Abstract
Development of vascular tissue is a remarkable example of intercellular communication and coordinated development involving hormonal signaling and tissue polarity. Thus far, studies on vascular patterning and regeneration have been conducted mainly in trees—woody plants—with a well-developed layer of vascular cambium and secondary tissues. Trees are difficult to use as genetic models, i.e., due to long generation time, unstable environmental conditions, and lack of available mutants and transgenic lines. Therefore, the use of the main genetic model plant Arabidopsis thaliana (L.) Heynh., with a wealth of available marker and transgenic lines, provides a unique opportunity to address molecular mechanism of vascular tissue formation and regeneration. With specific treatments, the tiny weed Arabidopsis can serve as a model to understand the growth of mighty trees and interconnect a tree physiology with molecular genetics and cell biology of Arabidopsis.
Keywords
- Arabidopsis
- vascular tissue
- vascular cambium
- secondary xylem
- auxin
- auxin transporters
- cellular polarity
- PIN proteins
1. Introduction
Various species and systems were used for the analysis of vascular tissue [1–5]; however,
In this review, we summarize information concerning secondary vascular tissue development in
2. Secondary vascular tissues in woody plants
Vascular tissue is a well function conducting system typical for all woody plants, among them in trees. In young plants, characteristic primary tissues such as procambium, primary xylem, and primary phloem, develop. During the secondary growth, vascular tissue undergoes the transition from primary into the secondary vascular patterning. Vascular cambium, secondary xylem, and secondary phloem form a closed ring on the stem circumference. They are arranged in the radial rows as a consequence of periclinal divisions of cambial cells [10–12]. The secondary growth is mostly characteristic for all woody plants, and production of the secondary vascular tissues is an important developmental feature of the plants [12, 13].
2.1. Vascular cambium
Vascular cambium plays a crucial role in the secondary growth and vascular tissue patterning in woody plants [14, 15]. Activity and functioning of vascular cambium decide about the amount of the secondary phloem and xylem, which are produced outward and inward the vascular cambium, respectively [12, 13]. This meristematic tissue is built from two types of cells: ray cambial cells producing secondary rays—transverse conducting system in tissues—and fusiform cambial cells, producing elements of the longitudinal conducting systems in woody plants. Characteristic feature of the vascular cambium is intrusive growth of the fusiform cambial cells and their periclinal divisions [13, 16, 17]. The intrusive growth is restricted to the ends of growing cells, when two neighboring cells grow in opposite directions. Periclinal divisions of cambial cells decide about production of cambial derivatives and secondary tissue element differentiation.
Vascular cambium is the tissue very much sensitive to mechanical injuries, such as wounding or grafting. However, it can easily regenerate under suitable conditions. It has been experimentally shown that cambium regeneration is mostly dependent on the tensile stress and pressure. Results obtained by Brown [18] indicate that cambium activity, cell divisions, and xylem formation can be easily affected by the pressure externally implied to the cambial strips. It is also documented in
It has been postulated that appropriate functioning of vascular cambium and its cyclic activity, i.e., periclinal divisions during the seasons, is strictly correlated with auxin signaling and auxin responses [21–23]. From the studies on
2.2. Secondary xylem
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
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.e.,
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
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.
2.3. Arabidopsis as a nonwoody plant example for vascular tissue formation
Since many years,
In contrast, in the
In the created
New approach, based on mechanical stimulation of the immature inflorescence stems of
3. Vascular tissue development and regeneration in mechanically stimulated inflorescence stems of Arabidopsis
In this paragraph, we will describe in detail the transition from primary to secondary tissue architecture in inflorescence stems of
3.1. Ontogenesis of vascular cambium
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
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]. The most spectacular seems to be correlations between auxin response and tissue polarity during cambium ontogenesis in analyzed
During analyzed process of cambium ontogenesis, tissue polarity is rapidly established in
In the described model, vascular cambium could be classified as “functioning” meristematic tissue, which actively produces cambial derivatives. Differentiation of cambial derivatives is a consequence of numerous periclinal divisions of fusiform cambial cells. Finally, the maturation of the cambial derivatives into secondary vascular tissue elements supported functionality of this meristematic tissue in the present model. The sequence of the changes could be useful for all comparative analysis of the cambium ontogenesis and xylogenesis both in
3.2. Secondary xylem formation in Arabidopsis stems
Reprogramming of the gene expression that accompanies xylogenesis and transdifferentiation of mesophyll cells into tracheary elements was extensively studied in
In
Patterning of vascular tissue and variety of tracheary elements developed as a dynamically operating water-conducting system and was extensively studied in the woody plants [13, 14]. However, mechanism regulating xylogenesis at cellular and molecular levels remains unclear, and many questions are unanswered. For example, differentiation of tracheids as a type of tracheary elements commonly found in trees, but for the first time detected in mechanically stimulated
3.3. Regeneration of vascular tissue in wounded Arabidopsis stems
In 1981, Sachs postulated canalization hypothesis according to which vasculature patterning is based on the positive feedback loop between auxin flow and cellular polarity. Consequently, in the primary uniform tissue, cellular auxin transporters emerge as the so-called auxin channels that transport the hormone through the tissue in the polar direction. Emergence of auxin channels is correlated with establishment of cellular polarity inside these specific auxin transport routs. Finally, new vessels develop directly along the auxin channels. Canalization hypothesis is strongly supported by many classical experiments with the incised plants, i.e., by wounding or grafting, which shows that emergence of auxin channels is correlated with increased auxin response and tissue repolarization [1, 2, 4, 5]. It is well documented that initially broadly elevated auxin response in wounded tissues is gradually restricted to narrow auxin channels, in which auxin level is still very high [4]. The obtained results showed that patterning of vascular tissue, explicitly visible during regeneration and new vasculature development, is dependent on new ways of canalized auxin flow.
Well-functioning vascular cambium plays the most important role for the secondary growth in the woody plants, both secondary xylem formation and stem thickness [14, 21, 22, 60]. Many results revealed an important role for this meristematic tissue during vasculature regeneration process. For decades analysis of vascular patterning and incised vascular cambium regeneration was restricted mainly to trees [61–63] because these woody plants undergo secondary growth with enlarged amount of secondary xylem (wood) and active cylinder of vascular cambium [64]. Studies were based mainly on the histological analysis, thus limited only to the final effects of regeneration. Thus, it was impossible to analyze vasculature regeneration, including vascular cambium, on the cellular and molecular levels. Some experimental studies on trees showed that in the wounded areas, the cambium and vascular tissue regenerate very fast both
Because of the difficulties in using woody plants as a convenient model system [52], mechanisms of cambium regeneration are still poorly understood. With the
Regeneration of vascular tissue in wounded
4. Role of plant hormone auxin and auxin transporters in vascular tissue development
Auxin is regarded as a multifunction plant hormone, which plays a fundamental role in developmental processes during organo- and morphogenesis. Auxin is a primary signal in regulation of many cellular processes, which control oriented divisions, cell elongation, or differentiation. At last, auxin is a key hormonal factor inducing vascularization—vascular tissue development, patterning, and regeneration. Polar auxin transport (PAT) manifested as physiological, basipetal direction of auxin flow represents a unique mechanism specific to plants. The cellular and molecular action of this process, explained in the chemiosmotic model, is based on auxin influx and efflux carriers, namely, AUX and PIN proteins, which actively participate in the cell-to-cell hormone transport [73–75]. The local auxin accumulation, its minima and maxima, or the so-called gradients in tissues are precisely controlled by this process.
4.1. Auxin as a primary signal inducing vascularization
The role of auxin as a primary signaling cue in vascularization has been widely discussed for decades. Experiments with radioactively labeled auxin show its maximum concentration in the meristematic tissues such as cambium [22, 57] and in adjacent cambial derivatives, differentiating into xylem [76]. Periodic fluctuation of auxin concentration in cambium influences the frequency of cambial cell divisions, production of cambial derivatives, and secondary vascular tissues. Disturbance of these correlations leads to many defects in cambium functioning and xylem formation. Using transgenic lines of
From the experimental studies on the vascularization
Several reports discussed auxin as a specific morphogenetic signal triggering cell fates during vascular tissue development and its maturation [78]. Locally created centers characterized by elevated auxin response become more competent for auxin flow through primarily uniform tissues. Auxin waves created in plant organs as a specific system of hormonal information that decide about realization of many developmental programs in plants, among them cambial activity and differential cambial responses [79, 80]. Thus analogically, gradual emergence of auxin channels and gradually narrowing auxin flow finally results in vascular strand differentiation. In other words, canalized auxin flux determined the paths of new vasculature development.
The canalization-predicted vasculature formation is especially observed during regeneration process, in new regenerated vessels after incision [1, 2, 4, 5, 8, 81]. Particularly important contributions to the role of auxin in the vascular tissue differentiation brought studies on
4.2. Role of auxin transporters in cellular and tissue polarity
The positive feedback loop between polar auxin flow and the polar, subcellular localization of the PIN-FORMED (PIN) auxin transport proteins [56] that, in turn, determine the auxin flow directionality is widely studied [53, 54, 84–86]. Many developmental processes, such as early embryogenesis or plant organ initiation, are strictly correlated with the establishment of local PIN-dependent auxin gradients that precede cell divisions and differentiation [54, 55, 87]. The expression of auxin efflux carrier genes, like
The role of auxin transporters in vascular tissue patterning is clearly visible in wounded inflorescence stems of
4.3. Auxin signaling pathways in vascular tissue patterning
Two related protein families—Aux/IAA and ARFs—are well-known key regulators of auxin-modulated gene expression and act in the TIR1-mediated signaling pathway [89, 90]. Members of ARF family share the characteristic arrangement of a highly conserved DNA-binding domain near the N-terminus, which appear to be capable to auxin response elements (AuxREs)—short conserved sequences (TGTCTC) that have been shown to be essential for auxin regulation of auxin-inducible genes [6]. It is likely that the ARF proteins are strongly involved in the vascularization downstream proteolytic SCFTIR1 complex machinery [80]. In support of this, an increased level of ARF transcripts was differentially regulated during the secondary growth, and three of them (ARF2, ARF4, and ARF5) had the most dramatic expression changes, indicating their putative roles in apical-basal signaling and xylogenesis [6, 42]. On the other hand, the
Auxin besides regulating a gene expression by the TIR1/AFB pathway can also inhibit internalization of the PIN proteins by a feedback regulation [92]. The underlying perception and signaling mechanism is unclear, but it does not involve transcription regulation and is distinct from the TIR pathway [93]. It may relay on the Auxin Binding Protein 1 (ABP1) since the ABP1 overexpressors increase the PIN internalization and mutations in the auxin binding pocket of ABP1 make the ABP1 effect on PIN internalization auxin-insensitive [88]; however, due to unreliable loss-of-function data [94, 95], this issue requires further clarification.
The identification of spatiotemporal gene expression pattern and the key components of auxin signaling pathway/pathways will greatly contribute to understanding of the molecular mechanisms involved in auxin-induced regeneration switch in cambial cells. In addition, the knowledge on genetic factors, such as ARFs, AFBs involved in the SCFTIR1 auxin receptor complex, PIN auxin efflux transporters, or AtHB family of early vascularization markers determining developmental plasticity of cambial cells, can be useful in genetic improvement of woody plants for environment and biotechnology purposes.
5. Genetic control of vascularization processes
Numerous genes differentially regulated during vascularization in woody plants are expected to be identified with the use of obtained
As indicated recently, transcription factor genes promoting secondary growth induction [42, 43] can be applied in genetic transformation to improve our knowledge on xylogenesis and regeneration capacity of woody plants. Several regulatory genes, like
The expression of the homeobox genes (
Homeostasis of vascular cambium with its non-disturbed functionality plays an important role in the vascularization [59]. However, genetic control of vascular cambium activity is poorly characterized. The role of the leucine-rich repeat receptor-like kinase (LRR-RLK) families in regulation of this lateral meristem homeostasis, underlying the role of
The most important role in the whole vascular-formation and regeneration machinery is played by auxin response genes referred to as early/primary auxin response genes. Three major classes of these genes,
Studies in the
It is widely postulated that important role in the vascularization is played also by gene expression that accompanies this process, like
6. Emergence of Arabidopsis as a good model system to study the vascular tissue formation and regeneration processes
For a long time, the herbaceous plant
Although the vascularization and regeneration in
The availability of numerous genetic and molecular tools in
7. Conclusions
Specifically manipulated
Knowledge about the molecular mechanisms regulating vascular tissue development in trees is incomplete, and such studies can take full practical advantages from a recently proposed new approach. Temporal analysis and experiments in trees are hampered mainly because of variability in environmental conditions, their long life cycle, and restricted amount of transgenic lines and mutants available.
Currently, new insights into the vascular tissue formation problematics can be obtained by using
Interdisciplinary scientific approach with the use of
Acknowledgments
This publication was funded by the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n° 282300.
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