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Background: Lianas present many interesting structural features that are linked to their climbing habit. Having lost substantial amounts of supporting tissue, these plants depend on external structures for support. Meanwhile, during their evolutionary history, they have gained additional conductive and storage tissues. The wood of lianas generally includes wider vessels, larger amounts of axial parenchyma, larger rays, and longer fibres than those of trees. Cambial variants represent another key anatomical feature of lianas. Aims: In this paper, we review various aspects of liana biology, including those associated with their vascular system and water conduction, secondary growth and seasonal responses to environmental variability, as well as aspects related to the evolution of their cambial variants. Methods: Examples from the Bignoniaceae and Leguminosae, the two most abundant liana taxa in the Neotropics, are presented in a series of case studies, bringing new data, such as the activity of the cambium during the dry seasons; the radial conducting elements that are associated with the habit; the cambial variant of Bignonieae that has evolved in a recapitulatory fashion; and the increased specialisation for photosynthate conduction by the phloem. Conclusions: Altogether, lianas represent an excellent model for studies on the convergent evolution of plants.
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... EvoDevo family, entailing considerable changes in stem development both in their external morphology, by the formation of twining stems, and in their vascular system conformations [7][8][9]. ...
... Stems furrowed by phloem wedges are one of the most common, widespread types of cambial variants in angiosperms [9,10,13]. They had been recorded within some of the richest neotropical liana lineages, such as Bignoniaceae and Sapindaceae [9,10,58,59], and their formation is intimately related to an increase in stem flexibility, breakage prevention when twisting or bending, and injury repair [7,14,[60][61][62]. ...
... Stems furrowed by phloem wedges are one of the most common, widespread types of cambial variants in angiosperms [9,10,13]. They had been recorded within some of the richest neotropical liana lineages, such as Bignoniaceae and Sapindaceae [9,10,58,59], and their formation is intimately related to an increase in stem flexibility, breakage prevention when twisting or bending, and injury repair [7,14,[60][61][62]. In Malpighiaceae, phloem wedges are also the most common cambial variant type. ...
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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.
... Surprisingly, in spite of their importance, studies investigating the connection between ray anatomical diversity and radial conductive efficiency are few (Pfautsch et al. 2015;Morris et al. 2016;Salomón et al. 2017;Pereira and Ribeiro 2018). In addition to their role in radial conduction, it is known that ray width and height have also a role in biomechanics, with plants of wide and high rays being more flexible, and therefore explaining the more common presence of these two feature combinations in lianas (Fisher and Ewers 1989;Mattheck and Kubler 1995;Burgert and Eckstein 2001;Reiterer et al. 2002a, b;Angyalossy et al. 2012Angyalossy et al. , 2015Gerolamo and Angyalossy 2017;Gerolamo et al. 2020). In experimental studies, rays also took a pivotal role in injury repair by compartmentalization (Armstrong et al. 1981;Shigo 1984;Fisher and Ewers 1989). ...
... Ray width, height and composition seem to have no relation to their climatic or geographic occurrence, being more related either to phylogenetic relationships or habits. For instance, several shrubs or secondarily woody species either lack rays or have rays with mostly upright and square cells, while lianas typically have wider, higher rays, and heterocellular mixed rays (Barghoorn 1941b;Baas and Schweingruber 1987;Lev-Yadun and Aloni 1995;Angyalossy et al. 2012Angyalossy et al. , 2015Carlquist 2013;Lens et al. 2013;Morris et al. 2016Morris et al. , 2018. Carlquist (2001) proposed that upright cells would favor the vertical rather than the radial distribution of water in narrow stems, explaining their predominant occurrence in shrubs and lianas, and as the early stages in ray ontogeny while the stems are still narrow (Barghoorn 1940(Barghoorn , 1941a. ...
... Unlike most types of cambial variants, which have evolved multiple times across vascular plants (Angyalossy et al. 2012, the compound stems and divided vascular cylinders evolved exclusively in Sapindaceae; both originate from an unusual distribution of the procambial strands in the primary body, which result in multiple secondary vascular cylinders in the adult stem (Schenck 1893; Araújo and Costa 2006;Tamaio and Angyalossy 2009;Chery et al. 2020a). Because what causes the different stem architecture in the majority of these lianas are the different architectures of the procambial strands in the primary body, some authors name these variants as "procambial variants", instead of the most common term cambial variants (Lopes et al. 2017). ...
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The Sapindales are a large order comprised of trees, shrubs, lianas and rarely herbs. This lineage is mostly pantropical with important temperate lineages, inclusing some of the most diverse, highly prized woods in the world, such as mahogany (Swietenia). In this study, we characterized the wood anatomy across eight of the nine Sapindales families, and leverage phylogenetic comparative methods to explore the evolution of wood traits in the order. We delimited 23 characters and reconstructed them onto the most recent time-calibrated phylogeny for the group. We found that ring-porosity is derived within the order, coinciding with the occupation of more seasonal climates; marginal parenchyma is ancestrally present, but largely lost in Anacardiaceae-Burseraceae-Kirkiaceae; vessels in radial chains are ancestrally absent but gained many times; scanty paratracheal parenchyma was ancestrally present with multiple evolutions of more abundant parenchyma. Anacardiaceae-Burseraceae-Kirkiaceae share tyloses and large vessel-ray pits. Radial ducts are exclusive to Anacardiaceae-Burseraceae, while traumatic ducts are exclusive to Meliaceae-Rutaceae-Simaroubaceae. Rays are generally 2–4 cells wide, heterocellular, but with multiple lineages evolving homocellular narrow rays or more heterocellular wide rays. Prismatic crystals are commonly located in rays in Anacardiaceae-Burseraceae while in the other families they are mainly in axial parenchyma. Silica bodies are abundant in Burseraceae, but also present in Anacardiaceae and Meliaceae. Lianas are exclusively in Anacardiaceae and Sapindaceae, with Sapindaceae displaying an enormous diversity of cambial variants. Our work unravels several potential synapomorphies of Sapindales major clades, and evolutionary patterns for the enormous wood anatomical diversity of the order. In addition, our work highlights variable characters worth of more detailed studies within individual families of the Sapindales.
... Here, we will focus on the typical characteristics of the secondary-growth mode of extant angiosperms and divergences from this bauplan. However, it is critical to note that there is an even larger diversity of recognized secondary growth modalities, some of which have been reviewed by Angyalossy et al. (2012Angyalossy et al. ( , 2015 and Tomescu and Groover (2019). For instance, in the roots of the late Permian glossopterid Vertebraria, large secondary xylem wedges alternate with lacunae (Decombeix et al., 2009), while stems with axial elements separated by extremely wide rays and lobed stems are found in numerous extant lineages (e.g., Trueba et al., 2015;Luna-Márquez et al., 2021), all examples where the interfascicular and fascicular cambia have independent, different activities. ...
... Heterochrony has also played a role in the emergence of unusual secondary growth ontogenies called "cambial variants" (Angyalossy et al., 2012. These cambial variants arise as an alternative activity of the vascular cambium that shifts the relative abundance and distribution of secondary tissues. ...
... The formation of ectopic neoformed vascular strands ( Figure 5A) can be explained by homeosis. Neoformed vascular cambia can form outside of the original vascular cambium (Carlquist, 2007;Angyalossy et al., 2012Angyalossy et al., , 2015 in the cortex (Cycas spp., Cycadaceae, Terrazas, 1991 Neoformations and successive cambia are two cambial variants (Angyalossy et al., 2012Acevedo-Rodríguez et al., 2015 onward). Despite the different tissues of origin, all neoformed cambia arise from parenchyma-rich regions because only the parenchyma cells have the potential to dedifferentiate and become meristematic again, owing to the lack of secondary cell wall lignification and maintenance of the nucleus. ...
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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. This article is protected by copyright. All rights reserved.
... The vascular system in the human body plays an important role in circulating nutrients, oxygen, and metabolic wastes. In general, the vascular system can be divided into three subsets of blood vessels: arteries, veins, and capillaries [1]. Different types of blood vessels possess varied configurations of tissues for exerting specific functions. ...
... Due to the lack of suitable in vitro aneurysm models to simulate the pathophysiological conditions causing the disease, detailed studies have not been carried out. Therefore, when using biotechnology to prepare aneurysm models in vitro, it is necessary to expand and explore new treatment methods for aneurysms based on the principle of the aneurysm formation mechanism [1,169]. ...
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As the leading causes of global death, cardiovascular diseases are generally initiated by artery-related disorders such as atherosclerosis, thrombosis, and aneurysm. Although clinical treatments have been developed to rescue patients suffering from artery-related disorders, the underlying pathologies of these arterial abnormalities are not fully understood. Biofabrication techniques pave the way to constructing diseased artery in vitro models using human vascular cells, biomaterials, and biomolecules, which are capable of recapitulating arterial pathophysiology with superior performance compared with conventional planar cell culture and experimental animal models. This review discusses the critical elements in the arterial microenvironment which are important considerations for recreating biomimetic human arteries with the desired disorders in vitro. Afterward, conventionally biofabricated platforms for the investigation of arterial diseases are summarized, along with their merits and shortcomings, followed by a comprehensive review of advanced biofabrication techniques and the progress of their applications in establishing diseased artery models.
... Within this large, diverse lineage, known as the lignophytes, numerous alternatives to this regular growth have evolved [13][14][15][16]. Modifications from the regular growth may derive from a single cambium with differential activity across its girth and/or multiple cambia [15,[17][18][19]. These alternative patterns of secondary growth produce diverse and complex stems architectures, also known as cambial variants [17,18]. ...
... Modifications from the regular growth may derive from a single cambium with differential activity across its girth and/or multiple cambia [15,[17][18][19]. These alternative patterns of secondary growth produce diverse and complex stems architectures, also known as cambial variants [17,18]. Many types of cambial variants are found in lineages containing lianas, although they also occur in trees, shrubs and herbs, aerial and underground organs [19,20]. ...
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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.
... Klaassen (1999) comprehensively monographed the wood anatomy of the family, including two species of Serjania. Non-self-supporting members of the Sapindaceae were studied by several researchers (Radlkofer 1875;Schenck 1893;Metcalfe & Chalk 1950;Johnson & Truscott 1956;Tamaio & Somner 2010;Angyalossy et al. 2012;Bastos et al. 2016;Lopes et al. 2017;Chery et al. 2020) due to distinctive and variant secondary growth. ...
... When sectioned, stems showed the presence of tangentially wide cambial cylinders and neoformations external to phloem wedges. Occurrence of phloem wedges and neo-formed vascular cylinders have been previously documented in the literature for Serjania (Schenck 1893;Solerder 1908;Araújo & Costa 2006Neves 2009;Tamaio & Angyalossy 2009;Tamaio & Somner 2010;Angyalossy et al. 2012;Borniego & Cabanillas 2014;Bastos et al. 2016). Bastos et al. (2016) reported nearly eight different types of cambial variants in different species of the Sapindaceae. ...
Article
The lianas in the family Sapindaceae are known for their unique secondary growth which differs from climbing species in other plant families in terms of their cambial variants. The present study deals with the stem anatomy of self-supporting and lianescent habit, development of phloem wedges, the ontogeny of cambial variants and structure of the secondary xylem in the stems of Serjania mexicana (L.) Willd. Thick stems (15–20 mm) were characterized by the presence of distinct phloem wedges and tangentially wide neo-formed cambial cylinders. As the stem diameter increases, there is a proportional increase in the number of phloem wedges and neo-formed vascular cylinders. The parenchymatous (pericyclic) cells external to phloem wedges that are located on the inner margin of the pericyclic fibres undergo dedifferentiation, become meristematic and form small segments of cambial cylinders. These cambia extend tangentially into wide and large segments of neoformations. Structurally, the secondary xylem and phloem of the neo-formed vascular cylinders remain similar to the derivatives produced by the regular vascular cambium. The secondary xylem is composed of vessels (wide and narrow), fibres, axial and ray parenchyma cells. The occurrence of perforated ray cells is a common feature in both regular and variant xylem.
... Larger vessels are thought to be at greater risk of implosion due to their larger lumen diameter (Hacke et al., 2001), and these vessels are speculated to be more prone to air-seeding because of their larger pitted wall areas (Hargrave et al., 1994;Jarbeau et al., 1995;Wheeler et al., 2005;Christman et al., 2009Christman et al., , 2012. Lianas have been shown to have large vessel diameter distributions within the same individual (Ewers et al., 1990;Angyalossy et al., 2012Angyalossy et al., , 2015Rosell and Olson, 2014;Meunier et al., 2020), but comparative data on vessel diameter distributions from co-occurring liana and tree species are lacking. Second, vessel density may also vary depending on the rainfall regime, as the density of xylem vessels is negatively related to groundwater availability (Schume et al., 2004). ...
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One of the most prominent changes in neotropical forests has been the increase in abundance and size of lianas. Studies suggest that lianas have more acquisitive strategies than trees, which could allow them to take advantage of water more effectively when it is available in water-limited forests, but few studies compared across growth form (i.e., lianas vs. trees) and forest type (i.e., wet vs. seasonally dry). We measured hydraulic and anatomical traits of co-occurring lianas and trees that convey drought resistance (xylem embolism resistance and intervessel pit membranes) and water transport capacity (xylem vessel diameter and density) in a seasonally dry and a wet evergreen tropical forest to address: (1) Are there differences between vulnerability to embolisms (P50—water potential at 50% loss of hydraulic conductivity) and hydraulic safety margins (HSM) across growth form and forest type? (2) How do vessel diameter and density vary across growth form and forest type? (3) Are there differences in xylem intervessel pit membrane thickness across growth form and forest type and does it predict xylem embolism vulnerability in trees and lianas? We examined hydraulic and xylem anatomical traits of 32 species—eight lianas and eight trees in each forest type. We found no difference in P50 and HSMs between lianas and trees and between the wetter and drier forest. Dry forest lianas had 81% greater maximum vessel diameter and 125% greater range in vessel diameter sizes than dry forest trees but, there was no significant difference between life forms in the wet forest. Dry forest species had 50% greater vessel density and 30% greater maximum pit membrane thickness than wet forest ones. Maximum pit membrane thickness was correlated to P50 and HSMs. The main difference between lianas and trees occurred in the dry forest, where lianas had larger maximum xylem vessel size than trees, implying that they have proportionally greater hydraulic conductive capacity than the trees in seasonal forests.
... High stem water storage (i.e. capacitance) resulting from abundant nonlignified parenchyma could also allow lianas to maintain hydraulic integrity during dry periods (Angyalossy et al., 2012;Isnard & Feild, 2015). Low resistance to hydraulic flow (i.e. ...
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Among tropical forests, lianas are predicted to have a growth advantage over trees during seasonal drought, with substantial implications for tree and forest dynamics. We tested the hypotheses that lianas maintain higher water status than trees during seasonal drought and that lianas maximize leaf cover to match high, dry‐season light conditions while trees are more limited by moisture availability during the dry season. We monitored the seasonal dynamics of predawn and midday leaf water potentials and leaf phenology for branches of 16 liana and 16 tree species in the canopy of two lowland tropical forests with contrasting rainfall regimes in Panama. In a wet, weakly seasonal forest, lianas maintained higher water balance than trees and maximized their leaf cover during dry‐season conditions, when light availability was high, while trees experienced drought stress. In a drier, strongly seasonal forest, lianas and trees displayed similar dry season reductions in leaf cover following strong decreases in soil water availability. Greater soil moisture availability and a higher capacity to maintain water status allow lianas to maintain the turgor potentials critical for plant growth in a wet and weakly seasonal forest but not in a dry and strongly seasonal forest.
... Accordingly, measurements of sieve element diameters might improve ecological models by widening the considered trait space and helping to capture a wider range of plant growth strategies (Li et al. 2015, Diaz et al. 2016. A robust association between growth and xylem anatomy, and tight scaling of xylem and phloem architectures has been reported for lianas (Carlquist 1988, Angyalossy et al. 2012 diameter, increased the prediction accuracy. Both variables were not among the ones with the highest relative value. ...
Article
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. While 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.
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The Apocynaceae subfamilies Secamonoideae and Asclepiadoideae have undergone several transitions during their evolution with regard to growth form and degree of woodiness. In this study, we present a wood anatomical overview of both subfamilies that complements previous work on the remaining Apocynaceae. Detailed microscopic wood descriptions using light and scanning electron microscopy were performed on 60 species that cover most Secamonoideae genera and all major woody Asclepiadoideae lineages. Our observations are in line with subfamilial and (sometimes sub)tribal delimitations. Furthermore, we present for the first time an overview of the estimated number of shifts from herbaceousness to (phylogenetically) derived woodiness in Asclepiadoideae, along with a derived woody species list with distribution and habitat information. In total, at least 168 derived woody species resulting from at least 28 independent woodiness transitions were found, with drought possibly being one of the main drivers of most of these transitions.
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RESUMO O corpus lignosum compositum, típico para as lianas da família Sapindaceae, é designado neste trabalho como "cilindro vascular composto". No caule de Serjania caracasana (Jacq.) Willd. essa variação cambial está representada por um cilindro vascular central circundado por oito cilindros vasculares periféricos. Não existe consenso quanto à terminologia que envolve essa estrutura, o que torna difícil uma abordagem anatômica desagregada de uma adequação terminológica. Nesse estudo, por meio da análise anatômica do caule, verificou-se que mesmo antes da vascularização há indícios do aspecto composto, com a formação de oito lobos que circundam a região central. Com o início da vascularização, cada lobo e a região central são denominados "cilindro vascular". O termo aqui adotado "cilindro vascular composto" é adequado, pois reflete a homologia entre os cilindros vasculares em S. caracasana através da origem procambial. Esse termo exibe um caráter descritivo que facilita a compreensão do conceito e mantém a relação de equivalência lingüística com o termo original - corpus lignosum compositum. Rejeita-se o termo "caule poliestélico" ou "caule multiestelar", pois os resultados aqui apresentados indicam a presença de um único estelo no caule.
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The accessory tissues of the hydrosystem consist of the parenchymatic contact tissue of the xylem rays, as weIl as the paratracheidal parenchyma in gymnosperms, and the paratracheal contact-parenchyma in angiosperms.