Evolution and Function of Leaf Venation Architecture: A Review

The leaves of extant terrestrial plants show highly diverseand elaborate patterns of leaf venation. One fundamental featureof many leaf venation patterns, especially in the case of angiospermleaves, is the presence of anastomoses. Anastomosing veins distinguisha network topologically from a simple dendritic (tree-like)pattern which represents the primitive venation architecture.The high degree of interspecific variation of entire venationpatterns as well as phenotypic plasticity of some venation properties,such as venation density, indicate the high selective pressureacting on this branching system. Few investigations deal withfunctional properties of the leaf venation system. The interrelationshipsbetween topological or geometric properties of the various leafvenation patterns and functional aspects are far from beingwell understood. In this review we summarize current knowledgeof interrelationships between the form and function of leafvenation and the evolution of leaf venation patterns. Sincethe functional aspects of architectural features of differentleaf venation patterns are considered, the review also refersto the topic of individual and intraspecific variation. Onebasic function of leaf venation is represented by its contributionto the mechanical behaviour of a leaf. Venation geometry anddensity influences mechanical stability and may affect, forexample, susceptibility to herbivory. Transport of water andcarbohydrates is the other basic function of this system andthe transport properties are also influenced by the venationarchitecture. These various functional aspects can be interpretedin an ecophysiological context. Copyright 2001 Annals of BotanyCompany Review, leaves, leaf venation, evolution, network, transport, flow, mechanical stabilization     

叶脉网络功能性状及其生态学意义

叶脉网络结构是叶脉系统在叶片里的分布和排列样式。早期叶脉网络结构研究主要集中在其分类学意义上; 近年来叶脉网络功能性状及其在植物水分利用上的意义已成为植物生态学研究的热点。该文介绍了叶脉网络功能性状的指标体系(包括叶脉密度、叶脉直径、叶脉之间的距离、叶脉闭合度等), 综述了叶脉网络功能性状与叶脉系统功能(包括水分、养分和光合产物等物质运输、机械支撑和虫害防御等)的关系, 叶脉网络功能性状与叶片其他功能性状(包括比叶重、叶寿命、光合速率、叶片大小、气孔密度等)的协同变异和权衡关系, 以及叶脉网络功能性状随环境因子(包括水分、温度、光照等)的变化规律等方面的最新研究进展。此外, 叶脉网络功能性状的研究成果也被应用于古环境重建、城市交通规划、流域规划及全球变化研究中。由于叶脉网络功能性状是环境因子与系统发育共同作用的结果, 未来开展分子—叶片—植物—生态系统等多尺度的叶脉网络功能性状研究, 理清叶脉网络功能性状与气孔失水—茎干导水—根系吸水等植物水分利用的关系, 将为预测植物及生态系统对全球变化的响应提供新的启示。     

Leaf architecture and ecophysiology of an early basal eudicot from the Early Cretaceous of Spain

Iterophyllum lobatum gen. et sp. nov. is reported from the late Barremian lithographic limestones of Las Hoyas, Spain. It consists of a simple, petiolate leaf, with a pinnately lobed lamina. The dentate thickened margin bears chloranthoid‐like glands at lobe apices and sinuses. The venation is pinnate and craspedodromous, with three discernible vein orders. Based on the low regularity of vein course and angles and the low leaf rank, such a venation pattern may represent an early evolved leaf archetype in early basal eudicots. An acropetal leaf development mode in I. lobatum is similar to that in several living Papaveraceae. The leaf architecture and ecophysiology, particularly the vein widths and the glands, indicate that I. lobatum leaves were aerial. The plant grew close to water in the wetland terrestrial ecosystem of Las Hoyas. Iterophyllum lobatum might have been an opportunist species in early ecological succession stages after wildfires. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 594–605.     

国产五味子科五种植物叶片脉序研究

首次报道了国产五味子科５种植物的叶脉特征,对科、属、种的特征作了描述,编排有分种检索表．通过与八角科叶脉的比较,支持建立五味子科与八角科的观点,认为五味子属的系统位置在南五味子属之后,并讨论了八角目的演化趋势     

Optimization of leaf morphology in relation to leaf water status: A theory

The leaf economic traits such as leaf area, maximum carbon assimilation rate, and venation are all correlated and related to water availability. Furthermore, leaves are often broad and large in humid areas and narrower in arid/semiarid and hot and cold areas. We use optimization theory to explain these patterns. We have created a constrained optimization leaf model linking leaf shape to vein structure that is integrated into coupled transpiration and carbon assimilation processes. The model maximizes net leaf carbon gain (NPP_leaf) over the loss of xylem water potential. Modeled relations between leaf traits are consistent with empirically observed patterns. As the results of the leaf shape–venation relation, our model further predicts that a broadleaf has overall higher NPP_leaf compared to a narrowleaf. In addition, a broadleaf has a lower stomatal resistance compared to a narrowleaf under the same level of constraint. With the same leaf area, a broadleaf will have, on average, larger conduits and lower total leaf xylem resistance and thus be more efficient in water transportation but less resistant to cavitation. By linking venation structure to leaf shape and using water potential as the constraint, our model provides a physical explanation for the general pattern of the covariance of leaf traits through the safety–efficiency trade‐off of leaf hydraulic design.     

Leaf Venation and Its Systematic Significance in Sapindaceae of China

Leaf venation of 27 species representing 25 genera of Sapindaceae (sstr.) of China was investigated for the first time. The pinnate venation pattern in most species is either camptodromous, or craspedodromous. Three types of leaf blade margin were observed, ie., entire, toothed and partite. The secondary veins are branched or unbranched. Most species have intersecondary veins. The tertiary veins of most species are reticulate and percurrent. The areoles are regular or irregular. Veinlets are simple, branched or absent. The delimitations of Xanthoceroideae and Lepisanthes sensu lato are supported by leaf venation characters. The close relationships among Dimocarpus, Litchi and Nephelium are supported by the evidence from leaf venation. A key to the species of Sapinaceae based on leaf venation characters is presented.     

Evolution of leaf form correlates with tropical-temperate transitions in Viburnum (Adoxaceae)

Strong latitudinal patterns in leaf form are well documented in floristic comparisons and palaeobotanical studies. However, there is little agreement about their functional significance; in fact, it is still unknown to what degree these patterns were generated by repeated evolutionary adaptation. We analysed leaf form in the woody angiosperm clade Viburnum (Adoxaceae) and document evolutionarily correlated shifts in leafing habit, leaf margin morphology, leaf shape and climate. Multiple independent shifts between tropical and temperate forest habitats have repeatedly been accompanied by a change between evergreen, elliptical leaves with entire margins and deciduous, more rounded leaves with toothed or lobed margins. These consistent shifts in Viburnum support repeated evolutionary adaptation as a major determinant of the global correlation between leaf form and mean annual temperature. Our results provide a new theoretical grounding for the inference of past climates using fossil leaf assemblages.     

中国无患子科植物的叶脉形态及其系统学意义

对国产狭义无患子科25属27种植物的叶脉形态特征进行了研究报道。结果表明：叶脉均属于羽状脉类型,其中多数为曲行羽状脉,部分为直行羽状脉;叶缘有全缘、具齿和深裂3种类型;二级叶脉具有分支和不分支两种类型;大部分种类具二级间脉,少数不具间脉或间脉不明显;多数种类的三级脉为结网型和贯串型并存;网眼的发育有完善和不完善2种类型;盲脉有简单、具分支和无盲脉3种类型。叶脉形态研究结果支持文冠果亚科以及广义鳞花木属概念,观察发现龙眼属、荔枝属与韶子属从脉序特征方面表现出较近的亲缘关系。编写了国产无患子科叶片脉序特征检索表。     

Heterogeneity in bean leaf mesophyll tissue and ion flux profiles: leaf electrophysiological characteristics correlate with the anatomical structure

It has been suggested for some time that the architectural properties of leaf venation are related to leaf functions; however, experimental evidence is scant and, when present, mainly investigates water or carbohydrate transport patterns. Transport of inorganic nutrients in relationship to leaf anatomical structure remains, to a large extent, an unexplored area in plant physiology. In this study, we correlated ion flux profiles with the anatomical structure of bean (Vicia faba L.) leaf mesophyll tissue using a non-invasive ion flux measuring technique (microelectrode ion flux estimation) and scanning electron microscopy. Quasi-periodic patterns of net H+ and K+ flux distributions were found when the mesophyll surface was scanned along the longitudinal axis with 0.1-0.2 mm increments. These patterns showed a high correlation with anatomical features of the mesophyll tissue (i.e. the distribution of vascular bundles). The observed flux profiles were not time-dependent, showed qualitative similarity in both light and dark conditions, and resulted in heterogeneous plant physiological responses. The possible physiological role of the observed findings, specifically in relation to stomatal 'patchiness' and phloem loading mechanisms, is discussed.     

Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis

In both plants and animals vein networks play an essential role in transporting nutrients. In plants veins may also provide mechanical support. The mechanism by which vein patterns are formed in a developing leaf remains largely unresolved. According to the canalization hypothesis, a signal inducing vein differentiation is transported in a polar manner and is channeled into narrow strands. Since inhibition of auxin transport affects venation patterns, auxin is likely to be part of the signal involved. However, it is not clear whether the canalization hypothesis, initially formulated over 25 years ago, is compatible with recent experimental data. In this paper we focus on three aspects of this question, and show that: (i) canalization models can account for an acropetal development of the midvein if vein formation is sink-driven; (ii) canalization models are in agreement with venation patterns resulting from inhibited auxin transport and (iii) loops and discontinuous venation patterns can be obtained assuming proper spacing of discrete auxin sources.     

Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture

Across plant species, leaves vary enormously in their size and their venation architecture, of which one major function is to replace water lost to transpiration. The leaf hydraulic conductance (K(leaf)) represents the capacity of the transport system to deliver water, allowing stomata to remain open for photosynthesis. Previous studies showed that K(leaf) relates to vein density (vein length per area). Additionally, venation architecture determines the sensitivity of K(leaf) to damage; severing the midrib caused K(leaf) and gas exchange to decline, with lesser impacts in leaves with higher major vein density that provided more numerous water flow pathways around the damaged vein. Because xylem embolism during dehydration also reduces K(leaf), we hypothesized that higher major vein density would also reduce hydraulic vulnerability. Smaller leaves, which generally have higher major vein density, would thus have lower hydraulic vulnerability. Tests using simulations with a spatially explicit model confirmed that smaller leaves with higher major vein density were more tolerant of major vein embolism. Additionally, for 10 species ranging strongly in drought tolerance, hydraulic vulnerability, determined as the leaf water potential at 50% and 80% loss of K(leaf), was lower with greater major vein density and smaller leaf size (|r| = 0.85-0.90; P < 0.01). These relationships were independent of other aspects of physiological and morphological drought tolerance. These findings point to a new functional role of venation architecture and small leaf size in drought tolerance, potentially contributing to well-known biogeographic trends in leaf size.     

绣球亚科的脉序研究

本文对绣球亚科全部９个属中选取４５个种或变种作了叶脉序的研究。绣球亚科除黄山梅属外,大体呈曲行羽状脉。叉叶蓝属,蛛网萼属和草绣球属同具真曲行羽状脉和相似的高级脉序;赤壁草属和冠盖藤属表现出明显的环结曲行羽状脉式样;钻地风属多呈现分支曲行羽状脉式样;常山属和绣球属包含多种过渡类型,与其它属密切相连。黄山梅属脉序为独特的羽状达缘型式样,明显表现出向掌状脉的过渡,与其它属不同。脉序研究支持Ｔａｋｈｔａｊａｎ系统把黄山梅属提升为亚科的处理,同时又表明从脉序性状来看,绣球亚科各属之间性状彼此重叠,没有十分明确的界限。     

Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis

The study of transgenic Arabidopsis lines with altered vascular patterns has revealed key players in the venation process, but details of the vascularization process are still unclear, partly because most lines have only been assessed qualitatively. Therefore, quantitative analyses are required to identify subtle perturbations in the pattern and to test dynamic modeling hypotheses using biological measurements. We developed an online framework, designated Leaf Image Analysis Interface (LIMANI), in which venation patterns are automatically segmented and measured on dark-field images. Image segmentation may be manually corrected through use of an interactive interface, allowing supervision and rectification steps in the automated image analysis pipeline and ensuring high-fidelity analysis. This online approach is advantageous for the user in terms of installation, software updates, computer load and data storage. The framework was used to study vascular differentiation during leaf development and to analyze the venation pattern in transgenic lines with contrasting cellular and leaf size traits. The results show the evolution of vascular traits during leaf development, suggest a self-organizing mechanism for leaf venation patterning, and reveal a tight balance between the number of end-points and branching points within the leaf vascular network that does not depend on the leaf developmental stage and cellular content, but on the leaf position on the rosette. These findings indicate that development of LIMANI improves understanding of the interaction between vascular patterning and leaf growth.     

Venation networks and the origin of the leaf economics spectrum

The leaf economics spectrum describes biome-invariant scaling functions for leaf functional traits that relate to global primary productivity and nutrient cycling. Here, we develop a comprehensive framework for the origin of this leaf economics spectrum based on venation-mediated economic strategies. We define a standardized set of traits - density, distance and loopiness - that provides a common language for the study of venation. We develop a novel quantitative model that uses these venation traits to model leaf-level physiology, and show that selection to optimize the venation network predicts the mean global trait-trait scaling relationships across 2548 species. Furthermore, using empirical venation data for 25 plant species, we test our model by predicting four key leaf functional traits related to leaf economics: net carbon assimilation rate, life span, leaf mass per area ratio and nitrogen content. Together, these results indicate that selection on venation geometry is a fundamental basis for understanding the diversity of leaf form and function, and the carbon balance of leaves. The model and associated predictions have broad implications for integrating venation network geometry with pattern and process in ecophysiology, ecology and palaeobotany.     

Correlated evolution of stem and leaf hydraulic traits in Pereskia (Cactaceae)

Recent studies have demonstrated significant correlations between stem and leaf hydraulic properties when comparing across species within ecological communities. This implies that these traits are co-evolving, but there have been few studies addressing plant water relations within an explicitly evolutionary framework. This study tests for correlated evolution among a suite of plant water-use traits and environmental parameters in seven species of Pereskia (Cactaceae), using phylogenetically independent contrasts. There were significant evolutionary correlations between leaf-specific xylem hydraulic conductivity, Huber Value, leaf stomatal pore index, leaf venation density and leaf size, but none of these traits appeared to be correlated with environmental water availability; only two water relations traits - mid-day leaf water potentials and photosynthetic water use efficiency - correlated with estimates of moisture regime. In Pereskia, it appears that many stem and leaf hydraulic properties thought to be critical to whole-plant water use have not evolved in response to habitat shifts in water availability. This may be because of the extremely conservative stomatal behavior and particular rooting strategy demonstrated by all Pereskia species investigated. These results highlight the need for a lineage-based approach to understand the relative roles of functional traits in ecological adaptation.     

植物叶片水力与经济性状权衡关系的研究进展

叶片既是植物光合产物形成的主要场所, 又是整株植物的水力瓶颈、应对灾难性水力失调的安全阀门, 是植物碳水耦合权衡的重要器官。叶经济型谱反映了叶片经济性状“投资-收益”的权衡, 为验证植物进化过程中形成的物种对策提供了适用的理论框架。叶片水力性状变化会影响叶片经济性状及植物存活和生长。因此, 探索植物叶片水力与经济性状的权衡关系, 对建立植物碳-水耦合模型、揭示植物水-碳投资机理、扩展植物性状型谱等均有重要意义。该文首先综述了叶片水力性状、经济性状及两者之间的权衡关系, 分析了叶片导水率与水力脆弱性、失膨点水势、水容、安全阈值等水力性状以及与叶片的形态、结构和气体交换功能性状之间的关系。然后, 从叶片形态、解剖和叶脉网络结构以及气孔功能方面探讨了叶片水力性状与经济性状的调节机制。最后, 提出今后应加强三方面的研究: (1)探索建立植物根-茎-叶水力输导系统的碳-氮-水资源的整株经济型谱, 以揭示植物功能结构耦合、高效固碳用水的生理生态学机制; (2)探索叶片水力安全、水力效率和固碳效率之间的普适性权衡关系, 以深入理解抗旱植物叶片构建的生物物理结构与生理代谢的关系; (3)探索个体水平碳水代谢关系、水分运输与生长速率的耦合, 为代谢推演理论和植物群落尺度预测提供基础。     

长果安息香属和秤锤树属植物叶片脉序研究

本文观察和描述了单种属长果安息香属和秤锤树属５种植物的叶脉特征。结果表明,两属植物的脉序特征比较一致;但各种之间也存在一些差别,根据这些差别可编出分种检索表;长果安息香与秤锤树属各种的三级脉特征明显不同,支持成立长果安息香属     

Trade-offs between plant leaf hydraulic and economic traits

Leaf is the most important organ for carbon-water coupling of a plant because it is the primary medium for photosynthesis. It also acts as the hydraulic bottleneck and safety valve against hydraulic catastrophic dysfunctions. The leaf economics spectrum, which reflects the balance between investments and returns of leaf economic traits, provides a useful framework for examining species strategies as shaped by their evolutionary history. Changes in leaf hydraulic traits will influence leaf economic traits as well as plant survival and growth. Exploring trade-offs between leaf hydraulic and economic traits is thus of significance for modeling carbon-water relations, understanding the mechanisms of water/carbon investments, and extending the leaf economic spectrum. In this review, we first examined the trade-offs between leaf hydraulic and economic traits. Specially, we analyzed the relationships between leaf hydraulic conductivity and hydraulic vulnerability, water potential at the turgor loss point, water capacitance, safety margin, and leaf morphological, structural and functional traits. We then discussed potential mechanisms regulating leaf hydraulic and economic traits from leaf morphology, anatomy, venation, and stomatal functions. Finally, we proposed future research to: (1) develop an integrated whole-plant economics spectrum, including carbon-nitrogen-water resources and root-stem-leaf hydraulic transport system that will help revealing ecophysiological mechanisms of plant structure-functional coupling, carbon sequestration and water use; (2) explore a generalized trade-offs among leaf hydraulic safety, hydraulic efficiency and carbon fixation efficiency to advance our understanding of the relationships between biophysical structure and physiological metabolism in plant leaf construction under drought stress; and (3) explore the carbon-water metabolic relationship and coupling of water transport and growth rate for the metabolic theory and predictions at community scale.     

grasviq: an image analysis framework for automatically quantifying vein number and morphology in grass leaves

Beyond facilitating transport and providing mechanical support to the leaf, veins have important roles in the performance and productivity of plants and the ecosystem. In recent decades, computational image analysis has accelerated the extraction and quantification of vein traits, benefiting fields of research from agriculture to climatology. However, most of the existing leaf vein image analysis programs have been developed for the reticulate venation found in dicots. Despite the agroeconomic importance of cereal grass crops, like Oryza sativa (rice) and Zea mays (maize), a dedicated image analysis program for the parallel venation found in monocots has yet to be developed. To address the need for an image-based vein phenotyping tool for model and agronomic grass species, we developed the grass vein image quantification (grasviq ) framework. Designed specifically for parallel venation, this framework automatically segments and quantifies vein patterns from images of cleared leaf pieces using classical computer vision techniques. Using image data sets from maize inbred lines and auxin biosynthesis and transport mutants in maize, we demonstrate the utility of grasviq for quantifying important vein traits, including vein density, vein width and interveinal distance. Furthermore, we show that the framework can resolve quantitative differences and identify vein patterning defects, which is advantageous for genetic experiments and mutant screens. We report that grasviq can perform high-throughput vein quantification, with precision on a par with that of manual quantification. Therefore, we envision that grasviq will be adopted for vein phenomics in maize and other grass species.     

Quantifying leaf venation patterns: two-dimensional maps

The leaf vasculature plays crucial roles in transport and mechanical support. Understanding how vein patterns develop and what underlies pattern variation between species has many implications from both physiological and evolutionary perspectives. We developed a method for extracting spatial vein pattern data from leaf images, such as vein densities and also the sizes and shapes of the vein reticulations. We used this method to quantify leaf venation patterns of the first rosette leaf of Arabidopsis thaliana throughout a series of developmental stages. In particular, we characterized the size and shape of vein network areoles (loops), which enlarge and are split by new veins as a leaf develops. Pattern parameters varied in time and space. In particular, we observed a distal to proximal gradient in loop shape (length/width ratio) which varied over time, and a margin-to-center gradient in loop sizes. Quantitative analyses of vein patterns at the tissue level provide a two-way link between theoretical models of patterning and molecular experimental work to further explore patterning mechanisms during development. Such analyses could also be used to investigate the effect of environmental factors on vein patterns, or to compare venation patterns from different species for evolutionary studies. The method also provides a framework for gathering and overlaying two-dimensional maps of point, line and surface morphological data.