Michael J. Aspinwall

Utilizing intraspecific variation in phenotypic plasticity to bolster agricultural and forest productivity under climate change

Climate change threatens the ability of agriculture and forestry to meet growing global demands for food, fibre and wood products. Information gathered from genotype-by-environment interactions (G × E), which demonstrate intraspecific variation in phenotypic plasticity (the ability of a genotype to alter its phenotype in response to environmental change), may prove important for bolstering agricultural and forest productivity under climate change. Nonetheless, very few studies have explicitly quantified genotype plasticity-productivity relationships in agriculture or forestry. Here, we conceptualize the importance of intraspecific variation in agricultural and forest species plasticity, and discuss the physiological and genetic factors contributing to intraspecific variation in phenotypic plasticity. Our discussion highlights the need for an integrated understanding of the mechanisms of G × E, more extensive assessments of genotypic responses to climate change under field conditions, and explicit testing of genotype plasticity-productivity relationships. Ultimately, further investigation of intraspecific variation in phenotypic plasticity in agriculture and forestry may prove important for identifying genotypes capable of increasing or sustaining productivity under more extreme climatic conditions.

BAAD: a biomass and allometry database for woody plants

Understanding how plants are constructed—i.e., how key size dimensions and the amount of mass invested in different tissues varies among individuals—is essential for modeling plant growth, carbon stocks, and energy fluxes in the terrestrial biosphere. Allocation patterns can differ through ontogeny, but also among coexisting species and among species adapted to different environments. While a variety of models dealing with biomass allocation exist, we lack a synthetic understanding of the underlying processes. This is partly due to the lack of suitable data sets for validating and parameterizing models. To that end, we present the Biomass And Allometry Database (BAAD) for woody plants. The BAAD contains 259 634 measurements collected in 176 different studies, from 21 084 individuals across 678 species. Most of these data come from existing publications. However, raw data were rarely made public at the time of publication. Thus, the BAAD contains data from different studies, transformed into standard units and variable names. The transformations were achieved using a common workflow for all raw data files. Other features that distinguish the BAAD are: (i) measurements were for individual plants rather than stand averages; (ii) individuals spanning a range of sizes were measured; (iii) plants from 0.01–100 m in height were included; and (iv) biomass was estimated directly, i.e., not indirectly via allometric equations (except in very large trees where biomass was estimated from detailed sub-sampling). We included both wild and artificially grown plants. The data set contains the following size metrics: total leaf area; area of stem cross-section including sapwood, heartwood, and bark; height of plant and crown base, crown area, and surface area; and the dry mass of leaf, stem, branches, sapwood, heartwood, bark, coarse roots, and fine root tissues. We also report other properties of individuals (age, leaf size, leaf mass per area, wood density, nitrogen content of leaves and wood), as well as information about the growing environment (location, light, experimental treatment, vegetation type) where available. It is our hope that making these data available will improve our ability to understand plant growth, ecosystem dynamics, and carbon cycling in the worlds vegetation.

Genetic variation in circadian regulation of nocturnal stomatal conductance enhances carbon assimilation and growth

Circadian resonance, whereby a plants endogenous rhythms are tuned to match environmental cues, has been repeatedly shown to be adaptive, although the underlying mechanisms remain elusive. Concomitantly, the adaptive value of nocturnal transpiration in C3 plants remains unknown because it occurs without carbon assimilation. These seemingly unrelated processes are interconnected because circadian regulation drives temporal patterns in nocturnal stomatal conductance, with maximum values occurring immediately before dawn for many species. We grew individuals of six Eucalyptus camaldulensis genotypes in naturally lit glasshouses and measured sunset, predawn and midday leaf gas exchange and whole-plant biomass production. We tested whether sunrise anticipation by the circadian clock and subsequent increases in genotype predawn stomatal conductance led to rapid stomatal opening upon illumination, ultimately affecting genotype differences in carbon assimilation and growth. We observed faster stomatal responses to light inputs at sunrise in genotypes with higher predawn stomatal conductance. Moreover, early morning and midday stomatal conductance and carbon assimilation, leaf area and total plant biomass were all positively correlated with predawn stomatal conductance across genotypes. Our results lead to the novel hypothesis that genotypic variation in the circadian-regulated capacity to anticipate sunrise could be an important factor underlying intraspecific variation in tree growth.

Does physiological acclimation to climate warming stabilize the ratio of canopy respiration to photosynthesis

Given the contrasting short-term temperature dependences of gross primary production (GPP) and autotrophic respiration, the fraction of GPP respired by trees is predicted to increase with warming, providing a positive feedback to climate change. However, physiological acclimation may dampen or eliminate this response. We measured the fluxes of aboveground respiration (Ra ), GPP and their ratio (Ra /GPP) in large, field-grown Eucalyptus tereticornis trees exposed to ambient or warmed air temperatures (+3°C). We report continuous measurements of whole-canopy CO2 exchange, direct temperature response curves of leaf and canopy respiration, leaf and branch wood respiration, and diurnal photosynthetic measurements. Warming reduced photosynthesis, whereas physiological acclimation prevented a coincident increase in Ra . Ambient and warmed trees had a common nonlinear relationship between the fraction of GPP that was respired above ground (Ra /GPP) and the mean daily temperature. Thus, warming significantly increased Ra /GPP by moving plants to higher positions on the shared Ra /GPP vs daily temperature relationship, but this effect was modest and only notable during hot conditions. Despite the physiological acclimation of autotrophic respiration to warming, increases in temperature and the frequency of heat waves may modestly increase tree Ra /GPP, contributing to a positive feedback between climate warming and atmospheric CO2 accumulation.

The effect of subambient to elevated atmospheric CO2 concentration on vascular function in Helianthus annuus: implications for plant response to climate change

Plant gas exchange is regulated by stomata, which coordinate leaf-level water loss with xylem transport. Stomatal opening responds to internal concentrations of CO₂ in the leaf, but changing CO₂ can also lead to changes in stomatal density that influence transpiration. Given that stomatal conductance increases under subambient concentrations of CO₂ and, conversely, that plants lose less water at elevated concentrations, can downstream effects of atmospheric CO₂ be observed in xylem tissue? We approached this problem by evaluating leaf stomatal density, xylem transport, xylem anatomy and resistance to cavitation in Helianthus annuus plants grown under three CO₂ regimes ranging from pre-industrial to elevated concentrations. Xylem transport, conduit size and stomatal density all increased at 290 ppm relative to ambient and elevated CO₂ concentrations. The shoots of the 290-ppm-grown plants were most vulnerable to cavitation, whereas xylem cavitation resistance did not differ in 390- and 480-ppm-grown plants. Our data indicate that, even as an indirect driver of water loss, CO₂ can affect xylem structure and water transport by coupling stomatal and xylem hydraulic functions during plant development. This plastic response has implications for plant water use under variable concentrations of CO₂, as well as the evolution of efficient xylem transport.

Promises and challenges of eco-physiological genomics in the field : tests of drought responses in switchgrass

Physiological and gene expression analyses across field and greenhouse experiments highlight diverse gene expression patterns that produce physiologically similar responses to soil water deficits. Identifying the physiological and genetic basis of stress tolerance in plants has proven to be critical to understanding adaptation in both agricultural and natural systems. However, many discoveries were initially made in the controlled conditions of greenhouses or laboratories, not in the field. To test the comparability of drought responses across field and greenhouse environments, we undertook three independent experiments using the switchgrass reference genotype Alamo AP13. We analyzed physiological and gene expression variation across four locations, two sampling times, and three years. Relatively similar physiological responses and expression coefficients of variation across experiments masked highly dissimilar gene expression responses to drought. Critically, a drought experiment utilizing small pots in the greenhouse elicited nearly identical physiological changes as an experiment conducted in the field, but an order of magnitude more differentially expressed genes. However, we were able to define a suite of several hundred genes that were differentially expressed across all experiments. This list was strongly enriched in photosynthesis, water status, and reactive oxygen species responsive genes. The strong across-experiment correlations between physiological plasticity—but not differential gene expression—highlight the complex and diverse genetic mechanisms that can produce phenotypically similar responses to various soil water deficits.

Leaf photosynthetic, economics and hydraulic traits are decoupled among genotypes of a widespread species of eucalypt grown under ambient and elevated CO2

Summary Leaf economics and hydraulic traits strongly influence photosynthesis. While the level of coordination among these traits can differ between sets of species, leaf functional trait coordination within species remains poorly understood. Furthermore, elevated concentrations of atmospheric CO2 commonly influence the expression of leaf photosynthetic, economics and hydraulic traits in contrasting ways, yet the effect of variable concentrations of atmospheric CO2 on patterns of trait coordination within species remains largely untested. We examined the relationships among key leaf photosynthetic (e.g. net photosynthesis and photosynthetic biochemistry), economics and water-use (e.g. leaf mass per unit area and stomatal conductance) and hydraulic traits (e.g. vein density) in 14 genotypes of Eucalyptus camaldulensis grown in ambient (aCO2) and elevated (eCO2) [CO2]. We examined the level of coordination among leaf traits in aCO2 and then assessed whether growth in eCO2 altered that coordination. We found that leaf traits related to photosynthetic capacity, economics and water-use, and hydraulics were decoupled among genotypes grown in aCO2, yet strong relationships were generally observed among suites of traits within each ‘functional group’. Significant responses to growth in eCO2 were observed for most leaf photosynthetic and economics and water-use traits, with the magnitude and direction of the response varying among traits. In contrast, leaf hydraulics traits were unaffected by variable growth CO2. Despite this, growth in eCO2 did not substantially alter patterns of leaf trait coordination observed in aCO2. These results suggest suites of leaf traits associated with photosynthetic capacity, economics and water-use and hydraulics, respectively, can form independent axes of variation among genotypes of a single species, regardless of growth CO2. Although growth in eCO2 did not substantially alter patterns of trait coordination, decoupling of leaf functional traits among genotypes may allow genetically distinct populations to produce novel combinations of traits that may be adaptive in response to changes in their local environment.

QTLs for biomass and developmental traits in switchgrass (Panicum virgatum).

Genetic and genomic resources have recently been developed for the bioenergy crop switchgrass (Panicum virgatum). Despite these advances, little research has been focused on identifying genetic loci involved in natural variation of important bioenergy traits, including biomass. Quantitative trait locus (QTL) mapping is typically used to discover loci that contribute to trait variation. Once identified, QTLs can be used to improve agronomically important traits through marker-assisted selection. In this study, we conducted QTL mapping in Austin, TX, USA, with a full-sib mapping population derived from a cross between tetraploid clones of two major switchgrass cultivars (Alamo-A4 and Kanlow-K5). We observed significant among-genotype variation for the vast majority of growth, morphological, and phenological traits measured on the mapping population. Overall, we discovered 27 significant QTLs across 23 traits. QTLs for biomass production colocalized on linkage group 9b across years, as well as with a major biomass QTL discovered in another recent switchgrass QTL study. The experiment was conducted under a rainout shelter, which allowed us to examine the effects of differential irrigation on trait values. We found very minimal effects of the reduced watering treatment on traits, with no significant effect on biomass production. Overall, the results of our study set the stage for future crop improvement through marker-assisted selection breeding.

Genetic effects on total phenolics, condensed tannins and non- structural carbohydrates in loblolly pine (Pinus taeda L.) needles

Carbon allocation to soluble phenolics (total phenolics, proanthocyanidins (PA)) and total non-structural carbohydrates (TNC; starch and soluble sugars) in needles of widely planted, highly productive loblolly pine (Pinus taeda L.) genotypes could impact stand resistance to herbivory, and biogeochemical cycling in the southeastern USA. However, genetic and growth-related effects on loblolly pine needle chemistry are not well characterized. Therefore, we investigated genetic and growth-related effects on foliar concentrations of total phenolics, PA and TNC in two different field studies. The first study contained nine different genotypes representing a range of genetic homogeneity, growing in a 2-year-old plantation on the coastal plain of North Carolina (NC), USA. The second study contained eight clones with different growth potentials planted in a 9-year-old clonal trial replicated at two sites (Georgia (GA) and South Carolina (SC), USA). In the first study (NC), we found no genetic effects on total phenolics, PA and TNC, and there was no relationship between genotype size and foliar biochemistry. In the second study, there were no differences in height growth between sites, but the SC site showed greater diameter (diameter at breast height (DBH)) and volume, most likely due to greater tree mortality (lower stocking) which reduced competition for resources and increased growth of remaining trees. We found a significant site × clone effect for total phenolics with lower productivity clones showing 27-30% higher total phenolic concentrations at the GA site where DBH and volume were lower. In contrast to the predictions of growth-defense theory, clone volume was positively associated with total phenolic concentrations at the higher volume SC site, and PA concentrations at the lower volume GA site. Overall, we found no evidence of a trade-off between genotype size and defense, and genetic potential for improved growth may include increased allocation to some secondary metabolites. These results imply that deployment of more productive loblolly pine genotypes will not reduce stand resistance to herbivory, but increased production of total phenolics and PA associated with higher genotype growth potential could reduce litter decomposition rates and therefore, nutrient availability.

Bioclimatic transect networks: powerful observatories of ecological change

Abstract Transects that traverse substantial climate gradients are important tools for climate change research and allow questions on the extent to which phenotypic variation associates with climate, the link between climate and species distributions, and variation in sensitivity to climate change among biomes to be addressed. However, the potential limitations of individual transect studies have recently been highlighted. Here, we argue that replicating and networking transects, along with the introduction of experimental treatments, addresses these concerns. Transect networks provide cost‐effective and robust insights into ecological and evolutionary adaptation and improve forecasting of ecosystem change. We draw on the experience and research facilitated by the Australian Transect Network to demonstrate our case, with examples, to clarify how population‐ and community‐level studies can be integrated with observations from multiple transects, manipulative experiments, genomics, and ecological modeling to gain novel insights into how species and systems respond to climate change. This integration can provide a spatiotemporal understanding of past and future climate‐induced changes, which will inform effective management actions for promoting biodiversity resilience.