The carbon balance of plants: economics, optimization, and trait spectra in a historical perspective.

Over fifty years have passed since the publication of Harold Mooney's formative paper, "The Carbon Balance of Plants" on pages 315-346 of Volume 3 (1972) of Annual Review of Ecology and Systematics. Arguably, the conceptual framework presented in that paper, and the work by Mooney and his students leading up to the paper, provided the foundational principles from which core disciplines emerged in plant economic theory, functional trait theory and, more generally, plant physiological ecology. Here, we revisit the primary impacts of those early discoveries to understand how researchers constructed major concepts in our understanding of plant adaptations, and where those concepts are likely to take us in the near future. The discipline of functional trait ecology, which is rooted in the principles of evolutionary and economic optimization, has captured the imagination of the plant physiological ecology research community, though its emphasis has shifted toward predicting species distributions and ecological roles across resource gradients. In the face of 'big-data' research pursuits that are revealing trait expression patterns at the cellular level and mass and energy exchange patterns at the planetary scale, an opportunity exists to reconnect the principles of plant carbon balance and evolutionary optimization with trait origins at the genetic and cellular scales and trait impacts at the global scale.

Leaf angle as a leaf and canopy trait: Rejuvenating its role in ecology with new technology.

Life on Earth depends on the conversion of solar energy to chemical energy by plants through photosynthesis. A fundamental challenge in optimizing photosynthesis is to adjust leaf angles to efficiently use the intercepted sunlight under the constraints of heat stress, water loss and competition. Despite the importance of leaf angle, until recently, we have lacked data and frameworks to describe and predict leaf angle dynamics and their impacts on leaves to the globe. We review the role of leaf angle in studies of ecophysiology, ecosystem ecology and earth system science, and highlight the essential yet understudied role of leaf angle as an ecological strategy to regulate plant carbon-water-energy nexus and to bridge leaf, canopy and earth system processes. Using two models, we show that leaf angle variations have significant impacts on not only canopy-scale photosynthesis, energy balance and water use efficiency but also light competition within the forest canopy. New techniques to measure leaf angles are emerging, opening opportunities to understand the rarely-measured intraspecific, interspecific, seasonal and interannual variations of leaf angles and their implications to plant biology and earth system science. We conclude by proposing three directions for future research.

The complicated legacy of E. O. Wilson with respect to genetics and human behavior.

Over the arc of his career, E. O. Wilson first embraced, then popularized, and finally rejected an extreme genetical hereditarian view of human nature. The controversy that ensued during the period of popularization (largely in the 1970s and 1980s) obscured the fact that empirical and theoretical research during this time undercut the assumptions necessary for this view. By the end of his career, Wilson accepted the fact that individual/kin selection models were insufficient to explain human behavior and society, and he began conducting research based upon multilevel (group) selection, an idea he had previously scorned.

Coordinated resource allocation to plant growth-defense tradeoffs.

Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G-D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed 'big data' resources including multi-omic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi-omics biology to better understand how selection has shaped the mechanisms of G-D tradeoffs. Multi-omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G-D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G-D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply- and demand-side perspectives of previous G-D tradeoff theories.

Trade-offs Among Resilience, Robustness, Stability, and Performance and How We Might Study Them.

Biological systems are likely to be constrained by trade-offs among robustness, resilience, and performance. A better understanding of these trade-offs is important for basic biology, as well as applications where biological systems can be designed for different goals. We focus on redundancy and plasticity as mechanisms governing some types of trade-offs, but mention others as well. Whether trade-offs are due to resource constraints or "design" constraints (i.e., structure of nodes and links within a network) will also affect the types of trade-offs that are important. Identifying common themes across scales of biological organization will require that researchers use similar approaches to quantifying robustness, resilience, and performance, using units that can be compared across systems.

Pollination in the Anthropocene: a Moth Can Learn Ozone-Altered Floral Blends.

Insect pollination is essential to many unmanaged and agricultural systems and as such is a key element in food production. However, floral scents that pollinating insects rely on to locate host plants may be altered by atmospheric oxidants, such as ozone, potentially making these cues less attractive or unrecognizable to foraging insects and decreasing pollinator efficacy. We demonstrate that levels of tropospheric ozone commonly found in many rural areas are sufficient to disrupt the innate attraction of the tobacco hawkmoth Manduca sexta to the odor of one of its preferred flowers, Nicotiana alata. However, we further find that visual navigation together with associative learning can offset this disruption. Foraging moths that initially find an ozone-altered floral scent unattractive can target an artificial flower using visual cues and associate the ozone-altered floral blend with a nectar reward. The ability to learn ozone-altered floral odors may enable pollinators to maintain communication with their co-evolutionary partners and reduce the negative impacts that anthropogenically elevated oxidants may have on plant-pollinator systems.

Solar-induced chlorophyll fluorescence and short-term photosynthetic response to drought.

Drought is among the most damaging climate extremes, potentially causing significant decline in ecosystem functioning and services at the regional to global scale, thus monitoring of drought events is critically important. Solar-induced chlorophyll fluorescence (SIF) has been found to strongly correlate with gross primary production on the global scale. Recent advances in the remote sensing of SIF allow for large-scale, real-time estimation of photosynthesis using this relationship. However, several studies have used SIF to quantify the impact of drought with mixed results, and the leaf-level mechanisms linking SIF and photosynthesis are unclear, particularly how the relationship may change under drought. We conducted a drought experiment with 2-yr old Populus deltoides. We measured leaf-level gas exchange, SIF, and pulse amplitude modulated (PAM) fluorescence before and during the 1-month drought. We found clear responses of net photosynthesis and stomatal conductance to water stress, however, SIF showed a smaller response to drought. Net photosynthesis (Anet ) and conductance dropped 94% and 95% on average over the drought, while SIF values only decreased slightly (21%). Electron transport rate dropped 64% when compared to the control over the last week of drought, but the electron transport chain did not completely shut down as Anet approached zero. Additionally, SIF yield (SIFy ) was positively correlated with steady-state fluorescence (Fs ) and negatively correlated with non-photochemical quenching (NPQ; R2  = 0.77). Both Fs and SIFy , after normalization by the minimum fluorescence from a dark-adapted sample (Fo ), showed a more pronounced drought response, although the results suggest the response is complicated by several factors. Leaf-level experiments can elucidate mechanisms behind large-scale remote sensing observations of ecosystem functioning. The value of SIF as an accurate estimator of photosynthesis may decrease during mild stress events of short duration, especially when the response is primarily stomatal and not fully coupled with the light reactions of photosynthesis. We discuss potential factors affecting the weak SIF response to drought, including upregulation of NPQ, change in internal leaf structure and chlorophyll concentration, and photorespiration. The results suggest that SIF is mainly controlled by the light reactions of photosynthesis, which operate on different timescales than the stomatal response.

Observing Severe Drought Influences on Ozone Air Pollution in California.

Drought conditions affect ozone air quality, potentially altering multiple terms in the O3 mass balance equation. Here, we present a multiyear observational analysis using data collected before, during, and after the record-breaking California drought (2011-2015) at the O3-polluted locations of Fresno and Bakersfield near the Sierra Nevada foothills. We separately assess drought influences on O3 chemical production ( PO3) from O3 concentration. We show that isoprene concentrations, which are a source of O3-forming organic reactivity, were relatively insensitive to early drought conditions but decreased by more than 50% during the most severe drought years (2014-2015), with recovery a function of location. We find drought-isoprene effects are temperature-dependent, even after accounting for changes in leaf area, consistent with laboratory studies but not previously observed at landscape scales with atmospheric observations. Drought-driven decreases in organic reactivity are contemporaneous with a change in dominant oxidation mechanism, with PO3 becoming more NO x-suppressed, leading to a decrease in PO3 of ∼20%. We infer reductions in atmospheric O3 loss of ∼15% during the most severe drought period, consistent with past observations of decreases in O3 uptake by plants. We consider drought-related trends in O3 variability on synoptic time scales by analyzing statistics of multiday high-O3 events. We discuss implications for regulating O3 air pollution in California and other locations under more prevalent drought conditions.

Soil aggregates as biogeochemical reactors and implications for soil-atmosphere exchange of greenhouse gases-A concept.

Soil-atmosphere exchange significantly influences the global atmospheric abundances of carbon dioxide (CO2 ), methane (CH4 ), and nitrous oxide (N2 O). These greenhouse gases (GHGs) have been extensively studied at the soil profile level and extrapolated to coarser scales (regional and global). However, finer scale studies of soil aggregation have not received much attention, even though elucidating the GHG activities at the full spectrum of scales rather than just coarse levels is essential for reducing the large uncertainties in the current atmospheric budgets of these gases. Through synthesizing relevant studies, we propose that aggregates, as relatively separate micro-environments embedded in a complex soil matrix, can be viewed as biogeochemical reactors of GHGs. Aggregate reactivity is determined by both aggregate size (which determines the reactor size) and the bulk soil environment including both biotic and abiotic factors (which further influence the reaction conditions). With a systematic, dynamic view of the soil system, implications of aggregate reactors for soil-atmosphere GHG exchange are determined by both an individual reactor's reactivity and dynamics in aggregate size distributions. Emerging evidence supports the contention that aggregate reactors significantly influence soil-atmosphere GHG exchange and may have global implications for carbon and nitrogen cycling. In the context of increasingly frequent and severe disturbances, we advocate more analyses of GHG activities at the aggregate scale. To complement data on aggregate reactors, we suggest developing bottom-up aggregate-based models (ABMs) that apply a trait-based approach and incorporate soil system heterogeneity.

Biodiversity matters in feedbacks between climate change and air quality: a study using an individual-based model.

Air quality is closely associated with climate change via the biosphere because plants release large quantities of volatile organic compounds (VOC) that mediate both gaseous pollutants and aerosol dynamics. Earlier studies, which considered only leaf physiology and simply scale up from leaf-level enhancements of emissions, suggest that climate warming enhances whole forest VOC emissions, and these increased VOC emissions aggravate ozone pollution and secondary organic aerosol formation. Using an individual-based forest VOC emissions model, UVAFME-VOC, that simulates system-level emissions by explicitly simulating forest community dynamics to the individual tree level, ecological competition among the individuals of differing size and age, and radiative transfer and leaf function through the canopy, we find that climate warming only sometimes stimulates isoprene emissions (the single largest source of non-methane hydrocarbon) in a southeastern U.S. forest. These complex patterns result from the combination of higher temperatures' stimulating emissions at the leaf level but decreasing the abundance of isoprene-emitting taxa at the community level by causing a decline in the abundance of isoprene-emitting species (Quercus spp.). This ecological effect eventually outweighs the physiological one, thus reducing overall emissions. Such reduced emissions have far-reaching implications for the climate-air-quality relationships that have been established on the paradigm of warming-enhancement VOC emissions from vegetation. This local scale modeling study suggests that community ecology rather than only individual physiology should be integrated into future studies of biosphere-climate-chemistry interactions.

Overexpression of microRNA408 enhances photosynthesis, growth, and seed yield in diverse plants.

The ability of a plant to produce grain, fruit, or forage depends ultimately on photosynthesis. There have been few attempts, however, to study microRNAs, which are a class of endogenous small RNAs post-transcriptionally programming gene expression, in relation to photosynthetic traits. We focused on miR408, one of the most conserved plant miRNAs, and overexpressed it in parallel in Arabidopsis, tobacco, and rice. The transgenic plants all exhibited increased copper content in the chloroplast, elevated abundance of plastocyanin, and an induction of photosynthetic genes. By means of gas exchange and optical spectroscopy analyses, we showed that higher expression of miR408 leads to enhanced photosynthesis through improving efficiency of irradiation utilization and the capacity for carbon dioxide fixation. Consequently, miR408 hyper-accumulating plants exhibited higher rate of vegetative growth. An enlargement of seed size was also observed in all three species overproducing miR408. Moreover, we conducted a 2-year-two-location field trial and observed miR408 overexpression in rice significantly increased yield, which was primarily attributed to an elevation in grain weight. Taken together, these results demonstrate that miR408 is a positive regulator of photosynthesis and that its genetic engineering is a promising route for enhancing photosynthetic performance and yield in diverse plants.

Widespread production of nonmicrobial greenhouse gases in soils.

Carbon dioxide (CO2 ), methane (CH4 ), and nitrous oxide (N2 O) are the three most important greenhouse gases (GHGs), and all show large uncertainties in their atmospheric budgets. Soils of natural and managed ecosystems play an extremely important role in modulating their atmospheric abundance. Mechanisms underlying the exchange of these GHGs at the soil-atmosphere interface are often assumed to be exclusively microbe-mediated (M-GHGs). We argue that it is a widespread phenomenon for soil systems to produce GHGs through nonmicrobial pathways (NM-GHGs) based on a review of the available evidence accumulated over the past half century. We find that five categories of mechanistic process, including photodegradation, thermal degradation, reactive oxidative species (ROS) oxidation, extracellular oxidative metabolism (EXOMET), and inorganic chemical reactions, can be identified as accounting for their production. These pathways are intricately coupled among themselves and with M-GHGs production and are subject to strong influences from regional and global change agents including, among others, climate warming, solar radiation, and alterations of atmospheric components. Preliminary estimates have suggested that NM-GHGs could play key roles in contributing to budgets of GHGs in the arid regions, whereas their global importance would be enhanced with accelerated global environmental changes. Therefore, more research should be undertaken, with a differentiation between NM-GHGs and M-GHGs, to further elucidate the underlying mechanisms, to investigate the impacts of various global change agents, and to quantify their contributions to regional and global GHGs budgets. These efforts will contribute to a more complete understanding of global carbon and nitrogen cycling and a reduction in the uncertainty of carbon-climate feedbacks in the Earth system.

Correlating species and spectral diversities using hyperspectral remote sensing in early-successional fields.

Advances in remote sensing technology can help estimate biodiversity at large spatial extents. To assess whether we could use hyperspectral visible near-infrared (VNIR) spectra to estimate species diversity, we examined the correlations between species diversity and spectral diversity in early-successional abandoned agricultural fields in the Ridge and Valley ecoregion of north-central Virginia at the Blandy Experimental Farm. We established plant community plots and collected vegetation surveys and ground-level hyperspectral data from 350 to 1,025 nm wavelengths. We related spectral diversity (standard deviations across spectra) with species diversity (Shannon-Weiner index) and evaluated whether these correlations differed among spectral regions throughout the visible and near-infrared wavelength regions, and across different spectral transformation techniques. We found positive correlations in the visible regions using band depth data, positive correlations in the near-infrared region using first derivatives of spectra, and weak to no correlations in the red-edge region using either of the two spectral transformation techniques. To investigate the role of pigment variability in these correlations, we estimated chlorophyll, carotenoid, and anthocyanin concentrations of five dominant species in the plots using spectral vegetation indices. Although interspecific variability in pigment levels exceeded intraspecific variability, chlorophyll was more varied within species than carotenoids and anthocyanins, contributing to the lack of correlation between species diversity and spectral diversity in the red-edge region. Interspecific differences in pigment levels, however, made it possible to differentiate these species remotely, contributing to the species-spectral diversity correlations. VNIR spectra can be used to estimate species diversity, but the relationships depend on the spectral region examined and the spectral transformation technique used.

The origin, diversification and adaptation of a major mangrove clade (Rhizophoreae) revealed by whole-genome sequencing.

Mangroves invade some very marginal habitats for woody plants-at the interface between land and sea. Since mangroves anchor tropical coastal communities globally, their origin, diversification and adaptation are of scientific significance, particularly at a time of global climate change. In this study, a combination of single-molecule long reads and the more conventional short reads are generated from Rhizophora apiculata for the de novo assembly of its genome to a near chromosome level. The longest scaffold, N50 and N90 for the R. apiculata genome, are 13.3 Mb, 5.4 Mb and 1.0 Mb, respectively. Short reads for the genomes and transcriptomes of eight related species are also generated. We find that the ancestor of Rhizophoreae experienced a whole-genome duplication ~70 Myrs ago, which is followed rather quickly by colonization and species diversification. Mangroves exhibit pan-exome modifications of amino acid (AA) usage as well as unusual AA substitutions among closely related species. The usage and substitution of AAs, unique among plants surveyed, is correlated with the rapid evolution of proteins in mangroves. A small subset of these substitutions is associated with mangroves' highly specialized traits (vivipary and red bark) thought to be adaptive in the intertidal habitats. Despite the many adaptive features, mangroves are among the least genetically diverse plants, likely the result of continual habitat turnovers caused by repeated rises and falls of sea level in the geologically recent past. Mangrove genomes thus inform about their past evolutionary success as well as portend a possibly difficult future.