Innovation, conservation, and repurposing of gene function in root cell type development.

Plant species have evolved myriads of solutions, including complex cell type development and regulation, to adapt to dynamic environments. To understand this cellular diversity, we profiled tomato root cell type translatomes. Using xylem differentiation in tomato, examples of functional innovation, repurposing, and conservation of transcription factors are described, relative to the model plant Arabidopsis. Repurposing and innovation of genes are further observed within an exodermis regulatory network and illustrate its function. Comparative translatome analyses of rice, tomato, and Arabidopsis cell populations suggest increased expression conservation of root meristems compared with other homologous populations. In addition, the functions of constitutively expressed genes are more conserved than those of cell type/tissue-enriched genes. These observations suggest that higher order properties of cell type and pan-cell type regulation are evolutionarily conserved between plants and animals.

Translational regulation contributes to the elevated CO2 response in two Solanum species.

Understanding the impact of elevated CO2 (eCO2 ) in global agriculture is important given climate change projections. Breeding climate-resilient crops depends on genetic variation within naturally varying populations. The effect of genetic variation in response to eCO2 is poorly understood, especially in crop species. We describe the different ways in which Solanum lycopersicum and its wild relative S. pennellii respond to eCO2 , from cell anatomy, to the transcriptome, and metabolome. We further validate the importance of translational regulation as a potential mechanism for plants to adaptively respond to rising levels of atmospheric CO2 .

Intensifying drought eliminates the expected benefits of elevated carbon dioxide for soybean.

Stimulation of C3 crop yield by rising concentrations of atmospheric carbon dioxide ([CO2]) is widely expected to counteract crop losses that are due to greater drought this century. But these expectations come from sparse field trials that have been biased towards mesic growth conditions. This eight-year study used precipitation manipulation and year-to-year variation in weather conditions at a unique open-air field facility to show that the stimulation of soybean yield by elevated [CO2] diminished to zero as drought intensified. Contrary to the prevalent expectation in the literature, rising [CO2] did not counteract the effect of strong drought on photosynthesis and yield because elevated [CO2] interacted with drought to modify stomatal function and canopy energy balance. This new insight from field experimentation under hot and dry conditions, which will become increasingly prevalent in the coming decades, highlights the likelihood of negative impacts from interacting global change factors on a key global commodity crop in its primary region of production.

Plant developmental responses to climate change.

Climate change is multi-faceted, and includes changing concentrations of greenhouse gases in the atmosphere, rising temperatures, changes in precipitation patterns, and increasing frequency of extreme weather events. Here, we focus on the effects of rising atmospheric CO2 concentrations, rising temperature, and drought stress and their interaction on plant developmental processes in leaves, roots, and in reproductive structures. While in some cases these responses are conserved across species, such as decreased root elongation, perturbation of root growth angle and reduced seed yield in response to drought, or an increase in root biomass in shallow soil in response to elevated CO2, most responses are variable within and between species and are dependent on developmental stage. These variable responses include species-specific thresholds that arrest development of reproductive structures, reduce root growth rate and the rate of leaf initiation and expansion in response to elevated temperature. Leaf developmental responses to elevated CO2 vary by cell type and by species. Variability also exists between C3 and C4 species in response to elevated CO2, especially in terms of growth and seed yield stimulation. At the molecular level, significantly less is understood regarding conservation and variability in molecular mechanisms underlying these traits. Abscisic acid-mediated changes in cell wall expansion likely underlie reductions in growth rate in response to drought, and changes in known regulators of flowering time likely underlie altered reproductive transitions in response to elevated temperature and CO2. Genes that underlie most other organ or tissue-level responses have largely only been identified in a single species in response to a single stress and their level of conservation is unknown. We conclude that there is a need for further research regarding the molecular mechanisms of plant developmental responses to climate change factors in general, and that this lack of data is particularly prevalent in the case of interactive effects of multiple climate change factors. As future growing conditions will likely expose plants to multiple climate change factors simultaneously, with a sum negative influence on global agriculture, further research in this area is critical.

Biochemical acclimation, stomatal limitation and precipitation patterns underlie decreases in photosynthetic stimulation of soybean (Glycine max) at elevated [CO2] and temperatures under fully open air field conditions.

The net effect of elevated [CO2] and temperature on photosynthetic acclimation and plant productivity is poorly resolved. We assessed the effects of canopy warming and fully open air [CO2] enrichment on (1) the acclimation of two biochemical parameters that frequently limit photosynthesis (A), the maximum carboxylation capacity of Rubisco (Vc,max) and the maximum potential linear electron flux through photosystem II (Jmax), (2) the associated responses of leaf structural and chemical properties related to A, as well as (3) the stomatal limitation (l) imposed on A, for soybean over two growing seasons in a conventionally managed agricultural field in Illinois, USA. Acclimation to elevated [CO2] was consistent over two growing seasons with respect to Vc,max and Jmax. However, elevated temperature significantly decreased Jmax contributing to lower photosynthetic stimulation by elevated CO2. Large seasonal differences in precipitation altered soil moisture availability modulating the complex effects of elevated temperature and CO2 on biochemical and structural properties related to A. Elevated temperature also reduced the benefit of elevated [CO2] by eliminating decreases in stomatal limitation at elevated [CO2]. These results highlight the critical importance of considering multiple environmental factors (i.e. temperature, moisture, [CO2]) when trying to predict plant productivity in the context of climate change.

Global warming can negate the expected CO2 stimulation in photosynthesis and productivity for soybean grown in the Midwestern United States.

Extensive evidence shows that increasing carbon dioxide concentration ([CO2]) stimulates, and increasing temperature decreases, both net photosynthetic carbon assimilation (A) and biomass production for C3 plants. However the [CO2]-induced stimulation in A is projected to increase further with warmer temperature. While the influence of increasing temperature and [CO2], independent of each other, on A and biomass production have been widely investigated, the interaction between these two major global changes has not been tested on field-grown crops. Here, the interactive effect of both elevated [CO2] (approximately 585 µmol mol(-1)) and temperature (+3.5°C) on soybean (Glycine max) A, biomass, and yield were tested over two growing seasons in the Temperature by Free-Air CO2 Enrichment experiment at the Soybean Free Air CO2 Enrichment facility. Measurements of A, stomatal conductance, and intercellular [CO2] were collected along with meteorological, water potential, and growth data. Elevated temperatures caused lower A, which was largely attributed to declines in stomatal conductance and intercellular [CO2] and led in turn to lower yields. Increasing both [CO2] and temperature stimulated A relative to elevated [CO2] alone on only two sampling days during 2009 and on no days in 2011. In 2011, the warmer of the two years, there were no observed increases in yield in the elevated temperature plots regardless of whether [CO2] was elevated. All treatments lowered the harvest index for soybean, although the effect of elevated [CO2] in 2011 was not statistically significant. These results provide a better understanding of the physiological responses of soybean to future climate change conditions and suggest that the potential is limited for elevated [CO2] to mitigate the influence of rising temperatures on photosynthesis, growth, and yields of C3 crops.

Minirhizotron imaging reveals that nodulation of field-grown soybean is enhanced by free-air CO2 enrichment only when combined with drought stress.

The rate of N2 fixation by a leguminous plant is a product of the activity of individual nodules and the number of nodules. Initiation of new nodules and N2 fixation per nodule are highly sensitive to environmental conditions. However, the effects of global environmental change on nodulation in the field are largely unknown. It is also unclear whether legumes regulate nodulation in response to environment solely by varying root production or also by varying nodule density per unit of root length. This study utilised minirhizotron imaging as a novel in situ method for assessing the number, size and distribution of nodules in field-grown soybean (Glycine max (L.) Merr.) exposed to elevated atmospheric CO2 ([CO2]) and reduced precipitation. We found that nodule numbers were 134-229% greater in soybeans grown at elevated [CO2] in combination with reduced precipitation, and this response was driven by greater nodule density per unit of root length. The benefits of additional nodules were probably offset by an unfavourable distribution of nodules in shallow, dry soil in reduced precipitation treatment under elevated [CO2] but not ambient [CO2]. In fact, significant decreases in seed and leaf nitrogen concentration also occurred only in elevated [CO2] with reduced precipitation. This study demonstrates the potential of minirhizotron imaging to reveal previously uncharacterised changes in nodule production and distribution in response to global environmental change.

Spectral reflectance from a soybean canopy exposed to elevated CO2 and O3.

By affecting the physiology and structure of plant canopies, increasing atmospheric CO(2) and O(3) influence the capacity of agroecosystems to capture light and convert that light energy into biomass, ultimately affecting productivity and yield. The objective of this study was to determine if established remote sensing indices could detect the direct and interactive effects of elevated CO(2) and elevated O(3) on the leaf area, chlorophyll content, and photosynthetic capacity of a soybean canopy growing under field conditions. Large plots of soybean (Glycine max) were exposed to ambient air (∼380 µmol CO(2) mol(-1)), elevated CO(2) (∼550 µmol mol(-1)), elevated O(3) (1.2× ambient), and combined elevated CO(2) plus elevated O(3) at the soybean free air gas concentration enrichment (SoyFACE) experiment. Canopy reflectance was measured weekly and the following indices were calculated from reflectance data: near infrared/red (NIR/red), normalized difference vegetation index (NDVI), canopy chlorophyll content index (chl. index), and photochemical reflectance index (PRI). Leaf area index (LAI) also was measured weekly. NIR/red and LAI were linearly correlated throughout the growing season; however, NDVI and LAI were correlated only up to LAI values of ∼3. Season-wide analysis demonstrated that elevated CO(2) significantly increased NIR/red, PRI, and chl. index, indicating a stimulation of LAI and photosynthetic carbon assimilation, as well as delayed senescence; however, analysis of individual dates resolved fewer statistically significant effects of elevated CO(2). Exposure to elevated O(3) decreased LAI throughout the growing season. Although NIR/red showed the same trend, the effect of O(3) on NIR/red was not statistically significant. Season-wide analysis showed significant effects of O(3) on PRI; however, analysis of individual dates revealed that this effect was only statistically significant on two dates. Elevated O(3) had minimal effects on the total canopy chlorophyll index. PRI appeared to be more sensitive to decreased photosynthetic capacity of the canopy as a whole compared with previously published single leaf gas exchange measurements at SoyFACE, possibly because PRI integrates the reflectance signal of older leaves with accumulated O(3) damage and healthy young, upper canopy leaves, enabling detection of significant decreases in photosynthetic carbon assimilation which have not been detected in previous studies which measured gas exchange of upper canopy leaves. When the canopy was exposed to elevated CO(2) and O(3) simultaneously, the deleterious effects of elevated O(3) were diminished. Reflectance data, while less sensitive than direct measurements of physiological/structural parameters, corroborate direct measurements of LAI and photosynthetic gas exchange made during the same season, as well as results from previous years at SoyFACE, demonstrating that these indices accurately represent structural and physiological effects of changing tropospheric chemistry on soybean growing in a field setting.