Living cells in wood. 1. Absence,scarcity and histology of axial parenchyma as keys to function

The diversity of expression in axial parenchyma (or lack of it) in woods is reviewed and synthesized with recent work in wood physiology, and questions and hypotheses relative to axial parenchyma anatomy are offered. Cell shape, location, abundance, size, wall characteristics and contents are all characteristics for the assessment of the physiological functions of axial parenchyma, a tissue that has been neglected in the consideration of how wood histology has evolved. Axial parenchyma occurrence should be considered with respect to mechanisms for the prevention and reversal of embolisms in tracheary elements. This mechanism complements cohesion–tension‐based water movement and root pressure as a way of maintaining flow in xylem. Septate fibres can substitute for axial parenchyma (‘axial parenchyma absent’) and account for water movement in xylem and for the supply of carbohydrate abundance underlying massive and sudden events of foliation, flowering and fruiting, as can fibre dimorphism and the co‐occurrence of septate fibres and axial parenchyma. Rayless woods may or may not contain axial parenchyma and are informative when analysing parenchyma function. Interconnections between ray and axial parenchyma are common, and so axial and radial parenchyma must be considered as complementary parts of a network, with distinctive but interactive functions. Upright ray cells and more numerous rays per millimetre enhance interconnection and are more often found in woods that contain tracheids. Vesselless woods in both gymnosperms and angiosperms have axial parenchyma, the distribution of which suggests a function in osmotic water shifting. Water and photosynthate storage in axial parenchyma may be associated with seasonal changes and with succulent or subsucculent modes of construction. Apotracheal axial parenchyma distribution often demonstrates storage functions that can be read independently of osmotic water shifting capabilities. Axial parenchyma may serve to both enhance mechanical strength or, when parenchyma is thin‐walled, as a tissue that adapts to volume change with a change in water content. Other functions of axial parenchyma (contributing resistance to pathogens; a site for the recovery of physical damage) are considered. The diagnostic features of axial parenchyma and septate fibres are reviewed in order to clarify distinctions and to aid in cell type identification. Systematic listings are given for particular axial parenchyma conditions (e.g. axial parenchyma ‘absent’ with septate fibres substituting). A knowledge of the axial parenchyma information presented here is desirable for a full understanding of xylem function. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177 , 291–321.     

Caryophyllales: a key group for understanding wood anatomy character states and their evolution

Definitions of character states in woods are softer than generally assumed, and more complex for workers to interpret. Only by a constant effort to transcend the limitations of glossaries can a more than partial understanding of wood anatomy and its evolution be achieved. The need for such an effort is most evident in a major group with sufficient wood diversity to demonstrate numerous problems in wood anatomical features. Caryophyllales s.l., with approximately 12 000 species, are such a group. Paradoxically, Caryophyllales offer many more interpretive problems than other ‘typically woody’ eudicot clades of comparable size: a wider range of wood structural patterns is represented in the order. An account of character expression diversity is presented for major wood characters of Caryophyllales. These characters include successive cambia (more extensively represented in Caryophyllales than elsewhere in angiosperms); vessel element perforation plates (non‐bordered and bordered, with and without constrictions); lateral wall pitting of vessels (notably pseudoscalariform patterns); vesturing and sculpturing on vessel walls; grouping of vessels; nature of tracheids and fibre‐tracheids, storying in libriform fibres, types of axial parenchyma, ray anatomy and shifts in ray ontogeny; juvenilism in rays; raylessness; occurrence of idioblasts; occurrence of a new cell type (ancistrocladan cells); correlations of raylessness with scattered bundle occurrence and other anatomical discoveries newly described and/or understood through the use of scanning electron microscopy and light microscopy. This study goes beyond summarizing or reportage and attempts interpretations in terms of shifts in degrees of juvenilism, diversification in habit, ecological occupancy strategies (with special attention to succulence) and phylogenetic change. Phylogenetic change in wood anatomy is held to be best interpreted when accompanied by an understanding of wood ontogeny, species ecology, species habit and taxonomic context. Wood anatomy of Caryophyllales demonstrates problems inherent in binary character definitions, mapping of morphological characters onto DNA‐based trees and attempts to analyse wood structure without taking into account ecological and habital features. The difficulties of bridging wood anatomy with physiology and ecology are briefly reviewed. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 164 , 342–393.     

Systematic and phylogenetic value of wood anatomy in Heteromorpheae (Apiaceae,Apioideae)

The wood anatomy of all four woody genera of the tribe Heteromorpheae (Apiaceae, subfamily Apioideae) has been described and compared, based on 40 wood samples (representing nine species of Anginon, one species of Glia, three species of Heteromorpha and two species of Polemannia). The four genera were found to be relatively similar in their wood anatomy. Helical thickenings on the vessel walls occur in all species investigated and appear to represent an ancestral character state and a symplesiomorphy for the tribes Bupleurieae and Heteromorpheae. Each of four genera has a diagnostically different combination of character states relating to the diameter of vessels, size of intervessel pits, length of fibres, presence and arrangement of banded axial parenchyma, size of rays and ray cells, and presence of septate fibres and crystals in the ray cells. The occurrence of marginal axial parenchyma in Anginon and Glia may be an additional synapomorphy for these taxa. Variation in the wood anatomy of 31 samples from nine species of Anginon is not correlated with habitat (Fynbos or Succulent Karoo Biomes), but instead appears to reflect adaptations to seasonal aridity found in both ecosystems. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 158 , 569–583.     

Wood and stem anatomy of woody Amaranthaceae s.s.: ecology, systematics and the problems of defining rays in dicotyledons

Wood and stem anatomy is studied for seven species of six genera (root anatomy also reported for one species) of Amaranthaceae s.s. Quantitative data on vessels correlate closely with relative xeromorphy of respective species, agreeing with values reported for dicotyledons without successive cambia in comparable habitats. Libriform fibre abundance increases and vessel diameter decreases as stems and roots of the annual Amaranthus caudatus mature. Long, thick-walled fibres in Bosea yervamora may be related to the upright nature of elongate semi-climbing stems. Non-bordered or minutely bordered perforation plates characterize Amaranthaceae, as they do most other Caryophyllales. Amaranthaceae have idioblastic cells containing druses, rhomboidal crystals or crystal sand: these forms intergrade and seem closely related. Rays are present in secondary xylem of the Amaranthaceae studied. Cells intermediate between ray cells and libriform fibres occur in Charpentiera elliptica . Degrees of diversity in rays and reports of raylessness in Amaranthaceae induce discussion of definition and identification of rays in dicotyledons; some sources recognize both rays and radial plates of conjunctive tissue in Amaranthaceae. The action of successive cambia is described: lateral meristem periclinal divisions produce secondary cortex externally, conjunctive tissue internally and yield vascular cambia as well. Vascular cambia produce secondary phloem and secondary xylem, in both ray and fascicular zones, as in a dicotyledon with a single cambium. Identification of meristem activity and appreciation of varied ray manifestations are essential in understanding the ontogeny of stems in Amaranthaceae (which have recently been united with Chenopodiaceae).  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 143 , 1–19.     

Fibre dimorphism: cell type diversification as an evolutionary strategy in angiosperm woods

Dimorphic fibres in angiosperm woods are designated when zones of two different kinds of fibres can be distinguished in transverse sections. The usage of most authors contrasts wider, thinner‐walled, shorter (sometimes storied) fibres with narrower, thicker‐walled fibres that have narrower lumina. The wider fibres can be distinguished in longitudinal sections from axial parenchyma, which usually consists of strands of two or more cells each surrounded by secondary walls (and thus different from septate fibres). This phenomenon occurs in some Araliaceae, Asteraceae, Fabaceae, Myrtales (notably Lythraceae), Sapindales (especially Sapindaceae), Urticales and even some Gnetales. Additional instances can doubtless be found, especially if instances of wide latewood fibres together with narrow earlywood fibres are included. There is little physiological evidence on differential functions of dimorphic fibres, except in Acer, in which hydrolysis of starch in the wide fibres is known to result in transfer of sugar into vessels early in the growing season. Starch storage in axial parenchyma may, in a complementary way, serve for embolism reversal and prevention and thus for maintenance of the water columns. Crystalliferous fibres (Myrtales, Sapindales) can be considered a form of fibre dimorphism that deters predation. Gelatinous fibres, often equated with tension wood, can also be considered as a form of fibre dimorphism. The evolutionary significance of fibre dimorphism is that a few small changes in fibre structure can result in the accomplishment of diversified functions. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 44–67.     

Systematic and ecological wood anatomy of Neotropical Schefflera (Araliaceae), with an emphasis on the Didymopanax group

Wood anatomy has been investigated from 35 species belonging to the Neotropical clade of the polyphyletic genus Schefflera (Araliaceae), representing three of the five subgroups (Didymopanax, Crepinella and Sciodaphyllum). The species examined are rather uniform in their wood structure, sharing the presence of scalariform and simple perforation plates, septate fibres and scanty paratracheal axial parenchyma. The observed variation in many wood characters showed statistically significant differences relative to latitude, climate and, especially, vegetation types. In particular, the intervessel pits are larger in species from higher latitudes and in seasonally dry habitats than those from lower latitudes and rainforests. Latitudinal and ecological trends in the variation of vessel element lengths, bar numbers on perforation plates, intervessel pit sizes and ray widths may be at least partially explained as effects of adaptation to drier environments in the course of dispersal outside the Amazonian region and diversification in the Atlantic Forest subclade and the Savannic subclade within the Didymopanax group. The occurrence of a granular annulus on the intervessel pit membranes in S. chimantensis and S. sprucei (both of the Crepinella group) is the first record of this feature in Araliaceae. In comparisons of Neotropical Schefflera with the other major clades of Schefflera sensu lato, wood anatomical diversity is consistent with the polyphyly of this genus based on molecular phylogenetic analyses. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 452–475.     

Successive cambia in Aizoaceae: products and process

The transverse and longitudinal sections of the stems and roots of 11 genera of Aizoaceae, representing a wide range of growth forms from hard fibrous stems to fibre‐free roots, were studied using light microscopy and scanning electron microscopy. In most of the genera, fibres are the first xylary product of each vascular cambium, followed by vessels in a parenchyma background. Variations on this pattern help to prove that fibres are produced by vascular cambia, except in Ruschia and Stayneria, in which both the lateral meristem and the vascular cambia produce fibres. Cylinders of conjunctive tissue parenchyma that alternate with the vascular cylinders are produced by the lateral meristem. The concept that the lateral meristem gives rise to the vascular cambia and secondary cortex is supported by photographic evidence. Radial divisions occur in the origin of the lateral meristem, and then again as vascular cambia arise from the lateral meristem; these radial divisions account for storeying in fibres and conjunctive tissue. Raylessness characterizes all Aizoaceae studied, with the exception of Tetragonia, which also differs from the remaining genera by having vasicentric axial parenchyma, a scattering of vessels amongst fibres, and the presence of druses instead of raphides. Several vascular cambia are typically formed per year. Several vascular cambia are active simultaneously in a given stem or root. Roots have fewer fibres and more abundant conjunctive tissue parenchyma than stems. Successive cambia result in an ideal dispersion of vascular tissue with respect to water and photosynthate storage and retrieval capabilities of the parenchyma, and to liana stem plans. The distribution and relative abundance of fibres, vessels, secondary phloem, and conjunctive tissue parenchyma relate primarily to habit and are not a good source of systematic data, with the probable exception of Tetragonia. The general pattern of lateral meristem and vascular cambial ontogeny is the same as in other families of the core Caryophyllales, although the patterns of the tissues produced are diverse. © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society, 2007, 153 , 141–155.     

The first record of fossil Vitaceae wood from the Southern Hemisphere,a new combination for Vitaceoxylon ramunculiformis,and reappraisal of the fossil record of the grape family (Vitaceae) from the Cenozoic of Australia

Austrovideira dettmannaegen. & sp. nov. from the early Oligocene Capella Flora in central Queensland is the first fossil Vitaceae wood described from the Southern Hemisphere. A new combination, Stafylioxylon ramunculiformis (Poole & Wilkinson) Pace & Rozefelds for a Northern Hemisphere fossil wood is also proposed. Austrovideira and Stafylioxylon share with Vitaceoxylon secondary xylem with two diameter classes of vessels, wide vessels usually solitary, narrow vessels forming radial chains, very wide and tall rays, scanty paratracheal parenchyma and septate fibres. Austrovideira differs from Vitaceoxylon in having scalariform intervessel pits and homocellular rays composed exclusively of procumbent cells. This combination of features is seen in the Ampelocissus‐Vitis clade, and a clearly stratified phloem with fibre bands alternating with all other axial elements and phloem rays rapidly dilating towards the periderm is restricted to Parthenocissus and Vitis. Stafylioxylon shares with Austrovideira the presence of scalariform intervessel pits but it differs from that genus in both ray composition and bark anatomy, as it lacks a stratified phloem. These fossil wood genera demonstrate that the lianescent habit in the Vitaceae was established by the Eocene in the Northern Hemisphere and by the Oligocene in the Southern Hemisphere. The pollen and seed fossil record shows that the Vitaceae were in Australia by the Eocene and fossil seeds suggest that the family had radiated by this time. The Oligocene Capella flora with two seed taxa and fossil wood (Austrovideira) provides further evidence of an Australian radiation. The fossil evidence, suggests a significant Gondwanic history for the family.     

Contributions to the Wood Anatomy of the Rubioideae (Rubiaceae)

Damnacanthus , Lasianthus, Saldinia, and Trichostachys are also included. Wood anatomical characters are compared with recent phylogenetic insights into the study group on the basis of molecular data. The observations demonstrate that the delimitation and separation of several taxa from the former Coussareeae/Morindeae/Prismatomerideae/Psychotrieae aggregate is supported by wood anatomical data. The Coussareeae can be distinguished from the other Rubioideae by their scanty parenchyma, septate libriform fibres, and the combination of uniseriate and very high multiseriate rays with sheath cells. Axial parenchyma bands and fibre-tracheids characterise Gynochtodes and some species of Morinda (Morindeae s.str.), but the latter genus is variable with respect to several features (e.g. vessel groupings and axial parenchyma distribution). Wood data support separation of Rennellia and Prismatomeris from Morindeae s.str.; vessels in both genera are exclusively solitary and axial parenchyma is always diffuse to diffuse-in-aggregates. Damnacanthus differs from the Morindeae alliance by the occurrence of septate fibres, absence of axial parenchyma, and the occasional presence of fibre wall thickenings. There are interesting similarities between members of the Lasianthus clade and the Pauridiantheae/Urophyleae group such as the sporadic occurrence of spiral thickenings in axial parenchyma cells. Received 26 January 2001/ Accepted in revised form 6 June 2001     

Relationships within balsaminoid Ericales: a wood anatomical approach

Wood samples of 49 specimens representing 31 species and 11 genera of woody balsaminoids, i.e., Balsaminaceae, Marcgraviaceae, Pellicieraceae, and Tetrameristaceae, were investigated using light microscopy and scanning electron microscopy. The wood structure of Marcgraviaceae, Pellicieraceae, and Tetrameristaceae is characterized by radial vessel multiples with simple perforation plates, alternate vessel pitting, apotracheal and paratracheal parenchyma, septate libriform fibers, and the presence of raphides in ray cells. Tetrameristaceae and Pellicieraceae are found to be closely related based on the occurrence of unilaterally compound vessel-ray pitting and multiseriate rays with long uniseriate ends. The narrow rays in Pelliciera are characteristic of this genus, but a broader concept of Tetrameristaceae including Pelliciera is favored. Within Marcgraviaceae, wide rays (more than five-seriate) are typical of the genus Marcgravia. Furthermore, there is evidence that the impact of altitude and habit plays an important role in the wood structure of this family. The wood structure of Balsaminaceae cannot be compared systematically with other balsaminoids because of their secondary woodiness. Balsaminaceae wood strongly differs due to the presence of exclusively upright ray cells in Impatiens niamniamensis, the absence of rays in Impatiens arguta, and the occurrence of several additional paedomorphic features in both species.     

Long‐term body pigmentation changes on a manta ray (Mobulidae)

Manta rays (genus Manta) are listed as vulnerable on the IUCN Red List based partly on population studies that use body coloration and ventral spot patterns to identify and count individuals, as a result of such patterns being considered unique and permanent during their lifetime. The present study reports the first evidence of long‐term coloration changes of manta rays based on observations of one captive individual. Darkening skin pigmentation was documented on the side of the head, the inner side of the cephalic lobes and the pectoral fin margin of the ventral side, and spot markings appeared on the gill slits within 9 months. These changes were most likely ontogenetic or were connected to maturation. The described specimen's coloration did not fulfill the taxonomic classification criteria of either manta ray species and rather resembled two different manta ray species at the beginning and end of the study. These results show that coloration patterns of manta rays are not as stable as has been assumed previously. Further studies are needed to identify the extent of such changes for accurate identification and classification of manta rays. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 406–414.     

From the Neotropics to the Namib: evidence for rapid ecological divergence following extreme long‐distance dispersal

Extreme long‐distance dispersal is an important process in plant biogeography. Such events can lead to rapid diversification due to founder effects, genetic drift and novel selection in recipient environments. Balloon vines (Cardiospermum spp.) are mainly Neotropical, but include two native southern African species, the endemic desert‐adapted C. pechuelii and the moist subtropical C. corindum (which also occurs in the Neotropics). We used phylogenetic approaches (internal transcribed spacer (ITS), rpl32 and trnL‐trnF DNA sequencing data) and population genetics (amplified fragment length polymorphism (AFLP) analyses) to confirm the long‐distance dispersal of C. corindum to southern Africa and to reveal the subsequent divergence of the morphologically and ecologically extreme but genetically close C. pechuelii. We could not judge whether incongruences between ecological requirements and morphology and gene trees for the African species resulted from ongoing gene flow or incomplete lineage sorting, but our findings do support recent divergence of C. pechuelii from C. corindum in Africa following transoceanic dispersal of the lineage. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 477–486.     

Ancient onset of geographical divergence,interpopulation genetic exchange,and natural selection on the Mc1r coat‐colour gene in the house mouse (Mus musculus)

We examined genetic variation in house mice from India and Pakistan, a predominant part of the predicted homeland of this species and also the territory of the subspecies Mus musculus castaneus (CAS), using a nuclear marker for seven tandemly arranged genes (Fanca–Spire2–Tcf25–Mc1r–Def8–Afg3l1–Dbndd1) and compared them with those previously determined for mice from other parts of Eurasia. Construction of a network with the concatenate sequences yielded three distinct clusters representing the three major subspecies groups: CAS, Mus musculus domesticus (DOM) and Mus musculus musculus (MUS). STRUCTURE analysis provided evidence for further subdivision of CAS into two main haplogroups within the Indian subcontinent. Single‐gene networks revealed not only gene‐specific architecture for subgrouping in CAS, but also allelic exchange among subspecies. These results suggest the earlier onset of allopatric divergence in the predicted homeland (the Middle East and Indian subcontinent) and subsequent intermittent admixing via gene flow across the CAS haplogroups and among the three subspecies groups. A comparison of the levels of nucleotide diversity among the gene regions revealed a less divergent state in the chromosome region containing Mc1r and its adjacent genes, indicative of a selective sweep, suggesting the involvement of natural selection in the Mc1r allelic variation. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 778–794.     

Polycentric vascular rays in Suaeda monoica and the control of ray initiation and spacing

Summary The early-formed xylem of Suaeda monoica Forssk. ex J. F. Gmel (Chenopodiaceae) is temporarily rayless. Vascular rays differentiate during later stages of its xylem ontogeny. The rays in Suaeda are heterogeneous, and some of them are aggregated. The mature xylem of this species is characterized by two unique types of vascular rays: (1) rays with several inside initiation centres of small cells formed by local frequent cell divisions in the cambium, and (2) huge xylem rays with radial phloem strands that are connected to the axial phloem. The spacing of the xylem rays is not even, and possible mechanisms controlling ray spacing are discussed. Our observations indicate that rays do not have an inhibitory zone around them in which ray initiation is prevented. The initiation of radial patterns of small cells which appear like inside rays within a large vascular ray suggests that initiation and spacing of rays is controlled by radial signal flows in relationship with axial signal fluxes.     

Systematic and phylogenetic implications of the wood anatomy of six Neotropical genera of Primulaceae

Our main goals were to identify diagnostic characters at the species, genus, and subfamily levels, find anatomical features with potential for future morphological and molecular (combined) phylogenetic analyses, and to reconstruct the evolution of wood anatomical characters in two subfamilies of Primulaceae in a molecular phylogenetic framework. We investigated twenty-seven species from the woody Myrsinoideae (4 genera) and Theophrastoideae (2 genera) using scanning electron, light, and epifluorescence microscopy. Samples were prepared using standard protocols. Based on the wood anatomical characters, we were able to identify synapomorphies and to detect evolutionary trends of interest for the genera and subfamilies. Both subfamilies share the presence of diffuse porosity, simple perforation plates, septate fibres, and scanty paratracheal axial parenchyma. Theophrastoideae species have rays?>?10 cells wide and short (<?350 µm) vessel elements, and Myrsinoideae have breakdown areas in rays and longer vessel elements. Ardisia and Stylogyne have scalariform intervessel pits, Myrsine exhibit breakdown areas in rays, and two Cybianthus species from subgenus Weilgetia have distinguishing features (e.g., scalariform perforation plate in C. nemoralis and the absence of rays in C. densiflorus). Overall, when combining characters, we were able to segregate the Neotropical Primulaceae subfamilies and genera from each other and from the subfamily Maesoideae based on wood anatomy.     

“Out-of-India” dispersal for Adina (tribe Naucleeae; family Rubiaceae): evidence from the early Eocene fossil record from India

This study reports the oldest fossil record of the genus Adina, A. vastanenesis n. sp., from the early Eocene of Vastan lignite mine (Cambay Shale Formation), Surat district, Gujarat. This fossil wood is characterized by diffuse porous wood, predominantly solitary tylosed vessels, simple perforations, scanty paratracheal to diffuse to sometimes diffuse in aggregate axial parenchyma, predominantly uniseriate to occasionally biseriate rays, and non septate fibres with bordered pits and shows its best resemblance with the modern species, Adina multifolia Haviland, belonging to the tribe Naucleeae (subfamily Cinchonoideae) of the family Rubiaceae. The present discovery becomes the first fossil record of the wood of Adina, which provides an insight about the Gondwanan origin either for the genus Adina or the tribe Naucleeae and its further dispersal to Southeast Asia.     

The earliest wood and its hydraulic properties documented in c. 407‐million‐year‐old fossils using synchrotron microtomography

We document xylem structure and hydraulic properties in the earliest woody plant A rmoricaphyton chateaupannense gen. nov. & sp. nov. based on c. 407‐million‐year‐old fossils from the Armorican Massif, western France. The plant was small, and the woody axes were narrow and permineralized in pyrite (FeS₂). We used standard palaeobotanical methods and employed propagation phase contrast X‐ray synchrotron microtomography (PPC‐SRμCT) to create three‐dimensional images of the wood and to evaluate its properties. The xylem comprised tracheids and rays, which developed from a cambium. Tracheids possessed an early extinct type of scalariform bordered pitting known as P‐type. Our observations indicate that wood evolved initially in plants of small stature that were members of Euphyllophytina, a clade that includes living seed plants, horsetails and ferns. Hydraulic properties were calculated from measurements taken from the PPC‐SRμCT images. The specific hydraulic conductivity of the xylem area was calculated as 8.7 kg m^?1 s^?1 and the mean cell thickness‐to‐span ratio (t/b)² of tracheids was 0.0372. The results show that the wood was suited to high conductive performance with low mechanical resistance to hydraulic tension. We argue that axis rigidity in the earliest woody plants initially evolved through the development of low‐density woods. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175 , 423–437.