Evolutionary lineage explains trait variation among 75 coexisting grass species.

Evolutionary history plays a key role driving patterns of trait variation across plant species. For scaling and modeling purposes, grass species are typically organized into C3 vs C4 plant functional types (PFTs). Plant functional type groupings may obscure important functional differences among species. Rather, grouping grasses by evolutionary lineage may better represent grass functional diversity. We measured 11 structural and physiological traits in situ from 75 grass species within the North American tallgrass prairie. We tested whether traits differed significantly among photosynthetic pathways or lineages (tribe) in annual and perennial grass species. Critically, we found evidence that grass traits varied among lineages, including independent origins of C4 photosynthesis. Using a rigorous model selection approach, tribe was included in the top models for five of nine traits for perennial species. Tribes were separable in a multivariate and phylogenetically controlled analysis of traits, owing to coordination of important structural and ecophysiological characteristics. Our findings suggest grouping grass species by photosynthetic pathway overlooks variation in several functional traits, particularly for C4 species. These results indicate that further assessment of lineage-based differences at other sites and across other grass species distributions may improve representation of C4 species in trait comparison analyses and modeling investigations.

Flow-network-controlled shape transformation of a thin membrane through differential fluid storage and surface expansion.

The mechanical properties of a thin, planar material, perfused by an embedded flow network, have been suggested to be potentially changeable locally and globally by fluid transport and storage, which can result in both small- and large-scale deformations such as out-of-plane buckling. In these processes, fluid absorption and storage eventually cause the material to locally swell. Different parts can hydrate and swell unevenly, prompting a differential expansion of the surface. In order to computationally study the hydraulically induced differential swelling and buckling of such a membrane, we develop a network model that describes both the membrane shape and fluid movement, coupling mechanics with hydrodynamics. We simulate the time-dependent fluid distribution in the flow network based on a spatially explicit resistor network model with local fluid-storage capacitance. The shape of the surface is modeled by a spring network produced by a tethered mesh discretization, in which local bond rest lengths are adjusted instantaneously according to associated local fluid content in the capacitors in a quasistatic way. We investigate the effects of various designs of the flow network, including overall hydraulic traits (resistance and capacitance) and hierarchical architecture (arrangement of major and minor veins), on the specific dynamics of membrane shape transformation. To quantify these effects, we explore the correlation between local Gaussian curvature and relative stored fluid content in each hierarchy by using linear regression, which reveals that stronger correlations could be induced by less densely connected major veins. This flow-controlled mechanism of shape transformation was inspired by the blooming of flowers through the unfolding of petals. It can potentially offer insights for other reversible motions observed in plants induced by differential turgor and water transport through the xylem vessels, as well as engineering applications.

The carbon economics of vegetative phase change.

Across plant species and biomes, a conserved set of leaf traits govern the economic strategy used to assimilate and invest carbon. As plants age, they face new challenges that may require shifts in this leaf economic strategy. In this study, we investigate the role of the developmental transition, vegetative phase change (VPC), in altering carbon economics as plants age. We used overexpression of microRNA 156 (miR156), the master regulator of VPC, to modulate the timing of VPC in Populus tremula x alba, Arabidopsis thaliana and Zea mays to understand the impact of this transition on leaf economic traits, including construction cost, payback time and return on investment. Here, we find that VPC causes a shift from a low-cost, quick return juvenile strategy to a high-cost, high-return adult strategy. The juvenile strategy is advantageous in light-limited conditions, whereas the adult strategy provides greater returns in high light. The transition between these strategies is correlated with the developmental decline in the level of miR156, suggesting that is regulated by the miR156/SPL pathway. Our results provide an ecophysiological explanation for the existence of juvenile and adult leaf types and suggest that natural selection for these alternative economic strategies could be an important factor in plant evolution.

Poor relationships between NEON Airborne Observation Platform data and field-based vegetation traits at a mesic grassland.

Understanding spatial and temporal variation in plant traits is needed to accurately predict how communities and ecosystems will respond to global change. The National Ecological Observatory Network's (NEON's) Airborne Observation Platform (AOP) provides hyperspectral images and associated data products at numerous field sites at 1 m spatial resolution, potentially allowing high-resolution trait mapping. We tested the accuracy of readily available data products of NEON's AOP, such as Leaf Area Index (LAI), Total Biomass, Ecosystem Structure (Canopy height model [CHM]), and Canopy Nitrogen, by comparing them to spatially extensive field measurements from a mesic tallgrass prairie. Correlations with AOP data products exhibited generally weak or no relationships with corresponding field measurements. The strongest relationships were between AOP LAI and ground-measured LAI (r = 0.32) and AOP Total Biomass and ground-measured biomass (r = 0.23). We also examined how well the full reflectance spectra (380-2,500 nm), as opposed to derived products, could predict vegetation traits using partial least-squares regression (PLSR) models. Among all the eight traits examined, only Nitrogen had a validation R2 of more than 0.25. For all vegetation traits, validation R2 ranged from 0.08 to 0.29 and the range of the root mean square error of prediction (RMSEP) was 14-64%. Our results suggest that currently available AOP-derived data products should not be used without extensive ground-based validation. Relationships using the full reflectance spectra may be more promising, although careful consideration of field and AOP data mismatches in space and/or time, biases in field-based measurements or AOP algorithms, and model uncertainty are needed. Finally, grassland sites may be especially challenging for airborne spectroscopy because of their high species diversity within a small area, mixed functional types of plant communities, and heterogeneous mosaics of disturbance and resource availability. Remote sensing observations are one of the most promising approaches to understanding ecological patterns across space and time. But the opportunity to engage a diverse community of NEON data users will depend on establishing rigorous links with in-situ field measurements across a diversity of sites.

Leaf Water Storage and Robustness to Intermittent Drought: A Spatially Explicit Capacitive Model for Leaf Hydraulics.

Leaf hydraulic networks play an important role not only in fluid transport but also in maintaining whole-plant water status through transient environmental changes in soil-based water supply or air humidity. Both water potential and hydraulic resistance vary spatially throughout the leaf transport network, consisting of xylem, stomata and water-storage cells, and portions of the leaf areas far from the leaf base can be disproportionately disadvantaged under water stress. Besides the suppression of transpiration and reduction of water loss caused by stomatal closure, the leaf capacitance of water storage, which can also vary locally, is thought to be crucial for the maintenance of leaf water status. In order to study the fluid dynamics in these networks, we develop a spatially explicit, capacitive model which is able to capture the local spatiotemporal changes of water potential and flow rate in monocotyledonous and dicotyledonous leaves. In electrical-circuit analogs described by Ohm's law, we implement linear capacitors imitating water storage, and we present both analytical calculations of a uniform one-dimensional model and numerical simulation methods for general spatially explicit network models, and their relation to conventional lumped-element models. Calculation and simulation results are shown for the uniform model, which mimics key properties of a monocotyledonous grass leaf. We illustrate water status of a well-watered leaf, and the lowering of water potential and transpiration rate caused by excised water source or reduced air humidity. We show that the time scales of these changes under water stress are hugely affected by leaf capacitance and resistances to capacitors, in addition to stomatal resistance. Through this modeling of a grass leaf, we confirm the presence of uneven water distribution over leaf area, and also discuss the importance of considering the spatial variation of leaf hydraulic traits in plant biology.

Imaging canopy temperature: shedding (thermal) light on ecosystem processes.

Canopy temperature Tcan is a key driver of plant function that emerges as a result of interacting biotic and abiotic processes and properties. However, understanding controls on Tcan and forecasting canopy responses to weather extremes and climate change are difficult due to sparse measurements of Tcan at appropriate spatial and temporal scales. Burgeoning observations of Tcan from thermal cameras enable evaluation of energy budget theory and better understanding of how environmental controls, leaf traits and canopy structure influence temperature patterns. The canopy scale is relevant for connecting to remote sensing and testing biosphere model predictions. We anticipate that future breakthroughs in understanding of ecosystem responses to climate change will result from multiscale observations of Tcan across a range of ecosystems.

MicroRNA156-mediated changes in leaf composition lead to altered photosynthetic traits during vegetative phase change.

Plant morphology and physiology change with growth and development. Some of these changes are due to change in plant size and some are the result of genetically programmed developmental transitions. In this study we investigate the role of the developmental transition, vegetative phase change (VPC), on morphological and photosynthetic changes. We used overexpression of microRNA156, the master regulator of VPC, to modulate the timing of VPC in Populus tremula × alba, Zea mays, and Arabidopsis thaliana to determine its role in trait variation independent of changes in size and overall age. Here, we find that juvenile and adult leaves in all three species photosynthesize at different rates and that these differences are due to phase-dependent changes in specific leaf area (SLA) and leaf N but not photosynthetic biochemistry. Further, we found juvenile leaves with high SLA were associated with better photosynthetic performance at low light levels. This study establishes a role for VPC in leaf composition and photosynthetic performance across diverse species and environments. Variation in leaf traits due to VPC are likely to provide distinct benefits under specific environments; as a result, selection on the timing of this transition could be a mechanism for environmental adaptation.

Stem water cryogenic extraction biases estimation in deuterium isotope composition of plant source water.

The hydrogen isotope ratio of water cryogenically extracted from plant stem samples (δ2Hstem_CVD) is routinely used to aid isotope applications that span hydrological, ecological, and paleoclimatological research. However, an increasing number of studies have shown that a key assumption of these applications-that δ2Hstem_CVD is equal to the δ2H of plant source water (δ2Hsource)-is not necessarily met in plants from various habitats. To examine this assumption, we purposedly designed an experimental system to allow independent measurements of δ2Hstem_CVD, δ2Hsource, and δ2H of water transported in xylem conduits (δ2Hxylem) under controlled conditions. Our measurements performed on nine woody plant species from diverse habitats revealed a consistent and significant depletion in δ2Hstem_CVD compared with both δ2Hsource and δ2Hxylem Meanwhile, no significant discrepancy was observed between δ2Hsource and δ2Hxylem in any of the plants investigated. These results cast significant doubt on the long-standing view that deuterium fractionation occurs during root water uptake and, alternatively, suggest that measurement bias inherent in the cryogenic extraction method is the root cause of δ2Hstem_CVD depletion. We used a rehydration experiment to show that the stem water cryogenic extraction error could originate from a dynamic exchange between organically bound deuterium and liquid water during water extraction. In light of our finding, we suggest caution when partitioning plant water sources and reconstructing past climates using hydrogen isotopes, and carefully propose that the paradigm-shifting phenomenon of ecohydrological separation ("two water worlds") is underpinned by an extraction artifact.

Lineage-based functional types: characterising functional diversity to enhance the representation of ecological behaviour in Land Surface Models.

Process-based vegetation models attempt to represent the wide range of trait variation in biomes by grouping ecologically similar species into plant functional types (PFTs). This approach has been successful in representing many aspects of plant physiology and biophysics but struggles to capture biogeographic history and ecological dynamics that determine biome boundaries and plant distributions. Grass-dominated ecosystems are broadly distributed across all vegetated continents and harbour large functional diversity, yet most Land Surface Models (LSMs) summarise grasses into two generic PFTs based primarily on differences between temperate C3 grasses and (sub)tropical C4 grasses. Incorporation of species-level trait variation is an active area of research to enhance the ecological realism of PFTs, which form the basis for vegetation processes and dynamics in LSMs. Using reported measurements, we developed grass functional trait values (physiological, structural, biochemical, anatomical, phenological, and disturbance-related) of dominant lineages to improve LSM representations. Our method is fundamentally different from previous efforts, as it uses phylogenetic relatedness to create lineage-based functional types (LFTs), situated between species-level trait data and PFT-level abstractions, thus providing a realistic representation of functional diversity and opening the door to the development of new vegetation models.

Estimating C4 photosynthesis parameters by fitting intensive A/Ci curves.

Measurements of photosynthetic assimilation rate as a function of intercellular CO2 (A/Ci curves) are widely used to estimate photosynthetic parameters for C3 species, yet few parameters have been reported for C4 plants, because of a lack of estimation methods. Here, we extend the framework of widely used estimation methods for C3 plants to build estimation tools by exclusively fitting intensive A/Ci curves (6-8 more sampling points) for C4 using three versions of photosynthesis models with different assumptions about carbonic anhydrase processes and ATP distribution. We use simulation analysis, out of sample tests, existing in vitro measurements and chlorophyll-fluorescence measurements to validate the new estimation methods. Of the five/six photosynthetic parameters obtained, sensitivity analyses show that maximal-Rubisco-carboxylation-rate, electron-transport-rate, maximal-PEP-carboxylation-rate, and carbonic-anhydrase were robust to variation in the input parameters, while day respiration and mesophyll conductance varied. Our method provides a way to estimate carbonic anhydrase activity, a new parameter, from A/Ci curves, yet also shows that models that do not explicitly consider carbonic anhydrase yield approximate results. The two photosynthesis models, differing in whether ATP could freely transport between RuBP and PEP regeneration processes yielded consistent results under high light, but they may diverge under low light intensities. Modeling results show selection for Rubisco of low specificity and high catalytic rate, low leakage of bundle sheath, and high PEPC affinity, which may further increase C4 efficiency.

C4 photosynthesis and climate through the lens of optimality.

CO2, temperature, water availability, and light intensity were all potential selective pressures that determined the competitive advantage and expansion of the C4 photosynthetic carbon-concentrating mechanism over the last ∼30 My. To tease apart how selective pressures varied along the ecological trajectory of C4 expansion and dominance, we coupled hydraulics to photosynthesis models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of nitrogen reallocation from the dark to the light reactions. We show here that the primary selective pressures favoring C4 dominance changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root ratios enabled by C4 led to an advantage without any initial difference in hydraulic properties. We further predict a reorganization of the hydraulic system leading to higher turgor-loss points and possibly lower hydraulic conductance. Selection on nitrogen reallocation varied with CO2 concentration. Through paleoclimate model simulations, we find that water limitation was the primary driver for a C4 advantage, with atmospheric CO2 as high as 600 ppm, thus confirming molecular-based estimates for C4 evolution in the Oligocene. Under these high-CO2 conditions, nitrogen reallocation was necessary. Low CO2 and high light, but not nitrogen reallocation, were the primary drivers for the mid- to late-Miocene global expansion of C4 We also predicted the timing and spatial distribution for origins of C4 ecological dominance. The predicted origins are broadly consistent with prior estimates, but expand upon them to include a center of origin in northwest Africa and a Miocene-long origin in Australia.

Assessing the interplay between canopy energy balance and photosynthesis with cellulose δ18O: large-scale patterns and independent ground-truthing.

There are few whole-canopy or ecosystem scale assessments of the interplay between canopy temperature and photosynthesis across both spatial and temporal scales. The stable oxygen isotope ratio (δ18O) of plant cellulose can be used to resolve a photosynthesis-weighted estimate of canopy temperature, but the method requires independent confirmation. We compare isotope-resolved canopy temperatures derived from multi-year homogenization of tree cellulose δ18O to canopy-air temperatures weighted by gross primary productivity (GPP) at multiple sites, ranging from warm temperate to boreal and subalpine forests. We also perform a sensitivity analysis for isotope-resolved canopy temperatures that showed errors in plant source water δ18O lead to the largest errors in canopy temperature estimation. The relationship between isotope-resolved canopy temperatures and GPP-weighted air temperatures was highly significant across sites (p < 0.0001, R2 = 0.82), thus offering confirmation of the isotope approach. The previously observed temperature invariance from temperate to boreal biomes was confirmed, but the greater elevation of canopy temperature above air temperature in the boreal forest was not. Based on the current analysis, we conclude that canopy temperatures in the boreal forest are as warm as those in temperate systems because day-time-growing-season air temperatures are similarly warm.

The energetic and carbon economic origins of leaf thermoregulation.

Leaf thermoregulation has been documented in a handful of studies, but the generality and origins of this pattern are unclear. We suggest that leaf thermoregulation is widespread in both space and time, and originates from the optimization of leaf traits to maximize leaf carbon gain across and within variable environments. Here we use global data for leaf temperatures, traits and photosynthesis to evaluate predictions from a novel theory of thermoregulation that synthesizes energy budget and carbon economics theories. Our results reveal that variation in leaf temperatures and physiological performance are tightly linked to leaf traits and carbon economics. The theory, parameterized with global averaged leaf traits and microclimate, predicts a moderate level of leaf thermoregulation across a broad air temperature gradient. These predictions are supported by independent data for diverse taxa spanning a global air temperature range of ∼60 °C. Moreover, our theory predicts that net carbon assimilation can be maximized by means of a trade-off between leaf thermal stability and photosynthetic stability. This prediction is supported by globally distributed data for leaf thermal and photosynthetic traits. Our results demonstrate that the temperatures of plant tissues, and not just air, are vital to developing more accurate Earth system models.

Stable isotopes in leaf water of terrestrial plants.

Leaf water contains naturally occurring stable isotopes of oxygen and hydrogen in abundances that vary spatially and temporally. When sufficiently understood, these can be harnessed for a wide range of applications. Here, we review the current state of knowledge of stable isotope enrichment of leaf water, and its relevance for isotopic signals incorporated into plant organic matter and atmospheric gases. Models describing evaporative enrichment of leaf water have become increasingly complex over time, reflecting enhanced spatial and temporal resolution. We recommend that practitioners choose a model with a level of complexity suited to their application, and provide guidance. At the same time, there exists some lingering uncertainty about the biophysical processes relevant to patterns of isotopic enrichment in leaf water. An important goal for future research is to link observed variations in isotopic composition to specific anatomical and physiological features of leaves that reflect differences in hydraulic design. New measurement techniques are developing rapidly, enabling determinations of both transpired and leaf water δ(18) O and δ(2) H to be made more easily and at higher temporal resolution than previously possible. We expect these technological advances to spur new developments in our understanding of patterns of stable isotope fractionation in leaf water.

Plant Thermoregulation: Energetics, Trait-Environment Interactions, and Carbon Economics.

Building a more predictive trait-based ecology requires mechanistic theory based on first principles. We present a general theoretical approach to link traits and climate. We use plant leaves to show how energy budgets (i) provide a foundation for understanding thermoregulation, (ii) explain mechanisms driving trait variation across environmental gradients, and (iii) guide selection on functional traits via carbon economics. Although plants are often considered to be poikilotherms, the data suggest that they are instead limited homeotherms. Leaf functional traits that promote limited homeothermy are adaptive because homeothermy maximizes instantaneous and lifetime carbon gain. This theory provides a process-based foundation for trait-climate analyses and shows that future studies should consider plant (not only air) temperatures.