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 ].
The most spectacular seems to be correlations between auxin response and tissue polarity during cambium ontogenesis in analyzed Arabidopsis stems. Already in the first few days, auxin concentration distinctly arises in the dedifferentiating parenchyma cells. At the early stages of the interfascicular cambium development, maximum auxin concentration is detected in parenchyma cells localized in the nearest neighborhood of vascular bundles, whereas in the later stages of this process, the zone of the cells with elevated auxin response is gradually extended toward the middle parts of the interfascicular regions, in the next few days after weight application [ 7 ].
The PINs are well-known auxin transport proteins involved in the cellular efflux of auxin and polar auxin transport in plant tissues [ 53 ]. In many developmental processes, the establishment of local PIN-dependent auxin gradient in cells is strictly correlated with cellular divisions and developmental reprogramming [ 54 , 55 ].
During analyzed process of cambium ontogenesis, tissue polarity is rapidly established in Arabidopsis stems. Amazingly, polarity of interfascicular parenchyma is indicated by polar localization of PIN1 auxin transport protein, which localizes at the basal plasma membranes of differentiating cells [ 56 ].
It has been documented that the protein appears in the basal plasma membranes of dedifferentiating parenchyma cells, not previously found in parenchymatic cells of immature mechanically noninduced Arabidopsis stems [ 7 ]. Moreover, both of the events—elevated auxin response and tissue polarization—are accompanied by periclinal divisions of the parenchyma cells Figure 3.
Divisions are temporarily correlated with the cellular events mentioned above and maintained in space. Namely, the first periclinally divided cells appear in the neighborhood of vascular bundles Figure 3A and B , but later the zone of dividing cells slowly extends toward the middle part of interfascicular regions. In consequence, parenchyma cells dedifferentiate into cambial cells, which definitely changes architecture of the interfascicular regions and decides about development of the interfascicular cambium Figure 3A.
According to the obtained results, it is tempting to conclude that auxin plays the most important role during cambium ontogenesis in Arabidopsis stems. Auxin seems to be a primary signal for cellular fate reprogramming and a crucial clue for stimulation of the dedifferentiational process in the interfascicular parenchyma zones. Periclinal divisions of interfascicular parenchyma cells and interfascicular cambium development in weight-induced Arabidopsis stems.
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 Arabidopsis model system and the analogical mechanisms studied in woody plants.
Thus, the mechanically stimulated Arabidopsis model with fully functional cambial meristem could help us in addressing the elusive vascularization mechanisms observed in the woody plants.
Reprogramming of the gene expression that accompanies xylogenesis and transdifferentiation of mesophyll cells into tracheary elements was extensively studied in in vitro cultures of zinnia Zinnia elegans [ 57 , 58 ]. However, the lack of the cambium stage in this experimental system prevents us from deciphering the role of cambium in wood formation.
Temporal gene expression pattern accompanies dedifferentiation of cambial cells into cambial derivatives, but their maturation into different types of tracheary elements is poorly characterized. Thus, numerous efforts have been focused on the identification of master regulatory genes required for this transition and revealing the key components of the vascular-differentiation-involved genetic network [ 48 , 59 ].
Periclinal divisions of the fusiform cambial cells lead to the development of secondary xylem derivatives in the early stage of xylogenesis. Changes in later stages of xylogenesis are correlated with maturation of cambial derivatives into tracheary elements and secondary vascular xylem development Figure 4.
During this process, such recognizable tracheary elements as vessels, fibers, or tracheids develop and create the layer of secondary xylem. Vessels are easily recognized, because of some diagnostic features such as secondary cell wall and open perforation plates on the opposite ends of the vessel members Figure 4C.
Vessels are arranged in threads of longitudinal strands in the vascular tissue. Amazingly, in the present Arabidopsis model, impressive variety of tracheary elements is detected, not previously documented in analyzed hypocotyls [ 37 , 38 ] or adult stems of Arabidopsis [ 39 — 41 ]. Secondary xylem in the weight stimulated stems of Arabidopsis. A Secondary xylem elements, like vessels and fibers, are produced from cambial derivatives after numerous periclinal divisions of fusiform cambial cells.
Cortex parenchyma is visible outside the secondary vascular tissues. B Schematic visualization of the tissue arrangement in stem and localization of the tissues showed in A is indicated by the square.
C Vessel strand developed parallel to longitudinal axis of stem. 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 Arabidopsis , led to important conclusions about the involvement of the artificial weight in wood formation.
Following stages of xylogenesis involving formation of the variety of tracheary elements, such as recognized tracheids, will be helpful in future analysis. In , 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. 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 in vivo [ 19 , 20 ] and in vitro [ 25 , 65 , 66 ]. Regeneration is accompanied by numerous anticlinal divisions of cambial cells and their dynamic intrusive growth [ 19 , 20 , 64 ], which finally leads to the reconstruction of vasculature and new vessel patterning in the incised regions [ 25 , 65 ].
In some instances, when the auxin flow is locally reversed, the so-called circular vessels develop [ 32 , 67 , 68 ]. In the nondisturbed woody plants, circular vessels are often found in branch junctions, above the axillary buds [ 68 ], whereas in incised plants, after transversal cuts and exogenous auxin application to stem segments, in wounded regions [ 32 , 67 ].
Accordingly, circular vessels occur in the form of rings and are presumably induced as a consequence of the circular auxin flow and the establishment of the circular polarity of individual cells that dedifferentiated into this type of vessels [ 67 ].
Thus, according to Sachs and Cohen [ 67 ], circular vessels develop as a response of individual cells to the auxin flux rather than to the high local auxin concentration. In nonwoody dicotyledonous plants characterized by primary tissue architecture, such as Phaseolus vulgaris , Pisum sativum , or Coleus sp.
New vessels are arranged either around the wound according to the presumable new auxin flow [ 69 ] or form the so-called bypass strands directly through the wound [ 3 ] or bridges between the neighboring vascular bundles [ 70 ]. Lack of the vascular cambium in the studied nonwoody plants restricted a detailed analysis of regeneration of this meristematic tissue and cellular events accompanying this process. Therefore in the used models, the most intriguing questions are still remained of answer: 1 what is the role of vascular cambium in vascular tissue regeneration?
Full verification of the postulated canalization hypothesis and identification of the molecular mechanisms accompanied vascular tissue regeneration are still limited. Because of the difficulties in using woody plants as a convenient model system [ 52 ], mechanisms of cambium regeneration are still poorly understood.
Thus, in control conditions, i. Otherwise, in incised stems i. As a consequence, new vessel strand arrangement is changed, because the new vasculature likely developed according to new directions of auxin cell-to-cell transport Figure 5. In wounded Arabidopsis stems, threads of new vessel strands develop above or around a wound Figure 5A and B , respectively. Interestingly, vessels above a wound regenerated faster, in the first days after wounding DAW 2 and 3 days , whereas vessel around a wound differentiated in the next few days, beginning the day 4 and circumventing the incised areas.
They developed from cells after their numerous, uneven divisions, what is commonly observed in the wounded tissue. The AtHB8 is positively regulated by auxin, and its extensive activity in wounded regions during vascular tissue regeneration suggested that AtHB8 might play a crucial role in the vasculature development [ 71 , 72 ].
The last observed way of vasculature regeneration is correlated with callus differentiation Figure 5C. Namely, in wounded areas vessels develop from previously proliferated callus tissue cells. Paths of vessel regeneration in wounded Arabidopsis stems. A Threads of short vessel members developed above a wound.
B Vessel strands regenerated around a wound. Arrows indicate regenerated vessel strands. Regeneration of vascular tissue in wounded Arabidopsis stems is accompanied by temporal and spatial changes following new vessel development. New vessel strands regenerated in the incised regions around a wound develop as a consequence of cambial cell regeneration.
Longitudinal continuum of vascular cambium is disturbed after the transversal cut. In such experimental system, rapid auxin response is found as a primary signal of the regeneration.
Merely at the first day after incision, elevated auxin concentration is observed above a wound and in the next few days also around a wound [ 8 ]. Vasculature regeneration is strictly correlated with tissue repolarization and establishment of new polarity in neighborhood of the wound.
Tissue repolarization always preceded emergence of PIN1-positive auxin channels Figure 6. As a consequence, layer of new vessels develops around a wound, and the regenerated vasculature becomes enlarged in the days following the incision.
Analysis of regeneration process in incised Arabidopsis stems strongly supported canalization hypothesis. Emergence of new vasculature is correlated here with elevated auxin response and changed polarity in auxin channels, from which new vessel strands develop in the wounded areas. 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. 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 Arabidopsis , elevated auxin response is easily found just in the cambial cells of both types of cambia Figure 7.
Auxin concentration is very high in the fascicular cambium bands, primary meristematic tissue in the vascular bundles Figure 7 , as well as in the interfascicular vascular cambium on the stem circumference Figure 7.
Elevated auxin concentration in cambium of non-incised Arabidopsis control stems. From the experimental studies on the vascularization in vitro , it appears that parenchyma callus tissue is the most convenient for the analysis.
Previously uniform callus can form vascular tissue bands or groups of vessels differentiation. However, the process can be realized only in the sufficiently thick callus tissue. It is shown that differentiated xylem in surrounded by cambium-like cells, which additionally are able to produce phloem elements in the inner callus regions.
Auxin-dependent vascularization is also shown in the studies with young Syringa sp. Combination of auxin and sucrose decides about the induction of vascularization in the axillary buds in vitro.
Moreover, dependent on the hormone and sucrose concentration, varied vascular tissues develop. 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 Pisum sp.
According to all experiments performed by Sachs, vascularization depends on the polar auxin transport, and new vascular band induction depends on the auxin concentration and polarity. Moreover, the early stages of vascular band differentiation are related to the canalization of the polar auxin flow.
A key role of auxin in promotion of canalized flow by itself and transport channels formation is commonly accented. However, the feedback mechanism between auxin flow, polarity, and vessel formation as a response to concentration gradients or directional auxin fluxes remains unclear [ 82 , 83 ]. 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 ]. Changes in PIN localization and tissue polarity in response to auxin that are presumably related to the directional vascular tissue patterning have been observed and modeled [ 4 , 5 , 46 , 88 ].
Moreover, in wounded pea or bean epicotyls, the PIN polarity was gradually rearranged marking the position of differentiating vessel strands [ 4 , 5 ]. Emergence of auxin channels is here visualized by PIN1 expression of the cellular auxin transporters. In Arabidopsis model with mechanically stimulated inflorescence stems, the subcellular PIN1 position was gradually stabilized and restricted only to cell sides in a first few days after weight application, along the presumable direction of the auxin flow [ 8 ].
Dynamic expression of both of the genes and gradual establishment of polarized PIN1 protein localization indicates the direction auxin flow during the vascular tissue patterning in analyzed leaves [ 47 ]. The role of auxin transporters in vascular tissue patterning is clearly visible in wounded inflorescence stems of Arabidopsis , during vascular cambium regeneration [ 8 ].
Rapid tissue repolarization indicated by reposition of PIN1 at cellular plasma membranes of differentiating cells is emphasized. Dynamic temporal changes in tissue polarity are correlated with varied auxin response and its accumulation above and around a wound. Whereas auxin concentration arises in few hours after wounding, maximum of auxin levels is established at auxin channels and preceded establishment of new polarity in wounded areas of Arabidopsis stems.
Cellular auxin transporters are characterized with changed position of PIN1 proteins. Thus, direction of auxin flow through the auxin channels is precisely determined. Both of the events are strictly correlated with each other and play a decisive role in vascular tissue development. 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 ].
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 ].
The underlying perception and signaling mechanism is unclear, but it does not involve transcription regulation and is distinct from the TIR pathway [ 93 ]. In addition, the knowledge on genetic factors, such as ARFs, AFBs involved in the SCF TIR1 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.
Numerous genes differentially regulated during vascularization in woody plants are expected to be identified with the use of obtained Arabidopsis model. Many of the genes were indicated to be involved in auxin responses implicating auxin engagement in regulation of vascular tissue development and patterning [ 42 , 43 ], and the same is expected for vascular tissue regeneration. Experimental data have proven a key role of auxin in variety of developmental processes [ 80 ]; however, the molecular, auxin-mediated mechanism involved in vasculature regeneration remains mostly unknown.
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. ANT regulates organ growth through the maintenance of meristematic tissue activity. The expression of the homeobox genes AtHB s is highly increased during xylem production and regarded as a positive regulator of the activity of procambial and cambial cells to differentiate [ 71 , 72 ].
Baima et al. Extensive activity of this gene was found in the regenerated tissues, suggesting intensive transcriptional reprogramming during new vessel development. In the model with functioning vascular cambium, expression of AtHB-8 is observed in differentiating cambial derivatives, in early stages of their maturation into the vessels Figure 8. The AtHB8 gene expression in differentiating vessels.
Longitudinal tangential section through the basal part of stem. 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. Two receptor-like kinases MOL1 more lateral growth1 and RUL1 reduced in lateral growth1 identified as opposing regulators of cambium activity were also reported [ 59 ].
Recently, the role of the homeobox transcription factor WOX4 wuschel-related homeobox 4 , as an essential cambium regulator positively regulated by PXY , has been revealed [ 59 , 97 ]. Plants, like other organisms, can be viewed as integrated systems that include different organs as well as specialized tissue and cell types related to particular functions of the different organs.
Plants consist generally of roots , stems and leaves. The roots are mostly underground, whereas the other two organs are mostly stems or entirely leaves above the ground and are together known as the shoot system. The three types of tissue in plants are ground tissue, dermal tissue and vascular tissue. All three organ types contain some of each type of tissue, though not in equal proportions. The different cell types included in vascular tissue — tracheids, vessel elements, companion cells and sieve tubes — are discussed later.
The first vascular plants date back to about to million years ago, which makes these trees close to eight times as old as mammals as a point of comparison, dinosaurs are believed to have gone extinct about 65 million years ago. These plants had no roots or leaves, only stems that served all of the functions of these early plants. Some of these plants from the far reaches of biological antiquity remain on Earth today. For example, lycophytes , which are nondescript in the present time, once featured individual plants that were over 35 meters about feet tall.
Xylem and phloem are two well-defined types of vascular tissue. Perhaps the most notable distinction between them is that xylem, which makes up most of the substance of wood, consists of the cell-wall remains of dead cells, whereas xylem contains living cells that include cytoplasm and cell membranes.
Xylem transports water and minerals from the ground up through the stem of the plant to the leaves and reproductive apparatus. Phloem, which runs mostly outside xylem the two always appear concurrently , conducts sugars and other nutrients made during photosynthesis to other sites in the plant. Xylem includes specialized cells called tracheids and vessel elements. Tracheids appear in all vascular plants, while vessel elements are found only in certain species, such as angiosperms.
These cells are tubular, as befitting structures meant for moving water, and they have openings called pits at their ends to allow some water to be exchanged between different cells. As noted, these cells are dead when they are functioning, with only their cells walls remaining. Phloem includes specialized cells of its own: sieve cells and companion cells. Sieve cells conduct sugars and other small molecules, and the cells have sieve plates at the end whose function is similar to that of pits in xylem cells.
While alive at maturity, they are nevertheless missing most of their original internal components.
0コメント