Xylem Maturation Research Articles

New material of the zosterophyllopsid Gosslingia from the Lower Devonian of Guizhou, southwestern China

Abstract The zosterophyllopsids had a widespread distribution and constituted a dominant component in many plant assemblages during the Early Devonian. Although a large number of zosterophyllopsids have been documented, knowledge about the paleogeographic distribution of different genera/species remains to be expanded by further fossil evidence. In this article, new material assigned to the genus Gosslingia Heard, 1927 and designated as Gosslingia cf. G. breconensis Heard, 1927 is described from a new locality of the Lower Devonian of Guizhou Province, China. The Guizhou material shows main axes that are pseudomonopodially branched, pseudomonopodial lateral branching systems, subaxillary tubercle branches, circinate apices, elliptical xylem strand, exarch maturation of xylem, and G-type tracheids, and exhibits considerable similarities with the type and only species of Gosslingia, Gosslingia breconensis. Our finding represents the first report of Gosslingia in the South China Block and the most convincing occurrence of this genus outside of Wales, UK. Gosslingia adds to the diversity of genera shared among the Early Devonian floras of South China, western Europe, and North America, along with Distichophytum Mägdefrau, Estinnophyton Fairon-Demaret, Zosterophyllum Penhallow, and others, and indicates that the dispersal of early vascular plants among different paleocontinents was more common than previously appreciated.

Aspartic proteases modulate programmed cell death and secondary cell wall synthesis during wood formation in poplar.

Programmed cell death (PCD) is essential for wood development in trees. However, the determination of crucial factors involved in xylem PCD of wood development is still lacking. Here, two Populus trichocarpa typical aspartic protease (AP) genes, AP17 and AP45, modulate xylem maturation, especially fibre PCD, during wood formation. AP17 and AP45 were dominantly expressed in the fibres of secondary xylem, as suggested by GUS expression in APpro::GUS transgenic plants. Cas9/gRNA-induced AP17 or AP45 mutants delayed secondary xylem fibre PCD, and ap17ap45 double mutants showed more serious defects. Conversely, AP17 overexpression caused premature PCD in secondary xylem fibres, indicating a positive modulation in wood fibre PCD. Loss of AP17 and AP45 did not alter wood fibre wall thickness, whereas the ap17ap45 mutants showed a low lignin content in wood. However, AP17 overexpression led to a significant decrease in wood fibre wall thickness and lignin content, revealing the involvement in secondary cell wall synthesis during wood formation. In addition, the ap17ap45 mutant and AP17 overexpression plants resulted in a significant increase in saccharification yield in wood. Overall, AP17 and AP45 are crucial modulators in xylem maturation during wood development, providing potential candidate genes for engineering lignocellulosic wood for biofuel utilization.

The regeneration factors ERF114 and ERF115 regulate auxin-mediated lateral root development in response to mechanical cues

Plants show an unparalleled regenerative capacity, allowing them to survive severe stress conditions, such as injury, herbivory attack, and harsh weather conditions. This potential not only replenishes tissues and restores damaged organs but can also give rise to whole plant bodies. Despite the intertwined nature of development and regeneration, common upstream cues and signaling mechanisms are largely unknown. Here, we demonstrate that in addition to being activators of regeneration, ETHYLENE RESPONSE FACTOR 114 (ERF114) and ERF115 govern developmental growth in the absence of wounding or injury. Increased ERF114 and ERF115 activity enhances auxin sensitivity, which is correlated with enhanced xylem maturation and lateral root formation, whereas their knockout results in a decrease in lateral roots. Moreover, we provide evidence that mechanical cues contribute to ERF114 and ERF115 expression in correlation with BZR1-mediated brassinosteroid signaling under both regenerative and developmental conditions. Antagonistically, cell wall integrity surveillance via mechanosensory FERONIA signaling suppresses their expression under both conditions. Taken together, our data suggest a molecular framework in which cell wall signals and mechanical strains regulate organ development and regenerative responses via ERF114- and ERF115-mediated auxin signaling.

Relationship between the xylem maturation process based on radial variations in wood properties and radial growth increments of stems in a fast-growing tree species, Liriodendron tulipifera

Promoting wood utilization from fast-growing tree species is one solution to address supply and demand issues relating to wood resources while sequestering carbon dioxide in large quantities. Information on the quality of wood from fast-growing tree species and its relationship with changes in stem size is essential for promoting the establishment of plantations and wood utilization of fast-growing tree species. To explore the relationship between the xylem maturation process and radial growth increments of stems in fast-growing tree species, we examined radial variations in annual ring widths and wood properties in Liriodendron tulipifera in Japan. The cambial ages at which current annual increment and mean annual increment values were greatest were 4.9 years and 7.4 years, respectively. Based on radial variations evaluated by mixed-effects modeling of wood properties, all properties increased or decreased near the pith before becoming stable towards the cambium. Changing ratios of multiple wood properties at 1-year intervals became stable after a cambial age of 9 years. These results point to an ecological strategy in L. tulipifera, in which there is a tradeoff between radial growth increments and wood properties. As part of this strategy, in response to competition among individual trees within a stand, the tree produces a large volume of xylem with lower physical and mechanical properties, allowing it to increase its volume faster than that of the surrounding trees. Subsequently, it produces xylem that is more stable, with greater physical and mechanical properties. This wood forms at a slower growth rate compared to the xylem that forms at the time of initial tree growth. Based on the ecological strategy adopted by L. tulipifera, wood that forms before a cambial age of 9 years can be used for utility applications, and wood that forms after a cambial age of 9 years can be used for structural applications.

Evaluation of Xylem Maturation Process and Effects of Radial Growth Rate on Cell Morphologies in Wood of Balsa (Ochroma Pryamidale) Trees

Evaluation of Xylem Maturation Process and Effects of Radial Growth Rate on Cell Morphologies in Wood of Balsa (Ochroma Pryamidale) Trees

LATERAL GROWTH AFFECTS XYLEM MATURATION PROPERTIES OF 8-YEAR-OLD BIG-LEAF MAHOGANY (SWIETENIA MACROPHYLLA)

The area of juvenile wood zone of an 8-year-old planted big-leaf mahogany (Swietenia macrophylla) was uniform regardless of diameter. Hence, it was assumed that xylem maturation is dependent on diameter. Radial distribution patterns with reference from the pith exhibited short fibre and vessel lengths, narrow vessel width and low xylem density, and exhibited gradual increase outward and became more or less stable near the bark. However, the radial distribution patterns of fibre width and modulus of elasticity were scattered regardless of tree diameter sizes. Fibre length, vessel length, vessel width and xylem density of the juvenile wood zones showed significant differences compared with the transition and mature wood zones. However, no significant difference was observed between transition wood zone and mature wood zone except for fibre length. A negative correlation was observed in fibre length, vessel length, vessel width and xylem density in terms of their relationship with diameter at breast height and the radial distribution of fibre (i.e. b-value), and the diameter boundaries of the three wood zones. At diameters 18.08, 17.36, 16.23 and 17.87 cm respectively, fibre length, vessel length, vessel width and xylem density can be used to identify xylem maturation boundary.

Secondary xylem maturation evaluated by modeling radial variations in anatomical characteristics and wood properties of Shorea macrophylla (De Vr.) Ashton planted in Sarawak, Malaysia

Xylem maturation depends on cambial age rather than diameter growth in Shorea macrophylla by the model selections for radial variations in cell length, wood fiber traits, and basic density. Radial variations in anatomical characteristics and wood properties were investigated in 23-year-old Shorea macrophylla (engkabang) trees planted in Sarawak, Malaysia. The effects of radial growth rates on anatomical characteristics and wood properties and the manner of xylem maturation were determined based on selected mixed-effects models. The best models of radial variation were fitted by linear functions for wood fiber length, wood fiber wall thickness, basic density, and compressive strength. Logarithmic functions were applied for vessel element length and vessel frequency, and quadratic functions were applied for vessel diameter and wood fiber diameter. Vessel diameter and wood fiber length were affected by radial growth rates although these effects on the other properties were minimal. In the fixed part of the models, the results showed small mean absolute error values of radial variation in relation to the distance from the pith according to vessel frequency and vessel diameter. In contrast, in relation to the estimated cambial age, smaller mean absolute error values were obtained for cell length, wood fiber traits, and basic density, suggesting that all properties varied from pith to bark in relation to the cambial age, except for vessel traits. Thus, in S. macrophylla, xylem maturation in cell length, wood fiber traits, and basic density were due to cambial age rather than diameter growth, but xylem maturation in vessel traits depended on diameter growth.

Analyses of Microstructure and Dynamic Deposition of Cell Wall Components in Xylem Provide Insights into Differences between Two Black Poplar Cultivars

The chemical composition of the cell wall varies between species and even within the same species, and impacts the properties of the cell wall. In this study, the dynamic chemical compositions of the xylem cell walls of two black poplar cultivars, Populus × euramericana ‘Zhonglin46’ and Populus × euramericana ‘Neva,’ were investigated in situ using stimulated Raman scattering microscopy (SRS). Meanwhile, the pectin structural features were examined using immunofluorescence methods. The results showed that Neva displayed faster thickening of the fiber cell walls than Zhonglin46 did, and it had a greater cell wall thickness in mature xylem. A faster deposition speed of lignin and cellulose during xylem maturation was revealed in Neva. Significantly higher lignin contents were found in the mature xylem of Neva compared with those of Zhonglin46, while no obvious differences in cellulose deposition in mature xylem were observed between the two cultivars. The patterns of pectin deposition during xylem maturation were similar in the two cultivars, but more pectin was found in the mature xylem of Neva than in that of Zhonglin46. The chemical deposition patterns account for the anatomical feature differences between the cultivars. These results provide valuable insights into the chemical deposition and anatomical differences between cultivars, and they might be helpful in understanding the wood growth processes and facilitating the utilization of different poplar cultivars.

Anatomy of Stigmaria asiatica Jongmans et Gothan from the Asselian (lowermost Permian) of Wuda Coalfield, Inner Mongolia, North China

Stigmaria asiatica Jongmans et Gothan is a common species from the Permo-Carboniferous of East Asia. It is characterized by a relatively slender rhizomorph and represents the underground rooting system of lowland arborescent lycopsids. This species from the Wuda Coalfield (Asselian, lower Permian) represents the recovery taxon dominating the subsequent peat-forming vegetation after a volcanic eruption destroyed the previous flora, termed the Wuda Tuff Flora (Chinese “vegetational Pompeii”). It is characterized by novel downward axes, probably for access to deeper groundwater. Here, the anatomy of S. asiatica, including that of the axes and rootlets, is reported in detail for the first time. The axis contains stelar tissues, including pith, primary and secondary xylem, and phloem, and both primary and secondary cortical tissues. The primary cortex is tripartite and is divided into inner, middle, and outer zones. Secondary cortex is produced in the interior of the outer cortex splitting the outer cortex into inner and outer portions. The homogeneous pith and mesarch primary xylem maturation of S. asiatica are different from previously recorded species of Stigmaria Brongniart. Rootlets are composed of a central monarch vascular bundle surrounded by inner cortex and a ring of outer cortex. A vacant region is present between the inner and outer cortices. In some cases, connectives between the inner and outer cortices are present. According to the presented statistical analysis, it is proposed that rootlets of S. asiatica were highly branched, with at least for 7 bifurcations. Rootlets, together with the downward penetrating rhizomorph, helped to both anchor the plant and search for and absorb deep groundwater.

Structural features and contribution of belowground buds to conservation of Fabaceae species in a seasonally dry Neotropical environment

Resprouting from belowground buds is an important mechanism to increase aboveground branching. This trait is particularly frequent in various members of Fabaceae. However, there are scant anatomical studies on belowground buds including information about their location in the plant body in these species. Herein we examined the anatomy of belowground buds and organs that support these buds in herbaceous and woody Fabaceae species. Adventitious buds located in the root-shoot transition zone (root crown) were the predominant type of belowground buds in herbaceous and subshrubby species. Moreover, some woody species showed lateral roots with root buds growing near the soil surface. The root structure was confirmed by the centripetal maturation of the primary xylem (exarch xylem). Anatomical analyses of Cenostigma pluviosum and Senna pilifera roots revealed numerous reparative buds that develop from calli. Reparative buds were formed only after injury to root tissues or shoot removal. On the other hand, the roots of Machaerium eriocarpum and Muellera nudiflora showed additional buds with bud traces connected to the primary xylem. Additional buds were found in uninjured young roots and in root segments that were kept in a greenhouse condition. Our findings show that the species examined of Fabaceae are able to resprout from adventitious buds located in roots and root crowns. This trait seems to be advantageous for conservation of these species in the Brazilian Chaco, which is characterised by dry seasons associated with frost and extensive cattle raising.

The occurrence and development of intraxylary phloem in young Aquilaria sinensis shoots

ABSTRACT Agarwoods such as Aquilaria spp. and Gyrinops spp. (Thymelaeaceae) produce interxylary phloem in their secondary xylem and intraxylary phloem at the periphery of the pith, facing the primary xylem. We studied young shoots of Aquilaria sinensis and characterized the development of its intraxylary phloem. It was initiated by the division of parenchyma cells localized in the outer parts of the ground meristem immediately following the maturation of first-formed primary xylem. Its nascent sieve plates bore donut-like structures, the individual pores of which were so small (less than 0.1 μm) that they were hardly visible under FE-SEM. Intraxylary phloem developed into mature tissue by means of the division and proliferation of parenchyma cells. During the shoots’ active growth period, the sieve pore sizes were 0.1–0.5 μm, with tubular elements passing through them. In the maturation stage, large clusters of sieve tubes continued to be differentiated in the intraxylary phloem. In the partial senescence stage observed in a three-centimeter-diameter branch, intraxylary phloem cells in the adaxial part became crushed, and sieve plates had pores over 1–2 μm in diameter without any callose deposition. Before and after the differentiation of interxylary phloem in the first and second internodes, callose staining detected more than twice as many sieve tubes in intraxylary phloem than in external phloem. However, after differentiation of interxylary phloem in the eleventh internode, more sieve tubes were found in interxylary phloem than in intraxylary and external phloem. This suggests that prior to the initiation of interxylary phloem intraxylary phloem acts as the principal phloem. After its differentiation, however, interxylary phloem takes over the role of principal phloem. Interxylary phloem thus acts as the predominant phloem in the translocation of photosynthates in Aquilaria sinensis.

Stress-Triggered Long-Distance Communication Leads to Phenotypic Plasticity: The Case of the Early Root Protoxylem Maturation Induced by Leaf Wounding in Arabidopsis.

Root architecture and xylem phenotypic plasticity influence crop productivity by affecting water and nutrient uptake, especially under those environmental stress, which limit water supply or imply excessive water losses. Xylem maturation depends on coordinated events of cell wall lignification and developmental programmed cell death (PCD), which could both be triggered by developmental- and/or stress-driven hydrogen peroxide (H2O2) production. Here, the effect of wounding of the cotyledonary leaf on root protoxylem maturation was explored in Arabidopsis thaliana by analysis under Laser Scanning Confocal Microscope (LSCM). Leaf wounding induced early root protoxylem maturation within 3 days from the injury, as after this time protoxylem position was found closer to the tip. The effect of leaf wounding on protoxylem maturation was independent from root growth or meristem size, that did not change after wounding. A strong H2O2 accumulation was detected in root protoxylem 6 h after leaf wounding. Furthermore, the H2O2 trap N,N1-dimethylthiourea (DMTU) reversed wound-induced early protoxylem maturation, confirming the need for H2O2 production in this signaling pathway.

The Effects of Radial Growth Rate on Wood Properties and Anatomical Characteristics and an Evaluation of the Xylem Maturation Process in a Tropical Fast-Growing Tree Species, Gmelina arborea

Abstract The aim of this study was to evaluate the effects of radial growth on wood properties and anatomical characteristics and to clarify the xylem maturation process in Gmelina arborea. Stem diameter, tree height, and stress-wave velocity were investigated for 54 5-year-old G. arborea trees planted in Indonesia. In addition, radial variations of wood properties (basic density and compressive strength parallel to the grain in green condition) and anatomical characteristics (fiber and vessel morphologies) were investigated for nine trees selected from three different radial growth categories (fast, medium, and slow growing). Stem diameter was positively significantly correlated with stress-wave velocity and compressive strength parallel to the grain in green condition. In addition, compressive strength and anatomical characteristics, except for wood fiber diameter, differed significantly among the radial growth categories. Radial variations of the wood properties and anatomical characteristics gradually increased, and then they showed constant values toward the bark. It is thought that the xylem maturation of G. arborea begins at approximately 5 cm from the pith. In addition, in a fast-growing tree species, such as G. arborea, the trees with faster stem diameter do not always form wood with low strength properties.

Evaluation of xylem maturation and the effects of radial growth rate on anatomical characteristics and wood properties of Azadirachta excelsa planted in Indonesia

The xylem-maturation process and the effects of radial growth rate on anatomical characteristics (vessel and fibre morphologies) and wood properties (basic density and compressive strength parallel to grain) were studied for 4-year-old Azadirachta excelsa planted in Indonesia. Mean values were 121 µm, 8.1 vessels/mm2, 16 µm, 1.4 µm, 0.33 mm, 0.98 mm, 0.40 g/cm3, and 27.3 MPa for vessel diameter (VD), vessel frequency, fibre diameter, fibre wall thickness, vessel element length, wood fibre length, basic density, and compressive strength parallel to the grain at green condition, respectively. With a few exceptions, no significant correlations were found between the stem diameter and the anatomical characteristics or wood properties, indicating that radial growth rate does not always affect the characteristics and properties of this species. On the other hand, almost the same radial variation patterns in VD were found in trees of a different stem diameter, suggesting that xylem maturation in this species might depend on diameter growth rather than cambial age.

Spatiotemporal distribution of essential elements through Populus leaf ontogeny.

We examined the spatiotemporal distribution and accumulation of calcium (Ca), potassium (K), and zinc (Zn) during the growth and maturation of grey poplar (Populus tremula × alba) leaves covering plastochrons 01 through 10. This period spans the sugar sink-to-source transition and requires coordinated changes of multiple core metabolic processes that likely involve alterations in essential and non-essential element distributions as tissues mature and effect a reversal in phloem flow direction. Whole-leaf elemental maps were obtained from dried specimens using micro X-ray fluorescence spectroscopy. Additional cross-sections of fresh leaves were scanned to check for tissue specificity in element accumulation. The anatomical distribution of Zn and K remains relatively consistent throughout leaf development; Ca accumulation varied across leaf developmental stages. The basipetal allocation of Ca to the leaf mesophyll matched spatially and temporally the sequence of phloem maturation, positive carbon balance, and sugar export from leaves. The accumulation of Ca likely reflects the maturation of xylem in minor veins and the enhancement of the transpiration stream. Our results independently confirm that xylem and phloem maturation are spatially and temporally coordinated with the onset of sugar export in leaves.

Growth characteristics and wood properties of 26-year-old Eucalyptus alba planted in Indonesia

Growth characteristics and wood properties were investigated for 26-year-old Eucalyptus alba trees grown in Ambon, Indonesia. The mean stem diameter and tree height were 27·9 cm and 19·5 m, respectively. In addition, the mean stress-wave velocity (SWV) of trees and basic density (BD) of outer wood (2 cm from the bark) were 3·23 km s− 1 and 0·67 g cm− 3, respectively. The mean BD of outer wood was almost the same in fast-growing and medium-growing trees. No significant correlations were found between stem diameter and SWV of trees and BD of outer wood. Based on the results, trees with faster-growing characteristics of E. alba do not always have the lower wood properties. Radial profiles in relation to relative distance from pith to bark were almost the same among three growth categories, suggesting that xylem maturation in E. alba might depend on cambial age.

Xylem development - from the cradle to the grave.

The development and growth of plants, as well as their successful adaptation to a variety of environments, is highly dependent on the conduction of water, nutrients and other important molecules throughout the plant body. Xylem is a specialized vascular tissue that serves as a conduit of water and minerals and provides mechanical support for upright growth. Wood, also known as secondary xylem, constitutes the major part of mature woody stems and roots. In the past two decades, a number of key factors including hormones, signal transducers and (post)transcriptional regulators have been shown to control xylem formation. We outline the main mechanisms shown to be essential for xylem development in various plant species, with an emphasis on Arabidopsis thaliana, as well as several tree species where xylem has a long history of investigation. We also summarize the processes which have been shown to be instrumental during xylem maturation. This includes mechanisms of cell wall formation and cell death which collectively complete xylem cell fate.

Anatomical characteristics and wood properties of Melaleuca leucadendron naturally growing in secondary forest in Indonesia

SummaryDynamic Young’s modulus of elasticity (DMOE) of logs, anatomical characteristics and wood properties were determined for naturally regenerated Melaleuca leucadendron trees grown in secondary forest in an area of peat swamp, South Kalimantan, Indonesia. The mean value of DMOE of logs was 7.99 GPa. Mean basic density (BD) and compressive strength (CS) ranged from 0.43 to 0.60 g cm−3 and 34.5 to 52.4 MPa, respectively. Vessel diameter and wood fibre length increased along the first 2 cm of the radius from the pith and then showed almost constant values between that point and the bark, suggesting that xylem maturation starts at about 2 cm from the pith. The wall thickness of wood fibres gradually increased from pith to bark, and the radial profile of this property was very similar to that of BD. There were significant differences in BD, CS and cell wall thickness of wood fibres among 10 selected logs, suggesting that BD and mechanical properties can be genetically improved by selecting mother trees.

Lignin and lignans in plant defence: Insight from expression profiling of cinnamyl alcohol dehydrogenase genes during development and following fungal infection in Populus

Cinnamyl alcohol dehydrogenase (CAD) catalyses the final step in the biosynthesis of monolignol, the main component of lignin. Lignins, deposited in the secondary cell wall, play a role in plant defence against pathogens. We re-analysed the phylogeny of CAD/CAD-like genes using sequences from recently sequenced genomes, and analysed the temporal and spatial expression profiles of CAD/CAD-like genes in Populus trichocarpa healthy and infected plants. Three fungal pathogens (Rhizoctonia solani, Fusarium oxysporum, and Cytospora sp.), varying in lifestyle and pathogenicity, were used for plant infection. Phylogenetic analyses showed that CAD/CAD-like genes were distributed in classes represented by all members from angiosperm lineages including basal angiosperms and Selaginella. The analysed genes showed different expression profiles during development and demonstrated that three genes were involved in primary xylem maturation while five may function in secondary xylem formation. Expression analysis following inoculation with fungal pathogens, showed that five genes were induced in either stem or leaves. These results add further evidence that CAD/CAD-like genes have evolved specialised functions in plant development and defence against various pest and pathogens. Two genes (PoptrCAD11 and PoptrCAD15), which were induced under various stresses, could be treated as universal markers of plant defence using lignification or lignan biosynthesis.

Coordinated action of β‐galactosidases in the cell wall of embryonic axes during chickpea germination and seedling growth

The plant cell wall is a dynamic structure whose constant modification is necessary for plant cells to grow and divide. In the cell walls of chickpea (Cicer arietinum) there are at least four β-galactosidases, whose presence and location in embryonic axes during the first 48 h of seed imbibition are discussed in this paper. We examined their roles as cell wall-modifying enzymes in germinative and/or post-germinative events. At the start of germination, only βV-Gal, and to a lesser extent βIV-Gal, appear in the axes before rupture of the testa, suggesting they are related to germination sensu stricto. Once the testa has broken, the four β-galactosidases are involved in growth and differentiation of the axes. Immunolocation of the different proteins in axes, which in part confirms previous results in seedlings and plants, allows assignment of post-germinative roles to βI-Gal and βIII-Gal as cell wall modifiers in vascular tissue elements. βIV-Gal and βV-Gal participate in the initial events of germination in which cell walls are involved: βV-Gal in cell proliferation, detachment of root cap cells and initial vascular tissue differentiation; both of them in xylem maturation; and βIV-Gal in thickening of the primary cell wall. Together with other cell wall-modifying enzymes, such as expansins and XTH, chickpea galactosidases might function in a sequential order in turnover of the primary cell wall, allowing the elongation of embryonic axes during seed germination.