ORCID ID: 0000-0001-9899-8101 (J.M.).Crassulacean acid metabolism (CAM) is a major physiological syndrome that has evolved independently in numerous land plant lineages. CAM plants are of great ecological significance, and there is increasing interest for their water-use efficiency and drought resistance. Integral to the improvement in water-use efficiency that CAM affords is a unique pattern of stomatal conductance, distinguished by primarily nocturnal opening and often extensive diurnal flexibility in response to environmental factors. Here, we assess how recent research has shed new light on the functional biology of CAM plant stomata and integration within the broader physiology and ecology of succulent organisms. Divergences in stomatal sensitivity to environmental and endogenous factors relative to C 3 species have been a key aspect of the evolution of functional CAM. Stomatal traits of CAM plants are closely coordinated with other leaf functional traits, and structural specialization of CAM stomatal complexes may be of undiagnosed functional relevance. We also highlight how salient results from ongoing work on C 3 plant stomatal biology could apply to CAM species. Key questions remaining relate to the interdependence between stomatal and mesophyll responses and are particularly relevant for bioengineering of CAM traits or bioenergy crops to exploit enhanced water-use efficiency and productivity on marginal land. With the increasing availability of powerful analytical tools and the emergence of new model systems for the study of the molecular basis of physiological traits in CAM plants, many exciting avenues for future research are open to intrepid investigators.
Water relations represent a pivotal nexus in plant biology due to the multiplicity of functions affected by water status. Hydraulic properties of plant parts are therefore likely to be relevant to evolutionary trends in many taxa. Bromeliaceae encompass a wealth of morphological, physiological and ecological variations and the geographical and bioclimatic range of the family is also extensive. The diversification of bromeliad lineages is known to be correlated with the origins of a suite of key innovations, many of which relate directly or indirectly to water relations. However, little information is known regarding the role of change in morphoanatomical and hydraulic traits in the evolutionary origins of the classical ecophysiological functional types in Bromeliaceae or how this role relates to the diversification of specific lineages. In this paper, I present a synthesis of the current knowledge on bromeliad water relations and a qualitative model of the evolution of relevant traits in the context of the functional types. I use this model to introduce a manifesto for a new research programme on the integrative biology and evolution of bromeliad water-use strategies. The need for a wide-ranging survey of morphoanatomical and hydraulic traits across Bromeliaceae is stressed, as this would provide extensive insight into structurefunction relationships of relevance to the evolutionary history of bromeliads and, more generally, to the evolutionary physiology of flowering plants.
The peculiar morphologies of succulent plants have been variously considered as grotesque monstrosities and exotic curiosities, but succulents have always been perceived as unique. The succulent syndrome is considered to be one of the most remarkable examples of convergent evolution across the plant kingdom. Common to all succulents is the presence of large cells for water storage. However, cellular succulence can occur in any vegetative plant organ, with the level of succulence in roots, stems, and leaves being subject to a certain degree of evolutionary coordination. Furthermore, cellular succulence scales up to morphological succulence according to various anatomical schemes that confer contrasting functional characteristics. This means that succulence is associated with a broad range of ecophysiological strategies and occurs in plants that have evolved in many different environments.
Succulent plants are iconic components of the florae of many terrestrial ecosystems, but despite having caused fascination and prompted investigation for centuries, they still harbour many secrets in terms of physiological function and evolution. Tackling these mysteries is important, as this will not only provide insights into the dynamics and details of the convergent evolution of a major adaptive syndrome, but also inform efforts to conserve endangered biodiversity and utilize the unique physiological characteristics of succulents for biofuel and biomass production. Here I review advances in the phylogeny and organismal biology of succulent plants, and discuss how insights from recent work in the wider fields of plant hydraulics and photosynthetic physiology may relate to succulents. The potential for the exploration of mechanistic relationships between anatomical structure and physiological function to improve our understanding of the constraints that have shaped the evolution of succulence is highlighted. Finally, attention is drawn to how new methodologies and technologies provide exciting opportunities to address the wide range of outstanding questions in succulent plant biology.
Leaf economic and hydraulic theories have rarely been applied to the ecological differentiation of speciose herbaceous plant radiations. The role of character trait divergences and network reorganization in the differentiation of the functional types in the megadiverse Neotropical Bromeliaceae was explored by quantifying a range of leaf economic and hydraulic traits in 50 diverse species. Functional types, which are defined by combinations of C 3 or Crassulacean acid metabolism (CAM) photosynthesis, terrestrial or epiphytic habits, and nonspecialized, tank-forming or atmospheric morphologies, segregated clearly in trait space. Most classical leaf economic relationships were supported, but they were weakened by the presence of succulence. Functional types differed in trait-network architecture, suggesting that rewiring of trait-networks caused by innovations in habit and photosynthetic pathway is an important aspect of ecological differentiation. The hydraulic data supported the coupling of leaf hydraulics and gas exchange, but not the hydraulic safety versus efficiency hypothesis, and hinted at an important role for the extra-xylary compartment in the control of bromeliad leaf hydraulics. Overall, our findings highlight the fundamental importance of structure-function relationships in the generation and maintenance of ecological diversity.
Herbaceous plants collectively known as geophytes, which regrow from belowground buds, are distributed around the globe and throughout the land plant tree of life. The geophytic habit is an evolutionarily and ecologically important growth form in plants, permitting novel life history strategies, enabling the occupation of more seasonal climates, mediating interactions between plants and their water and nutrient resources, and influencing macroevolutionary patterns by enabling differential diversification and adaptation. These taxa are excellent study systems for understanding how convergence on a similar growth habit (i.e., geophytism) can occur via different morphological and developmental mechanisms. Despite the importance of belowground organs for characterizing whole-plant morphological diversity, the morphology and evolution of these organs have been vastly understudied with most research focusing on only a few crop systems. Here, we clarify the terminology commonly used (and sometimes misused) to describe geophytes and their underground organs and highlight key evolutionary patterns of the belowground morphology of geophytic plants. Additionally, we advocate for increasing resources for geophyte research and implementing standardized ontological definitions of geophytic organs to improve our understanding of the factors controlling, promoting, and maintaining geophyte diversity.
Crassulacean acid metabolism (CAM) is a celebrated example of convergent evolution in plant ecophysiology. However, many unanswered questions surround the relationships among CAM, anatomy and morphology during evolutionary transitions in photosynthetic pathway. An excellent group in which to explore these issues is the Bromeliaceae, a diverse monocot family from the Neotropics in which CAM has evolved multiple times. Progress in the resolution of phylogenetic relationships among the bromeliads is opening new and exciting opportunities to investigate how evolutionary changes in leaf structure has tracked, or perhaps preceded, photosynthetic innovation. This paper presents an analysis of variation in leaf anatomical parameters across 163 C3 and CAM bromeliad species, demonstrating a clear divergence in the fundamental aspects of leaf structure in association with the photosynthetic pathway. Most strikingly, the mean volume of chlorenchyma cells of CAM species is 22 times higher than that of C3 species. In two bromeliad subfamilies (Pitcairnioideae and Tillandsioideae), independent transitions from C3 to CAM are associated with increased cell succulence, whereas evolutionary trends in tissue thickness and leaf air space content differ between CAM origins. Overall, leaf anatomy is clearly and strongly coupled with the photosynthetic pathway in the Bromeliaceae, where the independent origins of CAM have involved significant anatomical restructuring.
Mass and energy fluxes were measured over a field of Agave tequilana in Mexico using eddy covariance (EC) methodology. Data were gathered over 252 d, including the transition from wet to dry periods. Net ecosystem exchanges (FN,EC ) displayed a crassulacean acid metabolism (CAM) rhythm that alternated from CO2 sink at night to CO2 source during the day, and partitioned canopy fluxes (FA,EC ) showed a characteristic four-phase CO2 exchange pattern. Results were cross-validated against diel changes in titratable acidity, leaf-unfurling rates, energy exchange fluxes and reported biomass yields. Projected carbon balance (g C m(-2) year(-1) , mean ± 95% confidence interval) indicated the site was a net sink of -333 ± 24, of which contributions from soil respiration were +692 ± 7, and FA,EC was -1025 ± 25. EC estimated biomass yield was 20.1 Mg (dry) ha(-1) year(-1) . Average integrated daily FA,EC was -234 ± 5 mmol CO2 m(-2) d(-1) and persisted almost unchanged after 70 d of drought conditions. Regression analyses were performed on the EC data to identify the best environmental predictors of FA . Results suggest that the carbon acquisition strategy of Agave offers productivity and drought resilience advantages over conventional semi-arid C3 and C4 bioenergy candidates.
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