Perspectives on improving light distribution and light use efficiency in crop canopies.

Plant stands in nature differ markedly from most seen in modern agriculture. In a dense mixed stand, plants must vie for resources, including light, for greater survival and fitness. Competitive advantages over surrounding plants improve fitness of the individual, thus maintaining the competitive traits in the gene pool. In contrast, monoculture crop production strives to increase output at the stand level and thus benefits from cooperation to increase yield of the community. In choosing plants with higher yields to propagate and grow for food, humans may have inadvertently selected the best competitors rather than the best cooperators. Here, we discuss how this selection for competitiveness has led to overinvestment in characteristics that increase light interception and, consequently, sub-optimal light use efficiency in crop fields that constrains yield improvement. Decades of crop canopy modeling research have provided potential strategies for improving light distribution in crop canopies, and we review the current progress of these strategies, including balancing light distribution through reducing pigment concentration. Based on recent research revealing red-shifted photosynthetic pigments in algae and photosynthetic bacteria, we also discuss potential strategies for optimizing light interception and use through introducing alternative pigment types in crops. These strategies for improving light distribution and expanding the wavelengths of light beyond those traditionally defined for photosynthesis in plant canopies may have large implications for improving crop yield and closing the yield gap.

The effect of increasing temperature on crop photosynthesis: from enzymes to ecosystems.

As global land surface temperature continues to rise and heatwave events increase in frequency, duration, and/or intensity, our key food and fuel cropping systems will likely face increased heat-related stress. A large volume of literature exists on exploring measured and modelled impacts of rising temperature on crop photosynthesis, from enzymatic responses within the leaf up to larger ecosystem-scale responses that reflect seasonal and interannual crop responses to heat. This review discusses (i) how crop photosynthesis changes with temperature at the enzymatic scale within the leaf; (ii) how stomata and plant transport systems are affected by temperature; (iii) what features make a plant susceptible or tolerant to elevated temperature and heat stress; and (iv) how these temperature and heat effects compound at the ecosystem scale to affect crop yields. Throughout the review, we identify current advancements and future research trajectories that are needed to make our cropping systems more resilient to rising temperature and heat stress, which are both projected to occur due to current global fossil fuel emissions.

The Impacts of Fluctuating Light on Crop Performance.

Rapidly changing light conditions can reduce carbon gain and productivity in field crops because photosynthetic responses to light fluctuations are not instantaneous. Plant responses to fluctuating light occur across levels of organizational complexity from entire canopies to the biochemistry of a single reaction and across orders of magnitude of time. Although light availability and variation at the top of the canopy are largely dependent on the solar angle and degree of cloudiness, lower crop canopies rely more heavily on light in the form of sunflecks, the quantity of which depends mostly on canopy structure but also may be affected by wind. The ability of leaf photosynthesis to respond rapidly to these variations in light intensity is restricted by the relatively slow opening/closing of stomata, activation/deactivation of C3 cycle enzymes, and up-regulation/down-regulation of photoprotective processes. The metabolic complexity of C4 photosynthesis creates the apparently contradictory possibilities that C4 photosynthesis may be both more and less resilient than C3 to dynamic light regimes, depending on the frequency at which these light fluctuations occur. We review the current understanding of the underlying mechanisms of these limitations to photosynthesis in fluctuating light that have shown promise in improving the response times of photosynthesis-related processes to changes in light intensity.

Chlorophyll Can Be Reduced in Crop Canopies with Little Penalty to Photosynthesis.

The hypothesis that reducing chlorophyll content (Chl) can increase canopy photosynthesis in soybeans was tested using an advanced model of canopy photosynthesis. The relationship among leaf Chl, leaf optical properties, and photosynthetic biochemical capacity was measured in 67 soybean (Glycine max) accessions showing large variation in leaf Chl. These relationships were integrated into a biophysical model of canopy-scale photosynthesis to simulate the intercanopy light environment and carbon assimilation capacity of canopies with wild type, a Chl-deficient mutant (Y11y11), and 67 other mutants spanning the extremes of Chl to quantify the impact of variation in leaf-level Chl on canopy-scale photosynthetic assimilation and identify possible opportunities for improving canopy photosynthesis through Chl reduction. These simulations demonstrate that canopy photosynthesis should not increase with Chl reduction due to increases in leaf reflectance and nonoptimal distribution of canopy nitrogen. However, similar rates of canopy photosynthesis can be maintained with a 9% savings in leaf nitrogen resulting from decreased Chl. Additionally, analysis of these simulations indicate that the inability of Chl reductions to increase photosynthesis arises primarily from the connection between Chl and leaf reflectance and secondarily from the mismatch between the vertical distribution of leaf nitrogen and the light absorption profile. These simulations suggest that future work should explore the possibility of using reduced Chl to improve canopy performance by adapting the distribution of the "saved" nitrogen within the canopy to take greater advantage of the more deeply penetrating light.

Carbon assimilation in crops at high temperatures.

Global temperatures are rising, and higher rates of temperature increase are projected over land areas that encompass the globe's major agricultural regions. In addition to increased growing season temperatures, heat waves are predicted to become more common and severe. High temperatures can inhibit photosynthetic carbon gain of crop plants and thus threaten productivity, the effects of which may interact with other aspects of climate change. Here, we review the current literature assessing temperature effects on photosynthesis in key crops with special attention to field studies using crop canopy heating technology and in combination with other climate variables. We also discuss the biochemical reactions related to carbon fixation that may limit crop photosynthesis under warming temperatures and the current strategies for adaptation. Important progress has been made on several adaptation strategies demonstrating proof-of-concept for translating improved photosynthesis into higher yields. These are now poised to test in important food crops.

Yield response of field-grown soybean exposed to heat waves under current and elevated [CO2 ].

Elevated atmospheric CO2 concentration ([CO2 ]) generally enhances C3 plant productivity, whereas acute heat stress, which occurs during heat waves, generally elicits the opposite response. However, little is known about the interaction of these two variables, especially during key reproductive phases in important temperate food crops, such as soybean (Glycine max). Here, we grew soybean under elevated [CO2 ] and imposed high- (+9°C) and low- (+5°C) intensity heat waves during key temperature-sensitive reproductive stages (R1, flowering; R5, pod-filling) to determine how elevated [CO2 ] will interact with heat waves to influence soybean yield. High-intensity heat waves, which resulted in canopy temperatures that exceeded optimal growth temperatures for soybean, reduced yield compared to ambient conditions even under elevated [CO2 ]. This was largely due to heat stress on reproductive processes, especially during R5. Low-intensity heat waves did not affect yields when applied during R1 but increased yields when applied during R5 likely due to relatively lower canopy temperatures and higher soil moisture, which uncoupled the negative effects of heating on cellular- and leaf-level processes from plant-level carbon assimilation. Modeling soybean yields based on carbon assimilation alone underestimated yield loss with high-intensity heat waves and overestimated yield loss with low-intensity heat waves, thus supporting the influence of direct heat stress on reproductive processes in determining yield. These results have implications for rain-fed cropping systems and point toward a climatic tipping point for soybean yield when future heat waves exceed optimum temperature.

Photosynthetic energy conversion efficiency: setting a baseline for gauging future improvements in important food and biofuel crops.

The conversion efficiency (ε(c)) of absorbed radiation into biomass (MJ of dry matter per MJ of absorbed photosynthetically active radiation) is a component of yield potential that has been estimated at less than half the theoretical maximum. Various strategies have been proposed to improve ε(c), but a statistical analysis to establish baseline ε(c) levels across different crop functional types is lacking. Data from 164 published ε(c) studies conducted in relatively unstressed growth conditions were used to determine the means, greatest contributors to variation, and genetic trends in ε(c )across important food and biofuel crop species. ε(c) was greatest in biofuel crops (0.049-0.066), followed by C4 food crops (0.046-0.049), C3 nonlegumes (0.036-0.041), and finally C3 legumes (0.028-0.035). Despite confining our analysis to relatively unstressed growth conditions, total incident solar radiation and average growing season temperature most often accounted for the largest portion of ε(c) variability. Genetic improvements in ε(c), when present, were less than 0.7% per year, revealing the unrealized potential of improving ε(c) as a promising contributing strategy to meet projected future agricultural demand.

Light sheet microscopy reveals more gradual light attenuation in light-green versus dark-green soybean leaves.

Light wavelengths preferentially absorbed by chlorophyll (chl) often display steep absorption gradients. This over-saturates photosynthesis in upper chloroplasts and deprives lower chloroplasts of blue and red light. Reducing chl content could create a more even leaf light distribution and thereby increase leaf light-use efficiency and overall canopy photosynthesis. This was tested on soybean cultivar 'Clark' (WT) and a near-isogenic chl b deficient mutant, Y11y11, grown in controlled environment chambers and in the field. Light attenuation was quantified using a novel approach involving light sheet microscopy. Leaf adaxial and abaxial surfaces were illuminated separately with blue, red, and green wavelengths, and chl fluorescence was detected orthogonally to the illumination plane. Relative fluorescence was significantly greater in deeper layers of the Y11y11 mesophyll than in WT, with the greatest differences in blue, then red, and finally green light when illuminated from the adaxial surface. Modeled relative photosynthesis based on chlorophyll profiles and Beer's Law predicted less steep gradients in mutant relative photosynthesis rates compared to WT. Although photosynthetic light-use efficiency was greater in the field-grown mutant with ~50% lower chl, light-use efficiency was lower in the mutant when grown in chambers where chl was ~80% reduced. This difference is probably due to pleiotropic effects of the mutation that accompany very severe reductions in chlorophyll and may warrant further testing in other low-chl lines.

A meta-analysis of responses of canopy photosynthetic conversion efficiency to environmental factors reveals major causes of yield gap.

Improving plant energy conversion efficiency (εc) is crucial for increasing food and bioenergy crop production and yields. Using a meta-analysis, the effects of greenhouse gases, weather-related stresses projected to intensify due to climate change, and management practices including inputs, shading, and intercropping on εc were statistically quantified from 140 published studies to identify where improvements would have the largest impact on closing yield gaps. Variation in the response of εc to treatment type and dosage, plant characteristics, and growth conditions were also examined. Significant mean increases in εc were caused by elevated [CO2] (20%), shade (18%), and intercropping (15%). εc increased curvilinearly up to 55% with nitrogen additions whereas phosphorus application was most beneficial at low levels. Significant decreases in εc of -8.4% due to elevated [O3], -16.8% due to water stress, and -6.5% due to foliar damage were found. A non-significant decrease in εc of -17.3% was caused by temperature stress. These results identify the need to engineer greater stress tolerance and enhanced responses to positive factors such as [CO2] and nitrogen to improve average yields and yield potential. Optimizing management strategies will also enhance the benefits possible with intercropping, shade, and pest resilience. To determine optimal practices for εc improvement, further studies should be conducted in the field since several responses were exaggerated by non-field experimental conditions.

Field-grown soybean transcriptome shows diurnal patterns in photosynthesis-related processes.

Many plant physiological processes have diurnal patterns regulated by diurnal environmental changes and circadian rhythms, but the transcriptional underpinnings of many of these cycles have not been studied in major crop species under field conditions. Here, we monitored the transcriptome of field-grown soybean (Glycine max) during daylight hours in the middle of the growing season with RNA-seq. The analysis revealed 21% of soybean genes were differentially expressed over the course of the day. Expression of some circadian-related genes in field-grown soybean differed from previously reported expression patterns measured in controlled environments. Many genes in functional groups contributing to and/or depending on photosynthesis showed differential expression, with patterns particularly evident in the chlorophyll synthesis pathway. Gene regulatory network inference also revealed seven diurnally sensitive gene nodes involved with circadian rhythm, transcription regulation, cellular processes, and water transport. This study provides a diurnal overview of the transcriptome for an economically important field-grown crop and a basis for identifying pathways that could eventually be tailored to optimize diurnal regulation of carbon gain.

Photosynthesis, Light Use Efficiency, and Yield of Reduced-Chlorophyll Soybean Mutants in Field Conditions.

Reducing chlorophyll (chl) content may improve the conversion efficiency of absorbed photosynthetically active radiation into biomass and therefore yield in dense monoculture crops by improving light penetration and distribution within the canopy. The effects of reduced chl on leaf and canopy photosynthesis and photosynthetic efficiency were studied in two reportedly robust reduced-chl soybean mutants, Y11y11 and y9y9, in comparison to the wild-type (WT) "Clark" cultivar. Both mutants were characterized during the 2012 growing season whereas only the Y11y11 mutant was characterized during the 2013 growing season. Chl deficiency led to greater rates of leaf-level photosynthesis per absorbed photon early in the growing season when mutant chl content was ∼35% of the WT, but there was no effect on photosynthesis later in the season when mutant leaf chl approached 50% of the WT. Transient benefits of reduced chl at the leaf level did not translate to improvements in canopy-level processes. Reduced pigmentation in these mutants was linked to lower water use efficiency, which may have dampened any photosynthetic benefits of reduced chl, especially since both growing seasons experienced significant drought conditions. These results, while not confirming our hypothesis or an earlier published study in which the Y11y11 mutant significantly outyielded the WT, do demonstrate that soybean significantly overinvests in chl. Despite a >50% chl reduction, there was little negative impact on biomass accumulation or yield, and the small negative effects present were likely due to pleiotropic effects of the mutation. This outcome points to an opportunity to reinvest nitrogen and energy resources that would otherwise be used in pigment-proteins into increasing biochemical photosynthetic capacity, thereby improving canopy photosynthesis and biomass production.

Identical substitutions in magnesium chelatase paralogs result in chlorophyll-deficient soybean mutants.

The soybean [Glycine max (L.) Merr.] chlorophyll-deficient line MinnGold is a spontaneous mutant characterized by yellow foliage. Map-based cloning and transgenic complementation revealed that the mutant phenotype is caused by a nonsynonymous nucleotide substitution in the third exon of a Mg-chelatase subunit gene (ChlI1a) on chromosome 13. This gene was selected as a candidate for a different yellow foliage mutant, T219H (Y11y11), that had been previously mapped to chromosome 13. Although the phenotypes of MinnGold and T219H are clearly distinct, sequencing of ChlI1a in T219H identified a different nonsynonymous mutation in the third exon, only six base pairs from the MinnGold mutation. This information, along with previously published allelic tests, were used to identify and clone a third yellow foliage mutation, CD-5, which was previously mapped to chromosome 15. This mutation was identified in the ChlI1b gene, a paralog of ChlI1a. Sequencing of the ChlI1b allele in CD-5 identified a nonsynonymous substitution in the third exon that confers an identical amino acid change as the T219H substitution at ChlI1a. Protein sequence alignments of the two Mg-chelatase subunits indicated that the sites of amino acid modification in MinnGold, T219H, and CD-5 are highly conserved among photosynthetic species. These results suggest that amino acid alterations in this critical domain may create competitive inhibitory interactions between the mutant and wild-type ChlI1a and ChlI1b proteins.

Segregation distortion in a region containing a male-sterility, female-sterility locus in soybean.

In diploid segregation, each alternative allele has a 50% chance of being passed on to the offspring. Mutations in genes involved in the process of meiotic division or early stages of reproductive cell development can affect allele frequency in the gametes. In addition, competition among gametes and differential survival rates of gametes can lead to segregation distortion. In a recent transformation study, a male-sterile, female-sterile (MSFS) mutant was identified in the soybean cultivar, Williams. The mutant in heterozygous condition segregated 3 fertile:1 sterile in the progeny confirming monogenic inheritance. To map the lesion, we generated an F(2) mapping population by crossing the mutant (in heterozygous condition) with Minsoy (PI 27890). The F(2) progeny showed strong segregation distortion against the MSFS phenotype. The objectives of our study were to molecularly map the gene responsible for sterility in the soybean genome, to determine if the MSFS gene is a result of T-DNA insertion during Agrobacterium-mediated transformation, and to map the region that showed distorted segregation. The fertility/sterility locus was mapped to molecular linkage group (MLG) D1a (chromosome Gm01) using bulked segregant analysis. The closest marker, Satt531, mapped 9.4cM from the gene. Cloning of insertion sites for T-DNA in the mutant plants revealed that there are two copies of T-DNA in the genome. Physical locations of these insertion sites do not correlate with the map location of the MSFS gene, suggesting that MSFS mutation may not be associated with T-DNA insertions. Segregation distortion was most extreme at or around the st_A06-2/6 locus suggesting that sterility and segregation distortion are tightly linked attributes. Our results cue that the distorted segregation may be due to a gamete elimination system.