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Forests 2019, 10(4), 358; https://doi.org/10.3390/f10040358

Review
What Makes the Wood? Exploring the Molecular Mechanisms of Xylem Acclimation in Hardwoods to an Ever-Changing Environment
Forstbotanik und Baumphysiologie, Georg-August Universität Göttingen, Büsgenweg 2, 37077 Göttingen, Germany
*
Author to whom correspondence should be addressed.
Received: 28 February 2019 / Accepted: 23 April 2019 / Published: 25 April 2019

Abstract

:
Wood, also designated as secondary xylem, is the major structure that gives trees and other woody plants stability for upright growth and maintains the water supply from the roots to all other plant tissues. Over recent decades, our understanding of the cellular processes of wood formation (xylogenesis) has substantially increased. Plants as sessile organisms face a multitude of abiotic stresses, e.g., heat, drought, salinity and limiting nutrient availability that require them to adjust their wood structure to maintain stability and water conductivity. Because of global climate change, more drastic and sudden changes in temperature and longer periods without precipitation are expected to impact tree productivity in the near future. Thus, it is essential to understand the process of wood formation in trees under stress. Many traits, such as vessel frequency and size, fiber thickness and density change in response to different environmental stimuli. Here, we provide an overview of our current understanding of how abiotic stress factors affect wood formation on the molecular level focussing on the genes that have been identified in these processes.
Keywords:
wood formation; abiotic stress; nutrition; gene regulation; tree

1. Introduction: The Xylem Keeps the Stream of Life Flowing

The main function of the xylem besides granting plant stability is to ensure long-distance water transport driven by water transpiration from the leaves to the atmosphere [1,2]. Therefore, xylem vessels are connected to each other in order to form a large conduit system throughout the plant. During vessel formation, the cell wall between two adjacent vessel cells is degraded to build a continuum. A measure for the water transport capacity within the xylem is xylem hydraulic conductance, which is, among other factors, determined by the size of the xylem vessels. Vessels with higher diameter facilitate faster water transport, thereby resulting in a higher hydraulic conductance. The volumetric flow rate is proportional to the fourth power of the vessel radius according to the Hagen-Poiseuille law [3,4]. Thus, a small reduction in vessel lumen already results in a large reduction of hydraulic conductivity. A severe danger for plant viability is a disruption of this water flow, called embolism, which primarily occurs at the bordered pits [5,6]. When the conduits are filled with air or vapor instead of xylem sap, cavitation stops further water flux. This process is considered as one of the most life-threatening phenomena for plants [3,7]. Cavitation results in non-functional water conduits, which leads to a reduction in hydraulic conductivity and stomatal closure, thereby reduced photosynthetic activity, which finally can lead to the plant´s death [5,8]. It is therefore crucial for plants to develop mechanisms to prevent cavitation by modulating their xylem structure. The major adjustment is to form vessels with smaller diameter to reduce the risk of cavitation. An additional mechanism is to increase vessel stability, achieved by increasing vessel cell wall thickness [9]. As a result, vessel lumina decrease [9]. To counteract the reduction in hydraulic conductivity per vessel plants can increase the number of vessels in their xylem [9,10,11]. In this review, we will summarize the current knowledge on the molecular regulation of xylem acclimation in angiosperms with the focus on Populus species and identify knowledge gaps.

2. Anatomy and Molecular Biology of Wood Formation

2.1. What Makes the Stem?

Growth depends on the presence of cells, which are able to undergo division and differentiation processes. These cells are designated as stem cells [12]. In plants, four layers of stem cell harboring tissues are present: the root apical meristem, the shoot apical meristem, the vascular meristem (cambium) and the cork cambium. While the apical meristems are primarily responsible for longitudinal growth, which is not within the scope of this review, they also contribute to radial growth to a certain extent during primary growth. During primary growth of the stem, the stem cell layer deriving from the shoot apical meristem is designated as pro-cambium, which gives rise to the proto-xylem [13]. The procambial cells divide asymmetrically either into proto-phloem or proto-xylem precursor cells. Proto-phloem precursor cells further differentiate into sieve elements, phloem fibers, phloem parenchyma cells and companion cells, while proto-xylem precursor cells further diversify into xylem vessels, xylem fibers and ray parenchyma cells. The wood generated by the activity of the pro-cambium is designated as proto-xylem. An excellent overview on wood formation during primary growth has been published by Furuta and colleagues [14].
Wood is produced from the activity of vascular cambium that is composed of meristematic initials, which either differentiate to either phloem or xylem precursor cells. Xylem precursor cells further diversify into vessels, fibers and parenchyma cells in order to build up the xylem in angiosperms (Figure 1).
Secondary growth is what makes up the girth of the stem by generating the majority of the wood. The correct botanical denomination of this secondary wood is meta-xylem. It is also comprised of the three major components, vessels, fibers and parenchyma cells formed by the activity of the cambium. It should be noted that vessels are often surrounded by small living cells, the paratracheal parenchyma, which has important functions in the transport of compounds for example in Populus tremula x tremuloides, Fraxinus excelsior and Acer pseudoplatanus [15].
A major difference between the proto- and meta-xylem is the deposition of the secondary cell wall (SCW) compounds leading to structural differences: the SCW of proto-xylem vessels is build up in a helical shape, which allows for continuous growth as the SCW can be elongated during longitudinal growth [16]. The SCW of meta-xylem is deposited directly onto the primary cell wall resulting in a rigid structure around the vessel that is no longer able to expand.
The SCW is a complex structure, which is primarily composed of cellulose, hemicelluloses and lignin with addition of pectin and cell wall proteins. The composition of the SCW varies within the plant kingdom, e.g., in angiosperms SCWs contain 40%–50% cellulose, 20%–30% hemicelluloses and 25%–30% lignin [17]. Cellulose is a linear homopolymer of β-1,4-linked D-anhydroglucose molecules forming cellulose chains of varying length. These cellulose chains are then connected via Van-der-Waals interactions and hydrogen-bonds to form cellulose micro fibrils [18]. In contrast to cellulose, hemicellulose is chemically complex, consisting of polysaccharide heteropolymers of hexose and pentose sugars with a β-1,4-linked backbone of xyloglucans, xylans, mannans and glucomannans with a vast variety of side chains [19]. The main function of hemicellulose is the interconnection of cellulose micro fibrils and lignin [20]. Lignin provides rigidness and recalcitrance to the cell wall, with strong impact on wood properties by adding extra strength and water impermeability [21]. Lignin is built up by three phenylpropanoid compounds, also designated as monolignols: coniferyl alcohol (G), sinapyl alcohol (S) and p-coumaryl alcohol (H) [22] with G and S subunits being the main building blocks for lignin in angiosperms [23,24]. The combination of these monolignols via radical coupling constitutes a complex polymer, the composition of which varies with developmental and environmental stimuli. Interestingly, the lignin composition is also specific for different cell types, e.g., the lignin in fibers differs significantly from those of vessel elements as it shows a higher content of S-subunits [25].
Wood formation is, thus, characterized by a succession of four major steps, including cell division, cell expansion (elongation and radial enlargement), cell wall thickening (involving biosynthesis and deposition of cellulose, hemicelluloses, lignin and cell wall proteins), and finally programmed cell death [26].

2.2. Molecular Mechanism of Wood Formation

Our understanding of the molecular mechanisms of xylogenesis has massively increased in the last two decades. Several detailed reviews about the molecular mechanisms of wood formation have been published [13,16,26,27]. Here, we will shortly summarize the main aspects important for understanding the impact of environmental stimuli that alter wood formation (Figure 2). Wood formation is tightly controlled by two classes of transcription factors (TFs), namely the NAC family and the MYB family. Using Arabidopsis thaliana as a model system, several members of these two TF families have been shown to work in a hierarchical manner to regulate the transcription of genes necessary for wood formation [26]. The first level master switches all belong to the class of NAC TFs and their activation is crucial for the cell identity of wood cells. For example, SND1, NST1 and NST2 are responsible for fiber development, while VASCULAR-RELATED NAC DOMAIN 7 (VND7) controls differentiation of the proto-xylem and VASCULAR-RELATED NAC DOMAIN 6 (VND6) of the meta-xylem [28,29]. Several orthologs of these A. thaliana genes have been identified in Populus trichocarpa (Table 1). It is somewhat confusing that these master switch TFs are not termed VNDs, as in Arabidopsis but were named WOOD-related NAC DOMAIN (WND) transcription factors, yet they also belong to the family of NAC TFs and are closely related to the A. thaliana genes [30]. The expression of these master switches is modulated by fine-tuning factors like the HD-Zip transcription factors PtrAtHB.11 and PtrATHB.12 or PtrE2FC.1 [31,32]. The master switch WNDs further activate a group of MYB master switch TFs (PtrMYB2, PtrMYB3, PtrMYB20, PtrMYB21, [33,34]), which either directly regulate the biosynthesis of cellulose, hemicellulose, and lignin or lead to the activation of down-stream MYC and NAC TFs that promote or decrease the expression of cell wall biosynthesis genes (Table 1, Figure 2).
Cell wall biosynthesis requires the production of cellulose strands by cellulose synthases (CesA), which are homologs of prokaryotic celA genes [35] and were firstly characterized in the plant kingdom in A. thaliana [35]. The CesA proteins are localized across the plasma membrane using intracellular UDP-glucose to generate cellular strands towards the outside. Meanwhile, a whole CesA gene family comprised of 18 genes, of which four show xylem specific expression patterns, was discovered in P. trichocarpa [36,37]. A recent study revealed that during xylem formation, two different types of CesA complexes are necessary for cell expansion and cell wall thickening in Arabidopsis, indicating that CesA complex composition is dynamically changing [38]. Since these processes also occur in trees, it is likely that a similar mechanism is also present in woody plants, although there is no experimental evidence up to now.
The cell wall of the meta-xylem in trees is heavily lignified. Lignin biosynthesis is a very complex process starting with aromatic amino acids, mainly phenylalanine [39]. The main classes of dedicated enzymes required to produce lignin building units are 4-coumarate:CoA ligases (4CL), caffeic acid O-methyltransferases (COMT), cinnamoyl-CoA reductases (CCR), and cinnamyl alcohol dehydrogenases (CAD) [22]. Monolignols are transported from the cytosol into the cell wall [40], where they are polymerized by peroxidases (POD) and laccases (LAC), yielding lignin. However, only very few monolignol transporters have been identified by now, such as the Arabidopsis p-coumaryl alcohol transporter AtABCG29 [41,42].
As outlined above hemicelluloses are also very complex molecules. Therefore, it is not surprising that a variety of enzymes is necessary for their synthesis. These enzymes are summarized as Cellulose Synthase-Like (CSL) proteins [43], of which 30 have been identified in poplar [37]. Four CSL genes (PtrCSLA1, PtrCSLA2, PtrCSLA5, PtrCSLD6) are predominantly expressed in the xylem [37].
This rough overview on the regulatory mechanisms and main processes that are required for the main cell wall compounds provides only a glimpse into the complexity of the underlying processes. The composition of wood is important for its further use, e.g., as construction material, where durable material is necessary and for paper making, where fibers of a certain length are favorable, or for secondary biofuel production where easily accessible cellulose is needed. Therefore, it is not only important to know how wood is being produced, but also to understand how wood properties are changed in response to environmental cues.

3. Abiotic Stresses Affecting Wood Formation

3.1. Drought Severely Changes Xylem Anatomy

Drought has a major impact on wood and wood formation processes. Since the xylem is the tissue that enables water transport throughout the whole tree, it is pertinent to keep the xylem architecture intact and to acclimate it to changing water supply to prevent embolism [44,45]. The effects of drought on xylogenesis have been studied on several angiosperm species over the last decade. Poplar, in particular, was intensely studied [46,47]. Cambial cell layers are reduced under drought compared to well-watered plants [10,48]. When growth is still possible under water-limited conditions, poplars, regardless of whether they originate from dry or moist habitats, show reduced vessel lumina and an increased number of vessels compared to non-stressed plants (Populus x canescens, [49]; Populus euphratica, [11]; different Populus nigra genotypes originating from dry and moist areas, [10]), Figure 3). Moreover, Schreiber and colleagues reported a strong correlation between vessel diameter and cavitation resistance in five hybrid poplar clones in Alberta, Canada [50]. However, these acclimatory anatomical changes are not only confined to water-spending trees species like poplar but also to more drought tolerant species such as oak depending on the level of acclimation (Quercus pubescens > Quercus robur > Quercus petraea, [51]). The importance of this safety strategy is further corroborated by a study on dead trees performed in Italian forests [52]. Here, the authors compared the wood anatomy of dead trees to that of surviving trees of the same age. They found that dead trees had formed wide early vessels and no vessels with reduced lumen during dry periods in contrast to trees that survived this period [52].
Taken together, these studies suggest that angiosperms have developed a common mechanism to acclimate their xylem to increasing drought. The xylem, as stated earlier, is formed by vessels and fibers, with the vessels forming the pipe system that facilitates water transport [26]. Under drought the plant has to fortify the vessels by thickening the secondary cell wall to prevent cavitation, which results in a reduced water transportation rate due to diminished vessel lumina [11]. To compensate the loss in vessel lumen, more vessels are formed to restore the water transportation rate that is necessary for tree growth (Figure 3). Improving the resistance against drought-induced xylem cavitation is a crucial acclimation mechanism of plants to dry environments [8,53]. It is notable that these alterations resemble those of seasonal acclimation of wood to shorter day lengths and cold, which lead to the formation of tree rings. Tree rings are a result of changes in the activity of xylem building processes [54]. Interestingly, Arend and Fromm observed in 2007 that trees responded to drought with smaller vessel lumina only during the main growth season but not in fall, when late wood with small lumina was formed [48]. Still, controlled experiments to disentangle temperature and day lengths effects on wood anatomy and the impact of drought under these conditions are lacking.

3.2. Drought Leads to Major Transcriptional Remodelling

The molecular mechanism behind the reduction of vessel volume and cell wall strengthening has not yet been unravelled. One important tool to tackle this question is the analysis of wood transcriptomes to identify key genes in this acclimation processes. Wildhagen and colleagues (2018) found an altered expression of genes involved in cell wall polysaccharide biosynthesis (e.g., xyloglucan endotransglucosylase/hydrolases, UDP-XYL synthase 6, expansin A) in three poplar genotypes. This finding suggests that denser wood under drought is achieved by regulation of cellulose and hemicellulose biosynthesis; notably the lignin content was unaltered [10]. These changes unexpectedly resulted in a higher saccharification potential of wood formed under drought compared to wood of well-irrigated poplars [10]. If these changes were also responsible for the reduction in vessel volume has not been clarified yet. Vessel expansion depends on the activity of potassium (K+) uptake transporters (e.g., PtrKUP1) and outward rectifying K+ channels (e.g., PTORK) [55]. In agreement with a high requirement for K+ to regulate turgor pressure, the cambium contains the highest K+ concentrations [56]. Furthermore, KUPs show seasonal regulation with high expression levels in wood [57]. Since drought limits K+ acquisition from the soil [58], it is possible that changes in the osmotic control influence vessel size. However, this suggestion is currently speculative as an impact of drought on K+ channel transcription levels has only been reported for an ortholog of the Arabidopsis KUP2 which is positively correlated with fiber lumen under drought in P. nigra [10]. In addition, the concentration of soluble non-structural carbohydrates, sucrose in particular, has a major impact on vessel expansion. It has been shown that sucrose accumulation in the cambium correlates with cambial activity and cell expansion phase during xylogenesis in Populus x canadensis Mönch ‘I-214’ [59]. Interestingly, transgenic Populus tremula x alba suppressing the expression of the vacuolar sucrose efflux transporter PtaSUT4, are more susceptible to moderate drought compared to wild type plants. This suggests that sucrose also plays an important role in drought acclimation in addition to seasonal wood formation [60].
In addition to its influence on wood anatomy, drought has also major impact on the genes putatively involved cell wall biosynthesis. For instance, in P. trichocarpa, 119 genes related to cell wall organization, carbohydrate metabolism, and lipid metabolism were significantly differentially expressed. Among these genes four master switch regulators (PtrWND1, PtrWND1B, PtrWND2A, PtrWND2B) which are orthologs of the Arabidopsis ANAC043 (Table 1), as well as the secondary level regulators PtrMYB2, PtrMYB21 and Potri.009G061500 (an ortholog of Arabidopsis AtMYB83, Table 1) were downregulated [61], indicating major changes in the transcription of cell wall biosynthesis genes. Additionally, 29 laccases-encoding genes were also found to be differentially regulated [61]. Except for one laccase all other laccases were downregulated under drought [61]. These findings corroborate major changes in cell wall composition, though biochemical analyses were not conducted. It is clear that the supply with energy and precursors of cell wall components, especially carbohydrates, has to be sustained under drought since earlier studies showed strong correlations between growth and cambial carbohydrate concentrations [62]. However, transcriptome analyses also identified many genes involved in lipid metabolism [10,61]. There is now accumulating evidence for the role lipids in SCW formation: metabolomic and transcriptomic analyses revealed links between decreasing concentrations of sterols and fatty acids with increasing transcript levels of genes involved in β-oxidation and the glyoxylate cycle required for the production of carbohydrate precursors for SCW [63,64]. Transcriptome analysis of Eucalyptus xylem revealed a putative UDP-glucose:sterol glucosyltransferase, which produces sitosterol-cellodextrin. This molecule serves as a primer the elongation of β-1,4-glucan strands by the cellulose synthases [63,65]. These lipoglucan primers are discussed as being responsible for elongation by a special CesA isoform [66], forming a possible indirect link to channel carbon from lipids towards cellulose.
Other players, whose role in regulating drought acclimation has not yet been understood, are micro RNAs (miRNAs), which are widely known to function as regulatory molecules in gene expression under stress conditions [67,68]. A recent study identified five up- and seven down-regulated miRNAs in P. trichocarpa under drought stress, which in total regulate 72 targets according to degradome analysis. Among these were four UDP-glucosyl transferases, which transfer sugars to target molecules and have been shown to build up β-1,4-glucan from UDP-activated glucose [69,70].
It is important to mention that trees can recover from xylem embolism to a certain extent. To re-establish the water flow in the xylem it is necessary to refill the vessels [45]. Although this process is not yet fully understood, there is substantial evidence that paratracheal parenchyma cells also designated as vessel-associated cells (VACs) play an important role in this process [71]. As stated earlier, VACs are living cells surrounding the xylem vessels, which makes them ideal candidates to facilitate the refilling process [15]. To refill the vessels with water, a change in the osmotic gradient between VACs and vessel cells is indispensable. The most important osmotic compound in this regard is most likely sucrose [72]. Experimental evidence has been provided by mimicking xylem embolism in P. trichocarpa [72], which resulted in enhanced expression of α-amylases (PtrAMY1, PtrAMY2, PtrAMY3) leading to a reduction in starch content in the VACs [72]. Simultaneously, the expression of sucrose transporters (PtrSUT2a and PtrSUT2b) as well as aquaporins (PtrPIP1.2, PtrPIP1.4, PtrPIP1.5, PtrPIP2.2) was upregulated. These findings support that upon xylem embolism, starch is degraded to sucrose, which is transported from the VACs to the vessel cells leading to enhanced water uptake of the vessel cells via aquaporins. Upregulation of aquaporins of the PIP1 and PIP2 family in VACs has been observed in several tree species (P. trichocarpa [72,73,74], Populus x ‘Okanese’ [75], Juglas regia [76]), substantiating the hypothesis of VAC-mediated refilling of vessels upon embolism. It is still under discussion as to whether the VACs store sufficient carbohydrates for this process or if they are replenished by carbohydrate export from the phloem during embolism recovery [77].

3.3. Phytohormones Mediate Xylem Changes under Drought

Although transcriptomic studies have strongly enhanced our knowledge on plant drought responses and growth regulation, they cannot elucidate the underlying signals. In this regard phytohormones such as cytokinins, auxin, abscisic acid (ABA) and many others play crucial roles. The major plant hormone mediating drought stress is ABA [78,79]. Although drought has drastic effects on xylem formation, it is still unclear if ABA plays a direct role in regulating wood formation process. Circumstantial evidence suggests a role of ABA in fall for late wood formation because the concentration of ABA in the cambium increases in fall when cells with small lumina and thick cell walls are produced [80]. Reduction of stem radial growth under drought stress is accompanied by a strong increase in cambial ABA concentrations [81]. Therefore, ABA might play a negative role in secondary xylem development similar to that found for its function regulating bud dormancy [82], but no direct evidence on cellular or molecular level has been reported so far. An alternative suggestion was that enhanced ABA concentrations in fall might influence stomatal aperture, thereby leading to a decline in carbon fixation and consequently in a reduction in stem growth [83]. It is also possible that ABA interacts with the activity of auxin inhibited xylem initiation [84]. To understand the effect of ABA on wood formation in different environments it is necessary to get more insight on the molecular basis of wood formation and to identify the genes in ABA signaling which may affect the regulation of wood cell development. The first evidence for this idea was found in Arabidopsis, where ABA-dependent upregulation of the vessel specific master switch genes VND2, VND4 and VND6 was observed resulting in enhanced xylem differentiation [85].
Another important class of phytohormones involved in drought acclimation are cytokinins, trans-zeatin, kinetin and 6-benzylaminopurine in particular. Cytokinins are generally referred to as growth promoting phytohormones by initiating cell division (reviewed by [86]). Together with ethylene and auxin, cytokinins regulate cambial activity. In poplar, overexpression of the Arabidopsis CYTOKININ OXIDASE 2, an enzyme involved in cytokinin catabolism, resulted in non-detectable levels of the cytokinin trans-zeatin and its storage form zeatin-O-glucoside and lead to a reduced number of cambial cells, resulting in impaired wood formation [87]. Moreover, cytokinin activity was high in primary meristems supporting its function in early wood formation processes [88] and reduced in the cambial zone of drought stressed poplar, indicating a regulatory function of cytokinins under drought stress [89]. There is now increasing evidence that cytokinins interact with jasmonic acid. A reverse genetic approach showed that application of 10 μM methyl-jasmonic acid promotes xylem development in Arabidopsis roots [90]. In addition, exogenous application of jasmonic acid reduces the cytokinin responses in regard to xylem formation. A follow-up study provided evidence that drought stress also induces xylem development by increasing jasmonic acid responses and diminishing cytokinin responses [91]. These results imply that cytokinin activity is a negative regulator of xylem development under drought stress while jasmonic acid promotes xylogenesis. The molecular mechanism how cytokinins mediate xylem development is not yet fully understood, but it was shown that external application of 50 ng/mL kinetin downregulates the expression of the vessel specific master switch genes VND6 and VND7, which are important for proto- and meta-xylem differentiation [28]. Cytokinins are known to induce cell wall loosening expansion genes [92,93]. Application of 6-benzylaminopurine has a negative effect on cell wall thickness [94]. These findings corroborate the function of cytokinins as negative regulators of secondary xylem, yet there is still plenty of research necessary to identify the role of specific cytokinins in these processes.
Cytokinin levels in plants are affected by nitrogen supply and are implicated in stress responses [95,96]. It is possible that they also mediate nitrogen effects in wood. Under nitrogen starvation, wood properties resemble those of wood produced under drought with smaller vessel lumina and thicker fiber cell walls [97]. Under these conditions, secondary cell wall related transcription factors, like members of MYB, bHLH, WRKY and WD40 gene families, are up-regulated, leading to increased cell wall formation [97,98,99]. In contrast, under high nitrogen availability the secondary cell walls of fibers and vessels are thinner and the vessel lumina are expanded [97,99,100].
Notably, changes in nitrogen supply affected ABA and JA [101], which are known to mediate stress responses. Synergistic effects of drought stress and nitrogen availability, which both influence wood formation [101,102,103,104,105] have been noted [106,107,108]. For example, when water and nitrogen are sufficiently available, water supply increases nitrogen uptake, leading to larger vessel lumina and in turn to higher susceptibility to drought stress [109,110,111]. SCW-related genes are not suppressed by drought under high nitrogen supply, only under nitrogen limitation [112]. Consequently, water and nitrogen deprivation has a negative synergistic effect on secondary growth compared to either limitation alone [112,113]. These examples show that drought stress impacts on xylem development at different levels, clearly as an osmotic stress as demonstrated by PEG studies but also via its influence on tree nutrition. To generate or select more drought-resistant trees, it will be necessary to disentangle the complex hormonal network with emphasis on the mechanism of phytohormone accumulation, the transition of active to inactive forms and the turnover to identify the key mechanisms how water limitation affects xylem anatomy and cell wall composition.

3.4. Salt Severely Affects Wood Formation

Survival and productivity of trees are affected by salt through different processes, mainly related to osmotic stress, nutritional imbalances or ion toxicity [114,115]. High salt concentration within the plant itself can be toxic, resulting in the inhibition of many physiological and biochemical processes. Saline environments restrict the ability of plant to take up water and, therefore, reduce plant growth [116]. Uptake of salt facilitates water uptake and has been identified as a tolerance mechanism in poplars, P. euphratica in particular, which are acclimated to salt deserts [117]. Hence, the xylem originating from salinity affected meristem also exhibits modifications in its anatomical and chemical aspects [118]. It has been shown that salt stressed poplars have a reduced number of cell layers in cambial zone compared to control plants, indicating growth reduction [119]. Similar to drought-stressed poplars, vessel lumina of salt-exposed trees are reduced [119,120] and the vessel frequency is increased [121]. The sensitivity of these anatomical alterations to salt exposure depends on the salt-sensitivity of the species. For example, the salt-sensitive poplar species P. x canescens reacts strongly to moderate NaCl levels, while the salt-tolerant P. euphratica shows diminished cambial activity and decreased vessel lumina only after long-term exposure to higher salinity levels, i.e., 150 mM NaCl [120,121]. Among other reasons, diminished nutrient supply, in particular lower calcium and potassium supply caused decreased xylem radial growth under salt stress [119].
Salinity impairs the tree water status and may increase tension in the water-conducting system, promoting cavitation and subsequently, embolisms [118]. However, trees can reinforce the wall strength of conducting cells so as to prevent against vessel collapse under osmotic stress [122]. This phenomenon is also found in poplar vessel cell walls, which show a significant increase in strength when exposed to salinity [120]. Furthermore, increased vessel frequencies can at least partly compensate negative effects on hydraulic efficiency [121]. Cell wall reinforcement under salt stress goes along with drastic alterations in major wood compounds such as cellulose, hemicelluloses, and lignin [121]. The transcriptional changes found under these conditions were opposite to those found during tension wood formation in poplar [121]. Therefore, the type of wood developed under salinity was termed “pressure wood” [121].
Since the anatomical changes in secondary xylem under salt and drought stress might be of similar nature, the question arises if there are similar hormones involved in these processes. The activity of the vascular cambium largely determines the rate of wood formation and is strictly controlled by the interplay of several phytohormones [123]. Early studies demonstrate that a concentration gradient of auxin across the cambial zone regulates cell division and expansion of the xylem elements [124,125,126]. Osmotic stress in plants is known to influence auxin transport [127]. Using an auxin responsive reporter gene construct (GH3:GUS), an impact of salt on auxin activity was shown in poplar wood [128]. Associated with wood alteration, free-auxin levels decrease in developing xylem under salt stress. In contrast to salt susceptible grey poplar (P. x canescens), the salt tolerant P. euphratica shows only little reduction in auxin and moreover, an increase in indole-3-acetic acid-amido conjugates, which can be used as a source of auxin [120]. Overexpression of auxin amidohydrolase (ILL3) from poplar in Arabidopsis rendered the plants more salt tolerant [120], indicating an important function of auxin in salt acclimation. The signaling pathways show how auxin and other plant hormones affect gene regulation remains elusive.
Recent transcriptome comparisons of salt treated and non-stressed eucalypt trees uncovered responses of a large number of transcription factors (TFs) including members of the MYB TF family [129] to salt. Upregulation genes encoding transcription factors (EgrMYB20, EgrMYB47 and EgrMYB36) involved as master switches in secondary xylem development were observed in several eucalyptus genotypes tested, in particular under the higher (125 mM) salt treatment [130]. BplMYB46, a MYB gene from Betula platyphylla (birch), has also been reported to be involved in both abiotic stress tolerance and secondary wall biosynthesis [131]. BplMYB46 is predominantly expressed in stems and its expression is induced by NaCl [131]. In BplMYB46 overexpressing lines a positive effect on lignin and cellulose content but a negative effect on hemicellulose content was found. Correspondingly, the expression of genes related to lignin and cellulose biosynthesis (phenylalanine ammonia lyase (PAL), caffeoyl-CoA O-methyltransferase (CCoAOMT), 4-coumarate-coa ligase (4CL), POD, Laccase (LAC), cinnamoyl-CoA reductase (CCR), cellulose synthase (CesA) was significantly upregulated, and that of genes related to hemicellulose biosynthesis (e.g., fragile fiber (FRA) and irregular xylem (IRX)) was significantly down-regulated in BplMYB46 overexpressing lines. Hence, BplMYB46 functions in linking stress responses and cell wall properties [131]. Further functional analyses by forward and reverse genetic approaches are required to understand the acclimatory responses of trees to salt stress in more detail. While a number of candidate genes has already been studied for their involvement in enhancing salt tolerance in leaves or roots [47], systematic genetic studies targeting at enhanced xylem salt resistance are lacking.

4. Conclusions

Trees respond to environmental stress factors like drought and salt with the adjustment of xylem formation primarily to maintain the hydraulic function of the wood. These responses are strongly affected by nutrients, especially by major cations (K+, Ca2+) and by nitrogen availability. Interestingly, the anatomical changes in response to different environmental cues are quite similar and characterized by a reduction in xylem vessel lumina and fortification of secondary cell walls in vessels and fibers. However, the molecular regulations that act between the initial stimulus and the output, i.e., modified wood, are just poorly understood. It has become apparent that phytohormones play a crucial role in mediating those stress stimuli by modulating xylogenesis related genes like the NAC and MYB master switch regulators, which lead to stress specific gene transcription. Yet, this review shows that our picture of the processes leading to wood acclimation is far from being complete. In order to put the puzzle together, it will be important to not only continue investigating specific stimulus responses, but also to integrate the information of all processes to get a complete picture of wood stress acclimation. Transcriptome analyses helped us a lot in getting a better picture of the processes during stress acclimation, yet they mostly focus on gene clusters build by GO term or KEGG analyses. It will be crucial to exploit this powerful resource more in-depth in the future to get to the key genes involved in those regulatory mechanisms. Identification and functional characterization of candidate genes improving stress tolerance and/or growth under nutrient-limiting conditions will promote the generation of new genotypes either by improving trees by genetic engineering or by smart breeding. Significant advances have been made over recent years to build up an effective toolbox for the characterization of candidate genes, especially in poplar. While overexpression of candidate genes has been well established for years, the generation of loss-of-function mutants has always been difficult. However, recent advances in the CRISPR/Cas9 technology have provided researchers with a powerful tool to investigate gene function and to generate genetically modified trees.

Author Contributions

C.E., S.S., L.K., D.Y., G.J.S., A.K. and A.P. wrote the draft manuscript, C.E. and A.P. reviewed, edited and finalized the manuscript.

Funding

We are grateful for financial support in the frame of WATBIO (Development of improved perennial biomass crops for water stressed environments), which is a collaborative research project funded from the European Union’s Seventh Programme for research, technological development and demonstration under grant agreement No. 311929. S.S. acknowledges financial support by the DAAD, D.Y. by the C.S.C., and A.K. and G.J.S. by the graduate programme MaFO-Holz funded by the Lichtenberg programme of the country Lower Saxony.

Acknowledgments

We thank Merle Fastenrath for technical support with the anatomical studies used to prepare the figures in this review.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Cross-section of a 3 month old poplar stem illustrating the different steps of wood formation. Cross-section has been stained with Phloroglucinol/HCl. Purple color indicates lignification. Bar = 50 µm.
Figure 1. Cross-section of a 3 month old poplar stem illustrating the different steps of wood formation. Cross-section has been stained with Phloroglucinol/HCl. Purple color indicates lignification. Bar = 50 µm.
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Figure 2. Schematic representation of the molecular mechanisms and gene families leading to xylem formation and acclimation under various stresses.
Figure 2. Schematic representation of the molecular mechanisms and gene families leading to xylem formation and acclimation under various stresses.
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Figure 3. Comparison of non-stressed (A) and drought-stressed (B) xylem tissue of Populus tremula x tremuloides. B shows vessels with reduced size but increased vessel frequency. v: vessel cells, f: fiber cells, rp: ray parenchyma. Bar = 50 µm.
Figure 3. Comparison of non-stressed (A) and drought-stressed (B) xylem tissue of Populus tremula x tremuloides. B shows vessels with reduced size but increased vessel frequency. v: vessel cells, f: fiber cells, rp: ray parenchyma. Bar = 50 µm.
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Table 1. List of orthologs of Arabidopsis thaliana wood-formation associated transcription factors present in Populus trichocarpa.
Table 1. List of orthologs of Arabidopsis thaliana wood-formation associated transcription factors present in Populus trichocarpa.
Gene FunctionPotri IDPopulus Gene NameAGI IDArabidopsis Gene Name
Fine-tuning factorsPotri.001G188800Ptr-ATHB.12At1G52150AtHB15/AtCNA/AtICU4
Potri.003G050100Ptr-ATHB.11At1G52150AtHB15/AtCNA/AtICU4
Potri.001G197000 AT3G13890AtMYB26
no annotated ortholog At3G32090AtWRKY12
Potri.002G023400Ptr-E2FC.1/E2FcAt1G47870AtE2Fc
Potri.001G061200PtrNAC053AT5G13180AtVNI2/AtANAC083
Master regulators (NAC)no annotated ortholog At1G32770AtNST3/AtSND1/AtANAC012
Potri.001G448400PtrWND1B/NAC063/PtVNS11At2G46770AtANAC043/AtNST1
Potri.002G178700PtrWND2B/NAC061/PtVNS10AT2G46770AtANAC043/AtNST1
Potri.011G153300PtrWND1A/NAC068/PtVNS12AT2G46770AtANAC043/AtNST1
Potri.014G104800PtrWND2A/NAC065/PtVNS09AT2G46770AtANAC043/AtNST1
Potri.015G127400PtrWND3A/NAC050/PtVNS05AT1G12260AtANAC007/AtNAC007/ATVND4
Potri.012G126500PtrWND3B/NAC037/PtVNS06AT1G12260AtANAC007/AtNAC007/ATVND4
Potri.001G120000PtrWND4A/NAC038/PtVNS03AT1G12260AtANAC007/AtNAC007/ATVND4
Potri.003G113000PtrWND4B/NAC046/PtVNS04AT1G12260AtANAC007/AtNAC007/ATVND4
Potri.007G014400PtrWND5A/NAC025/PtVNS01AT2G18060AtANAC037/AtVND1
Potri.005G116800PtrWND5B/NAC039/PtVNS02AT2G18060AtANAC037/AtVND1
Potri.013G113100PtrWND6A/NAC055/PtVNS07AT1G71930AtANAC030/AtVND7
Potri.019G083600PtrWND6B/NAC060/PtVNS08AT1G71930AtANAC030/AtVND7
Potri.015G002900PtrNAC147AT1G71930AtANAC030/AtVND7
no annotated ortholog At3G61910AtNST2
Potri.004G107200 At5G62380AtVND6
Potri.004G107400 At5G62380AtVND6
Potri.005G082700PtrNAC144At5G62380AtVND6
Potri.006G231300 At5G62380AtVND6
Potri.014G163600 At5G62380AtVND6
no annotated ortholog At4G36160AtVND2/AtANAC076
no annotated ortholog At5G66300AtVND3/AtANAC105
no annotated ortholog At1G62700AtVND5
Second Level Regulators (MYB)Potri.001G258700PtrMYB2At5G12870AtMYB46
Potri.009G053900PtrMYB21At5G12870AtMYB46
Potri.001G267300 At3G08500AtMYB83
Potri.009G061500 At3G08500AtMYB83
Third Level RegulatorsPotri.004G049300 AT4G28500AtSND2/AtANAC073
Potri.007G135300 AT4G28500AtSND2/AtANAC073
Potri.011G058400 AT4G28500AtSND2/AtANAC073
Potri.017G016700 AT4G28500AtSND2/AtANAC073
no annotated ortholog AT1G28470AtSND3
no annotated ortholog At1G63910AtMYB103
Potri.002G073500 At1G17950AtMYB52
Potri.005G186400PtrMYB158/PtrMYB.50At1G17950AtMYB52
Potri.007G134500PtrMYB161/PtrMYB.43At1G17950AtMYB52
Potri.012G039400PtrMYB167/PtrMYB.41At1G17950AtMYB52
Potri.015G033600PtrMYB090/PtrMYB.38At1G17950AtMYB52
no annotated ortholog At3G48920AtMYB45
no annotated ortholog At1G16490AtMYB58
Potri.005G096600 At1G79180AtMYB63
Potri.007G067600 At1G79180AtMYB63
Potri.019G118900 At1G79180AtMYB63
Potri.015G129100 At4G22680AtMYB85
Potri.001G112200PtrKNAT7.1At1G62990AtKNAT7

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