IntroductionIn the absence of global change, it is estimated that the world will need up to 56% more food produced by 2050 relative to 20101. This requirement will be substantially elevated by crop losses caused by increasing extreme climate events2. Current rates of crop yield increase are insufficient to meet this future requirement and new innovations are therefore needed. Photosynthesis, given its low efficiency in crops relative to the theoretical maximum, has emerged as a promising target for bioengineering. Transgenic up-regulation of specific photosynthetic enzymes has already been shown to increase photosynthesis and in turn the yields of rice and soybean in the field3,4. Here we demonstrate a different approach that would substantially increase crop photosynthetic productivity.Higher plant photosynthesis is primarily driven by photons in the visible spectrum (400–700 nm). While photons in the far-red (FR) spectral region (700–800 nm) are generally insufficient to sustain the full operation of the entire photosynthetic electron transport chain, since they are not absorbed by Photosystem II, FR photons contain sufficient energy to drive charge separation in reaction centers and, in turn, CO2 assimilation5. Indeed, some species of cyanobacteria grow autotrophically in FR light6,7,8, and do so using different strategies9.These cyanobacteria modify pigment type and composition in response to an increasing ratio of FR to visible light in a process called far-red light photoacclimation (FaRLiP). In visible light, they use chlorophyll a (Chl a), as in higher plants, but when grown in environments depleted of visible light but rich in FR light, the longer-wavelength-absorbing chlorophyll d (Chl d) and f (Chl f) are synthesized10. For example, when grown under FR light, the FaRLiP-capable cyanobacterium, Chroococcidiopsis thermalis contains ~90% Chl a, ~10% Chl f, and 90%), independent of the growth radiant energy spectrum, and have a far larger capacity to use FR light of up to 750 nm for photosynthesis8,17. The almost exclusive presence of Chl d results in a high energetic connectivity in both photosystems of Acaryochloris, which therefore reach higher photochemical yields than the photosystems of Chroococcidiopsis thermalis15,18.Incorporation of the FR light adaptations of these cyanobacteria into crop plants has been frequently suggested as a potential strategy to increase photosynthesis and crop productivity, thereby improving crop yields9,19. However, the magnitude of this benefit has not previously been estimated, despite this being key in determining how worthwhile such an effort would be versus the other opportunities for increasing crop yields via improving other steps of the photosynthetic process20.Adding far-red absorbing capacity would likely have different effects across the canopy, which need to be taken into account. Leaves at the top of crop canopies capture most (80–90%) incoming visible light and their photosynthesis can be light-saturated for much of the day. Therefore, in full sunlight, capturing the additional energy of FR light in these already photon-saturated leaves would only increase the probability of photodamage. However, in modern crop canopies with several layers of leaves, those in the lower canopy are starved of visible photons for most of the day, excepting a few sunflecks, and so contribute little to crop photosynthesis, net carbon gain, and yield21. Leaves transmit >90% of FR photons, so while these lower canopy leaves are starved of visible photons, they are bathed in FR photons22. As such, the ratio of FR/visible photons rises from 90%)33,34,35, effectively utilizing FR from 700 to 750 nm. Second, FaRLiP cyanobacteria like Chroococcidiopsis thermalis, containing mostly Chl a and small amounts of Chl f (ca. 10%), can utilize FR light from 700 to 800 nm5. These cyanobacterial approaches were independently evaluated using a soybean canopy model to focus on photon absorption and photosynthetic efficiency over the course of a day, providing a basis for generalized predictions in other crops. Our simulations indicated that incorporating Chl d and Chl f into plants could increase productivity by as much as 26%, which if achieved would be massive compared to current rates of improvement of around 1–2% per year, and achieved only in the most intensively bred crops36.By incorporating Chl d into photosynthetic proteins (photosystems and antenna), the FR absorption of leaves could be dramatically increased. In particular, the measurements on Acaryochloris marina cells have shown that Chl d-containing photosynthetic proteins potentially absorb 86% of FR photons (701–750 nm, Supplementary Fig. 1c and Supplementary Table 1). Using this FR absorption fraction as the maximum limit, we explored two FR utilization strategies in crop canopies: constant leaf FR absorption fraction across the canopy (Strategy 1, Fig. 3a) and increasing absorption as the FR/R photon ratio rises with depth into the canopy (Strategy 2, Fig. 3b). Strategy 2 focuses on enhancing FR absorption predominantly in the middle and lower parts of the canopy (Fig. 3d), where leaves typically receive limited visible light. This targeted increase in light absorption (Fig. 3b), effectively improves photon distribution throughout the canopy. The strategy results in an estimated 13.7% increase in the net daily canopy CO2 assimilation (Ac), with an 11.6% increase in light absorption (Supplementary Table 2, Fig. 3g, h). While the increase in Ac is similar for both strategies, Strategy 2 reduces the risk of photoinhibition, photodamage and heating of the uppermost leaves, presenting a significant advantage over Strategy 1.Incorporating Chl f into crop leaves could enable absorption and utilization of a broader FR range, from 700 up to 800 nm. However, given that Chl f comprises only about 10% of the total Chl content in Chroococcidiopsis thermalis, we mimicked this strategy by limiting the amount of Chl f incorporated into crop leaves. Our simulations suggest that even a low absorption fraction of 0.1 could boost Ac up to 18.4% (Fig. 4a, Supplementary Table 3). If Chl f’s induction is also linked to FR/R increase with depth into the canopy (as with Strategy 2 of Chl d), simulated daily Ac increases to 26.1 % for upper wavelength limits of 800 nm (Supplementary Table 3).To optimize the use of FR photons in photosynthesis through Chl d and Chl f, we evaluated the impact of these chlorophylls across various growth stages. Inducing Chl d/f at vegetative stage might not be fully beneficial (Fig. 2 and Supplementary Fig. 3) as the canopy isn’t fully developed and light penetration is not yet limited. Additionally, the water uses efficiency declines with increased absorption of FR photon, which could adversely affect soybean growth in regions with inadequate precipitation or limited irrigation capacity. Our proposed Strategy 2 involves enhancing the expression of Chl d or Chl f at the reproductive stage, particularly in the lower parts of the canopy where there are less visible photons but a higher proportion of FR photons. Adjusting the expression levels of Chl d or Chl f in response to the FR/R ratio can significantly improve light use efficiency of the canopy (Supplementary Tables 2 and 3). The improvement in CO2 assimilation can be achieved under well-watered conditions, as transpiration may also rise with increased light absorption. However, the overall water use efficiency of the modified soybean canopy shows a slight improvement (Supplementary Tables 2 and 3), which slightly reduces the cost of water used per unit of CO2 assimilation. Consequently, this strategy not only boosts productivity but also has the potential to enhance yield per unit of water used, i.e. increase sustainability.This adaptive expression can be mediated by phytochromes, which are light-sensing proteins found in both plants and cyanobacteria37. FaRLiP cyanobacteria use the red/far-red, knotless phytochrome, RfpA, to detect FR light and trigger the signal cascade that allows transcription of the FaRLiP gene cluster which results in the accumulation of Chl f in the photosystems. Similarly, plants phytochromes similarly detect shade through changes in the ratio of FR/R, triggering specific gene expression responses to adapt to light conditions38. Leveraging phytochrome-mediated transcriptional regulation provides a practical method to bioengineer increased Chl d or Chl f content as shade intensifies with depth into the canopy19,39.We have shown how incorporation of FR absorbing chlorophylls could increase crop carbon assimilation by 26% in the critical pod-filling phase of soybean growth. A perennial question is whether increased photosynthesis will actually result in increased yield. For soybean, as for wheat and rice, countless experiments have shown that when photosynthesis is artificially increased by elevation of CO2 concentration around the crop in the field a concomitant increase in yield is obtained40,41,42. Similarly, where photosynthetic efficiency has been increased by transgenic modifications significant yield increases have been achieved in the field3,4,43. One concern is that more yield will require more resource, in particular nitrogen. When soybean photosynthesis, and in turn yield, was increased by transgenic improvement of photosynthesis or in separate experiments by season-long growth in the field under elevated CO2 the protein and nitrogen content of the seed was unchanged, despite yield increases of 20% or more4,40,44. Since, in common with agronomic practice, no fertilizer was added in these field experiments, this parallel increase in nitrogen could only be explained by a portion of the additional photosynthate fueling additional N-fixation by the associated root-nodule Bradyrhizobia.Introducing Chl d and Chl f into plant leaves will involve two primary steps: biosynthesis of these chlorophylls and their subsequent integration into plant photosystems. The biosynthesis of Chl d and Chl f is considered feasible based on their structural differences from Chl a: Chl d differs from Chl a with a formyl group replacing the ethenyl group at the C3 site and Chl f has a formyl group in place of the methyl group at the C2 site. The enzyme that converts Chl a to Chl f in cyanobacteria, Chl f synthase (ChlF), has been identified as a paralog of the D1 (PsbA) protein of the photosystem II45. Transgenic expression of the ChlF protein in Synechocystis sp. PCC 6803 and Synechococcus sp. PCC 7002 resulted in the synthesis of Chl f45,46. The enzyme for Chl d synthesis is unknown, but it is hypothesized that Chl d can be synthesized from Chl a in a single step utilizing molecular oxygen47,48. These results suggest that bioengineering crops to produce Chl f or Chl d (once the enzyme is known) would only require the expression of a single gene.However, efficient FR photon utilization in crops requires not only the synthesis of these chlorophylls but also their integration into remodeled photosynthetic complexes. This requires designing pigment binding sites selective for Chl d and f. In this respect, it is promising that experimental studies have shown that the proteins of in vitro assembled plant light-harvesting complexes can bind Chl d and Chl f at specific sites49,50. Fine tuning of the binding sites to enhance their affinity for specific Chls and further shift their absorption into the far-red is underway51, guided by the analysis of the Chl d and f binding sites of far-red photosystems18.Furthermore, to ensure high light-harvesting and electron transport efficiency, the number and location of the far-red absorbing pigments should be carefully considered18,21. This is particularly important because the harvested energy must be quickly transferred to the reaction center to maximize conversion efficiency. To ensure a high trapping efficiency within the engineered plant photosystems, it may also be necessary to engineer Chl d/f binding sites within the reaction centers of both photosystems, creating red-shifted primary donors analogous to those found in A. marina or FaRLiP cyanobacterial photosystems. Interestingly, PSII from A. marina and FaRLiP cyanobacteria have evolved different strategies to perform charge separation with lower energy photons. A. marina PSII maximizes charge separation efficiency at the expense of increased recombination reactions, while FaRLiP PSII takes the opposite approach. In an engineered plant PSII containing Chl d/f as the primary donor, there is the potential to engineer an approach that is a hybrid of the two aforementioned scenarios. Although this aspect remains to be experimentally verified, the results here now show this would be of great value.The question that initiated this study was whether the considerable effort needed in discovery and translation to implement longer wavelength chlorophylls in crops would be valuable. The clear answer from this analysis is that it would be immensely valuable. Indeed, if the daunting challenge of providing sufficient food in the second half of this century is to be met, all efforts are needed whether increasing photosynthetic efficiency, improved crop protection, environmental tolerance or agronomy42. Under ideal growing conditions, crop biomass production is determined by the amount of sunlight photons captured and the efficiency with which these are transduced into carbon assimilation52. Incorporating Chl d/f increases the number of utilizable photons for crops. Recent findings have identified many optimization targets to improve leaf photosynthetic conversion efficiency under high light conditions32,52,53, including manipulating CO2 diffusion54, increasing the content or the turnover number of Rubisco3,55,56, engineering photorespiratory bypasses57, and integrating algal, cyanobacterial or C4 CO2 concentration mechanisms into C3 plants58,59. However, in the field, photosynthesis, especially in the middle and lower canopy parts, is often light-limited. Enhancing the absorption and utilization of FR light by leaves can mitigate light limitation of the leaves in the middle and lower canopy. Therefore, combining the changes listed above that increase light-saturated photosynthesis with use of FR light would be synergistic, providing a greater scope for improving canopy photosynthetic efficiency and much needed increases in yield potential, implementable across most crops.MethodsThe photon flux density of FR at earth surfaceThe distributions of energy density (I; J m−2 s−1 nm−1) of a solar spectrum (ASTM G173-03, https://www.nrel.gov/grid/solar-resource/spectra-am1.5.html, The AM1.5 Global tilt) was used to calculate the photon flux density (Q; mol m−2 s−1) at each wavelength (Fig. 1):$$Q=\frac{I\lambda }{{hc}{N}_{A}}$$(1)where λ is wavelength (m); c the speed of light (3.00 × 108 m s−1); NA Avogadro’s number (6.02 × 1023 mol−1); and h Planck’s constant (6.626 ×10−34 J s). The receiving surface is defined in the standards as an inclined plane at 37° tilt toward the equator, facing the sun.The light distribution in a soybean canopyStem positions, leaf lengths, widths, petiole lengths and angles for trifoliate leaves were measured from soybean plants (Glycine max L. Merr., Pioneer 93B15) growing on the University of Illinois South Farms. Plants were sampled at multiple developmental stages during the whole growing season from the day of year (DOY) 168 to 26760. Following standard agronomic practice, the row spacing of the canopy was 38 cm, and plant spacing within the rows 10 cm (Supplementary Fig. 7). From this the 3D architecture of the crop canopy was recreated. The surface of each leaf was divided into ‘pixels’ of approximately 1 cm260,61. Photon fluxes for each wavelength range (blue, green, red, and FR) were calculated for each leaf ‘pixel’ at hourly intervals from 06:00 – 18:00 on Aug 18th, 2023, in Champaign IL, US (40.11 N, 88.21 W) using a forward ray-tracing algorithm (FastTracer)62. At every hour, the direct and diffuse light entering and within the canopy is predicted together with scattered radiation due to reflection from, and transmission through, the leaves within the canopy. Leaf reflectance and transmission were specified separately for each wavelength category (blue, green, red, and FR) according to parameters listed in Table 1. The total absorbed photon flux density (Qabs, Eq. (2)) for each leaf ‘pixel’ was computed by summing the absorbed fluxes from all wavelength ranges.$${Q}_{{abs}}={Q}_{{abs}{{\_}}B}+{Q}_{{abs}{{\_}}G}{+Q}_{{abs}{{\_}}R}+{Q}_{{abs}{{\_}}{FR}}$$(2)where \({Q}_{{abs\_B}},\,{Q}_{{abs\_G}}{,{Q}}_{{abs\_R}}\,{\rm{and}}\,{Q}_{{abs\_FR}}\) are absorbed blue, green, red, and far-red light respectively. Atmospheric transmittance was set as 0.80 to estimate the incident direct and diffuse photon fluxes reaching the top of the canopy at each time point on a sunny day.Leaf ecophysiologyThe leaf‐level ecophysiology model63 used in this study couples the physical and biochemical processes that regulate photosynthesis and gas exchange. Specifically, the model simultaneously calculates the boundary layer conductance to vapor and heat, leaf temperature, transpiration (E), net CO2 assimilation (A), intercellular CO2 concentration (Ci), and stomatal conductance (gs) under different environmental conditions. It was implemented across all canopy “pixels” in the 3D model.A of soybean leaf is described by the steady-state FvCB biochemical model photosynthetic CO2 assimilation64. Here, A is assumed to be constrained by either RuBP carboxylase-oxygenase (Rubisco) activity (\({W}_{c}\)) or by the rate of ribulose-1,5-bisphosphate (RuBP) regeneration (\({W}_{j}\)):$$A=min \left({W}_{c},\,{W}_{j}\right)\left(1-\frac{{\varGamma }^{*}}{{C}_{i}}\right)-{R}_{d}$$(3)$${W}_{c}=\frac{{V}_{{cmax}}\cdot {C}_{i}}{{C}_{i}+{K}_{c}(1+\frac{O}{{K}_{o}})}$$(4)$${W}_{j}=\frac{J\cdot {C}_{i}}{4.5{C}_{i}+10.5{\varGamma }^{*}}$$(5)where Γ* is the chloroplast CO2 partial pressure when both Rd and CO2 assimilation are equal such that net A = 0, Rd is mitochondrial respiration. Vcmax is the maximum rate of carboxylation, Kc and Ko are the Michaelis-Menten constants of Rubisco for CO2 and O2, respectively, and O is the oxygen concentration. Photosynthesis is more likely limited by ATP availability rather than NADPH (Supplementary Note 1, Supplementary Figs. 8 and 9), hence we use the ATP limited Wj equation (Eq. (5)). The electron transport rate (J) is described by a non-rectangular hyperbolic function65:$$J=\frac{{Q}_{2}+{J}_{max }-\sqrt{{\left({Q}_{2}+{J}_{max }\right)}^{2}-4\theta \,{Q}_{2}\,{J}_{max }}}{2\theta }$$(6)$${Q}_{2}={0.5Q}_{{abs}}{\varPhi }_{{PSII}}$$(7)\({Q}_{{abs}}\) is the amount of absorbed photosynthetically active photon flux available for electron transport (Eq. (2)). ΦPSII, the maximum quantum yield of photosystem II; θ is a curvature factor. 0.5 represent the proportion of \({Q}_{{abs}}\) that reaches photosystem II51. Parameters and values are listed in Supplementary Table 4.Canopy photosynthesis and water use efficiencyNet canopy CO2 assimilation was calculated by summing A values of all leaves ‘pixels’ over the daylight hours (Eq. (8)).$${Ac}=\frac{\sum ({A}_{i}\cdot {S}_{i})}{{S}_{{ground}}}$$(8)where Sground represents the ground area occupied by the simulated canopy (Supplementary Fig. 7). Ai is net leaf CO2 assimilation rate of a leaf pixel (i), and Si is the corresponding leaf area of the leaf pixel. Canopy transpiration (Ec) was similarly calculated by summing transpiration rate of every leaf pixel (Ei) using Eq. (9)$${Ec}=\frac{\sum ({E}_{i}\cdot {S}_{i})}{{S}_{{ground}}}$$(9)Water use efficiency (WUE) of the canopy was calculated as the ratio of Ac to Ec (Eq. (10)):$${WUE}=\frac{{Ac}}{{Ec}}$$(10)Simulations were conducted in MATLAB 2019a (Mathworks, https://uk.mathworks.com).The measurement of reflectance and transmittance spectra of Chlorophyll dAcaryochloris marina MBIC 11017 was photoautotrophically grown in IMK medium at 25 °C at a constant irradiance of 20 μE m−2 s−1. Chl d was extracted from A. marina cells using 100% ice-cold methanol and incubated in dark at 4 °C for 15 min48, samples were then centrifuged, and the clear supernatant was collected for subsequent measurement. Transmittance spectra of Chl d in methanol were measured using at room temperature on a Cary 4000 UV–VIS spectrophotometer. Room-temperature absorption spectra of A. marina cells were measured on Cary 4000 UV–Vis-spectrophotometer equipped with an integrating diffuse reflectance sphere (DRA-CA-50, Labsphere) to correct for light scattering.Both Acaryochloris cell suspensions and extracted Chl d in methanol were diluted to various concentrations for measuring their reflectance and transmittance spectra (Supplementary Fig. 1). Reflectance and transmittance values at an Optical Density of 5 (at 350–800 nm) were estimated using linear interpolation (interp1 function in MATLAB).Reporting summaryFurther information on research design is available in the Nature Portfolio Reporting Summary linked to this article.Data availabilityAll reflectance and transmittance spectra data are provided in Supplementary Information file. Source data are provided with this paper.Code availabilityCode that supports the findings of this study are available at GitHub [https://github.com/yuwangcn/Chld_Chlf_in_soybean].ReferencesVan Dijk, M., Morley, T., Rau, M. L. & Saghai, Y. A meta-analysis of projected global food demand and population at risk of hunger for the period 2010–2050. Nat. Food 2, 494–501 (2021).Google Scholar Hasegawa, T. et al. Extreme climate events increase risk of global food insecurity and adaptation needs. Nat. Food 2, 587–595 (2021).Google Scholar Yoon, D.-K. et al. 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Biochemical models of leaf photosynthesis (CSIRO Publishing, 2000).Download referencesAcknowledgementsWe thank Edward Lochocki, Lynn Doran, Elena Pelech, Coralie Salesse-Smith, Cindy Chan and Jeff Hansen for their comments and advice on earlier versions of this manuscript. Award number 1-612289, S.L. is supported by Stanley O. Ikenberry Endowment. Grant number 714.018.001, R.C. and T.O. are supported by the Dutch organization for Scientific research (NWO) via a TOP grant.Author informationAuthors and AffiliationsSchool of Life Sciences, Nanjing University, Nanjing, Jiangsu, ChinaYu WangCarl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USAYu Wang & Stephen P. LongDepartment of Physics and Astronomy, Faculty of Science, Vrije Universiteit Amsterdam, Amsterdam, The NetherlandsThomas J. Oliver & Roberta CroceDepartments of Plant Biology and of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USAStephen P. LongAuthorsYu WangView author publicationsSearch author on:PubMed Google ScholarThomas J. OliverView author publicationsSearch author on:PubMed Google ScholarRoberta CroceView author publicationsSearch author on:PubMed Google ScholarStephen P. LongView author publicationsSearch author on:PubMed Google ScholarContributionsY.W., R.C. and S.P.L. designed the study. Y.W. performed computational analysis. T.O. conducted the measurements of reflectance and transmittance spectra of Chl d. Y.W., T.O., R.C. and S.P.L. wrote the paper.Corresponding authorsCorrespondence to Yu Wang or Stephen P. Long.Ethics declarationsCompeting interestsThe authors declare no competing interests.Peer reviewPeer review informationNature Communications thanks Christine Foyer and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. 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