Limited effects of xylem anatomy on embolism resistance in cycad leaves.

Drought-induced xylem embolism is a primary cause of plant mortality. Although c. 70% of cycads are threatened by extinction and extant cycads diversified during a period of increasing aridification, the vulnerability of cycads to embolism spread has been overlooked. We quantified the vulnerability to drought-induced embolism, pressure-volume curves, in situ water potentials, and a suite of xylem anatomical traits of leaf pinnae and rachises for 20 cycad species. We tested whether anatomical traits were linked to hydraulic safety in cycads. Compared with other major vascular plant clades, cycads exhibited similar embolism resistance to angiosperms and pteridophytes but were more vulnerable to embolism than noncycad gymnosperms. All 20 cycads had both tracheids and vessels, the proportions of which were unrelated to embolism resistance. Only vessel pit membrane fraction was positively correlated to embolism resistance, contrary to angiosperms. Water potential at turgor loss was significantly correlated to embolism resistance among cycads. Our results show that cycads exhibit low resistance to xylem embolism and that xylem anatomical traits - particularly vessels - may influence embolism resistance together with tracheids. This study highlights the importance of understanding the mechanisms of drought resistance in evolutionarily unique and threatened lineages like the cycads.

Rethinking economic theories of plant water use.

A central assumption in plant ecophysiology is that carbon is the primary currency for plant fitness. To this end, plants are thought to maximize carbon gain and any deviations from maximum carbon gain are ascribed to resource limitations (e.g., temperature, drought), biophysical limitations (e.g., biophysical limits on cell size), or variation in plant life history that may prioritize future carbon gain over current carbon gain (i.e., applying an economic discount rate to carbon). Compared to living in water, living on land made accessing CO2 substantially easier: CO2 diffuses approximately 10,000 times faster in air than in water. However, because this CO2 must diffuse into the aqueous environment of the living mesophyll cells where photosynthetic metabolism occurs (The´roux-Rancourt et al. 2021), the greater CO2 supply of the terrestrial lifestyle also comes with a cost: losing approximately 200-400 molecules of water by transpiration for every molecule of CO2 fixed by photosynthesis (Nobel et al. 2005). Water, therefore, is considered a valuable resource to be conserved and not wasted. As such, much of the field of plant ecophysiology posits carbon as the central currency for which water is traded.

Hydraulic differences between flowers and leaves are driven primarily by pressure-volume traits and water loss.

Flowers are critical for successful reproduction and have been a major axis of diversification among angiosperms. As the frequency and severity of droughts are increasing globally, maintaining water balance of flowers is crucial for food security and other ecosystem services that rely on flowering. Yet remarkably little is known about the hydraulic strategies of flowers. We characterized hydraulic strategies of leaves and flowers of ten species by combining anatomical observations using light and scanning electron microscopy with measurements of hydraulic physiology (minimum diffusive conductance (g min) and pressure-volume (PV) curves parameters). We predicted that flowers would exhibit higher g min and higher hydraulic capacitance than leaves, which would be associated with differences in intervessel pit traits because of their different hydraulic strategies. We found that, compared to leaves, flowers exhibited: 1) higher g min, which was associated with higher hydraulic capacitance (C T); 2) lower variation in intervessel pit traits and differences in pit membrane area and pit aperture shape; and 3) independent coordination between intervessel pit traits and other anatomical and physiological traits; 4) independent evolution of most traits in flowers and leaves, resulting in 5) large differences in the regions of multivariate trait space occupied by flowers and leaves. Furthermore, across organs intervessel pit trait variation was orthogonal to variation in other anatomical and physiological traits, suggesting that pit traits represent an independent axis of variation that have as yet been unquantified in flowers. These results suggest that flowers, employ a drought-avoidant strategy of maintaining high capacitance that compensates for their higher g min to prevent excessive declines in water potentials. This drought-avoidant strategy may have relaxed selection on intervessel pit traits and allowed them to vary independently from other anatomical and physiological traits. Furthermore, the independent evolution of floral and foliar anatomical and physiological traits highlights their modular development despite being borne from the same apical meristem.

Coordination of intertracheid pit traits and climate effects among cycads.

Interconduit pit membranes, which are permeable regions in the primary cell wall that connect to adjacent conduits, play a crucial role in water relations and the movement of nutrients between xylem conduits. However, how pit membrane characteristics might influence water-carbon coupling remains poorly investigated in cycads. We examined pit characteristics, the anatomical and photosynthetic traits of 13 cycads from a common garden, to determine if pit traits and their coordination are related to water relations and carbon economy. We found that the pit traits of cycads were highly variable and that cycads exhibited a similar tradeoff between pit density and pit area as other plant lineages. Unlike other plant lineages (1) pit membranes, pit apertures, and pit shapes of cycads were not coordinated as in angiosperms; (2) cycads exhibited larger pit membrane areas but lower pit densities relative to ferns and angiosperms, but smaller and similar pit membrane densities to non-cycad gymnosperms; (3) cycad pit membrane areas and densities were partially coordinated with anatomical traits, with hydraulic supply of the rachis positively coordinated with photosynthesis, whereas pit aperture areas and fractions were negatively coordinated with photosynthetic traits; (4) cycad pit traits reflected adaptation to wetter habitats for Cycadaceae and drier habitats for Zamiaceae. The large variation in pit traits, the unique pit membrane size and density, and the partial coordination of pit traits with anatomical and physiological traits of the rachis and pinna among cycads may have facilitated their dominance in a variety of ecosystems from the Mesozoic to modern times.

Diverse mangroves deviate from other angiosperms in their genome size, leaf cell size and cell packing density relationships.

BACKGROUND AND AIMS: While genome size limits the minimum sizes and maximum numbers of cells that can be packed into a given leaf volume, mature cell sizes can be substantially larger than their meristematic precursors and vary in response to abiotic conditions. Mangroves are iconic examples of how abiotic conditions can influence the evolution of plant phenotypes. METHODS: Here, we examined the coordination between genome size, leaf cell sizes, cell packing densities and leaf size in 13 mangrove species across four sites in China. Four of these species occurred at more than one site, allowing us to test the effect of climate on leaf anatomy. RESULTS: We found that genome sizes of mangroves were very small compared to other angiosperms, but, like other angiosperms, mangrove cells were always larger than the minimum size defined by genome size. Increasing mean annual temperature of a growth site led to higher packing densities of veins (Dv) and stomata (Ds) and smaller epidermal cells but had no effect on stomatal size. In contrast to other angiosperms, mangroves exhibited (1) a negative relationship between guard cell size and genome size; (2) epidermal cells that were smaller than stomata; and (3) coordination between Dv and Ds that was not mediated by epidermal cell size. Furthermore, mangrove epidermal cell sizes and packing densities covaried with leaf size. CONCLUSIONS: While mangroves exhibited coordination between veins and stomata and attained a maximum theoretical stomatal conductance similar to that of other angiosperms, the tissue-level tradeoffs underlying these similar relationships across species and environments were markedly different, perhaps indicative of the unique structural and physiological adaptations of mangroves to their stressful environments.

Localized growth and remodelling drives spongy mesophyll morphogenesis.

The spongy mesophyll is a complex, porous tissue found in plant leaves that enables carbon capture and provides mechanical stability. Unlike many other biological tissues, which remain confluent throughout development, the spongy mesophyll must develop from an initially confluent tissue into a tortuous network of cells with a large proportion of intercellular airspace. How the airspace in the spongy mesophyll develops while the tissue remains mechanically stable is unknown. Here, we use computer simulations of deformable polygons to develop a purely mechanical model for the development of the spongy mesophyll tissue. By stipulating that cell wall growth and remodelling occurs only near void space, our computational model is able to recapitulate spongy mesophyll development observed in Arabidopsis thaliana leaves. We find that robust generation of pore space in the spongy mesophyll requires a balance of cell growth, adhesion, stiffness and tissue pressure to ensure cell networks become porous yet maintain mechanical stability. The success of this mechanical model of morphogenesis suggests that simple physical principles can coordinate and drive the development of complex plant tissues like the spongy mesophyll.

Seeing Yourself as a Scientist: Increasing Science Identity Using Professional Development Modules Designed for Undergraduate Students.

As educators, we should not assume that students are progressing toward intended STEM careers simply because they have persisted and received a STEM degree. In addition to learning biology content and scientific skills, students need guidance in making optimal career choices. In this study, we present seven career development modules designed specifically to motivate students to consider their successes as scientists and to consider applying their biological knowledge and scientific skills to a range of biology careers. These modules highlight the value and the utility of a biology degree and are, therefore, designed to increase students' self-confidence as well as their science and biology identities. The career development modules presented here are easy to implement and, in our experience, encourage engagement and class discussions. Our analyses confirm that these modules collectively increase student science and biology identities, two predictors for entry into STEM careers.

Coordination of hydraulic thresholds across roots, stems, and leaves of two co-occurring mangrove species.

Mangroves are frequently inundated with saline water and have evolved different anatomical and physiological mechanisms to filter and, in some species, excrete excess salt from the water they take up. Because salts impose osmotic stress, interspecific differences in salt tolerance and salt management strategy may influence physiological responses to drought throughout the entire plant hydraulic pathway, from roots to leaves. Here, we characterized embolism vulnerability simultaneously in leaves, stems, and roots of seedlings of two mangrove species (Avicennia marina and Bruguiera gymnorrhiza) along with turgor-loss points in roots and leaves and xylem anatomical traits. In both species, the water potentials causing 50% of total embolism were less negative in roots and leaves than they were in stems, but the water potentials causing incipient embolism (5%) were similar in roots, stems, and leaves. Stomatal closure in leaves and turgor loss in both leaves and roots occurred at water potentials only slightly less negative than the water potentials causing 5% of total embolism. Xylem anatomical traits were unrelated to vulnerability to embolism. Vulnerability segmentation may be important in limiting embolism spread into stems from more vulnerable roots and leaves. Interspecific differences in salt tolerance affected hydraulic traits from roots to leaves: the salt-secretor A. marina lost turgor at more negative water potentials and had more embolism-resistant xylem than the salt-excluder B. gymnorrhiza. Characterizing physiological thresholds of roots may help to explain recent mangrove mortality after drought and extended saltwater inundation.

Structural organization of the spongy mesophyll.

Many plant leaves have two layers of photosynthetic tissue: the palisade and spongy mesophyll. Whereas palisade mesophyll consists of tightly packed columnar cells, the structure of spongy mesophyll is not well characterized and often treated as a random assemblage of irregularly shaped cells. Using micro-computed tomography imaging, topological analysis, and a comparative physiological framework, we examined the structure of the spongy mesophyll in 40 species from 30 genera with laminar leaves and reticulate venation. A spectrum of spongy mesophyll diversity encompassed two dominant phenotypes: first, an ordered, honeycomblike tissue structure that emerged from the spatial coordination of multilobed cells, conforming to the physical principles of Euler's law; and second, a less-ordered, isotropic network of cells. Phenotypic variation was associated with transitions in cell size, cell packing density, mesophyll surface-area-to-volume ratio, vein density, and maximum photosynthetic rate. These results show that simple principles may govern the organization and scaling of the spongy mesophyll in many plants and demonstrate the presence of structural patterns associated with leaf function. This improved understanding of mesophyll anatomy provides new opportunities for spatially explicit analyses of leaf development, physiology, and biomechanics.

Resource users as land-sea links in coastal and marine socioecological systems.

Coastal zones, which connect terrestrial and aquatic ecosystems, are among the most resource-rich regions globally and home to nearly 40% of the global human population. Because human land-based activities can alter natural processes in ways that affect adjacent aquatic ecosystems, land-sea interactions are increasingly recognized as critical to coastal conservation planning and governance. However, the complex socioeconomic dynamics inherent in coastal and marine socioecological systems (SESs) have received little consideration. Drawing on knowledge generalized from long-term studies in Caribbean Nicaragua, we devised a conceptual framework that clarifies the multiple ways socioeconomically driven behavior can link the land and sea. In addition to other ecosystem effects, the framework illustrates how feedbacks resulting from changes to aquatic resources can influence terrestrial resource management decisions and land uses. We assessed the framework by applying it to empirical studies from a variety of coastal SESs. The results suggest its broad applicability and highlighted the paucity of research that explicitly investigates the effects of human behavior on coastal SES dynamics. We encourage researchers and policy makers to consider direct, indirect, and bidirectional cross-ecosystem links that move beyond traditionally recognized land-to-sea processes.

Los Usuarios de Recursos como Conexiones entre la Tierra y el Mar dentro de los Sistemas Socioecológicos Marinos y Costeros Resumen Las zonas costeras, que conectan los ecosistemas terrestres y acuáticos, se encuentran entre las regiones más ricas en recursos a nivel mundial y además albergan a casi el 40% de la población humana de todo el mundo. Ya que las actividades humanas terrestres pueden alterar los procesos naturales de manera que terminan por afectar a los ecosistemas acuáticos adyacentes, cada vez se reconoce más a las interacciones tierra-mar como críticas para la planeación de la conservación y la gestión costera. Sin embargo, las complejas dinámicas socioeconómicas inherentes a los sistemas socioecológicos (SES) marinos y costeros han recibido poca atención. Con el conocimiento generalizado a partir de los estudios a largo plazo realizados en el Caribe de Nicaragua como punto de partida, diseñamos un marco conceptual que clarifica las múltiples formas en las que el comportamiento con origen socioeconómico puede conectar a la tierra y al mar. Sumado a otros efectos de los ecosistemas, el marco conceptual ilustró cómo los comentarios resultantes de los cambios ocurridos en los recursos acuáticos pueden influir sobre las decisiones de manejo de recursos terrestres y de uso de suelo. Evaluamos el marco conceptual mediante su aplicación a los estudios empíricos de una variedad de SES costeros. Los resultados sugirieron su aplicabilidad generalizada y resaltaron la escasez de investigaciones busquen específicamente los efectos del comportamiento humano sobre las dinámicas de los SES costeros. Alentamos a los investigadores y a los formuladores de políticas a considerar las conexiones directas, indirectas y bidireccionales entre ecosistemas que van más allá de los procesos de tierra a mar reconocidos tradicionalmente.

Reintegrating Biology Through the Nexus of Energy, Information, and Matter.

Information, energy, and matter are fundamental properties of all levels of biological organization, and life emerges from the continuous flux of matter, energy, and information. This perspective piece defines and explains each of the three pillars of this nexus. We propose that a quantitative characterization of the complex interconversions between matter, energy, and information that comprise this nexus will help us derive biological insights that connect phenomena across different levels of biological organization. We articulate examples from multiple biological scales that highlight how this nexus approach leads to a more complete understanding of the biological system. Metrics of energy, information, and matter can provide a common currency that helps link phenomena across levels of biological organization. The propagation of energy and information through levels of biological organization can result in emergent properties and system-wide changes that impact other hierarchical levels. Deeper consideration of measured imbalances in energy, information, and matter can help researchers identify key factors that influence system function at one scale, highlighting avenues to link phenomena across levels of biological organization and develop predictive models of biological systems.

Mammals with Small Populations Do Not Exhibit Larger Genomes.

Genome size in cellular organisms varies by six orders of magnitude, yet the cause of this large variation remains unexplained. The influential Drift-Barrier Hypothesis proposes that large genomes tend to evolve in small populations due to inefficient selection. However, to our knowledge no explicit tests of the Drift-Barrier Hypothesis have been reported. We performed the first explicit test, by comparing estimated census population size and genome size in mammals while incorporating potential covariates and the effect of shared evolutionary history. We found a lack of correlation between census population size and genome size among 199 species of mammals. These results suggest that population size is not the predominant factor influencing genome size and that the Drift-Barrier Hypothesis should be considered provisional.

Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size.

Maintaining high rates of photosynthesis in leaves requires efficient movement of CO2 from the atmosphere to the mesophyll cells inside the leaf where CO2 is converted into sugar. CO2 diffusion inside the leaf depends directly on the structure of the mesophyll cells and their surrounding airspace, which have been difficult to characterize because of their inherently three-dimensional organization. Yet faster CO2 diffusion inside the leaf was probably critical in elevating rates of photosynthesis that occurred among angiosperm lineages. Here we characterize the three-dimensional surface area of the leaf mesophyll across vascular plants. We show that genome size determines the sizes and packing densities of cells in all leaf tissues and that smaller cells enable more mesophyll surface area to be packed into the leaf volume, facilitating higher CO2 diffusion. Measurements and modelling revealed that the spongy mesophyll layer better facilitates gaseous phase diffusion while the palisade mesophyll layer better facilitates liquid-phase diffusion. Our results demonstrate that genome downsizing among the angiosperms was critical to restructuring the entire pathway of CO2 diffusion into and through the leaf, maintaining high rates of CO2 supply to the leaf mesophyll despite declining atmospheric CO2 levels during the Cretaceous.

Diversification, disparification and hybridization in the desert shrubs Encelia.

There are multiple hypotheses for the spectacular plant diversity found in deserts. We explore how different factors, including the roles of ecological opportunity and selection, promote diversification and disparification in Encelia, a lineage of woody plants in the deserts of the Americas. Using a nearly complete species-level phylogeny based on double-digest restriction-aided sequencing along with a broad set of phenotypic traits, we estimate divergence times and diversification rates, identify instances of hybridization, quantify trait disparity and assess phenotypic divergence across environmental gradients. We show that Encelia originated and diversified recently (mid-Pleistocene) and rapidly, with rates comparable to notable adaptive radiations in plants. Encelia probably originated in the hot deserts of North America, with subsequent diversification across steep environmental gradients. We uncover multiple instances of gene flow between species. The radiation of Encelia is characterized by fast rates of phenotypic evolution, trait lability and extreme disparity across environments and between species pairs with overlapping geographic ranges. Encelia exemplifies how interspecific gene flow in combination with high trait lability can enable exceptionally fast diversification and disparification across steep environmental gradients.

Towards the flower economics spectrum.

Understanding how floral traits affect reproduction is key for understanding genetic diversity, speciation, and trait evolution in the face of global changes and pollinator decline. However, there has not yet been a unified framework to characterize the major trade-offs and axes of floral trait variation. Here, we propose the development of a floral economics spectrum (FES) that incorporates the multiple pathways by which floral traits can be shaped by multiple agents of selection acting on multiple flower functions. For example, while pollinator-mediated selection has been considered the primary factor affecting flower evolution, selection by nonpollinator agents can reinforce or oppose pollinator selection, and, therefore, affect floral trait variation. In addition to pollinators, the FES should consider nonpollinator biotic agents and floral physiological costs, broadening the drivers of floral traits beyond pollinators. We discuss how coordinated evolution and trade-offs among floral traits and between floral and vegetative traits may influence the distribution of floral traits across biomes and lineages, thereby influencing organismal evolution and community assembly.

Natural selection maintains species despite frequent hybridization in the desert shrub Encelia.

Natural selection is an important driver of genetic and phenotypic differentiation between species. For species in which potential gene flow is high but realized gene flow is low, adaptation via natural selection may be a particularly important force maintaining species. For a recent radiation of New World desert shrubs (Encelia: Asteraceae), we use fine-scale geographic sampling and population genomics to determine patterns of gene flow across two hybrid zones formed between two independent pairs of species with parapatric distributions. After finding evidence for extremely strong selection at both hybrid zones, we use a combination of field experiments, high-resolution imaging, and physiological measurements to determine the ecological basis for selection at one of the hybrid zones. Our results identify multiple ecological mechanisms of selection (drought, salinity, herbivory, and burial) that together are sufficient to maintain species boundaries despite high rates of hybridization. Given that multiple pairs of Encelia species hybridize at ecologically divergent parapatric boundaries, such mechanisms may maintain species boundaries throughout Encelia.

Anatomical and hydraulic responses to desiccation in emergent conifer seedlings.

PREMISE: The young seedling life stage is critical for reforestation after disturbance and for species migration under climate change, yet little is known regarding their basic hydraulic function or vulnerability to drought. Here, we sought to characterize responses to desiccation including hydraulic vulnerability, xylem anatomical traits, and impacts on other stem tissues that contribute to hydraulic functioning. METHODS: Larix occidentalis, Pseudotsuga menziesii, and Pinus ponderosa (all ≤6 weeks old) were imaged using x-ray computed microtomography during desiccation to assess seedling biomechanical responses with concurrently measured hydraulic conductivity (ks ) and water potential (Ψ) to assess vulnerability to xylem embolism formation and other tissue damage. RESULTS: In non-stressed samples for all species, pith and cortical cells appeared circular and well hydrated, but they started to empty and deform with decreasing Ψ which resulted in cell tearing and eventual collapse. Despite the severity of this structural damage, the vascular cambium remained well hydrated even under the most severe drought. There were significant differences among species in vulnerability to xylem embolism formation, with 78% xylem embolism in L. occidentalis by Ψ of -2.1 MPa, but only 47.7% and 62.1% in P. ponderosa and P. menziesii at -4.27 and -6.73 MPa, respectively. CONCLUSIONS: Larix occidentalis seedlings appeared to be more susceptible to secondary xylem embolism compared to the other two species, but all three maintained hydration of the vascular cambium under severe stress, which could facilitate hydraulic recovery by regrowth of xylem when stress is relieved.

Hydraulic conductance, resistance, and resilience: how leaves of a tropical epiphyte respond to drought.

PREMISE: Because of its broad range in the neotropical rainforest and within tree canopies, the tank bromeliad Guzmania monostachia was investigated as a model of how varying leaf hydraulic conductance (Kleaf ) could help plants resist and recover from episodic drought. The two pathways of Kleaf , inside and outside the xylem, were also examined to determine the sites and causes of major hydraulic resistances within the leaf. METHODS: We measured leaf hydraulic conductance for plants in the field and laboratory under wet, dry, and rewetted conditions and applied physiological, anatomical, and gene expression analysis with modeling to investigate changes in Kleaf . RESULTS: After 7 d with no rain in the field or 14 days with no water in the glasshouse, Kleaf decreased by 50% yet increased to hydrated values within 4 d of tank refilling. Staining to detect embolism combined with modeling indicated that changes outside the xylem were of greater importance to Kleaf than were changes inside the xylem and were associated with changes in intercellular air spaces (aerenchyma), aquaporin expression and inhibition, and cuticular conductance. CONCLUSIONS: Low values for all conductances during drying, particularly in pathways outside the xylem, lead to hydraulic resilience for this species and may also contribute to its broad environmental tolerances.