vascular bundles in the stele of stems are arranged in an
orderly pattern. The protostele is arranged in such a way that the
xylem is located as a solid mass in the center, and the phloem
surrounds this solid mass. However, in siphonosteles, the solid mass of
xylem is separated by parenchyma cells. Vascular bundles are organized
as a ring in the stems of most gymnosperms and dicots or distributed
throughout the ground tissue in the stems of most
monocots.
Although the molecular mechanisms determining vascular patterns are
largely unknown, the aspects of vascular differentiation have been
intensively studied using physiological, biochemical, and molecular
approaches. It has been shown that auxin is the major controlling
factor for induction of vascular differentiation in both in vitro and
in vivo conditions (Aloni, 1987 Because of the lack of tools to study vascular patterning, no
regulatory genes controlling the organization of vascular tissues have
been identified. Nevertheless, a number of genes associated with xylem
and phloem differentiation have been characterized. Through
differential screening and subtractive hybridization, a number of cDNAs
whose mRNAs were differentially expressed during xylogenesis were
isolated from in vitro tracheary elements induced from isolated zinnia
mesophyll cells (Demura and Fukuda, 1993 Considering the existence of naturally diverse vascular patterns among
plant groups, we can study the genetic control of vascular pattern
formation by mutational analysis. A number of mutants affecting
formation of midvein or minor veins in leaves have been isolated in
grasses (for review, see Nelson and Dengler, 1997 In summary, the vascular mutants isolated so far affect vascular
differentiation or leaf venation. To our knowledge, no mutants with a
global alteration in vascular patterns of Arabidopsis stems have been
reported. To better understand the mechanisms controlling vascular
patterns, it is important to isolate mutants with a global alteration
in vascular patterns.
Intrigued by the diverse patterns of vascular tissues in vascular
plants, we have initiated a genetic approach to studying vascular
pattern formation in the model dicot Arabidopsis. By screening
ethyl methanesulfonate-mutagenized populations of Arabidopsis, we have
successfully isolated a novel mutant with a dramatic change of vascular
patterns in stems. The most noticeable change in the avb1
mutant was the transformation of the collateral vascular bundles into
amphivasal vascular bundles in the stems. Also altered in the
avb1 mutant was the arrangement of vascular bundles in the
stele. Isolation of the avb1 mutant provided a tool for
investigating the evolutionary mechanisms of vascular pattern
formation.
Mutant Screening
Light Microscopy Arabidopsis stem segments were fixed overnight in 4% paraformaldehyde at 4°C. After dehydration through a gradient series of ethanol, the stem segments were embedded in paraffin. The embedded segments were then sectioned with a microtome and thin sections were transferred onto poly-L-Lys-coated slides. After deparaffinizing in xylene and rehydration through a gradient series of ethonal, sections were stained with toluidine blue and observed under a compound microscope with bright-field illumination.Evans Blue Dye Transport Inflorescence stems were cut under water and the lower ends of stems were then submerged in a 0.1% Evans blue dye solution. After 10 min, serial sections were prepared from the upper part of the stems (not submerged in the solution). The sections were observed immediately under a dissection microscope with dark-field illumination or stained with phloroglucinol-HCl before observation.Auxin Polar Transport Assay Inflorescence stems of 6-week-old plants were used for the auxin polar transport activity assay as described previously by Okada et al. (1991) . Stem segments were cut into 2.5-cm lengths and the upper ends
were submerged in a Murashige and Skoog medium containing 80 nCi
mL 1 [1-14C]IAA
(American Radiolabeled Chemicals, St. Louis, MO). After 6- or 20-h
incubations, 0.5-cm-long parts (not submerged in the solution) were cut
from the opposite ends of segments. The cut parts were incubated
overnight in a scintillation cocktail and shaken, and the radioactivity
was measured in a scintillation counter.
Genetic Analysis The mutant was backcrossed with wild-type Columbia. Stem sections of the F1 plants were stained with toluidine blue to examine vascular patterns. After the F1 plants were selfed, the F2 plants were analyzed for segregation of the mutation by examining the vascular patterns of stem sections.
Vascular Development in Wild-Type Arabidopsis Stems Wild-type Arabidopsis inflorescence stems developed a vascular pattern similar to that found in most dicots (Fig. 1A). In the stele the vascular bundles were arranged in a ring. Typically, about eight discrete vascular bundles developed in the top part of the stem. During the maturation of the stems interfascicular fibers differentiated between vascular bundles to form a continuous ring of sclerified cells (Zhong et al., 1997). Within the vascular bundle, the arrangement of vascular tissues
was collateral, i.e. xylem was located on the inner side of the bundle
and phloem was located on the outer side of the bundle (Fig. 1, A and
C). It was obvious that one to two layers of cambial initials were
present in the vascular bundle of an old stem (Fig. 1C), indicating
that the bundle retained the potential for further growth. The
arrangements of vascular tissues within the bundle and of vascular
bundles in the stele were consistent throughout the development of
stems.
Isolation of a Mutant with an Altered Vascular Pattern in Stems To understand the genetic control of vascular pattern formation, we screened ethyl methanesulfonate-mutagenized M2 populations of Arabidopsis ecotype Columbia for mutants with altered vascular patterns. Inflorescence stems of 8-week-old plants were free-hand sectioned and stained with toluidine blue to reveal vascular patterns. After screening 100,000 M2 plants, we isolated an avb1 (amphivasal vascular bundle) mutant with a dramatic change of vascular patterns in stems (Fig. 1B).
Origin of the Extra Bundles in the Pith
Vascular Organization in Leaves and Roots of the avb1 Mutant We examined further the vascular patterns in leaves and roots. Veins in the wild-type leaves formed a continuous reticulum (Fig. 3A). A similar venation pattern was seen in the avb1 mutant (Fig. 3B), indicating that the avb1 mutation did not alter the leaf venation pattern. However, the avb1 mutation altered the arrangement of vascular tissues within leaf veins. The organization of vascular tissues within the bundles of wild-type leaves was collateral (Fig. 3C), a pattern similar to that in the wild-type stems (Fig. 1C). In the vascular bundles of avb1 leaves, a layer of vessel elements formed a ring (Fig. 3D), a pattern similar to that seen in the vascular bundles of the avb1 stems (Fig. 1D). This indicated that the avb1 mutation affected the arrangement of vascular tissues within the bundles in both stems and leaves.
Functional Analysis of Vascular Bundles in the Mutant Because some vascular bundles were abnormally positioned in the avb1 internodes, we examined whether they were all functional for transport. To do this, a stem of the avb1 mutant was cut and the basal end was immersed in an Evans blue solution. After a 10-min incubation the upper part of the stem, which was not submerged in the dye, was sectioned to examine the presence of the dye in vascular bundles. If the vessel elements were connected to each other, the Evans blue dye should have been transported to the upper part of the stem through the vessels. The blue dye was seen in every vascular bundle in the stem section of the avb1 mutant (Fig. 3G). The Evans blue-staining pattern was the same as the distribution pattern of vascular bundles (Fig. 3H), indicating that vessels in each vascular bundle of the mutant are functional for transport and that the vascular strands are interconnected.Morphology of the avb1 Mutant The avb1 mutation changed the morphology of the plant (Fig. 4). The wild-type inflorescence stems were straight (Fig. 4A). The lower part of the stems had regularly spaced cauline leaves and branches (Fig. 4, A and C). No difference was observed at the top part of the stems between the wild type and the avb1 mutant (Fig. 4, A and B). However, the morphology of the lower part of the stems was altered in the mutant. In the avb1 mutant, the main inflorescence stem was curled and more cauline leaves and branches were produced with irregular spacing along the lower part of the stem (see arrow in Fig. 4D). Frequently, several branches emerged next to each other on the stem (Fig. 4D), and occasionally the cauline leaf blade was fused along the internode to the next node (data not shown).
Auxin Polar Transport in avb1 Stems Auxin has been shown to be required for vascular differentiation (Aloni, 1987) and several mutants with defects of vascular differentiation were shown to be associated with reduced auxin polar
transport in stems (Carland and McHale, 1996; Przemeck et al., 1996).
Because the avb1 mutant showed a dramatic alteration in
vascular patterns, it is important to investigate whether the mutation
affected the auxin polar transport activity in the stems. As shown in
Figure 5, the auxin polar transport assay
showed that the basipetal auxin transport activity in the stems of the
avb1 mutant was the same as that in the stems of the wild
type. The auxin transport activity in both mutant and wild-type stems
was effectively inhibited by the auxin polar transport inhibitor
2,3,5-triiodobenzoic acid. These results indicated that the alteration
in vascular patterns in the avb1 mutant was not accompanied
by a disruption in auxin polar transport activity.
Genetic Analysis of the avb1 Mutant We tested whether the mutation was dominant or recessive. The avb1 mutant was backcrossed with wild-type Arabidopsis ecotype Columbia. The stems of F1 plants (total of 50 plants) were examined for vascular patterns. In the stems of F1 plants, one to three bundles were amphivasal; the other bundles were the same as those seen in the wild type. No extra bundles were seen in the pith (Fig. 2B; Table I). A minor alteration of vascular patterns occurred in the F1 heterozygotes, suggesting that the mutation is partially dominant.
Stems of most dicots have a similar vascular organization, i.e.
vascular tissues are collateral within the bundle and vascular bundles
collectively are arranged in a ring. This type of vascular pattern was
conserved during the evolution of dicot plants. However, other
vascular patterns have developed in some dicots. For example, bicollateral bundles are common in the families Apocynaceae,
Asclepiadaceae, Compositae, Conolvulaceae, Cucurbitaceae,
Myrtaceae, and Solanaceae. In dicots such as Begonia,
Mesembryanthemum, Rheum, and Rumex, amphicribral
bundles occur as medullary bundles, which run through the pith
(Mauseth, 1988 The Collateral Vascular Bundles Are Transformed into Amphivasal
Vascular Bundles in the avb1 Mutant
Vascular Bundles Abnormally Penetrate into the Pith in the avb1 Mutant The other dramatic change in the avb1 mutant is the abnormal positioning of vascular bundles in the pith of stems, which disrupts the normal arrangement of vascular bundles in the stele of stems. This abnormal pattern resulted from branching of the vascular bundles into the pith (Fig. 2). Although it is not clear whether these branching vascular bundles in the avb1 mutant are leaf or branch traces, leaf and branch traces in the wild type are never seen to penetrate into the pith. Thus, it is obvious that the disruption in the ring-like organization of vascular bundles in the stele of mutant stems resulted from mutation of the AVB1 locus.
Vascular Bundles in the Pith of the avb1 Stems Are Functional for Transport Two lines of evidence indicate that the bundles that appeared in the pith of the mutant stems are connected with normal vascular bundles. Serial sections of the avb1 stems clearly showed that the bundles seen in the pith branched from normal vascular bundles (Fig. 2). Furthermore, the Evans blue dye-transport experiment showed that the bundles in the pith of mutant stems also functioned for transport of the dye (Fig. 3). These results indicate that appearance of vascular tissues in the pith of mutant stems is not due to random differentiation but is coordinated with the differentiation of bundles at the periphery of the stele.Auxin Polar Transport Activity Is Not Altered in the avb1 Mutant It has been demonstrated that the plant hormones auxin and cytokinin are inducers of vascular tissue formation, and the polarity of vascular differentiation is determined by the direction of polar auxin flow (Sachs, 1981; Aloni, 1987). Thus, it is reasonable to
question whether the abnormal vascular patterns seen in the avb1 mutant are due to an alteration in auxin polar
transport. The auxin polar transport activity in the avb1
stems was indistinguishable from that in the wild type (Fig. 5),
indicating that the auxin polar transport activity is not disrupted in
the mutant. This is different from the monopteros and
lop1 mutants, both of which exhibited defects in auxin polar
transport. The lop1 mutant exhibited a bifurcated and
twisted midvein in leaves (Carland and McHale, 1996), whereas the
monopteros mutant altered the alignment and interconnection
of tracheary elements (Przemeck et al., 1996). A number of other
mutants with altered auxin polar transport have been isolated (Okada et
al., 1991; Bennett et al., 1995; Ruegger et al., 1997). These mutants
appeared not to affect the arrangement of vascular tissues, indicating
that an alteration in polar auxin transport activity may not result in
a defect in vascular pattern formation.
The avb1 Mutant Exhibits Pleiotropic Phenotypes In addition to the dramatic alteration in vascular patterns, the avb1 mutant exhibited morphological changes such as curled stems and proliferation of branch stems (Fig. 4). It is not clear whether there is any correlation between the alteration of vascular patterns and the morphological changes. It seems unlikely that the morphological changes directly lead to an alteration in vascular patterns. A number of mutants with dramatic morphological changes, such as a mutant with twisted stems (Feldmann, 1991) and mutants with
faciated stems (Leyser and Furner, 1992; Clark et al., 1993), have been
isolated but no global alteration in vascular patterns were reported in
these mutants. One may argue that proliferation of branch stems may be
related to production of extra vascular bundles in the pith of the
avb1 stems. It is possible that the vascular bundles in the
piths of the avb1 stems are branch traces. However, branch
and leaf traces in the wild-type stems never penetrate into the pith,
indicating that penetration of the extra bundles in the piths of the
avb1 stems unlikely results from the production of extra
branch stems or leaves.
The AVB1 Locus and the Evolution of Amphivasal Vascular Bundles The angiosperms arose in the early Cretaceous period, some 125 million years ago or more (Heywood, 1993). It is considered that the
angiosperms evolved from some primitive gymnosperm (Raven et al.,
1992). The ancient angiosperm "ancestor" was thought to precede the
divergent evolution of monocots and dicots (Langenheim and Thimann,
1982). Because the gymnosperms typically have collateral bundle
patterns in primary vascular tissues of stems, the collateral bundle
pattern might be an ancestral type of vascular bundle in the
angiosperms. The collateral bundle pattern is still dominant in the
angiosperms, and other types of bundles such as amphivasal, amphicribral, or bicollateral bundles arose in a limited numbers of
families. For example, the amphivasal vascular bundles have been seen
only in some monocots (Mauseth, 1988). Plants such as Acorus, Convallaria, and some Xanthorrhoeaceae
have the amphivasal bundles in the primary stems. Plants such as
Aloe arborescens and Dracaena develop secondary
vascular bundles with the amphivasal arrangement.
* Corresponding author; e-mail ye{at}dogwood.botany.uga.edu; fax 1-706-542-1805. Received November 11, 1998;
accepted January 23, 1999.
Abbreviations: BAC, bacterial artificial chromosome. CAPS, codominant cleaved, amplified polymorphic sequence.
We thank the Arabidopsis Biological Resource Center (Ohio State University, Columbus) for providing clones EST34D1 and EST138D19; Glenn Freshour for preparation of sections in Figure 1, C and D; and Dr. Roni Aloni for his suggestions concerning the manuscript. J.J.T. was an undergraduate student at Washington University (St. Louis, MO) when she participated in this project.
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R. Zhong and Z.-H. Ye 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., April 15, 2004; 45(4): 369 - 385. [Abstract] [Full Text] [PDF]
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G. Parker, R. Schofield, B. Sundberg, and S. Turner Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis Development, May 15, 2003; 130(10): 2139 - 2148. [Abstract] [Full Text] [PDF]
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E. Scarpella, S. Rueb, and A. H. Meijer The RADICLELESS1 gene is required for vascular pattern formation in rice Development, February 15, 2003; 130(4): 645 - 658. [Abstract] [Full Text] [PDF]
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J. Booker, S. Chatfield, and O. Leyser Auxin Acts in Xylem-Associated or Medullary Cells to Mediate Apical Dominance PLANT CELL, February 1, 2003; 15(2): 495 - 507. [Abstract] [Full Text] [PDF]
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S. Huang, R. E. Cerny, D. S. Bhat, and S. M. Brown Cloning of an Arabidopsis Patatin-Like Gene, STURDY, by Activation T-DNA Tagging Plant Physiology, February 1, 2001; 125(2): 573 - 584. [Abstract] [Full Text]
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Abstract
Introduction
-amylase (Wang et al.,
1995
-CAACAAGCGAAACTAGGGT-3
