Morpho‐anatomical diversity of the underground systems of Arrojadoa (Cactaceae), an endemic Brazilian genus

Members of Arrojadoa exhibit a variety of underground structures that can originate from roots or stems. Although the development of underground structures of stem origin in Arrojadoa represents a unique trait among Cactaceae of eastern Brazil, no detailed reports on the morphological diversity of such structures are available. The present morpho‐anatomical study of the underground systems of Arrojadoa has demonstrated that a single species can exhibit one or more structural types, such as single or branched stem tubers, short thick stems and/or long subterranean stems, thick and fleshy contractile roots and normal fibrous roots. Various morpho‐anatomical structures relating to the underground storage systems in Arrojadoa spp. have also been observed, including thick contractile roots consisting mainly of secondary xylem formed by fibrous wood with wide‐band tracheids (WBTs) and underground stems with a wide cortical region and WBTs‐type wood. Based on the evidence presented, we suggest that such traits, together with the occurrence of contractile roots associated with underground stems, are important adaptive strategies for the survival of the plants during seasonal drought in areas of cerrado (savannah), campo rupestre (rocky uplands) and caatinga (dry thorny scrubland). © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 108–128.     

A new method for vulnerability analysis of small xylem areas reveals that compression wood of Norway spruce has lower hydraulic safety than opposite wood

Compression wood is formed at the underside of conifer twigs to keep branches at their equilibrium position. It differs from opposite wood anatomically and subsequently in its mechanical and hydraulic properties. The specific hydraulic conductivity (k_s) and vulnerability to drought‐induced embolism (loss of conductivity versus water potential ψ) in twigs of Norway spruce [Picea abies (L.) Karst.] were studied via cryo‐scanning electron microscope observations, dye experiments and a newly developed ‘Micro‐Sperry’ apparatus. This new technique enabled conductivity measurements in small xylem areas by insertion of syringe cannulas into twig samples. The hydraulic properties were related to anatomical parameters (tracheid diameter, wall thickness). Compression wood exhibited 79% lower k_s than opposite wood corresponding to smaller tracheid diameters. Vulnerability was higher in compression wood despite its narrower tracheids and thicker cell walls. The P₅₀ (ψ at 50% loss of conductivity) was ?3.6 MPa in opposite but only ?3.2 MPa in compression wood. Low hydraulic efficiency and low hydraulic safety indicate that compression wood has primarily a mechanical function.     

Functional lifespans of xylem vessels: Development,hydraulic function,and post‐function of vessels in several species of woody plants

Premise of the Study

Xylem vessels transition through different stages during their functional lifespan, including expansion and development of vessel elements, transition to vessel hydraulic functionality, and eventual transition to post‐functionality. We used information on vessel development and function to develop a model of vessel lifespan for woody plants.

Methods

We examined vessel functional lifespan using repeated anatomical sampling throughout the growing season, combined with active‐xylem staining to evaluate vessel hydraulic transport functionality. These data were combined with a literature review. The transitions between vessel functional lifespans for several species are illustrated, including grapevine (Vitis vinifera L., Vitaceae), English oak (Quercus robur L., Fagaceae), American chestnut [Castanea dentata (Marshall) Borkh.; Fagaceae], and several arid and semi‐arid shrub species.

Key Results

In intact woody plants, development and maturation of vessel elements may be gradual. Once hydraulically functional, vessel elements connect to form a vessel network that is responsible for bulk hydraulic flow through the xylem. Vessels become nonfunctional due to the formation of gas emboli. In some species and under some conditions, vessel functionality of embolized conduits may be restored through refilling. Blockages, such as tyloses, gels, or gums, indicate permanent losses in hydraulic functional capacity; however, there may be some interesting exceptions to permanent loss of functionality for gel‐based blockages.

Conclusions

The gradual development and maturation of vessel elements in woody plants, variation in the onset of functionality between different populations of vessels throughout the growing season, and differences in the timing of vessel transitions to post‐functionality are important aspects of plant hydraulic function.     

Fungal colonization of the rooting system of the early land plant Asteroxylon mackiei from the 407‐Myr‐old Rhynie Chert (Scotland,UK)

Associations between plants and fungi were an important and varied feature of early terrestrial ecosystems, but in most instances their biological functions remain poorly understood. We document a new species of fungus colonizing the rooting system of the early lycopod Asteroxylon mackiei, based on exceptionally well‐preserved fossils from the Rhynie Chert. We investigated historical petrographic thin sections using standard optical microscopy and confocal laser scanning microscopy. P alaeozoosporites renaultii gen. nov., sp. nov. colonized the inner cortex of the plant rooting system. The fungus had an aseptate thallus with isotomous or sympodial branching. The mycelium bore distinctive porate, globose to elongated structures that we interpret as zoosporangia and resting sporangia. Doubts remain over the precise systematic affinity of P. renaultii, which closely resembles chytrids. Whereas most of the Rhynie Chert plants developed symbiotic associations of the mycorrhizal type, it seems that this was not the case for Asteroxylon mackiei, which possessed the most evolved rooting system among the Rhynie Chert plants. We argue that the new root‐borne fungus was probably parasitic. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 201–213.     

Polar auxin transport is implicated in vessel differentiation and spatial patterning during secondary growth in Populus

Premise of the Study

Dimensions and spatial distribution of vessels are critically important features of woody stems, allowing for adaptation to different environments through their effects on hydraulic efficiency and vulnerability to embolism. Although our understanding of vessel development is poor, basipetal transport of auxin through the cambial zone may play an important role.

Methods

Stems of Populus tremula ×alba were treated with the auxin transport inhibitor N‐1‐naphthylphthalamic acid (NPA) in a longitudinal strip along the length of the lower stem. Vessel lumen diameter, circularity, and length; xylem growth; tension wood area; and hydraulic conductivity before and after a high pressure flush were determined on both NPA‐treated and control plants.

Key Results

NPA‐treated stems formed aberrant vessels that were short, small in diameter, highly clustered, and angular in cross section, whereas xylem formed on the untreated side of the stem contained typical vessels that were similar to those of controls. NPA‐treated stems had reduced specific conductivity relative to controls, but this difference was eliminated by the high‐pressure flush. The control treatment (lanolin + dimethyl sulfoxide) reduced xylem growth and increased tension wood formation, but never produced the aberrant vessel patterning seen in NPA‐treated stems.

Conclusions

These results are consistent with a model of vessel development in which basipetal polar auxin transport through the xylem‐side cambial derivatives is required for proper expansion and patterning of vessels and demonstrate that reduced auxin transport can produce stems with altered stem hydraulic properties.     

WOOD ANATOMY OF BUBBIA (WINTERACEAE), WITH COMMENTS ON ORIGIN OF VESSELS IN DICOTYLEDONS

Quantitative and qualitative features of wood anatomy are reported for ten collections of seven species of Bubbia. Variations on the basic plan for Winteraceae can be interpreted in terms of taxonomic and ecological distinctions. Tracheid length is correlated with plant size and habit: tracheids are shortest in shrubs. Tracheid wall thickness and ray cell wall thickness distinguish species. Ray cell procumbency and multiseriate ray width increase with age. Growth rings occur only in a species from stream margins. SEM studies reveal absence of a warty layer within tracheids. Helical thickenings are absent. Presence of these two features in Pseudowintera may be correlated with the cool temperate habitats of that genus. Overlap areas of tracheids in Bubbia show various degrees of scalariform pitting, ranging from none (B. semecarpoides) to abundant presence (B. balansae). Perforation-like pits in tracheids of the latter prove, with SEM studies, to have pit membranes containing porosities less than 1 μm in diameter. Scalariform pitting on overlap areas is absent in earlier secondary xylem and increases during later secondary xylem. Scalariform lateral wall pitting can occur in abnormally wide tracheids formed after pauses in cambial activity. These facts show that primitive dicotyledon woods like those of Bubbia can activate genetic information for scalariform end wall patterns and lateral wall pitting such as primitive vessels show without the intervention of paedomorphosis. Paedomorphosis in dicotyledon woods is held still to apply only to special herbaceous and herblike growth forms, not to primarily woody plants. Progenesis (in xylem, loss of secondary xylem) is not held to be necessary to account for the scalariform patterns seen in tracheary elements of primitive dicotyledons. Reasons are given for rejection of the hypothesis that Winteraceae and other woody dicotyledons (Amborella, Sarcandra, Tetracentron, Trochodendron) are secondarily vesselless.     

Structural determinants of increased susceptibility to dehydration‐induced cavitation in post‐fire resprouting chaparral shrubs

It is well established that transpiration and photosynthetic rates generally increase in resprouting shoots after fire in chaparral shrublands. By contrast, little is known about how plant hydraulic function varies during this same recovery period. We hypothesized that vascular traits, both functional and structural, would also shift in order to support this heightened level of gas exchange and growth. We examined stem xylem‐specific hydraulic conductivity (K_s) and resistance to cavitation (P₅₀) for eight chaparral shrub species as well as several potential xylem structural determinants of hydraulic function and compared established unburned plants and co‐occurring post‐fire resprouting plants. Unburned plants were generally more resistant to cavitation than resprouting plants, but the two groups did not differ in K_s. Resprouting plants had altered vessel structure compared with unburned plants, with resprouting plants having both wider diameter vessels and higher inter‐vessel pit density. For biomechanics, unburned plants had both stronger and denser stem xylem tissue than resprouting plants. Shifts in hydraulic structure and function resulted in resprouting plants being more vulnerable to dehydration. The interaction between time since disturbance (i.e. resprouting versus established stands) and drought may complicate attempts to predict mortality risk of resprouting plants.     

Photosynthetic pathway alters xylem structure and hydraulic function in herbaceous plants

Plants using the C₄ photosynthetic pathway have greater water use efficiency (WUE) than C₃ plants of similar ecological function. Consequently, for equivalent rates of photosynthesis in identical climates, C₄ plants do not need to acquire and transport as much water as C₃ species. Because the structure of xylem tissue reflects hydraulic demand by the leaf canopy, a reduction in water transport requirements due to C₄ photosynthesis should affect the evolution of xylem characteristics in C₄ plants. In a comparison of stem hydraulic conductivity and vascular anatomy between eight C₃ and eight C₄ herbaceous species, C₄ plants had lower hydraulic conductivity per unit leaf area (K_L) than C₃ species of similar life form. When averages from all the species were pooled together, the mean K_L for the C₄ species was 1.60 × 10^?4 kg m^?1 s^?1 MPa^?1, which was only one‐third of the mean K_L of 4.65 × 10^?4 kg m^?1 s^?1 MPa^?1 determined for the C₃ species. The differences in K_L between C₃ and C₄ species corresponded to the two‐ to three‐fold differences in WUE observed between C₃ and C₄ plants. In the C₄ species from arid regions, the difference in K_L was associated with a lower hydraulic conductivity per xylem area, smaller and shorter vessels, and less vulnerable xylem to cavitation, indicating the C₄ species had evolved safer xylem than the C₃ species. In the plants from resource‐rich areas, such as the C₄ weed Amaranthus retroflexus, hydraulic conductivity per xylem area and xylem anatomy were similar to that of the C₃ species, but the C₄ plants had greater leaf area per xylem area. The results indicate the WUE advantage of C₄ photosynthesis allows for greater flexibility in hydraulic design and potential fitness. In resource‐rich environments in which competition is high, an existing hydraulic design can support greater leaf area, allowing for higher carbon gain, growth and competitive potential. In arid regions, C₄ plants evolved safer xylem, which can increase survival and performance during drought events.     

Xylem phenology and wood production: resolving the chicken‐or‐egg dilemma

Delays in the start of the growing season reduce the period available for growth and the amount of xylem production. However, a higher number of developing tracheids could prolong cell differentiation and, consequently, lengthen the growing season. The relationship between the amount and duration of cell production in the xylem remains an unresolved issue. The aim of this study was to resolve the chicken‐or‐egg causality dilemma about duration of growth and cell production through simple‐ and double‐cause models. This was achieved by (1) analysing the intra‐annual growth dynamics of the xylem in Picea mariana (Mill.) BSP during 2006–2009 in two contrasting sites of the boreal forest of Quebec, Canada, and (2) extracting the dates of onset and ending of xylem formation and the number of radial cells along the tree ring. A higher number of cells was linked to an earlier onset (r = 0.74) and later ending (r = 0.61) of cell differentiation. The absence of a relationship between the residuals of the onset and ending of xylogenesis (r_p = ?0.06) indicated that cell production influenced the correlation between the two phenophases of the xylem. These results demonstrated that a higher number of cells produced delay the ending of xylem maturation, so extending the duration of wood formation.     

Petrified plants from the cretaceous of the Kwanto mountains,central Japan. III. A polyxylic cycadean trunk,Sanchucycas gigantea gen. et sp. nov.

Sanchucycas gigantea gen. et sp. nov. is a fossil cycadophyte trunk from the Lower Cretaceous (Late Barremian—Early Aptian) Sebayashi Formation of the Sanchu area, Gunma Prefecture. It has polycyclic vascular bundles, pitted tracheids, uni- to hexaseriate rays, one or two large cross field pits, and mucilage sacs.Sanchucycas is most closely comparable withCycas andEncephalartos among living members of the Cycadales, but is distinct in its large number of xylem cylinders constituting a thick polyxylic wood, and in having mucilage sacs contrary to canals. This is the earliest record of polyxylic cycadean stems. Contributions from the Laboratory of Phylogenetic Botany, Chiba University no. 122.     

A plumber's-eye view of xylem water transport in woody plants

We present a practical for university-level students aimed at measuring and comparing xylem hydraulic properties of co-existing plant species. After sampling branches of several woody species in the field, their main hydraulic properties were measured using a simple set-up. Hydraulic conductivity (K_h ) was calculated as the ratio between water flow through a plant segment and the pressure gradient driving the flow. The percent reduction in conductivity due to xylem embolism (i.e. air-filled conduits) was estimated by comparing K_h before and after flushing the measure segments to remove all native embolism. Raw hydraulic conductivity was standardised by cross-sectional wood area or supported leaf area to obtain more meaningful measures of conducting capacity. The results showed differences among study species, particularly between conifers and angiosperms. These differences are briefly discussed in terms of wood anatomy and the general biology of the species. Overall the practical provides a good opportunity for students to appreciate the main aspects of xylem water transport and the constraints it imposes on plant water relations.     

Wood borer performance and wood characteristics of drought‐stressed Scots pine seedlings

Four‐year‐old Scots pine [Pinus sylvestris L. (Pinaceae)] seedlings were exposed to medium and severe drought stress for two consecutive years. The anatomical properties of drought‐stressed Scots pine wood and their impact on the performance of destructive wood boring early instars of Hylotrupes bajulus L. (Coleoptera: Cerambycidae) were studied. Drought stress significantly decreased diameter of earlywood tracheids in both growing years and diameter of latewood tracheids after the second growing season only. Cell lumen area was significantly decreased by both medium and severe drought stress compared to well‐watered controls. In addition, area of cell lumen was significantly smaller in severe drought than in medium drought treatment. The drought stress marginally increased the number of resin canals in the wood, but did not affect the size of resin canals either in wood or bark. The relative growth rate of xylophagous H. bajulus neonatal larvae was not significantly affected by drought stress during the 106‐day feeding period on Scots pine wood blocks. The results show that although water availability was an important factor affecting the development and anatomy of wood cells, observed changes in wood characteristics did not affect the performance of early instars feeding on wood processed from drought‐stressed young Scots pine seedlings.     

Histochemical Study of Xylem Cells in In Vitro Culture of Iris sibirica L.

In this study, lignin content data are presented for annual regenerant Iris sibirica plants, comparable to those in six-year-old intact plants. The structure of the shoots of Iris sibirica grown on artificial nutrient media was studied by the histochemical method. Features of the formation of the xylem in Iris sibirica on artificial nutrient media were revealed. Regenerants very quickly developed a complex system consisting of vascular bundles containing sieve tubes, vessels and tracheids, and hydrocyte systems. Hydrocytes of Iris sibirica were tracheids with lignified thickening, but, in contrast to tracheids and vessels of xylem (they are formed based on procambium or cambium—special lateral primary or secondary meristem), hydrocytes differentiated from the cells of permanent tissues (like phellogen), which probably possessed meristematic activity at the time of differentiation. In Iris sibirica hydrocytes covered the vascular bundle by the thick layer and strung along it up to a certain height. High lignin content in young regenerant Iris sibirica plants was due to the formation of the dense tissue from lignified tracheal elements. The study of the differentiation of xylem elements under controlled conditions can serve as a model for our understanding of wood formation processes.

     

PtxtPME1 and homogalacturonans influence xylem hydraulic properties in poplar

While the xylem hydraulic properties, such as vulnerability to cavitation (VC), are of paramount importance in drought resistance, their genetic determinants remain unexplored. There is evidence that pectins and their methylation pattern are involved, but the detail of their involvement and the corresponding genes need to be clarified. We analyzed the hydraulic properties of the 35S::PME1 transgenic aspen that ectopically under‐ or over‐express a xylem‐abundant pectin methyl esterase, PtxtPME1. We also produced and analyzed 4CL1::PGII transgenic poplars expressing a fungal polygalacturonase, AnPGII, under the control of the Ptxa4CL1 promoter that is active in the developing xylem after xylem cell expansion. Both the 35S::PME1 under‐ and over‐expressing aspen lines developed xylem with lower‐specific hydraulic conductivity and lower VC, while the 4CL1::PGII plants developed xylem with a higher VC. These xylem hydraulic changes were associated with modifications in xylem structure or in intervessel pit structure that can result in changes in mechanical behavior of the pit membrane. This study shows that homogalacturonans and their methylation pattern influence xylem hydraulic properties, through its effect on xylem cell expansion and on intervessel pit properties and it show a role for PtxtPME1 in the xylem hydraulic properties.     

Cellular level observation of water loss and the refilling of tracheids in the xylem of Cryptomeria japonica during heartwood formation

The mechanism of heartwood formation in Cryptomeria japonica D. Don has long been studied since heartwood formation is a fundamental physiological feature of trees. In this study, the water distribution in the xylem of C. japonica was investigated at the cellular level to reveal the role of water distribution in the xylem during heartwood formation. Samples were taken from different heights of each trunk, in which the phases of heartwood formation differed. These were designated as SIH, which consisted of sapwood, intermediate wood, and heartwood; SI, which consisted of sapwood and intermediate wood but no heartwood; and S-all, which consisted entirely of sapwood. Cryo-scanning electron microscopic observations of the heartwood-formed (SIH) and non-heartwood-formed (SI and S-all) xylem revealed different patterns of water distribution changes in tracheids between the latewood and earlywood. In the latewood, almost all tracheids were filled with water in all areas from the sapwood to the heartwood (98–100% of tracheids had water in their lumina). In the earlywood, however, the water distribution differed between the sapwood (95–99%), intermediate wood (7–12%), and heartwood (4–100%). Many of the tracheids in the xylem, where the sapwood changed to intermediate wood lost water. In the heartwood, some tracheids remained empty, while others were refilled with water. These results suggest that the water distribution changes in individual tracheids are closely related to heartwood formation. Water loss from tracheids may be an important factor inducing heartwood formation in the xylem of C. japonica.     

Cavitation of intercellular spaces is critical to establishment of hydraulic properties of compression wood of Chamaecyparis obtusa seedlings

Background and Aims When the orientation of the stems of conifers departs from the vertical as a result of environmental influences, conifers form compression wood that results in restoration of verticality. It is well known that intercellular spaces are formed between tracheids in compression wood, but the function of these spaces remains to be clarified. In the present study, we evaluated the impact of these spaces in artificially induced compression wood in Chamaecyparis obtusa seedlings.Methods We monitored the presence or absence of liquid in the intercellular spaces of differentiating xylem by cryo-scanning electron microscopy. In addition, we analysed the relationship between intercellular spaces and the hydraulic properties of the compression wood.Key Results Initially, we detected small intercellular spaces with liquid in regions in which the profiles of tracheids were not rounded in transverse surfaces, indicating that the intercellular spaces had originally contained no gases. In the regions where tracheids had formed secondary walls, we found that some intercellular spaces had lost their liquid. Cavitation of intercellular spaces would affect hydraulic conductivity as a consequence of the induction of cavitation in neighbouring tracheids.Conclusions Our observations suggest that cavitation of intercellular spaces is the critical event that affects not only the functions of intercellular spaces but also the hydraulic properties of compression wood.     

Litter‐trapping plants: filter‐feeders of the plant kingdom

Litter‐trapping plants have specialized growth habits and morphologies that enable them to capture falling leaf litter and other debris, which the plants use for nutrition after the litter has decayed. Litter is trapped via rosettes of leaves, specially modified leaves and/or upward‐growing roots (so‐called ‘root baskets’). Litter‐trappers, both epiphytic and terrestrial, are found throughout the tropics, with only a few extra‐tropical species, and they have evolved in many plant families. The trapped litter mass is a source of nutrients for litter‐trapping plants, as well as food and housing for commensal organisms. Despite their unique mode of life, litter‐trapping plants are not well documented, and many questions remain about their distribution, physiology and evolution.–© 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 554–586.     

Overexpression and cosuppression of xylem‐related genes in an early xylem differentiation stage‐specific manner by the AtTED4 promoter

Tissue‐specific overexpression of useful genes, which we can design according to their cause‐and‐effect relationships, often gives valuable gain‐of‐function phenotypes. To develop genetic tools in woody biomass engineering, we produced a collection of Arabidopsis lines that possess chimeric genes of a promoter of an early xylem differentiation stage‐specific gene, Arabidopsis Tracheary Element Differentiation‐related 4 (AtTED4) and late xylem development‐associated genes, many of which are uncharacterized. The AtTED4 promoter directed the expected expression of transgenes in developing vascular tissues from young to mature stage. Of T2 lines examined, 42%, 49% and 9% were judged as lines with the nonrepeat type insertion, the simple repeat type insertion and the other repeat type insertion of transgenes. In 174 T3 lines, overexpression lines were confirmed for 37 genes, whereas only cosuppression lines were produced for eight genes. The AtTED4 promoter activity was high enough to overexpress a wide range of genes over wild‐type expression levels, even though the wild‐type expression is much higher than AtTED4 expression for several genes. As a typical example, we investigated phenotypes of pAtTED4::At5g60490 plants, in which both overexpression and cosuppression lines were included. Overexpression but not cosuppression lines showed accelerated xylem development, suggesting the positive role of At5g60490 in xylem development. Taken together, this study provides valuable results about behaviours of various genes expressed under an early xylem‐specific promoter and about usefulness of their lines as genetic tools in woody biomass engineering.