Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host physiology and leaf chemistry

Atmospheric CO₂ concentrations are predicted to double within the next century. Despite this trend, the extent and mechanisms through which elevated CO₂ affects plant diseases remain uncertain. In this study, we assessed how elevated CO₂ affects a foliar fungal pathogen, Phyllosticta minima, of Acer rubrum growing in the understory at the Duke Forest free‐air CO₂ enrichment experiment in Durham, North Carolina. Surveys of A. rubrum saplings in the 6th, 7th, and 8th years of the CO₂ exposure revealed that elevated CO₂ significantly reduced disease incidence, with 22%, 27%, and 8% fewer saplings and 14%, 4%, and 5% fewer leaves infected per plant in the three consecutive years, respectively. Elevated CO₂ also significantly reduced disease severity in infected plants in all years (e.g. mean lesion area reduced 35%, 50%, and 10% in 2002, 2003, and 2004, respectively). To assess the mechanisms underlying these changes, we combined leaf structural, physiological and chemical analyses with growth chamber studies of P. minima growth and host infection. In vitro exponential growth rates of P. minima were enhanced by 17% under elevated CO₂, discounting the possibility that disease reductions were because of direct negative effects of elevated CO₂ on fungal performance. Scanning electron micrographs (SEM) verified that conidia germ tubes of P. minima infect A. rubrum leaves by entering through the stomata. While stomatal size and density were unchanged, stomatal conductance was reduced by 21–36% under elevated CO₂, providing smaller openings for infecting germ tubes. Reduced disease severity under elevated CO₂ was likely due to altered leaf chemistry and reduced nutritive quality; elevated CO₂ reduced leaf N by 20% and increased the C : N ratio by 20%, total phenolics by 15%, and tannins by 14% (P<0.05 for each factor). The potential dual mechanism we describe here of reduced stomatal opening and altered leaf chemistry that results in reduced disease incidence and severity under elevated CO₂ may be prevalent in many plant pathosystems where the pathogen targets the stomata.     

Elevated carbon dioxide and ozone alter productivity and ecosystem carbon content in northern temperate forests

Three young northern temperate forest communities in the north‐central United States were exposed to factorial combinations of elevated carbon dioxide (CO₂) and tropospheric ozone (O₃) for 11 years. Here, we report results from an extensive sampling of plant biomass and soil conducted at the conclusion of the experiment that enabled us to estimate ecosystem carbon (C) content and cumulative net primary productivity (NPP). Elevated CO₂ enhanced ecosystem C content by 11%, whereas elevated O₃ decreased ecosystem C content by 9%. There was little variation in treatment effects on C content across communities and no meaningful interactions between CO₂ and O₃. Treatment effects on ecosystem C content resulted primarily from changes in the near‐surface mineral soil and tree C, particularly differences in woody tissues. Excluding the mineral soil, cumulative NPP was a strong predictor of ecosystem C content (r² = 0.96). Elevated CO₂ enhanced cumulative NPP by 39%, a consequence of a 28% increase in canopy nitrogen (N) content (g N m^?2) and a 28% increase in N productivity (NPP/canopy N). In contrast, elevated O₃ lowered NPP by 10% because of a 21% decrease in canopy N, but did not impact N productivity. Consequently, as the marginal impact of canopy N on NPP (?NPP/?N) decreased through time with further canopy development, the O₃ effect on NPP dissipated. Within the mineral soil, there was less C in the top 0.1 m of soil under elevated O₃ and less soil C from 0.1 to 0.2 m in depth under elevated CO₂. Overall, these results suggest that elevated CO₂ may create a sustained increase in NPP, whereas the long‐term effect of elevated O₃ on NPP will be smaller than expected. However, changes in soil C are not well‐understood and limit our ability to predict changes in ecosystem C content.     

New insights into the cellular mechanisms of plant growth at elevated atmospheric carbon dioxide concentrations

Rising atmospheric carbon dioxide concentration ([CO₂]) significantly influences plant growth, development, and biomass. Increased photosynthesis rate, together with lower stomatal conductance, has been identified as the key factors that stimulate plant growth at elevated [CO₂] (e[CO₂]). However, variations in photosynthesis and stomatal conductance alone cannot fully explain the dynamic changes in plant growth. Stimulation of photosynthesis at e[CO₂] is always associated with post‐photosynthetic secondary metabolic processes that include carbon and nitrogen metabolism, cell cycle functions, and hormonal regulation. Most studies have focused on photosynthesis and stomatal conductance in response to e[CO₂], despite the emerging evidence of e[CO₂]'s role in moderating secondary metabolism in plants. In this review, we briefly discuss the effects of e[CO₂] on photosynthesis and stomatal conductance and then focus on the changes in other cellular mechanisms and growth processes at e[CO₂] in relation to plant growth and development. Finally, knowledge gaps in understanding plant growth responses to e[CO₂] have been identified with the aim of improving crop productivity under a CO₂ rich atmosphere.     

The severity of wheat diseases increases when plants and pathogens are acclimatized to elevated carbon dioxide

Wheat diseases present a constant and evolving threat to food security. We have little understanding as to how increased atmospheric carbon dioxide levels will affect wheat diseases and thus the security of grain supply. Atmospheric CO₂ exceeded the 400 ppmv benchmark in 2013 and is predicted to double or even treble by the end of the century. This study investigated the impact of both pathogen and wheat acclimation to elevated CO₂ on the development of Fusarium head blight (FHB) and Septoria tritici blotch (STB) disease of wheat. Here, plants and pathogens were cultivated under either 390 or 780 ppmv CO₂ for a period (two wheat generations, multiple pathogen subcultures) prior to standard disease trials. Acclimation of pathogens and the wheat cultivar Remus to elevated CO₂ increased the severity of both STB and FHB diseases, relative to ambient conditions. The effect of CO₂ on disease development was greater for FHB than for STB. The highest FHB disease levels and associated yield losses were recorded for elevated CO₂‐acclimated pathogen on elevated CO₂‐acclimated wheat. When similar FHB experiments were conducted using the disease‐resistant cultivar CM82036, pathogen acclimation significantly enhanced disease levels and yield loss under elevated CO₂ conditions, thereby indicating a reduction in the effectiveness of the defence pathways innate to this wheat cultivar. We conclude that acclimation to elevated CO₂ over the coming decades will have a significant influence on the outcome of plant–pathogen interactions and the durability of disease resistance.     

The role of temperature in determining the stimulation of CO2 assimilation at elevated carbon dioxide concentration in soybean seedlings

Soybean ( Glycine max cv. Clark) was grown at both ambient (ca 350 μmol mol⁻¹) and elevated (ca 700 μmol mol⁻¹) CO₂ concentration at 5 growth temperatures (constant day/night temperatures of 20, 25, 30, 35 and 40°C) for 17–22 days after sowing to determine the interaction between temperature and CO₂ concentration on photosynthesis (measured as A, the rate of CO₂ assimilation per unit leaf area) at both the single leaf and whole plant level. Single leaves of soybean demonstrated increasingly greater stimulation of A at elevated CO₂ as temperature increased from 25 to 35°C (i.e. optimal growth rates). At 40°C, primary leaves failed to develop and plants eventually died. In contrast, for both whole plant A and total biomass production, increasing temperature resulted in less stimulation by elevated CO₂ concentration. For whole plants, increased CO₂ stimulated leaf area more as growth temperature increased. Differences between the response of A to elevated CO₂ for single leaves and whole plants may be related to increased self-shading experienced by whole plants at elevated CO₂ as temperature increased. Results from the present study suggest that self-shading could limit the response of CO₂ assimilation rate and the growth response of soybean plants if temperature and CO₂ increase concurrently, and illustrate that light may be an important consideration in predicting the relative stimulation of photosynthesis by elevated CO₂ at the whole plant level.     

Effects of carbon dioxide concentration on the interactive effects of temperature and water vapour on stomatal conductance in soybean

Soybeans were grown at three CO₂ concentrations in outdoor growth chambers and at two concentrations in controlled-environment growth chambers to investigate the interactive effects of CO₂, temperature and leaf-to-air vapour pressure difference (LAVPD) on stomatal conductance. The decline in stomatal conductance with CO₂ was a function of both leaf temperature and LAVPD. In the field measurements, stomatal conductance was more sensitive to LAVPD at low CO₂ at 30 °C but not at 35 °C. There was also a direct increase in conductance with temperature, which was greater at the two elevated carbon dioxide concentrations. Environmental growth chamber results showed that the relative stomatal sensitivity to LAVPD decreased with both leaf temperature and CO₂. Measurements in the environmental growth chamber were also performed at the opposing CO₂, and these experiments indicate that the stomatal sensitivity to LAVPD was determined more by growth CO₂ than by measurement CO₂. Two models that describe stomatal responses to LAVPD were compared with the outdoor data to evaluate whether these models described adequately the interactive effects of CO₂, LAVPD and temperature.     

Season-long elevation of ozone concentration to projected 2050 levels under fully open-air conditions substantially decreases the growth and production of soybean

Mean surface ozone concentration is predicted to increase 23% by 2050. Previous chamber studies of crops report large yield losses caused by elevation of tropospheric ozone, and have been the basis for projecting economic loss. This is the first study with a food crop (soybean, Glycine max) using free-air gas concentration enrichment (FACE) technology for ozone fumigation. A 23% increase in ozone concentration from an average daytime ambient 56 p.p.b. to a treatment 69 p.p.b. over two growing seasons decreased seed yield by 20%. Total above-ground net primary production decreased by 17% without altering dry mass allocation among shoot organs, except seed. Fewer live leaves and decreased photosynthesis in late grain filling appear to drive the ozone-induced losses in production and yield. These results validate previous chamber studies suggesting that soybean yields will decrease under increasing ozone exposure. In fact, these results suggest that when treated under open-air conditions yield losses may be even greater than the large losses already reported in earlier chamber studies. Yield losses with elevated ozone were greater in the second year following a severe hailstorm, suggesting that losses caused by ozone might be exacerbated by extreme climatic events.     

Production and fitness of Fusarium pseudograminearum inoculum at elevated carbon dioxide in FACE

Rising atmospheric carbon dioxide (CO₂) concentration is increasingly affecting food production but how plant diseases will influence production and quality of food under rising CO₂ is not well understood. With increased plant biomass at high CO₂ the stubble‐borne fungal pathogen Fusarium pseudograminearum causing crown rot (CR) of wheat may become more severe. We have studied inoculum production by Fusarium using fungal biomass per unit wheat stubble, stem browning from CR and the saprophytic fitness of Fusarium strains isolated from two wheat varieties grown in 2007 and 2008 at ambient and elevated CO₂ in free‐air CO₂ enrichment (FACE) with or without irrigation and once in a controlled environment. Fungal biomass, determined using primers for fungal ribosomal 18s and the TRI5 gene, increased significantly at elevated CO₂ in two of the three studies. Stem browning increased significantly at elevated CO₂ in the 2007 FACE study. At elevated CO₂ increased stem browning was not influenced by irrigation in a susceptible variety but in a resistant variety stem browning increased by 68% without irrigation. Wheat variety was significant in regression models explaining stem browning and Fusarium biomass but pathogen biomass at the two CO₂ levels was not significantly linked to stem browning. Fusarium isolates from ambient and elevated CO₂ did not differ significantly in their saprophytic fitness measured by the rate of colonization of wheat straw. We show that under elevated CO₂Fusarium inoculum in stubbles will be amplified from increased crop and pathogen biomass while unimpeded saprophytic fitness will retain its effectiveness. If resistant varieties cannot completely stop infection, Fusarium will rapidly colonize stubble to further increase inoculum once the crop is harvested. Research should move beyond documenting the influence of elevated CO₂ to developing disease management strategies from improved knowledge of pathogen biology and host resistance under rising CO₂.     

Effects of doubled atmospheric carbon dioxide concentration on the responses of assimilation and conductance to humidity

Experiments were performed to determine if growth at elevated partial pressure of CO₂ altered the sensitivity of leaf water vapour conductance and rate of CO₂ assimilation to the leaf-to-air difference in the partial pressure of water vapour (Δw). Comparisons were made between plants grown and measured at 350 and 700 μPa Pa^?1 partial pressures of CO₂ for amaranth, soybean and sunflower grown in controlled environment chambers, soybean grown outdoors in pots, and orchard grass grown in field plots. In amaranth, soybean and orchard grass, both the absolute and the relative sensitivity of conductance to Δw at the leaf surface were less in plants grown and measured at the elevated CO₂. In sunflower, there was no change in the sensitivity of conductance to Δw for the two CO₂ partial pressures. Tests in soybeans and amaranth showed that the change in sensitivity resulted from elevated CO₂ during the measurement of the Δw response. Assimilation rate of CO₂ was not altered by Δw in amaranth, which has C₄ metabolism. In sunflower, the assimilation rate of plants grown and measured at elevated CO₂ was insensitive to Δw, consistent with the response of assimilation rate to intercellular CO₂ partial pressure in the prevailing range. In soybean, the sensitivity of assimilation rate to Δw was not different between CO₂ treatments, in contrast to what would be expected from the response of assimilation rate to intercellular CO₂ partial pressure.     

Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis

The effects of elevated carbon dioxide on plant–herbivore interactions have been summarized in a number of narrative reviews and metaanalyses, while accompanying elevation of temperature has not received sufficient attention. The goal of our study is to search, by means of metaanalysis, for a general pattern in responses of herbivores, and plant characteristics important for herbivores, to simultaneous experimental increase of carbon dioxide and temperature (ECET) in comparison with both ambient conditions and responses to elevated CO₂ (EC) and temperature (ET) applied separately. Our database includes 42 papers describing studies of 31 plant species and seven herbivore species. Nitrogen concentration and C/N ratio in plants decreased under both EC and ECET treatments, whereas ET had no significant effect. Concentrations of nonstructural carbohydrates and phenolics increased in EC, decreased in ET and did not change in ECET treatments, whereas terpenes did not respond to EC but increased in both ET and ECET; leaf toughness increased in both EC and ECET. Responses of defensive secondary compounds to treatments differed between woody and green tissues as well as between gymnosperm and angiosperm plants. Insect herbivore performance was adversely affected by EC, favoured by ET, and not modified by ECET. Our analysis allowed to distinguish three types of relationships between CO₂ and temperature elevation: (1) responses to EC do not depend on temperature (nitrogen, C/N, leaf toughness, phenolics in angiosperm leaves), (2) responses to EC are mitigated by ET (sugars and starch, terpenes in needles of gymnosperms, insect performance) and (3) effects emerge only under ECET (nitrogen in gymnosperms, and phenolics and terpenes in woody tissues). This result indicates that conclusions of CO₂ elevation studies cannot be directly extrapolated to a more realistic climate change scenario. The predicted negative effects of CO₂ elevation on herbivores are likely to be mitigated by temperature increase.     

Smaller than predicted increase in aboveground net primary production and yield of field-grown soybean under fully open-air [CO2] elevation

The Intergovernmental Panel on Climate Change projects that atmospheric [CO₂] will reach 550 ppm by 2050. Numerous assessments of plant response to elevated [CO₂] have been conducted in chambers and enclosures, with only a few studies reporting responses in fully open‐air, field conditions. Reported yields for the world's two major grain crops, wheat and rice, are substantially lower in free‐air CO₂ enrichment (FACE) than predicted from similar elevated [CO₂] experiments within chambers. This discrepancy has major implications for forecasting future global food supply. Globally, the leguminous‐crop soybean (Glycine max (L.) Merr.) is planted on more land than any other dicotyledonous crop. Previous studies have shown that total dry mass production increased on average 37% in response to increasing [CO₂] to approximately 700 ppm, but harvestable yield will increase only 24%. Is this representative of soybean responses under open‐air field conditions? The effects of elevation of [CO₂] to 550 ppm on total production, partitioning and yield of soybean over 3 years are reported. This is the first FACE study of soybean ( http://www.soyface.uiuc.edu ) and the first on crops in the Midwest of North America, one of the major food production regions of the globe. Although increases in both aboveground net primary production (17–18%) and yield (15%) were consistent across three growing seasons and two cultivars, the relative stimulation was less than projected from previous chamber experiments. As in previous studies, partitioning to seed dry mass decreased; however, net production during vegetative growth did not increase and crop maturation was delayed, not accelerated as previously reported. These results suggest that chamber studies may have over‐estimated the stimulatory effect of rising [CO₂], with important implications on global food supply forecasts.     

Impact of elevated carbon dioxide on the rhizosphere communities of Carex arenaria and Festuca rubra

The increase in atmospheric carbon dioxide (CO₂) levels is predicted to stimulate plant carbon (C) fixation, potentially influencing the size, structure and function of micro- and mesofaunal communities inhabiting the rhizosphere. To assess the effects of increased atmospheric CO₂ on bacterial, fungal and nematode communities in the rhizosphere, Carex arenaria (a nonmycorrhizal plant species) and Festuca rubra (a mycorrhizal plant species) were grown in three dune soils under controlled soil temperature and moisture conditions, while subjecting the aboveground compartment to defined atmospheric conditions differing in CO₂ concentrations (350 and 700 μL L⁻¹). Real-time polymerase chain reaction (PCR) and PCR-denaturing gradient gel electrophoresis methods were used to examine effects on the size and structure of rhizosphere communities. Multivariate analysis of community profiles showed that bacteria were most affected by elevated CO₂, and fungi and nematodes to a lesser extent. The influence of elevated CO₂ was plant dependent, with the mycorrhizal plant ( F. rubra ) exerting a greater influence on bacterial and fungal communities. Biomarker data indicated that arbuscular mycorrhizal fungi (AMF) may play an important role in the observed soil community responses. Effects of elevated CO₂ were also soil dependent, with greater influence observed in the more organic-rich soils, which also supported higher levels of AMF colonization. These results indicate that responses of soil-borne communities to elevated CO₂ are different for bacteria, fungi and nematodes and dependent on the plant type and soil nutrient availability.     

Biomass increases attributed to both faster tree growth and altered allometric relationships under long‐term carbon dioxide enrichment at a temperate forest

Increases in atmospheric carbon dioxide (CO₂) concentrations are expected to lead to increases in the rate of tree biomass accumulation, at least temporarily. On the one hand, trees may simply grow faster under higher CO₂ concentrations, preserving the allometric relations that prevailed under lower CO₂ concentrations. Alternatively, the allometric relations themselves may change. In this study, the effects of elevated CO₂ (eCO₂) on tree biomass and allometric relations were jointly assessed. Over 100 trees, grown at Duke Forest, NC, USA, were harvested from eight plots. Half of the plots had been subjected to CO₂ enrichment from 1996 to 2010. Several subplots had also been subjected to nitrogen fertilization from 2005 to 2010. Allometric equations were developed to predict tree height, stem volume, and aboveground biomass components for loblolly pine (Pinus taeda L.), the dominant tree species, and broad‐leaved species. Using the same diameter‐based allometric equations for biomass, it was estimated that plots with eCO₂ contained 21% more aboveground biomass, consistent with previous studies. However, eCO₂ significantly affected allometry, and these changes had an additional effect on biomass. In particular, P. taeda trees at a given diameter were observed to be taller under eCO₂ than under ambient CO₂ due to changes in both the allometric scaling exponent and intercept. Accounting for allometric change increased the treatment effect of eCO₂ on aboveground biomass from a 21% to a 27% increase. No allometric changes for the nondominant broad‐leaved species were identified, nor were allometric changes associated with nitrogen fertilization. For P. taeda, it is concluded that eCO₂ affects allometries, and that knowledge of allometry changes is necessary to accurately compute biomass under eCO₂. Further observations are needed to determine whether this assessment holds for other taxa.