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Inferring Plant Acclimation and Improving Model Generalizability With Differentiable Physics‐Informed Machine Learning of Photosynthesis

Net photosynthesis (A N ) is a key component of the global carbon cycle influencing climate feedback over decadal scales. Although plant acclimation to environmental changes can modify A N , traditional vegetation models in Earth system models (ESMs) often rely on plant functional type (PFT)-specific parameterizations or simplified acclimation assumptions limiting generalizability across time, space, and PFTs. In this study, we developed a differentiable photosynthesis model to learn the environmental dependencies of V c,max25 (maximum carboxylation rate at 25°C, representing photosynthetic capacity), as this genre of hybrid physics-informed machine learning can seamlessly train neural networks and process-based equations together. Compared to PFT-specific parameterization of V c,max25 , learning the environment dependencies of key photosynthetic parameters improved model spatiotemporal generalizability. Applying environmental acclimation to V c,max25 led to substantial variations in global mean A N indicating the need to address acclimation in ESMs. The model effectively captured multivariate observations (V c,max25 , A N , and stomatal conductance (g s )) simultaneously with multivariate constraints, improving generalization across space and PFTs. It also learned sensible acclimation relationships of V c,max25 to different environmental conditions. The model explained more than 54%, 57%, and 62% of the variance of A N , g s , and V c,max25 , respectively, presenting a first global-scale spatial test benchmark of A N and g s . These results highlight the potential for differentiable modeling to enhance process-based modules in ESMs and effectively leverage information from large, multivariate data sets.

54 ENVIRONMENTAL SCIENCES

Observations and modeling reveal that heatwaves reduce photosynthesis, plant carbon reserves, and net carbon uptake

Heatwaves threaten ecosystem carbon balances, yet the mechanisms driving short-term carbon flux responses remain poorly understood. Here, integrating high-frequency eddy covariance (EC) data from 140 global flux tower sites (872 site-years) with detailed process-based modeling, we examine ecosystem responses during and immediately after heatwaves. We show that heatwaves caused a −40% (range [−29%, −128%]) reduction in net ecosystem productivity (NEP) compared to pre-heatwave values, with this reduction persisting over the following two weeks (−38% range [+3%, −154%]). We attributed NEP decreases to photosynthesis decreases more than to ecosystem respiration (RE) increases. Forest sites had greater NEP decreases during heatwaves than non-forest sites, but remained carbon sinks afterwards, indicating resilience. Our modeling analysis of extreme heatwaves at selected EC sites shows that decreased photosynthesis, increased maintenance respiration, and decreased plant non-structural carbon reserves during heatwaves drive carbon cycle changes that persist for weeks. Consistent with phenocam observations, we modeled a reduction in leaf area index caused by reduced non-structural carbon reserves, leading to early leaf senescence and longer-term impacts. Ongoing increases in heatwaves are therefore likely to reduce NEP across a range of ecosystems, exacerbating carbon cycle feedback.

carbon cycle

Meta-omics reveals role of photosynthesis in microbially induced carbonate precipitation at a CO2-rich geyser

Abstract Microbially induced carbonate precipitation (MICP) is a natural process with potential biotechnological applications to address both carbon sequestration and sustainable construction needs. However, our understanding of the microbial processes involved in MICP is limited to a few well-researched pathways such as ureolytic hydrolysis. To expand our knowledge of MICP, we conducted an omics-based study on sedimentary communities from travertine around the CO2-driven Crystal Geyser near Green River, Utah. Using metagenomics and metaproteomics, we identified the community members and potential metabolic pathways involved in MICP. We found variations in microbial community composition between the two sites we sampled, but Rhodobacterales were consistently the most abundant order, including both chemoheterotrophs and anoxygenic phototrophs. We also identified several highly abundant genera of Cyanobacteriales. The dominance of these community members across both sites and the abundant presence of photosynthesis-related proteins suggest that photosynthesis could play a role in MICP at Crystal Geyser. We also found abundant bacterial proteins involved in phosphorous starvation response at both sites suggesting that P-limitation shapes both composition and function of the microbial community driving MICP.

Violette, Marlene J.

Lighting the way: Compelling open questions in photosynthesis research

Abstract Photosynthesis—the conversion of energy from sunlight into chemical energy—is essential for life on Earth. Yet there is much we do not understand about photosynthetic energy conversion on a fundamental level: how it evolved and the extent of its diversity, its dynamics, and all the components and connections involved in its regulation. In this commentary, researchers working on fundamental aspects of photosynthesis including the light-dependent reactions, photorespiration, and C4 photosynthetic metabolism pose and discuss what they view as the most compelling open questions in their areas of research.

Eckardt, Nancy A. (ORCID:0000000316581412)

Disruption of starch biosynthesis and triacylglycerol degradation impairs growth but improves photosynthesis in Arabidopsis

Enhancing lipid accumulation by redirecting carbon from starch to triacylglycerol (TAG) in vegetative tissues is a promising strategy for developing high-energy-density crops for bioenergy production. However, our understanding of how starch and TAG metabolism interact and how this interaction affects growth and photosynthesis is incomplete. Here, we investigated the metabolic and physiological consequences of disrupting starch biosynthesis and TAG turnover in Arabidopsis thaliana by generating single, double, and triple mutants involving ADG1 (starch biosynthesis), TGD1 (lipid trafficking), and SDP1\\\\\\\\r\\\\\\\\n(TAG lipase). Unexpectedly, elimination of starch biosynthesis lowered TAG levels in the high-TAG-accumulating tgd1 mutant, primarily through enhanced TAG breakdown. This decline was completely reversed by sucrose supplementation, suggesting that TAG degradation was induced by carbon limitation.\\\\\\\\r\\\\\\\\nGenetic suppression of TAG turnover via SDP1 disruption in the starchless tgd1 adg1-1 background led to a nine-fold rise in leaf TAG accumulation in the tgd1 sdp1 adg1-1 triple mutant, together with enhanced photosynthetic performance. However, this metabolic reprogramming incurred growth penalties.\\\\\\\\r\\\\\\\\nOur results highlight the role of dynamic TAG turnover in maintaining metabolic balance and photosynthesis in starch-deficient backgrounds. These findings underscore the need for refined metabolic engineering strategies that coordinate TAG biosynthesis and degradation to optimize lipid accumulation in bioenergy crops.

59 BASIC BIOLOGICAL SCIENCES

Contributions of David Mauzerall to photosynthesis research - celebrating his 95 th birthday

We honor here Professor David Mauzerall, a pioneer in the fields of photochemistry and photobiology of porphyrins and chlorophylls in vitro and in vivo, on the occasion of his 95th birthday. Throughout his career at The Rockefeller University, he refined our understanding of how chlorophyll converts light energy into chemical energy. He exploited top-of-the-line laser technology in developing photoacoustics and a variety of other innovative experimental approaches. His experimental work and conceptual insights contributed greatly to our understanding of photosynthesis and the possible role of photosynthesis in the origin of life. His contributions include many landmark single-authored and collaborative papers, and his legacy includes the training of others who have become authorities themselves. After providing a brief description of his research accomplishments, we include tributes from several of his coworkers and his daughters highlighting their valuable experiences with David Mauzerall on this milestone birthday.

59 BASIC BIOLOGICAL SCIENCES

Relating seasonal patterns of the AVHRR vegetation index to simulated photosynthesis and transpiration of forests in different climates

Weekly AVHRR Normalized Difference Vegetation Index (NDVI) values for 1983-1984 for seven sites of diverse climate in North America were correlated with results of an ecosystem simulation model of a hypothetical forest stand for the corresponding period at each site. The tendency of raw NDVI data to overpredict photosynthesis and transpiration on water limited sites was shown to be partially corrected by using an aridity index of annual radiation/annual precipitation. The results suggest that estimates of vegetation productivity using the global vegetation index are only accurate as annual integrations, unless unsubsampled local area coverage NDVI data can be tested against forest photosynthesis, transpiration and aboveground net primary production data measured at shorter time intervals.

Running, Steven W.

Calculating Irradiance For Photosynthesis In The Ocean

Mathematical model predicts available and usable irradiances. Yields estimates of irradiance available for photosynthesis (Epar) and irradiance usable for photosynthesis (Epur) as functions of depth in ocean. Describes Epur and Epar in terms of spectral parameters measured remotely (from satellites or airplanes). These irradiances useful in studies of photosynthetic productivity of phytoplankton in euphotic layer.

Collins, Donald J.

Nutrient control of phytoplankton photosynthesis in the western North Atlantic

Results from several years of oceanographic cruises are reported which show that the parameters of the photosynthesis-light curve of the flora of the North Sargasso Sea are remarkably constant in magnitude, except during the spring phytoplankton bloom when their magnitudes are noticeably higher. These results are interpreted as providing direct evidence for nutrient control of photosynthesis in the open ocean. The findings also reinforce the plausibility of using biogeochemical provinces to partition the ocean into manageable units for basin- or global-scale analysis. They show that seasonal changes in critical parameter should not be overlooked if robust carbon budgets are to be constructed, and illustrate the value of attacking the parameters that control the key fluxes, rather than the fluxes themselves, when investigating the ocean carbon cycle.

Platt, Trevor

An Optical Index of Phytoplankton Photoacclimation and Its Relation to Light-Saturated Photosynthesis in the Sea

In relation to understanding ocean biology at the global scale, one of NASA's primary foci has been measurements of near-surface concentrations of phytoplankton chlorophyll. Chlorophyll is an important light-absorbing pigment in phytoplankton. The absorbed light energy is used to fix carbon in the process of photosynthesis. Photosynthesis, in turn, is critical to the growth of phytoplankton and the function of entire marine ecosystems. Thus, the use of satellite surface chlorophyll data to estimate primary production in the ocean has been a key focus of much biological oceanography research. One of the major challenges in this research is to develop relationships that allow a given chlorophyll concentration (a standing stock) to be interpreted in terms of carbon fixation (a rate). This problem centers on the description of the light-saturated photosynthetic rate, Pbmax. In this paper, we describe how optical measurements of light attenuation provide information on particulate organic carbon (POC) concentrations. We then show how the ratio of POC to chlorophyll (Theta) provides critical information on variability in Pbmax. We then test this relationship between Theta and Pbmax using field data from a variety of open ocean ecosystems.

Behrenfeld, Michael J.

Growth and photosynthesis of Japanese flowering cherry under simulated microgravity conditions

The photosynthetic rate, the leaf characteristics related to photosynthesis, such as the chlorophyll content, chlorophyll a/b ratio and density of the stomata, the leaf area and the dry weight in seedlings of Japanese flowering cherry grown under normal gravity and simulated microgravity conditions were examined. No significant differences were found in the photosynthetic rates between the two conditions. Moreover, leaf characteristics such as the chlorophyll content, chlorophyll a/b ratio and density of the stomata in the seedlings grown under the simulated microgravity condition were not affected. However, the photosynthetic product of the whole seedling under the simulated microgravity condition increased compared with the control due to its leaf area increase. The results suggest that dynamic gravitational stimulus controls the partitioning of the products of photosynthesis.

Weightlessness Simulation

The effects of UV radiation A and B on diurnal variation in photosynthesis in three taxonomically and ecologically diverse microbial mats

Photosynthetic primary production, the basis of most global food chains, is inhibited by UV radiation. Evaluating UV inhibition is therefore important for assessing the role of natural levels of UV radiation in regulating ecosystem behavior as well as the potential impact of stratospheric ozone depletion on global ecosystems. As both photosynthesis and UV fluxes are subject to diurnal variations, we examined the diurnal variability of the effect of UV radiation on photosynthesis in three diverse algal mats. In one of the mats (Cyanidium caldarium) a small mean decrease in primary productivity over the whole day occurred when both UVA and UVB were screened out. In two of the mats (Lyngbya aestuarii and Zygogonium sp.) we found a mean increase in the total primary productivity over the day when UVB alone was screened and a further increase when UVA and UVB were both screened out. Variations in the effects of UV radiation were found at different times of the day. This diurnal variability may be because even under the same solar radiation flux, there are different factors that may control photosynthetic rate, including nutritional status and other physiological processes in the cell. The results show the importance of assessing the complete diurnal productivity. For some of the time points the increase in the mean was still within the standard deviations in primary productivity, illustrating the difficulty in dissecting UV effects from other natural variations.

Ultraviolet Rays

Real-Time Imaging of Ground Cover: Relationships with Radiation Capture, Canopy Photosynthesis, and Daily Growth Rate

Cumulative absorbed radiation is highly correlated with crop biomass and yield. In this chapter we describe the use of a digital camera and commercial imaging software for estimating daily radiation capture, canopy photosynthesis, and relative growth rate. Digital images were used to determine percentage of ground cover of lettuce (Lactuca sativa L.) communities grown at five temperatures. Plants were grown in a steady-state, 10-chamber CO2 gas exchange system, which was used to measure canopy photosynthesis and daily carbon gain. Daily measurements of percentage of ground cover were highly correlated with daily measurements of both absorbed radiation (r(sup 2) = 0.99) and daily carbon gain (r(sup 2) = 0.99). Differences among temperature treatments indicated that these relationships were influenced by leaf angle, leaf area index, and chlorophyll content. An analysis of the daily images also provided good estimates of relative growth rates, which were verified by gas exchange measurements of daily carbon gain. In a separate study we found that images taken at hourly intervals were effective for monitoring real-time growth. Our data suggests that hourly images can be used for early detection of plant stress. Applications, limitations, and potential errors are discussed. We have long known that crop yield is determined by the efficiency of four component processes: (i) radiation capture, (ii) quantum yield, (iii) carbon use efficiency, and (iv) carbon partitioning efficiency (Charles-Edwards, 1982; Penning de Vries & van Laar, 1982; Thornley, 1976). More than one-half century ago, Watson (1947, 1952) showed that variation in radiation capture accounted for almost all of the variation in yield between sites in temperate regions, because the three other components are relatively constant when the crop is not severely stressed. More recently, Monteith (1977) reviewed the literature on the close correlation between radiation capture and yield. Bugbee and Monje (1992) demonstrated the close relationship between absorbed radiation and yield in an optimal environment.

Klassen, S. P.

Acclimation of Plant Populations to Shade: Photosynthesis, Respiration, and Carbon Use Efficiency

Cloudy days cause an abrupt reduction in daily photosynthetic photon flux (PPF), but we have a poor understanding of how plants acclimate to this change. We used a unique lo-chamber, steady-state, gas-exchange system to continuously measure daily photosynthesis and night respiration of populations of a starch accumulator [tomato (Lycopersicone scukntum Mill. cv. Micro-Tina)] and a sucrose accumulator [lettuce (Latuca sativa L ev. Grand Rapids)] over 42 days. AI1 measurements were done at elevated CO2, (1200micr-/mol) avoid any CO2 limitations and included both shoots and roots. We integrated photosynthesis and respiration measurements separately to determine daily net carbon gain and carbon use efficiency (CUE) as the ratio of daily net C gain to total day-time C fixed over the 42-day period. After 16 to 20 days of growth in constant PPF, plants in some chambers were subjected to an abrupt PPF reduction to simulate shade or a series of cloudy days. The immediate effect and the long term acclimation rate w'ere assessed from canopy quantum yield and carbon use efficiency. The effect of shade on carbon use efficiency and acclimation was much slower than predicted by widely used growth models. It took 12 days for tomato populations to recover their original CUE and lettuce CUE never completely acclimated. Tomatoes, the starch accumulator, acclimated to low light more rapidly than lettuce, the sucrose accumulator. Plant growth models should be modified to include the photosynthesis/respiration imbalance and resulting inefficiency of carbon gain associated with changing PIT conditions on cloudy days.

Frantz, Jonathan M.

High-Efficiency Artificial Photosynthesis Using a Novel Alkaline Membrane Cell

A new cell designed to mimic the photosynthetic processes of plants to convert carbon dioxide into carbonaceous products and oxygen at high efficiency, has an improved configuration using a polymer membrane electrolyte and an alkaline medium. This increases efficiency of the artificial photosynthetic process, achieves high conversion rates, permits the use of inexpensive catalysts, and widens the range of products generated by this type of process. The alkaline membrane electrolyte allows for the continuous generation of sodium formate without the need for any additional separation system. The electrolyte type, pH, electrocatalyst type, and cell voltage were found to have a strong effect on the efficiency of conversion of carbon dioxide to formate. Indium electrodes were found to have higher conversion efficiency compared to lead. Bicarbonate electrolyte offers higher conversion efficiency and higher rates than water solutions saturated with carbon dioxide. pH values between 8 and 9 lead to the maximum values of efficiency. The operating cell voltage of 2.5 V, or higher, ensures conversion of the carbon dioxide to formate, although the hydrogen evolution reaction begins to compete strongly with the formate production reaction at higher cell voltages. Formate is produced at indium and lead electrodes at a conversion efficiency of 48 mg of CO2/kilojoule of energy input. This efficiency is about eight times that of natural photosynthesis in green plants. The electrochemical method of artificial photosynthesis is a promising approach for the conversion, separation and sequestration of carbon dioxide for confined environments as in space habitats, and also for carbon dioxide management in the terrestrial context. The heart of the reactor is a membrane cell fabricated from an alkaline polymer electrolyte membrane and catalyst- coated electrodes. This cell is assembled and held in compression in gold-plated hardware. The cathode side of the cell is supplied with carbon dioxide-saturated water or bicarbonate solution. The anode side of the cell is supplied with sodium hydroxide solution. The solutions are circulated past the electrodes in the electrochemical cell using pumps. A regulated power supply provides the electrical energy required for the reactions. Photovoltaic cells can be used to better mimic the photosynthetic reaction. The current flowing through the electrochemical cell, and the cell voltage, are monitored during experimentation. The products of the electrochemical reduction of carbon dioxide are allowed to accumulate in the cathode reservoir. Samples of the cathode solution are withdrawn for product analysis. Oxygen is generated on the anode side and is allowed to vent out of the reservoir.

Narayan, Sri

Effects of CO2 Concentration on Leaf Photosynthesis and Stomatal Conductance of Potatoes Grown Under Different Irradiance Levels and Photoperiods

Potato (Solanum tuberosum L.) cvs. Russet Burbank, Denali, and Norland, were grown in environmental rooms controlled at approx 350 micro mol/mol (ambient during years 1987/1988) and 1000 micro mol/mol (enriched) CO2 concentrations. Plants and electric lamps were arranged to provide two irradiance zones, 400 and 800 micro mol/mol/square m/S PPF and studies were repeated using two photoperiods (12-h light / 12-h dark and continuous light). Leaf photosynthetic rates and leaf stomatal conductance were measured using fully expanded, upper canopy leaves at weekly intervals throughout growth (21 through 84 days after transplanting). Increasing the CO2 from approx 350 to 1000 micro mol/mol under the 12-h photoperiod increased leaf photosynthetic rates by 39% at 400 micro mol/mol/square m/S PPF and 27% at 800 micro mol/mol/square m/S PPF. Increasing the CO2 from approx 350 to 1000 micro mol/mol under continuous light decreased leaf photosynthetic rates by 7% at 400 micro mol/mol/square m/S PPF and 13% at 800 micro mol/mol/square m/S PPF. Increasing the CO2 from approx 350 to 1000 micro mol/mol under the 12-h photoperiod plants decreased stomatal conductance by an average of 26% at 400 micro mol/mol/square m/S PPF and 42% at 800 micro mol/mol/square m/S PPF. Under continuous light, CO2 enrichment resulted in a small increase (2%) of stomatal conductance at 400 micro mol/mol/square m/S PPF, and a small decrease (3%) at 800 micro mol/mol/square m/S PPF. Results indicate that CO2 enrichment under the 12-h photoperiod showed the expected increase in photosynthesis and decrease in stomatal conductance for a C3 species like potato, but the decreases in leaf photosynthetic rates and minimal effect on conductance from CO2 enrichment under continuous light were not expected. The plant leaves under continuous light showed more chlorosis and some rusty flecking versus plants under the 12-h photoperiod, suggesting the continuous light was more stressful on the plants. The increased rates of leaf photosynthesis with increased CO2 concentration paralleled trends in biomass production (published previously) but were not proportional to the biomass yields.

Wheeler, R. M.

Efficiency of Photosynthesis in a Chl d-Utilizing Cyanobacterium is Comparable to or Higher than that in Chl a-Utilizing Oxygenic Species

The cyanobacterium Acaryochloris marina uses chlorophyll d to carry out oxygenic photosynthesis in environments depleted in visible and enhanced in lower-energy, far-red light. However, the extent to which low photon energies limit the efficiency of oxygenic photochemistry in A. marina is not known. Here, we report the first direct measurements of the energy-storage efficiency of the photosynthetic light reactions in A. marina whole cells,and find it is comparable to or higher than that in typical, chlorophyll a-utilizing oxygenic species. This finding indicates that oxygenic photosynthesis is not fundamentally limited at the photon energies employed by A. marina, and therefore is potentially viable in even longer-wavelength light environments.

Mielke, S. P.

Development of a Photosynthesis Measurement Chamber under Different Airspeeds for Applications in Future Space Crop-Production Facilities

Space crop production systems are being developed to grow fresh produce in-situ to supplement the astronauts’ diet, but the required ventilation rates for crops in different gravity environments remains poorly understood. The reduction or lack of buoyancy-driven convection in reduced gravity environments leads to impaired gas exchange (CO2 absorption, water transpiration and O2 release) at the leaf surface if no extra ventilation is provided, and this could lead to a reduction in biomass production in the long run. To better characterize the influence of different airspeeds on photosynthesis and be able to model this in low gravity, a chamber was designed to interface with a LI-6800 portable photosynthesis system. This paper details the design of this chamber, specifically made to measure whole-plant and small canopy gas exchange at different airspeeds. The fans provide turbulent mixing in the chamber to ensure that it behaves like a continuous stirred tank reactor (CSTR)and that the residence time distribution (RTD) is the same for any fan speed; the computational fluid dynamic (CFD) model of the gas domain (the air in the chamber) hence uses a k-omega turbulence model. An airflow map of the chamber was created using anemometer measurements for the different airspeeds tested, and this was used together with the CFD simulation results to relate the experimentally measured fan outputs to actual airspeeds on top of an artificial plant. Environmental parameters (air temperature, relative humidity, CO2level) are controlled by the LI-6800. This work was funded by NASA Space Biology through the NASA postdoctoral program / USRA.

Lucie Poulet