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First published online June 17, 2005; 10.1104/pp.104.057901 Plant Physiology 138:1383-1395 (2005) © 2005 American Society of Plant Biologists
A RING Domain Gene Is Expressed in Different Cell Types of Leaf Trace, Stem, and Juvenile Bundles in the Stem Vascular System of Zinnia1Department of Cell and Developmental Biology, John Innes Centre, Colney, Norwich NR4 7UH, United Kingdom
The in vitro zinnia (Zinnia elegans) mesophyll cell system, in which leaf mesophyll cells are induced to transdifferentiate into tracheary elements with high synchrony, has become an established model for studying xylogenesis. The architecture of the stem vascular system of zinnia cv Envy contains three anatomically distinct vascular bundles at different stages of development. Juvenile vascular strands of the subapical region develop into mature vascular strands with leaf trace segments and stem segments. Characteristic patterns of gene expression in juvenile, leaf trace, and stem bundles are revealed by a molecular marker, a RING domain-encoding gene, ZeRH2.1, originally isolated from a zinnia cDNA library derived from differentiating in vitro cultures. Using RNA in situ hybridization, we show that ZeRH2.1 is expressed preferentially in two specific cell types in mature zinnia stems. In leaf trace bundles, ZeRH2.1 transcript is abundant in xylem parenchyma cells, while in stem bundles it is abundant in phloem companion cells. Both of these cell types show wall ingrowths characteristic of transfer cells. In addition, ZeRH2.1 transcript is abundant in some phloem cells of juvenile bundles and in leaf palisade parenchyma. The complex and developmentally regulated expression pattern of ZeRH2.1 reveals heterogeneity in the vascular anatomy of the zinnia stem. We discuss a potential function for this gene in intercellular transport processes.
Modern dicot angiosperms possess a highly evolved vascular system that is periodically renewed and augmented by the activity of cambial cells (Foster and Gifford, 1959  ). The vascular system is patterned early in embryo development as a central cylinder, with a central core of cambium, surrounded by phloem and xylem. After germination, roots maintain the vasculature as a central strand, but, in the stem, the central vascular cylinder differentiates as a fixed number of vascular strands. This species-specific base number of vascular strands is then maintained by the plant as the minimum number of vascular strands (Esau, 1962). The arrangement of vascular strands is further elaborated by branching and anastomosis to supply lateral organs, like leaves and axillary branches.
The postembryonic development of the stem vascular system results in an anatomically complex structure. Procambial strands at the apical meristem form protoxylem and protophloem elements of young bundles, which are gradually displaced by metaxylem and metaphloem as each stem segment matures. The anatomy of a mature bundle is, therefore, different from that of a young bundle (Esau, 1962
The neighboring parenchyma and companion cells of the conducting elements in the shoot also differentiate. These cells frequently develop wall ingrowths, characteristic of transfer cells. Xylem parenchyma of the leaf traces develop extensive wall ingrowths in the upper internode region. Phloem companion cells develop transfer cells in the nodal complex and are mostly associated with vascular connections to the axillary bud (Gunning et al., 1970 Although the anatomy of the stem vascular system has been meticulously studied, the molecular genetics underpinning its inherent heterogeneity is largely mysterious. In this article, we show how the dynamic nature of vascular development is revealed by the complex expression pattern of the ZeRH2.1 gene.
The ZeRH2.1 gene fragment was isolated during a complementary DNA-amplified fragment length polymorphism (cDNA-AFLP) analysis (Milioni et al., 2002 In this article, we have integrated a detailed anatomical analysis of the zinnia vasculature with gene expression analysis to explain the complex in situ pattern of ZeRH2.1. We describe how the development of the stem vascular system results in differential expression patterns of the ZeRH2.1 gene in anatomically distinct vascular bundles. We propose a role for the ZeRH2.1 gene in intercellular transport processes and in transfer cell function.
Expression Pattern of ZeRH2.1 during Formation of Tracheary Elements in the Zinnia System
Using a cDNA-AFLP approach, Milioni et al. (2002)
We have estimated previously that 80% of the expression patterns observed in cDNA-AFLP gels can be confirmed by reverse transcription (RT)-PCR or northern gel-blot analyses (Milioni et al., 2002 ). The cDNA-AFLP analysis indicated that ZeRH2.1 was first expressed 4 h after addition of auxin and cytokinin to the culture medium in the zinnia system. However, the expression pattern of ZeRH2.1 using RT-PCR is not consistent with the cDNA-AFLP pattern and showed that the gene is expressed in freshly isolated mesophyll cells and at all stages of the time course of tracheary element formation in the zinnia system (Fig. 1D) and also in cultures containing either auxin or cytokinin alone (data not shown).
The term mature zone is used to describe stem sections obtained from any internode between node two and the hypocotyl, counting from the first fully expanded leaf at the shoot apex, as node one (Fig. 2B). Sections were taken from plants with three or four nodes.
The vascular system in the zinnia stem is characteristic of many dicotyledons and forms a hollow cylinder sandwiched between dermal and ground tissue (Sachs, 1875 ). Long-running vascular strands form individual units of the stem vascular system, which are separated by interfascicular regions. These vascular strands are composed of collateral vascular bundles, with phloem located outside the xylem (Fig. 2, A and C). In situ hybridization of the ZeRH2.1 antisense riboprobe with transverse sections from the mature zone of the zinnia stem showed that almost all cells contain low levels of transcript (Fig. 2C). Control experiments using the sense probe showed no detectable signal (data not shown). However, certain cells in the vascular bundles show a much higher abundance of transcript. The expression pattern of ZeRH2.1 in vascular bundles 1, 3, 5, 7, 9, and 11, as numbered in the transverse section shown in Figure 2A, is different from that in the other bundles in the stem (Fig. 2C). Clearly, two classes of vascular bundles are represented in a single transverse section taken from the mature zone of the zinnia stem (Fig. 2C).
To understand the underlying differences between these two classes of vascular bundles, we need to describe the morphology of the vasculature. The arrangement of leaves along the zinnia stem is decussate, with alternating pairs of leaves at right angles to the pairs of leaves at the nodes above and below (Fig. 2B). Each leaf, which is simple, entire, and obtuse, is connected directly to the stem without a petiole and is trilacunar, that is, supplied by three vascular traces, a midrib and two flanking sideribs (Fig. 2B) that are directly connected to the central stem vasculature. In a stem transverse section, therefore, six such vascular bundles will be present and are referred to here as leaf trace bundles (Eames and MacDaniels, 1925 The ZeRH2.1 expression pattern provides a molecular marker that distinguishes the leaf trace bundles from the stem bundles. The leaf trace bundles (Fig. 2, C and D) show enhanced expression of ZeRH2.1 in xylem parenchyma cells, between the rows of xylem conducting elements, but basal levels in phloem cells. However, stem bundles have only basal levels of transcript in their xylem parenchyma cells, but instead have abundant transcript in particular phloem cells (Fig. 2E). At higher magnification (Fig. 2F), the transcript is most abundant in small companion cells next to larger sieve elements. Abundant transcript is also present in some cells in the interfascicular region (Fig. 2, C and G). As shown in Figure 2G, these small cells appear comparable to the companion cells of Figure 2F and may represent young phloem of new developing vascular tissues. Vascular bundles of the hypocotyl do not have abundant transcript in xylem or phloem cells (data not shown).
To explain the distinct labeling pattern of the ZeRH2.1 riboprobe in the two classes of vascular bundles, we analyzed the detailed anatomy of these bundles, using light and electron microscopies. The leaf trace bundle (Fig. 3A) has an arrangement of xylem and phloem cell types very different from that of the stem bundle (Fig. 3D). The phloem of the leaf trace bundle is capped by a larger group of fiber cells and has relatively little active phloem, and the xylem tracheids are arranged in clear radial rows flanked by densely cytoplasmic xylem parenchyma cells (Fig. 3A). At higher magnification, light microscopy (Fig. 3B) and transmission electron microscopy (Fig. 3C) reveal elaborate labyrinthine cell wall invaginations in the xylem parenchyma cells. Cells with this adaptation are commonly known as transfer cells and are characteristic of nodal xylem parenchyma (Pate and Gunning, 1972
By contrast, stem bundles (Fig. 3D) have a smaller proportion of phloem fibers and most of the phloem comprises functional companion cells and sieve tube elements (Fig. 3, H and I). The xylem is arranged in an irregular network of vessels and supporting parenchyma cells, which are not so densely cytoplasmic as in leaf trace bundles (Fig. 3D). Micrographs at higher magnifications (Fig. 3, E and F) show that the xylem parenchyma cell walls are secondarily thickened and do not develop transfer cell-like morphology. However, the phloem companion cells of stem bundles have developed peg-like wall ingrowths (Fig. 3I). Hypocotyl bundles (Fig. 4B) have a morphology characteristic of mature stem bundles. The xylem vessels are irregularly arranged and surrounding parenchyma cells are secondarily thickened. However, unlike young stem bundles, there are few phloem cells and these do not show clear companion cell or sieve element morphology.
In the interfascicular zone, where ZeRH2.1 transcript is detected in small cells, young vascular bundles develop. Recent divisions of a phloem mother cell into a sieve element and a companion cell can easily be identified (Fig. 3G). The companion cells have a characteristic triangular shape and dense cytoplasm. Enlarged cells destined to be xylem vessel elements are also identifiable.
Stem sections were obtained from just above the first node with fully open leaves. The vascular bundles in this young part of the stem are anatomically similar without distinct stem bundle or leaf trace bundle morphology, and will be referred to as juvenile bundles. The expression pattern of the ZeRH2.1 gene in juvenile bundles is distinct from that of either stem or leaf trace bundles of the mature stem. Expression of ZeRH2.1 is not enhanced in any of the cell types of the xylem (Fig. 4, F–H). Although xylem tracheids of these bundles are radially arranged in a similar fashion to leaf trace bundles (Fig. 4C), the surrounding parenchyma cells are not densely cytoplasmic nor do they show transfer cell-like morphology (Fig. 4D). However, abundant transcript was detected in the phloem (Fig. 4, F–I). As shown in Figure 4G, the expression of the ZeRH2.1 gene is enhanced in three to four cell layers of phloem. Precursors of phloem fiber cells do not express the gene. Almost all of the phloem cells of a recently divided, very young bundle show accumulation of the transcript (Fig. 4H), as no fiber cells have developed yet. At higher magnification (Fig. 4I), gene expression in the juvenile bundles is confined to some of the larger cells of the phloem. The phloem companion cells of juvenile bundles do not develop wall ingrowths and are roughly the same size as sieve elements (Fig. 4E) and parenchyma cells. It is therefore hard to establish in which phloem cell type the gene is expressed. The transverse section in Figure 4, F and K, shows the anatomy of a node subtending a leaf pair above node 1. The overlaid boundary in Figure 4K marks the outline of one of the two future leaves that will arise at this node. The leaf traces destined to supply the future leaf have already diverged from the stem (Fig. 4F, black arrowheads), although the leaf remains physically attached to the main stem. Xylem parenchyma cells of the diverged midrib bundle, which are likely to be in the transition state to form transfer cells, strongly express ZeRH2.1 (Fig. 4J). A similar pattern of expression was detected in the siderib bundles but was absent from all of the vascular bundles in the central vasculature. In addition to the leaf trace bundles, cells positioned at the top half of the leaf (Fig. 4F, arrows), the future palisade mesophyll cells, also show enhanced gene expression; however, spongy mesophyll cells or the neighboring stem cortical cells do not show up-regulation of the transcript (Fig. 4F). The expression pattern of the molecular marker ZeRH2.1 in different types of vascular bundles is summarized in Figure 5.
Interconnections of Leaf and Stem Vascular Bundles Two developmental anatomy questions arise from the above observations: (1) how are the leaf trace and the stem bundles connected to each other, and (2) what happens to the stem vasculature after the six leaf trace bundles have supplied the leaves? To address these questions, we resolved the arrangement of the vasculature in the zinnia stem (Fig. 6). The hypocotyl has four vascular strands, each of which divides once to bring the number of vascular strands to eight. Four of these eight strands divide once again to supply the first pair of leaves, bringing the total number of vascular strands to 12. This represents the base number for zinnia, which the plant will maintain by continued divisions of the vascular strands. At the apical meristem, all of the bundles are identical and show juvenile bundle morphology. Vascular strands that have diverged out from the central vasculature as leaf traces develop leaf trace bundle morphology. As the stem elongates and internodes develop, continuing leaf traces within the central vasculature also develop leaf trace bundle morphology (indicated by green lines in Fig. 6) in the upper region of the internode. As the vascular strand increases in distance from the node, which it supplied as a leaf trace, it undergoes a morphological transition from leaf trace bundle to stem bundle, represented by transition of green lines into black lines, in Figure 6. The peripheral part of the xylem develops irregular metaxylem, characteristic of stem bundles, whereas the internal part of the newly formed bundle contains protoxylem elements with leaf trace bundle characteristics (Fig. 3D) and xylem parenchyma cells with wall ingrowths (Fig. 4A). In mature stem bundles, lacunae form in the protoxylem as the stem elongates and the cells are subject to stretching forces (Fig. 4B). Interestingly, protoxylem tracheids are not obliterated (Fig. 4B), perhaps because of the mechanical support provided by the thick walls of neighboring transfer cells. Older parts of the stem with very long internodes show only stem bundle morphology, illustrated in Figure 6 by black lines, between the hypocotyl and node 4.
The central stem vasculature only contains six leaf trace bundles at one node, as the vascular bundles supplying the leaf do not continue above that node, shown within the blue rectangle of Figure 6. For example, the vascular supply to leaves of node 2 terminates at that node, and node 1 does not contain any leaf trace bundles that have supplied node 2. Similarly, below the supply node as well, leaf trace bundle morphology remains confined to a single internode. As shown in Figure 6, the siderib bundles branch out just below the supply node. This is not the case for midribs, which originate two nodes below the supply node. The midrib bundle for node 2, for example, originates by the merging of two bundles from node 4. The midrib bundles acquire stem bundle morphology before reaching the node below the supply node; node 2 midrib, for example, will show stem bundle morphology when observed at node 3.
The development of the postembryonic stem vascular system involves three processes: (1) the differentiation of juvenile bundles into leaf trace bundles and stem bundles, (2) the specialization of vascular cells for specific function, and (3) the differentiation of the vascular network as a coherent unit. We have used the expression pattern of a zinnia gene, ZeRH2.1, as a molecular marker to help track the differentiation of the zinnia stem vascular system as the plant matures (Fig. 5).
A number of in situ hybridization studies have reported zinnia gene expression patterns in vascular bundles of the zinnia stem. However, these studies were either limited to the young zone (Demura and Fukuda, 1994 Understanding the differential expression pattern of ZeRH2.1 in different developmental zones of the zinnia stem required careful analysis of the anatomy. As zinnia is an established model system for studying xylogenesis, detailed characterization of the stem vascular network is important for functional analysis of the genes in vivo. We define two zones in the stem, a young zone, above the first fully expanded leaf, and a mature zone, between the second open leaf and the hypocotyl (Fig. 5). Juvenile bundles in the young zone have a uniform anatomy, consisting of protophloem and radially arranged tracheids of protoxylem. Juvenile bundles then develop into leaf trace bundles in which xylem parenchyma cells have differentiated into transfer cells, supporting radially arranged protoxylem tracheids. The phloem of these bundles is characterized by metaphloem and is largely composed of companion cells and sieve elements. As the plant grows, the internodes elongate and the long-running vascular strands develop irregularly arranged metaxylem vessels, characteristic of stem bundle morphology (Figs. 3, D–F, and 6). The internal cells of newly formed stem bundles are protoxylem cells (Figs. 2E and 3D), which are later stretched and displaced as metaxylem is formed (Fig. 4A).
In the mature stem, leaf trace bundles show strong up-regulation of the ZeRH2.1 transcript in the xylem parenchyma (Figs. 2, C and D , and 5), whereas stem bundles have abundant transcript in phloem companion cells (Figs. 2, C, E, and F, and 5). Both xylem parenchyma of the leaf trace bundles and companion cells of the stem bundles have been modified into transfer cells (Fig. 3, C and I). Xylem and phloem transfer cells belong to two different classes (Pate and Gunning, 1972
Transfer cell differentiation is coordinated with organ development and occurs at specific locations across particular developmental windows (Pate and Gunning, 1972 The xylem parenchyma cells of the stem bundles have only basal levels of the ZeRH2.1 transcript (Fig. 2E). As shown in Figure 3, D to F, the peripheral xylem cells of stem bundles that are formed in the long-running internodes have thickened xylem parenchyma without transfer cell-like wall ingrowths. However, the internal xylem cells of these bundles consist of protoxylem with characteristic wall ingrowths in xylem parenchyma cells (Fig. 4A). It is possible that older transfer cells associated with the protoxylem at the internal end of the vascular bundle are no longer functional in stem bundles. As stem bundles age, protoxylem is stretched and then becomes displaced (Fig. 4B). Our results show that only the leaf trace bundle transfer cells, which are in close proximity to the node, contain abundant ZeRH2.1 transcript. In hypocotyl bundles, no up-regulated expression of the ZeRH2.1 gene is observed (data not shown) and no transfer cells remain (Fig. 4B).
In the in vitro zinnia system, at least two different cell fates are represented: cells that form tracheary elements and the cells that do not. Several lines of evidence, together with the fact that dilution of cell number in the culture results in suppression of tracheary element formation, suggest that the population of living mesophyll cells that do not differentiate are required to support those differentiating to become tracheary elements (Matsubayashi et al., 1999
In the angiosperm stem, the relationship of transfer cells with foliar traces holds regardless of the class of structure that a node may subtend; traces to cotyledons, scale leaves, stipules, and various kinds of floral bracts all carry xylem transfer cells just as does the vascular supply to the true leaf (Gunning et al., 1970 ZeRH2.1 transcript, however, is also up-regulated in some cells that do not develop transfer cell morphology. In juvenile bundles, the phloem cells accumulate ZeRH2.1 transcript but do not develop wall ingrowths (Fig. 4, E–I). The leaf palisade parenchyma also accumulates transcript without development of transfer cell morphology (Fig. 4, F and K). This observation is consistent with the constitutive expression pattern of ZeRH2.1 in the in vitro zinnia system derived from leaf mesophyll and palisade cells (Fig. 1D). The enhanced levels of ZeRH2.1 transcript in different cell types may be correlated with their involvement in enhanced transportation. Xylem parenchyma cells of leaf trace bundles, companion cells of stem bundles, and phloem cells of juvenile bundles are all placed at crucial junctions of active transportation. Leaf palisade parenchyma cells actively export photosynthates to the rest of the plant. Therefore, we hypothesize that the ZeRH2.1 gene has a role to play during active transport, with more abundant transcript identifying sites of major intercellular transport.
How the ZeRH2.1 gene product might facilitate transport remains to be determined. The protein sequence contains a RING domain (Fig. 1). RING domain-containing proteins are components of supramolecular assemblies in cells that act in a variety of unrelated biochemical reactions. Kentsis et al. (2002)
In conclusion, our study integrates the complex expression pattern of a molecular marker with the differentiation of the stem vascular system of zinnia. The developmental progression of juvenile bundles to leaf trace bundles, stem bundles, and hypocotyl bundles is marked by the differential expression patterns of the ZeRH2.1 gene. As all four types of bundles show distinct anatomical characteristics, expression patterns of other vascular genes are likely to follow suit. The most similar sequence to ZeRH2.1 belongs to cluster 2.3 in the classification of RING domain-containing genes in Arabidopsis (Kosarev et al., 2002
Plant Material Seeds of Zinnia elegans cv Envy were obtained from Stokes Seeds, Chiltern, UK. Plants were grown in short-day conditions with 60% humidity at 26°C. Plants with two to three fully expanded leaves were used for in situ hybridization and anatomical studies.
Mesophyll cells were isolated from zinnia leaves and induced to differentiate to tracheary elements in vitro as described previously (Domingo et al., 1998
Total RNA and poly(A+) RNA was prepared as described by Milioni et al. (2002)
Total RNA was extracted from zinnia culture cells as described by Milioni et al. (2002) The 26S rRNA fragment, isolated by cDNA-AFLP, was used as a control for equal loading of total RNA. Primers for the 26S rRNA (5'-AAAGGATTCTACCAGTCGCTTGATGGGA-3' and 5'-ACGCCTCTAAGTCAGAATCCGGGCTAGA-3') were mixed with the above reaction.
Zinnia plants, with two to three fully expanded leaves, were used for fixation and embedding. One-centimeter-long pieces of stem were cut from near to the apical meristem, nodes of open leaves, internode region, and hypocotyl. Stem pieces were placed in fixative immediately after cutting. Tissue fixation was performed as described by Wisniewski et al. (1999)
Gene-specific, digoxygenin-labeled riboprobes were generated from a 357-bp fragment derived from the 3' end of the ZeRH2.1 cDNA sequence. T3 and T7 sites of the TOPO sequencing vector were used to make sense and antisense riboprobes. The plasmid was linearized using the NotI and SpeI sites for antisense and sense probes, respectively. Linearized plasmid was purified by phenol-chloroform extraction and quantified using a Bio-Rad spectrometer. Riboprobe synthesis and in situ hybridization were performed as described by Wisniewski et al. (1999)
Serial hand sections of the zinnia stem were used to determine the vascular strand arrangement.
Tissues were fixed and embedded in LR White resin as described previously (Vandenbosch et al., 1989 Upon request, all novel materials described in this publication will be made available in a timely manner for noncommercial research purposes, subject to the requisite permission from any third-party owners of all or parts of the material. Obtaining any permission will be the responsibility of the requestor. Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession number AJ867840.
We thank Jaap Nijsse (Wageningen University, Wageningen, The Netherlands) for useful advice to determine vascular arrangement, and JIF-Nuffield fellow Ranu Dhalla (John Innes Centre, Colney, UK) for assistance with RT-PCR. P.D. performed the experiments and drafted the manuscript, B.W. sectioned blocks for histology, N.S. performed plant husbandry and cell cultures, D.M. isolated the cDNA-AFLP fragment corresponding to a partial sequence of ZeRH2.1, and K.R. and M.C.M. cosupervised the work and cowrote the manuscript. Received December 8, 2004; returned for revision March 23, 2005; accepted April 20, 2005.
1 This work was supported by the Leverhulme Trust (grant to P.D.), the European Union EDEN project (no. QLK5–CT–2001–00443 to P.D.), the Biotechnology and Biological Sciences Research Council (grant to K.R. and B.W.), and The Royal Society (grant to M.C.M.). 
2 Present address: Department of Agricultural Biotechnology, Agricultural University of Athens, Athens, Greece.
3 Present address: Department of Biological Sciences, Purdue University, West Lafayette, IN 47907–1392. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.057901. * Corresponding author; e-mail mmccann{at}bilbo.bio.purdue.edu; fax 765–496–1496.
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402 Borden KLB (1998) RING fingers and B-boxes: zinc-binding protein-protein interaction domains. Biochem Cell Biol 76: 351–358[CrossRef][ISI][Medline] Borden KLB (2000) RING domains: master builders of molecular scaffolds? J Mol Biol 295: 1103–1112[CrossRef][ISI][Medline] Brzovic PS, Rajagopal P, Hoyt DW, King MC, Klevit RE (2001) Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat Struct Biol 8: 833–837[CrossRef][ISI][Medline] Dahiya P, Brewin NJ (2000) Immunogold localization of callose and other cell wall components in pea nodule transfer cells. Protoplasma 214: 210–218[CrossRef] Demura T, Fukuda H (1994) Novel vascular cell-specific genes whose expression is regulated temporally and spatially during vascular system development. Plant Cell 6: 967–981[Abstract] Domingo C, Roberts K, Stacey NJ, Connerton I, Ruiz-Teran F, McCann MC (1998) A pectate lyase from Zinnia elegans is auxin inducible. Plant J 13: 17–28[CrossRef][ISI][Medline] Eames AJ, MacDaniels LH (1925) An Introduction to Plant Anatomy. McGraw-Hill, London
Endo S, Demura T, Fukuda H (2001) Inhibition of proteasome activity by the TED4 protein in extracellular space: a novel mechanism for protection of living cells from injury caused by dying cells. Plant Cell Physiol 42: 9–19 Esau K (1962) Anatomy of Seed Plants. John Wiley & Sons, London Foster AS, Gifford EM (1959) Comparative Morphology of Vascular Plants. W.H. Freeman and Company, San Francisco
Fukuda H, Komamine A (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 65: 57–60
Funk V, Kositsup B, Zhao CS, Beers EP (2002) The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog. Plant Physiol 128: 84–94 Groover AT, Pattishall A, Jones AM (2003) IAA8 expression during vascular cell differentiation. Plant Mol Biol 51: 427–435[CrossRef][ISI][Medline] Gunning BES, Pate JS, Green LW (1970) Transfer cells in vascular system of stems: taxonomy, association with nodes, and structure. Protoplasma 71: 147–171[CrossRef] Harrington GN, Franceschi VR, Offler CE, Patrick JW, Tegeder M, Frommer WB, Harper JF, Hitz WD (1997) Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Vicia faba seed. Protoplasma 197: 160–173[CrossRef]
Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680
Im KH, Cosgrove DT, Jones AM (2000) Subcellular localization of expansin mRNA in xylem cells. Plant Physiol 123: 463–470 Kentsis A, Dwyer EC, Perez JM, Sharma M, Chen A, Pan ZQ, Borden KLB (2001) The RING domains of the promyelocytic leukemia protein PML and the arenaviral protein Z repress translation by directly inhibiting translation initiation factor eIF4E. J Mol Biol 312: 609–623[CrossRef][ISI][Medline]
Kentsis A, Gordon RE, Borden KLB (2002) Control of biochemical reactions through supramolecular RING domain self-assembly. Proc Natl Acad Sci USA 99: 15404–15409 Kosarev P, Mayer KFX, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3: 0016.1–0016.12 Liu L, Eriksson KEL, Dean JFD (1999) Localization of hydrogen peroxide production in Zinnia elegans L. stems. Phytochemistry 52: 545–554[CrossRef]
Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y (1999) The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of zinnia. Plant Physiol 120: 1043–1048
McCann MC, Stacey NJ, Dahiya P, Milioni D, Sado PE, Roberts K (2001) Zinnia: Everybody needs good neighbors. Plant Physiol 127: 1380–1382
Milioni D, Sado PE, Stacey NJ, Roberts K, McCann MC (2002) Early gene expression associated with the commitment and differentiation of a plant tracheary element is revealed by cDNA-amplified fragment length polymorphism analysis. Plant Cell 14: 2813–2824 Motose H, Fukuda H, Sugiyama M (2001) Involvement of local intercellular communication in the differentiation of zinnia mesophyll cells into tracheary elements. Planta 213: 121–131[CrossRef][ISI][Medline] Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873–878[CrossRef][Medline] Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2002) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54: 431–454[CrossRef]
Ohashi-Ito K, Demura T, Fukuda H (2002) Promotion of transcript accumulation of novel Zinnia immature xylem-specific HD-Zip III homeobox genes by brassinosteroids. Plant Cell Physiol 43: 1146–1153 Ohashi-Ito K, Demura T, Fukuda H (2003) Analysis of the HD-Zip III homeobox gene ZeHB-13 in relation to vascular differentiation in Zinnia. Plant Cell Physiol 44: S170
Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44: 1350–1358 Pate JS, Gunning BES (1972) Transfer cells. Annu Rev Plant Physiol 23: 173–196 Peng HZ, Begg GE, Schultz DC, Friedman JR, Jensen DE, Speicher DW, Rauscher FJ (2000) Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box coiled-coil domain-mediated protein-protein interactions. J Mol Biol 295: 1139–1162[CrossRef][Medline] Sachs JV (1875) Textbook of Botany. Clarendon Press, Oxford Saurin AJ, Borden KLB, Boddy MN, Freemont PS (1996) Does this have a familiar RING? Trends Biochem Sci 21: 208–214[CrossRef][ISI][Medline]
Torii KU, Stoop-Myer CD, Okamoto H, Coleman JE, Matsui M, Deng XW (1999) The RING finger motif of photomorphogenic repressor COP1 specifically interacts with the RING-H2 motif of a novel Arabidopsis protein. J Biol Chem 274: 27674–27681 Vandenbosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J 8: 335–341[ISI][Medline] Wisniewski JP, Gardner CD, Brewin NJ (1999) Isolation of lipoxygenase cDNA clones from pea nodule mRNA. Plant Mol Biol 39: 775–783[CrossRef][ISI][Medline] Ye ZH (1996) Expression patterns of the cinnamic acid 4-hydroxylase gene during lignification in Zinnia elegans. Plant Sci 121: 133–141[CrossRef]
Ye ZH, Varner JE (1994) Expression of an auxin-regulated and cytokinin-regulated gene in cambial region in Zinnia. Proc Natl Acad Sci USA 91: 6539–6543 Ye ZH, Varner JE (1995) Differential expression of 2 o-methyltransferases in lignin biosynthesis in Zinnia elegans. Plant Physiol 108: 459–467[Abstract] This article has been cited by other articles:
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