Ontogeny, anatomical structure and function of lobed stems in the evolution of the climbing growth form in Malvaceae (Byttneria Loefl.).

BACKGROUND AND AIMS: Byttneria is one of the few climbing genera in Malvaceae. Some Byttneria are known for their lobed stems. We explore the development of these stems, how they have evolved within the group and their relevance in the evolution of the climbing growth form in Malvaceae. METHODS: We combine developmental anatomical work with phylogenetic comparative methods. We use Byttneria divaricata and B. filipes as models in the anatomical work, a review of herbarium vouchers, and the most recent phylogeny of Byttneria and allies to elucidate how these stems evolved within the clade under maximum-likelihood and Bayesian approaches. We use Pagel94 tests to analyse the correlated evolution of lobed stems and prickles. KEY RESULTS: Each lobe coincides with one of the five vascular bundles. By augmented activity of the fascicular cambium in the lobes coupled with reduced activity of the interfascicular cambium in the interlobes, secondary growth increases the lobulation already present during primary growth. Within Byttneria and allies, lobed young stems appeared at least three times, once in Ayenia and twice in the paraphyletic Byttneria. Lobed adult stems were conserved in Byttneria s.s., where lobed adult stems in combination with prickles were shown to have evolved as a climbing mechanism within the group; prickles were lost once within Byttneria s.s., in a shrubby subclade. Byttneria Clade 2 comprises climbers with twining cylindrical adult stems and no prickles, which constitutes a different climbing mechanism in the group. CONCLUSIONS: We provide evidence of one of the few cambial variants known whose secondary body reflects the primary body vasculature and show that lobed adult stems and prickles in Byttneria could be used in the new delimitation of genera in the group. Lobed stems independently appeared in climbing Grewia, suggesting a convergence favouring the climbing growth form.

The role of ontogeny in wood diversity and evolution.

Evolutionary developmental biology (evo-devo) explores the link between developmental patterning and phenotypic change through evolutionary time. In this review, we highlight the scientific advancements in understanding xylem evolution afforded by the evo-devo approach, opportunities for further engagement, and future research directions for the field. We review evidence that (1) heterochrony-the change in rate and timing of developmental events, (2) homeosis-the ontogenetic replacement of features, (3) heterometry-the change in quantity of a feature, (4) exaptation-the co-opting and repurposing of an ancestral feature, (5) the interplay between developmental and capacity constraints, and (6) novelty-the emergence of a novel feature, have all contributed to generating the diversity of woods. We present opportunities for future research engagement, which combine wood ontogeny within the context of robust phylogenetic hypotheses, and molecular biology.

Interspecific anatomical differences result in similar highly flexible stems in Bignoniaceae lianas.

PREMISE: Lianas are intriguing forest components in the tropics worldwide. They are characterized by thin and flexible stems, which have been related to a unique stem anatomy. Here, we hypothesized that the anatomical diversity of lianas, varying in shapes, proportions, and dimensions of tissues and cell types, would result in different stem bending stiffnesses across species. To test this hypothesis, we chose four abundant liana species of central Amazonia belonging to the monophyletic tribe Bignonieae (Bignoniaceae) and compared their basal stems for their anatomical architectures and bending properties. METHODS: Measurements of anatomical architecture and bending stiffness (structural Young's modulus) included light microscopy observations and three-point bending tests, which were performed on basal stems of eight individuals from four Bignonieae species. All analyses, including comparisons among species and relationships between stem stiffness and anatomical architecture, were performed using linear models. RESULTS: Although the anatomical architecture of each species consists of different qualitative and quantitative combinations of both tissues and cell types in basal stems, all species analyzed showed similarly lower bending stiffnesses. This similarity was shown to be directly related to high bark contribution to the second moment of area, vessel area and ray width. CONCLUSIONS: Similar values of stem bending stiffness were encountered in four liana species analyzed despite their variable anatomical architectures. This pattern provides new evidence of how different quantitative combinations of tissue and cell types in the basal stems of lianas can generate similarly low levels of stiffness in a group of closely related species.

Diversity, distribution, development, and evolution of medullary bundles in Nyctaginaceae.

PREMISE: Medullary bundles, i.e., vascular units in the pith, have evolved multiple times in vascular plants. However, no study has ever explored their anatomical diversity and evolution within a phylogenetic framework. Here, we investigated the development of the primary vascular system within Nyctaginaceae showing how medullary bundles diversified within the family. METHODS: Development of 62 species from 25 of the 31 genera of Nyctaginaceae in stem samples was thoroughly studied with light microscopy and micro-computed tomography. Ancestral states were reconstructed using a maximum likelihood approach. RESULTS: Two subtypes of eusteles were found, the regular eustele, lacking medullary bundles, observed exclusively in representatives of Leucastereae, and the polycyclic eustele, containing medullary bundles, found in all the remaining taxa. Medullary bundles had the same origin and development, but the organization was variable and independent of phyllotaxy. Within the polycyclic eustele, medullary bundles developed first, followed by the formation of a continuous concentric procambium, which forms a ring of vascular bundles enclosing the initially formed medullary bundles. The regular eustele emerged as a synapomorphy of Leucastereae, while the medullary bundles were shown to be a symplesiomorphy for Nyctaginaceae. CONCLUSIONS: Medullary bundles in Nyctaginaceae developed by a single shared pathway, that involved the departure of vascular traces from lateral organs toward the pith. These medullary bundles were encircled by a continuous concentric procambium that also constituted the polycyclic eustele, which was likely a symplesiomorphy for Nyctaginaceae with one single reversion to the regular eustele.

First report of laticifers in lianas of Malpighiaceae and their phylogenetic implications.

PREMISE: Laticifers have evolved multiple times in angiosperms and have been interpreted as a key innovation involved in plant defense mechanisms. In Malpighiaceae, laticifers were previously known from a single lineage of trees and shrubs, the Galphimia clade, but with detailed anatomical analyses here, we show that their distribution is broader in the family, also encompassing large clades of lianas. METHODS: From 15 genera, 70 species of Malpighiaceae were surveyed through careful anatomical ontogenetic analysis of roots, stems, and leaves and detailed histochemical tests to elucidate the nature of laticifers and latex in the family. RESULTS: Articulated anastomosing laticifers were encountered in roots, stems, and leaves of two distantly related megadiverse genera of Malpighiaceae lianas: Stigmaphyllon (stigmaphylloid clade) and Tetrapterys s.s. (tetrapteroid clade). From the apex downward, in Stigmaphyllon the laticifers are derived from the procambium and from the cambium during its early activity and are present in the outermost part of the vascular cylinder of stems and leaves and in the pericycle of roots, whereas in Tetrapterys s.s. they are derived from the ground meristem, procambium, and cambium throughout the plant body and are present in the cortex and pith, either the pericycle in roots or the outermost part of the vascular system in stems and leaves, and the primary and secondary phloem. CONCLUSIONS: Laticifers seem to have evolved at least three times independently in Malpighiaceae, once in a lineage of trees and shrubs and twice in two distantly related megadiverse lianescent lineages. Laticifer evolution in Malpighiaceae is homoplastic and may be related to increases in species diversification.

Height-related scaling of phloem anatomy and the evolution of sieve element end wall types in woody plants.

In the sieve elements (SEs) of the phloem, carbohydrates are transported throughout the whole plant from their site of production to sites of consumption or storage. SE structure, especially of the pore-rich end walls, has a direct effect on translocation efficiency. Differences in pore size and other features were interpreted as an evolutionary trend towards reduced hydraulic resistance. However, this has never been confirmed. Anatomical data of 447 species of woody angiosperms and gymnosperms were used for a phylogenetic analysis of end wall types, calculation of hydraulic resistance and correlation analysis with morphological and physiological variables. end wall types were defined according to pore arrangement: either grouped into a single area (simple) or into multiple areas along the end wall (compound). Convergent evolution of end wall types was demonstrated in woody angiosperms. In addition, an optimization of end wall resistance with plant height was discovered, but found to be independent of end wall type. While physiological factors also showed no correlation with end wall types, the number of sieve areas per end wall was found to scale with SE length. The results exclude the minimization of hydraulic resistance as evolutionary driver of different end wall types, contradicting this long-standing assumption. Instead, end wall type might depend on SE length.

Secondary phloem diversity and evolution in Bignonieae (Bignoniaceae).

BACKGROUND AND AIMS: Phloem evolution has been explored in the literature across very broad scales, either for vascular plants as a whole or for major plant groups, such as the monocotyledons or the former dicotyledons. However, it has never been examined in a way that would elucidate evolutionary shifts leading to the diversification of phloem in single lineages. Therefore, the present study explores in detail the patterns of phloem evolution in the tribe Bignonieae (Bignoniaceae). This group represents a particularly good model for phloem studies since it is known to have a very conspicuous and diverse phloem. METHODS: A total of 19 phloem characters were coded in 56 species from all 21 genera currently recognized in the tribe Bignonieae, accounting for phloem wedge growth and for all the anatomical cell diversity encountered in the phloem. Phloem evolution was explored by reconstructing ancestral character states using maximum-likelihood assumptions with a time-calibrated molecular phylogeny for the group. Directionality and the effect of phylogenetic transformations in the current variation of quantitative traits and evolutionary correlations of selected discrete phloem traits were also tested under a maximum-likelihood approach. KEY RESULTS: Individual phloem features are quite diverse in the tribe, but generally conserved within smaller clades. Contrasting phloem patterns were found when comparing major groups, with certain lineages having the phloem marked by a background of phloem fibres where all other cells are embedded, tangentially arranged sieve tubes and sieve-tubecentric parenchyma. In contrast, other lineages exhibited a scarcely fibrous phloem, regularly stratified phloem, sieve tube elements in radial or diffuse arrangement, and diffuse parenchyma. We found signals of directional evolution in fibre abundance and number of sieve areas, which increased in the 'Fridericia and allies extended clade' and decreased in the 'Multiples of four extended clade', resulting in no signal of directionality when the whole Bignonieae was considered. In contrast, no indication of directional evolution was found for the axial parenchyma, either in single clades within Bignonieae or in the entire tribe. Positive correlation was found between sieve element length and both sieve plate type and the presence of a storied structure. Correlated evolution was also found between fibre abundance and several traits, such as sieve tube arrangement, sieve plate type, parenchyma arrangement, ray lignification and number of companion cells. CONCLUSIONS: The secondary phloem of Bignonieae is extremely diverse, with sister lineages exhibiting distinct phloem anatomies derived from contrasting patterns of evolution in fibre abundance. Fibre abundance in the tribe has diversified in correlation with sieve tube arrangement, sieve tube morphology, number of companion cells and parenchyma type. The results challenge long-standing hypotheses regarding general trends in cell abundance and morphological cell evolution within the phloem, and demonstrate the need to expand studies in phloem anatomy both at a narrow taxonomic scale and at a broad one, such as to families and orders.

Priorities for Bark Anatomical Research: Study Venues and Open Questions.

The bark fulfils several essential functions in vascular plants and yields a wealth of raw materials, but the understanding of bark structure and function strongly lags behind our knowledge with respect to other plant tissues. The recent technological advances in sampling and preparation of barks for anatomical studies, along with the establishment of an agreed bark terminology, paved the way for more bark anatomical research. Whilst datasets reveal bark's taxonomic and functional diversity in various ecosystems, a better understanding of the bark can advance the understanding of plants' physiological and environmental challenges and solutions. We propose a set of priorities for understanding and further developing bark anatomical studies, including periderm structure in woody plants, phloem phenology, methods in bark anatomy research, bark functional ecology, relationships between bark macroscopic appearance, and its microscopic structure and discuss how to achieve these ambitious goals.

Phloem wedges in Malpighiaceae: origin, structure, diversification, and systematic relevance.

BACKGROUND: Phloem wedges furrowing the wood are one of the most notorious, widespread types of cambial variants in Angiosperms. Many lianas in Malpighiaceae show these variations in the arrangement of the secondary tissues. Here we explore their ontogeny, structure, and evolution in Malpighiaceae, where phloem wedges appeared multiple times, showing how they have contributed to the anatomical diversification of the family. Using a broad sampling with 143 species from 50 genera, covering all major lineages in Malpighiaceae, we crossed data from ontogeny, stem anatomy, and phylogenetic comparative methods to determine ontogenetic trajectories, final anatomical architectures, and evolution within the most recent phylogeny for the family. RESULTS: Phloem wedges appeared exclusively in lianas and disappeared in shrub lineages nested within liana lineages. At the onset of development, the vascular cambium is regular, producing secondary tissues homogeneously across its girth, but soon, portions of the cambium in between the leaf insertions switch their activity producing less wood and more phloem, initially generating phloem arcs, which progress into phloem wedges. In the formation of these wedges, two ontogenetic trajectories were found, one that maintains the continuity of the cambium, and another where the cambium gets dissected. Phloem wedges frequently remain as the main cambial variant in several lineages, while in others there are additional steps toward more complex cambial variants, such as fissured stems, or included phloem wedges, the latter a novel type of interxylary phloem first described for the family. CONCLUSIONS: Phloem wedges evolved exclusively in lianas, with two different ontogenies explaining the 10 independent origins of phloem wedges in Malpighiaceae. The presence of phloem wedges has favored the evolution of even more complex cambial variants such as fissured stems and interxylary phloem.

Linking the evolution of development of stem vascular system in Nyctaginaceae and its correlation to habit and species diversification.

BACKGROUND: Alternative patterns of secondary growth in stems of Nyctaginaceae is present in all growth habits of the family and have been known for a long time. However, the interpretation of types of cambial variants have been controversial, given that different authors have given them different developmental interpretations. The different growth habits coupled with an enormous stem anatomical diversity offers the unique opportunity to investigate the evolution of complex developments, to address how these anatomies shifted within habits, and how the acquisition of novel cambial variants and habit transitions impacted the diversification of the family. METHODS: We integrated developmental data with a phylogenetic framework to investigate the diversity and evolution of stem anatomy in Nyctaginaceae using phylogenetic comparative methods, reconstructing ancestral states, and examining whether anatomical shifts correspond to species diversification rate shifts in the family. RESULTS: Two types of cambial variants, interxylary phloem and successive cambia, were recorded in Nyctaginaceae, which result from four different ontogenies. These ontogenetic trajectories depart from two distinct primary vascular structures (regular or polycyclic eustele) yet, they contain shared developmental stages which generate stem morphologies with deconstructed boundaries of morphological categories (continuum morphology). Unlike our a priori hypotheses, interxylary phloem is reconstructed as the ancestral character for the family, with three ontogenies characterized as successive cambia evolving in few taxa. Cambial variants are not contingent on habits, and their transitions are independent from species diversification. CONCLUSIONS: Our findings suggest that multiple developmental mechanisms, such as heterochrony and heterotopy, generate the transitions between interxylary phloem and successive cambia. Intermediate between these two extremes are present in Nyctaginaceae, suggesting a continuum morphology across the family as a generator of anatomical diversity.

Diameters of phloem sieve elements can predict stem growth rates of woody plants.

Understanding forest dynamics is crucial to addressing climate change and reforestation challenges. Plant anatomy can help predict growth rates of woody plants, contributing key information on forest dynamics. Although features of the water-transport system (xylem) have long been used to predict plant growth, the potential contribution of carbon-transporting tissue (phloem) remains virtually unexplored. Here, we use data from 347 woody plant species to investigate whether species-specific stem diameter growth rates can be predicted by the diameter of both the xylem and phloem conducting cells when corrected for phylogenetic relatedness. We found positive correlations between growth rate, phloem sieve element diameter and xylem vessel diameter in liana species sampled in the field. Moreover, we obtained similar results for data extracted from the Xylem Database, an online repository of functional, anatomical and image data for woody plant species. Information from this database confirmed the correlation of sieve element diameter and growth rate across woody plants of various growth forms. Furthermore, we used data subsets to explore potential influences of biomes, growth forms and botanical family association. Subsequently, we combined anatomical and geoclimatic data to train an artificial neural network to predict growth rates. Our results demonstrate that sugar transport architecture is associated with growth rate to a similar degree as water-transport architecture. Furthermore, our results illustrate the potential value of artificial neural networks for modeling plant growth under future climatic scenarios.

Evolution of disparity between the regular and variant phloem in Bignonieae (Bignoniaceae).

PREMISE OF THE STUDY: The phloem is a plant tissue with a critical role in plant nutrition and signaling. However, little is still known about the evolution of this tissue. In lianas of the Bignoniaceae, two distinct types of phloem coexist: a regular and a variant phloem. The cells associated with these two phloem types are known to be anatomically different; however, it is still unclear what steps were involved in the evolution of such differences. METHODS: Here we studied the anatomical development of the regular and variant phloem in representatives of all 21 genera of Bignonieae and used a phylogenetic framework to investigate the timing of changes associated with the evolution of each phloem type. KEY RESULTS: We found that the variant phloem always appears in a determinate location, between the leaf orthostichies. Furthermore, the variant phloem was mostly occupied by very wide sieve tubes and generally included a higher concentration of fibers, indicating an increase in conduction and mechanical support. On the other hand, the regular phloem included much more parenchyma, more and wider rays, and tiny sieve tubes that resembled terminal sieve tubes from plants with seasonal formation of vascular tissues; these findings suggest reduced conduction and higher storage capacity in the regular phloem. CONCLUSIONS: Overall, differences between the regular and variant phloem increased over time, leading to further specialization in conduction in the variant phloem and an increase in storage specialization in the regular phloem.

Polishing entire stems and roots using sandpaper under water: An alternative method for macroscopic analyses.

PREMISE: Polishing entire stem and root samples is an effective method for studying their anatomy; however, polishing fresh samples to preserve woods with soft tissues or barks is challenging given that soft tissues shrink when dried. We propose sanding fresh or liquid-preserved samples under water as an alternative, given that it preserves all tissues in an intact and clear state. METHODS AND RESULTS: By manually grinding the surface of the samples under water using three ascending grits of waterproof sandpapers, an excellent polished sanded surface is obtained. The wood swarf goes into the water without clogging the cell lumina, rendering the surfaces adequate for cell visualization and description. We show results in palms, liana stems, roots, and wood blocks. CONCLUSIONS: Using this simple, inexpensive, rapid technique, it is possible to polish either fresh, dry, or liquid-preserved woody plant samples, preserving the integrity of both the soft and hard tissues and allowing for detailed observations of the stems and roots.

Modifications during Early Plant Development Promote the Evolution of Nature's Most Complex Woods.

Secondary growth is the developmental process by which woody plants grow radially. The most complex presentations of secondary growth are found in lianas (woody vines) as a result of the unique demand to maintain stems that can twist without breaking. The complex woody forms in lianas arise as non-circular stem outlines, aberrant tissue configurations, and/or shifts in the relative abundance of secondary tissues. Previous studies demonstrate that abnormal activity of the vascular cambium leads to variant secondary growth; however, the developmental and evolutionary basis for this shift is still largely unknown. Here, we adopt an integrative approach, leveraging techniques from historically distinct disciplines-developmental anatomy and phylogenetic comparative methods-to elucidate the evolution of development of the complex woody forms in a large lineage of tropical lianas, Paullinia L. (Sapindaceae). We find that all forms of variant secondary growth trace back to the same modification during early stem development, which results in young plants with lobed stem outlines and a discontinuous distribution of vascular bundles. By placing development in a phylogenetic context, we further show that the lobed primary plant bauplan is the evolutionary precursor to all complex woody forms. We find evidence for three evolutionary mechanisms that generate phenotypic novelty: exaptation and co-opting of the ancestral bauplan, the quasi-independence of the interfascicular and fascicular cambia, and the inclusion of additional developmental stages to the end of the ancestral ontogeny. Our study demonstrates the utility of integrating developmental data within a phylogenetic framework to investigate the evolution of complex traits.

The rise and evolution of the cambial variant in Bignonieae (Bignoniaceae).

Cambial variants represent a form of secondary growth that creates great stem anatomical diversity in lianas. Despite the importance of cambial variants, nothing is known about the developmental mechanisms that may have led to the current diversity seen in these stems. Here, a thorough anatomical analysis of all genera along the phylogeny of Bignonieae (Bignoniaceae) was carried out in order to detect when in their ontogeny and phylogeny there were shifts leading to different stem anatomical patterns. We found that all species depart from a common developmental basis, with a continuous, regularly growing cambium. Initial development is then followed by the modification of four equidistant portions of the cambium that reduce the production of xylem and increase the production of phloem, the former with much larger sieve tubes and an extended lifespan. In most species, the formerly continuous cambium becomes disjunct, with cambial portions within phloem wedges and cambial portions between them. Other anatomical modifications such as the formation of multiples of four phloem wedges, multiple-dissected phloem wedges, and included phloem wedges take place thereafter. The fact that each novel trait raised on the ontogenetic trajectory appeared in subsequently more recent ancestors on the phylogeny suggests a recapitulatory history. This recapitulation is, however, caused by the terminal addition of evolutionary novelties rather than a truly heterochronic process. Truly heterochronic processes were only found in shrubby species, which resemble juveniles of their ancestors, as a result of a decelerated phloem formation by the variant cambia. In addition, the modular evolution of phloem and xylem in Bignonieae seems to indicate that stem anatomical modifications in this group occurred at the level of cambial initials.

Taxonomic revision of Mcvaughia W.R.Anderson (Malpighiaceae): notes on vegetative and reproductive anatomy and the description of a new species.

A taxonomic revision of Mcvaughia is presented, including the description of a new species from the state of Piauí, Brazil, and notes on wood, secondary phloem, leaf, and floral morpho-anatomy. We present a key to the species, full morphological descriptions, a distribution map, and notes on distribution, ecology, etymology, and conservation status for each species.