The putative poplar CLV1 orthologue, PttCLV1 , was shown to have a higher expression in the phloem than in the cambial zone and the xylem Schrader et al. The GFP expression driven by the CLV1 promoter has been localized in the cambial zone and in secondary phloem of the root—hypocotyl junction of Arabidopsis Zhao et al. The overexpression of either Arabidopsis STM or poplar ARK1 in aspen resulted in a similar bushy and highly branched phenotype, reflecting the formation and the outgrowth of ectopic meristem during primary growth Groover et al.
Although a continuous ring of lignified secondary xylem was present at the stem base of 6-month-old trees, the boundary between the cambium and secondary xylem was wavy compared with WT and there were almost no lignified phloem fibres Groover et al.
As suggested by these authors, these data are compatible with a regulation model analogous in both the cambium and the SAM of aspen, in which STM expression in the cambial zone would repress the AS homologue. If xylem and phloem differentiation is regulated by a mechanism similar to the one controlling organ formation in the SAM, it can be expected that a balance exists between AS and STM homologue gene expression within the cambial zone to promote vascular tissue differentiation.
The expression of the closest homologue of AS1 was not detected in the poplar cambial zone Schrader et al. Vascular development is essential for plant growth and relies on a tight integration of cell proliferation, cell-fate determination, cell differentiation, and patterning, leading to xylem and phloem formation.
In the last decade, several molecular determinants involved in the regulatory mechanisms controlling these developmental processes in Arabidopsis have been uncovered, thanks to reverse and forward genetics. For instance, the pendent phenotype of the rev mutants, the absence of phloem in the primary root of the wol mutant, the production of xylem in place of phloem in the apl mutant, the increased production of phloem in the brl1 mutant, or the opposite roles of the HD-ZIP III and KAN transcription factors illustrate the complexity of vascular system development in plants.
Beside these genetic controls, integration of hormone signals particularly auxin and BRs appears to be equally important for the appropriate continuity and patterning of procambium and vascular tissues as manifested by the phenotype of Arabidopsis plants with reduced PAT. Considerations on the functioning of primary SAM and secondary vascular cambium meristems suggest overlapping regulatory mechanisms between them, but also specific characteristics for each of these two plant meristems Schrader et al.
Although homologue genes have been reported to be expressed in the cambium Schrader et al. On the other hand, SAM and vascular cambium have several specific features. One of the major differences between the SAM and the cambium is the ability of vegetative SAM to become determinate in order to ensure flower production.
By contrast, the indeterminate state of the cambium is critical to ensure perennial growth. Although significant progress has been made in the identification of genes involved in the biosynthesis of cell wall components, including lignin Boerjan et al. The recent availability of the Populus genome sequence Tuskan et al.
The comparison of Arabidopsis and Populus genomes revealed that the relative frequency of protein domains is similar in both genomes Tuskan et al. However, these authors showed that Populus has more protein-coding genes than Arabidopsis and that some genes are overrepresented in Populus compared with the Arabidopsis genome, such as genes associated with meristem development and cell wall biosynthesis.
Therefore, dissimilarities in growth patterns amongst taxa could result from variations in gene expression levels, but also from the expression of various sets of genes at different stages of growth. The authors would like to warmly thank Sylvia Burssens and Anne-Marie Catesson for critical reading of the manuscript, Pierre Martens for designing Fig.
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Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Molecular determinants of vascular development during primary growth phase. Molecular determinants of vascular development during secondary growth. Concluding remarks. From primary to secondary growth: origin and development of the vascular system.
E-mail: mbaucher ulb. Oxford Academic. Mondher El Jaziri. Olivier Vandeputte. Revision received:. Select Format Select format. Permissions Icon Permissions.
Abstract Vascular tissue differentiation is essential to enable plant growth and follows well-structured and complex developmental patterns. Arabidopsis , cambium , phloem , Populus , primary growth , secondary growth , vascular system development , xylem. Table 1. Gene family Gene name Post-embryonic expression in vascular tissues Loss-of-function phenotype Gain-of-function phenotype Downregulation Overexpression References 1. Open in new tab. Open in new tab Download slide. Development of the vascular system in the inflorescence stem of Arabidopsis.
Google Scholar Crossref. Search ADS. Ultrastructural changes in cambial cell derivatives during xylem differentiation in poplar. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Google Scholar PubMed. Formation of the shoot apical meristem in Arabidopsis thaliana : an analysis of development in the wild type and in the shoot meristemless mutant.
KNAT6 : an Arabidopsis homeobox gene involved in meristem activity and organ separation. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Pattern of differentiation of the first vascular elements in the embryo and seedling of Arabidopsis thaliana. Vascular differentiation and transition in the seedling of Arabidopsis thaliana Brassicaceae.
The eli1 mutation reveals a link between cell expansion and secondary cell wall formation in Arabidopsis thaliana. The identification of CVP1 reveals a role for sterols in vascular patterning. Secondary xylem development in Arabidopsis : a model for wood formation. Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Lignin-like compounds and sporopollenin in Coleochaete , an algal model for land plant ancestry.
Plant cell wall biosynthesis: genetic, biochemical and functional genomics approaches to the identification of key genes. In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. In this review, we first examine the evolutionary events that gave rise to the tracheophytes, followed by analysis of the genetic and hormonal networks that cooperate to orchestrate vascular development in the gymnosperms and angiosperms.
The two essential functions performed by the vascular system, namely the delivery of resources water, essential mineral nutrients, sugars and amino acids to the various plant organs and provision of mechanical support are next discussed. Here, we focus on critical questions relating to structural and physiological properties controlling the delivery of material through the xylem and phloem. Furuta, K. Molecular control of cell specification and cell differentiation during procambial development.
Kubo, M. Transcription switches for protoxylem and metaxylem vessel formation. This paper reports that VND transcription factors are sufficient to induce cell wall modifications that are typical of xylem cells in various other cell types. Plant Cell 22 , — Yamaguchi, M. Taylor-Teeples, M. An Arabidopsis gene regulatory network for secondary cell wall synthesis.
Xu, B. Contribution of NAC transcription factors to plant adaptation to land. This paper demonstrates that VND transcription factors that mediate xylem differentiation in vascular plants control differentiation of water-conducting cells in a moss. Fisher, K. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Hirakawa, Y. Ito, Y. Dodeca-CLE peptides as suppressors of plant stem cell differentiation.
Kondo, Y. Dettmer, J. The authors identify nucleases that mediate phloem cell differentiation, as well as their transcriptional regulators. Clowes, F. The cytogenerative centre in roots with broad columellas. New Phytol. The promeristem and the minimal constructional centre in grass root apices. Sabatini, S. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99 , — Brunoud, G. A novel sensor to map auxin response and distribution at high spatio-temporal resolution.
Liao, C. Reporters for sensitive and quantitative measurement of auxin response. Methods 12 , — Sarkar, A. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Wildwater, M. Willemsen, V.
Cell 15 , — Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature , 62—65 Short-range control of cell differentiation in the Arabidopsis root meristem. Aida, M. Galinha, C. Matsumoto-Kitano, M. Cytokinins are central regulators of cambial activity. Kuroha, T. Plant Cell 21 , — Tokunaga, H. Arabidopsis lonely guy LOG multiple mutants reveal a central role of the LOG-dependent pathway in cytokinin activation. Cytokinin signaling regulates cambial development in poplar.
Dello Ioio, R. A genetic framework for the control of cell division and differentiation in the root meristem. Whitford, R. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Etchells, J. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division.
Suer, S. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23 , — Download references. The authors would like to thank Jos Wendrich, Wouter Smet and Colette ten Hove for critical reading of the manuscript. Research on vascular development in D. You can also search for this author in PubMed Google Scholar. Correspondence to Dolf Weijers. One of the three major tissue types in plants, located between the outer layer epidermis and the inner vascular cylinder.
The embryonic leaves of the plant; post-embryonically, the first true leaves are formed from the shoot apical meristem. Changes of the cell wall components [ 26 — 28 ] and gene expression during the cyclic activity of vascular cambium [ 29 , 30 ], correlated with the rapid cytoskeleton rearrangement in differentiating cells [ 31 ], indicate that this meristematic tissue plays a crucial role in the secondary growth of woody plants and decides about their adaptation to variable environmental conditions.
In the most typical form, secondary xylem, also called a wood, is found in stems and roots of the woody plants.
The secondary xylem, a longitudinal conducting system in trees, develops from the cambial derivatives, which during the maturation process is differentiated into elements of the wood-like vessels, fibers, and tracheids [ 13 , 15 ]. Vessels of the secondary xylem form strands parallel to the longitudinal axis of the organs—stems or roots. Every vessel strand is consisted of single vessel elements, the so-called vessel members, connected with each other by open perforation plates localized on their apical-basal ends [ 12 ].
It is postulated that direction of vessel differentiation is dependent on direction of auxin flow. Thus, in nondisturbed stems, vessels developed according to the polar auxin transport PAT in the apical-basal direction whereas in incised organs—according to newly established direction of auxin flow—circumventing the wounded regions. Correlations between auxin flow and vasculature patterning were experimentally documented in woody plants after wounding [ 32 ] as well as nonwoody models [ 4 , 5 , 8 ].
Characteristic feature for all types of vessels primary protoxylem, metaxylem, and secondary xylem vessels is the secondary cell wall. Different patterning of the secondary cell wall is realized during vessel maturation process and depends on the type of vessel [ 14 ]. During the maturation process, protoplasts of differentiating vessels disappeared. Frequently, the lumen of the vessel members is enlarged in comparison to other tracheary elements, mainly in a wood of such species as Fraxinus excelsior , Quercus borealis , or Ulmus americana [ 13 ].
In many cases, length of the vessel members is different than the length of the fusiform cambial cells from which they developed. Interestingly, longitudinal vessel strands change the orientation to the longitudinal axis of stems. Such fluctuations are observed as the wavy grain patterning of wood in many trees [ 33 ].
Fibers of the secondary xylem are recognized as one of the longest tracheary elements, characterized by the tapered cell ends and reduced lumen. As a consequence of their intensive intrusive growth, fibers could be even few times longer than the fusiform cambial cells and their derivatives.
Particular type of the woody fibers is the so-called gelatin fibers, developed as a layer of the reaction wood in many deciduous as well as coniferous trees, i. Inner layer of secondary cell wall of these fibers is built mainly from cellulose. The presence of the callose and callose-like cell wall components plays here an important role in mechanical properties of the wood [ 34 ].
Tracheids, other tracheary elements of secondary xylem, are nonperforated, long cells with the bordered pits. Dependently on the type of a wood, tracheids are classified as 1 vessel-like tracheids arranged in longitudinal, similar to vessels conducting strands, commonly found in Carpinus sp. The last of them develop as a conducting and storage water system but also play mechanical functions and in some species could be the main component of the softwood of gymnosperms [ 36 ]; they are found also in some angiosperms, i.
Besides of the dead, water-conducting elements of the secondary xylem mentioned above, in many cases secondary vascular tissue of woody plants is compound with the xylem parenchyma cells, which remain alive for a long time to finally die in the programmed cell death PCD process [ 12 ].
Thorough knowledge about the genetic and molecular mechanisms involved in vascular tissue functioning, development, and regeneration is eagerly expected. Different molecular components involved in the determination of developmental plasticity of cambial cells have been searched for with special interest focused on the key regulators of vascularization.
Genes involved in auxin response, auxin signaling pathways, and tissue and cellular polarity during vascular tissue development induced in vascular cambium should be extensively studied for detailed characterization of this process. Since many years, Arabidopsis is nominated as a good model for studies of vascular tissue formation, because under suitable conditions, Arabidopsis can undergo secondary growth in hypocotyls, when enlarged layer of secondary xylem develops during xylogenesis [ 37 ].
Xylogenesis in hypocotyls is comparable to xylogenesis in roots. Development of secondary xylem is divided here into two phases: the early phase, xylem is building from vessels and numerous parenchyma cells, and in the second, later phase, also called xylem expansion, enlarged amount of xylem elements develops mainly vessels and fibers [ 37 , 38 ]. It is well documented that vascular tissue develops not only in hypocotyls [ 37 ] but also in the matured inflorescence stems [ 39 — 41 ], in their basal parts [ 42 — 45 ].
With the use of Arabidopsis , the correlation between auxin signaling and tissue polarity has been intensively studied and modeled [ 46 — 49 ]. However, because of lack of some important vasculature features such as a variety of typical phenotype features and functional cambium, these models could not be used for full analysis and description of vascular tissue development and compared to the analogical process in trees.
For example, in both Arabidopsis models mentioned above, rays were not found. Also intrusive growth typical for fusiform cambial cells was not confirmed. Finally, impressive variety of tracheary elements, among them tracheids, commonly found in trees, were not observed in Arabidopsis mature stems and hypocotyls, which underwent secondary growth [ 50 ].
In contrast, in the Arabidopsis inflorescence stems stimulated mechanically by an artificial weight, the transition from primary to secondary tissue architecture leads to the development of all vasculature features mimicking secondary vascular tissues in woody plants.
According to the new approach, immature inflorescence stems 9—10 cm tall were firstly decapitated with the sharp razor blade shoot apex and flowers were removed. Next, the artificial weight 2. Stems were additionally supported by a wood stick to avoid their bending. Importantly, the axillary buds grown above the leave rosettes were not removed, thus remaining the natural source of endogenous auxin. This experimental approach has been extensively described [ 7 , 8 ].
It was speculated that the weight carried by the stem serves as a mechanically stimulated signal for wood formation [ 7 , 8 , 42 , 51 ]. According to Ko and coauthors [ 42 ], mechanical stimulation of immature inflorescence stems of Arabidopsis increases polar auxin transport and promotes the secondary growth.
Moreover, the secondary vascular tissues develop in a very short time, namely, in 6 days [ 7 ], which is much faster than in hypocotyls [ 37 , 38 ] or mature inflorescence stems of Arabidopsis [ 44 , 45 ]. According to the obtained results, both types of cambial cells develop: 1 ray cambial cells, very short and almost round cells arranged in single-row rays mimicking transverse conducting system in woody plants, and 2 fusiform cambial cells, long, tapered-end cells, characterized by the intrusive growth and periclinal divisions, play here an important role in secondary tissue element differentiation.
The phenomenon of intrusive growth of fusiform cambial cells is described for the first time in the mechanically stimulated Arabidopsis stems Figure 1A — D , not found in the previously analyzed models. Neighboring cells start their growth in the opposite directions, but the growth is restricted to the tips of the cells, which slide along the radial cell walls and provide the elongation of the fusiform cambial cells Figure 1A , C , and D.
Intrusive growth of the fusiform cambial cells in mechanically stimulated Arabidopsis stems. A Schematic visualization of two intrusively growing cells 1 two neighboring cells with still non-intrusively growing ends, 2 beginning of the intrusive growth of the opposite ends, 3 advanced intrusive growth along the radial cell walls of the cells.
Asterisks indicate neighbor cells and their intrusively growing ends. B—D Intrusively growing fusiform cambial cells in temporal steps corresponding to situation visualized in A. New approach, based on mechanical stimulation of the immature inflorescence stems of Arabidopsis [ 7 , 8 , 42 , 51 ], is expected to elucidate the phenomenon of vascular tissue formation and regeneration at cellular and molecular level—processes commonly studied in woody plants, but not fully explained yet, because of some experimental and environmental difficulties in these plants [ 52 ].
Thus, Arabidopsis comes out as a good model system for vascular tissue patterning. In this paragraph, we will describe in detail the transition from primary to secondary tissue architecture in inflorescence stems of Arabidopsis as the important step in obtaining a suitable model for secondary vascular tissue analysis, following the temporal and spatial changes during vascular cambium ontogenesis, xylem formation, and vascular tissue regeneration in weight-induced Arabidopsis.
Ontogenesis of vascular cambium is correlated with temporal and spatial changes on the stem circumference. Usually, formation of a closed ring of cambium is preceded by dedifferentiation of parenchyma cells into cambial cells and the so-called interfascicular cambium development. This process is commonly observed in young woody plants during their secondary growth [ 12 ].
It has been confirmed by histological analyses that the first dedifferentiated parenchyma cells are localized next to the vascular bundles in the early stages of the interfascicular cambium development [ 12 ]. With the time, the regions of dedifferentiating parenchyma cells are extended and finally enclosed as continuous ring on the stem circumference.
The mechanism of these changes is still not clarified. The basic question is which of the cellular events trigger the parenchyma cell dedifferentiation? In mechanically stimulated Arabidopsis stems, vascular cambium develops from fascicular cambium and interfascicular cambium bands Figure 2.
Fascicular cambium develops as a primary meristematic tissue in vascular bundles, localized in the inner parts of immature stems characterized by primary tissue architecture. The vascular bundles are separated by interfascicular parenchyma bands with nonpericlinally dividing parenchyma cells Figure 2A and B. Outside these regions, few layers of cortex and single layer of the epidermis are situated.
Middle parts of the stems consisted of the enlarged, thin-cell wall pith parenchyma cells. One- or few-layer supporting tissue with characteristic thick-cell wall interfascicular fibers plays mechanical function in immature stems Figure 2B.
In immature stems of Arabidopsis , 6 days after weight application, the architecture of the basal parts of such stems diametrically changes. At the beginning of the secondary growth, interfascicular cambium develops in the interfascicular regions of stems, as a consequence of parenchyma cell dedifferentiation Figure 2C and D. Interestingly, the most inner layer of interfascicular parenchyma cells dedifferentiates into the interfascicular cambium.
Typically, it is a single layer of parenchyma cells localized between vascular bundles. Finally, during the transition from the primary to the secondary tissue architecture of Arabidopsis stems, fascicular and interfascicular cambium forms fully enclosed ring of vascular cambium on stem circumference Figure 2D.
Transition from primary to secondary tissue architecture in weight applied inflorescence stems of Arabidopsis. A Schematic visualization of the tissue arrangement in immature inflorescence stems of Arabidopsis. B Cross section through the basal parts of stem with the primary tissues—vascular bundles with fascicular cambium are separated by the interfascicular parenchyma. The most inner layer of interfascicular parenchyma cells will dedifferentiate into cambial cells asterisks.
C Schematic visualization of the secondary vascular tissues with closed ring of vascular cambium on stems circumference. D Layer of periclinally dividing interfascicular cambial cells as a part of the ring of vascular cambium. The first developed vessels are indicated by asterisks lignin in the secondary cell walls stained with 0. The whole process of cambium ontogenesis is strictly correlated with such cellular events as elevated auxin response in interfascicular parenchyma, polarity of parenchyma cells dedifferentiating into the cambium, their periclinal divisions, and changes of their cell wall components [ 7 ].
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