From remotely-sensed solar-induced chlorophyll fluorescence to ecosystem structure, function, and service: Part II-Harnessing data.

Although our observing capabilities of solar-induced chlorophyll fluorescence (SIF) have been growing rapidly, the quality and consistency of SIF datasets are still in an active stage of research and development. As a result, there are considerable inconsistencies among diverse SIF datasets at all scales and the widespread applications of them have led to contradictory findings. The present review is the second of the two companion reviews, and data oriented. It aims to (1) synthesize the variety, scale, and uncertainty of existing SIF datasets, (2) synthesize the diverse applications in the sector of ecology, agriculture, hydrology, climate, and socioeconomics, and (3) clarify how such data inconsistency superimposed with the theoretical complexities laid out in (Sun et al., 2023) may impact process interpretation of various applications and contribute to inconsistent findings. We emphasize that accurate interpretation of the functional relationships between SIF and other ecological indicators is contingent upon complete understanding of SIF data quality and uncertainty. Biases and uncertainties in SIF observations can significantly confound interpretation of their relationships and how such relationships respond to environmental variations. Built upon our syntheses, we summarize existing gaps and uncertainties in current SIF observations. Further, we offer our perspectives on innovations needed to help improve informing ecosystem structure, function, and service under climate change, including enhancing in-situ SIF observing capability especially in "data desert" regions, improving cross-instrument data standardization and network coordination, and advancing applications by fully harnessing theory and data.

An exploratory steady-state redox model of photosynthetic linear electron transport for use in complete modelling of photosynthesis for broad applications.

A photochemical model of photosynthetic electron transport (PET) is needed to integrate photophysics, photochemistry, and biochemistry to determine redox conditions of electron carriers and enzymes for plant stress assessment and mechanistically link sun-induced chlorophyll fluorescence to carbon assimilation for remotely sensing photosynthesis. Towards this goal, we derived photochemical equations governing the states and redox reactions of complexes and electron carriers along the PET chain. These equations allow the redox conditions of the mobile plastoquinone pool and the cytochrome b6 f complex (Cyt) to be inferred with typical fluorometry. The equations agreed well with fluorometry measurements from diverse C3 /C4 species across environments in the relationship between the PET rate and fraction of open photosystem II reaction centres. We found the oxidation of plastoquinol by Cyt is the bottleneck of PET, and genetically improving the oxidation of plastoquinol by Cyt may enhance the efficiency of PET and photosynthesis across species. Redox reactions and photochemical and biochemical interactions are highly redundant in their complex controls of PET. Although individual reaction rate constants cannot be resolved, they appear in parameter groups which can be collectively inferred with fluorometry measurements for broad applications. The new photochemical model developed enables advances in different fronts of photosynthesis research.

The effect of shift in physiological and anatomical traits on light use efficiency under cotton domestication.

The effect of crop domestication on photosynthetic productivity has been well-studied, but at present, none examines its impacts on leaf anatomy and, consequently, light use efficiency in cotton. We investigated leaf and vein anatomy traits, light use efficiency (LUE) and gas exchange in 26 wild and 30 domesticated genotypes of cotton grown under field conditions. The results showed that domestication resulted in a higher photosynthetic rate, higher stomatal conductance, and lower lamina mass per area. Higher LUE was underpinned by the thicker leaves, greater vein volume, elongated palisade and higher chlorophyll content, although there was no difference in the apparent quantum yield. The lower vein mass per area in domesticated genotypes contributed to the reduction of lamina mass per area, but there was no decrease in vein length per area. Our study suggests that domestication has triggered a considerable shift in physiological and anatomical traits to support the increase in LUE.

From remotely sensed solar-induced chlorophyll fluorescence to ecosystem structure, function, and service: Part I-Harnessing theory.

Solar-induced chlorophyll fluorescence (SIF) is a remotely sensed optical signal emitted during the light reactions of photosynthesis. The past two decades have witnessed an explosion in availability of SIF data at increasingly higher spatial and temporal resolutions, sparking applications in diverse research sectors (e.g., ecology, agriculture, hydrology, climate, and socioeconomics). These applications must deal with complexities caused by tremendous variations in scale and the impacts of interacting and superimposing plant physiology and three-dimensional vegetation structure on the emission and scattering of SIF. At present, these complexities have not been overcome. To advance future research, the two companion reviews aim to (1) develop an analytical framework for inferring terrestrial vegetation structures and function that are tied to SIF emission, (2) synthesize progress and identify challenges in SIF research via the lens of multi-sector applications, and (3) map out actionable solutions to tackle these challenges and offer our vision for research priorities over the next 5-10 years based on the proposed analytical framework. This paper is the first of the two companion reviews, and theory oriented. It introduces a theoretically rigorous yet practically applicable analytical framework. Guided by this framework, we offer theoretical perspectives on three overarching questions: (1) The forward (mechanism) question-How are the dynamics of SIF affected by terrestrial ecosystem structure and function? (2) The inference question: What aspects of terrestrial ecosystem structure, function, and service can be reliably inferred from remotely sensed SIF and how? (3) The innovation question: What innovations are needed to realize the full potential of SIF remote sensing for real-world applications under climate change? The analytical framework elucidates that process complexity must be appreciated in inferring ecosystem structure and function from the observed SIF; this framework can serve as a diagnosis and inference tool for versatile applications across diverse spatial and temporal scales.

Granal thylakoid structure and function: explaining an enduring mystery of higher plants.

In higher plants, photosystems II and I are found in grana stacks and unstacked stroma lamellae, respectively. To connect them, electron carriers negotiate tortuous multi-media paths and are subject to macromolecular blocking. Why does evolution select an apparently unnecessary, inefficient bipartition? Here we systematically explain this perplexing phenomenon. We propose that grana stacks, acting like bellows in accordions, increase the degree of ultrastructural control on photosynthesis through thylakoid swelling/shrinking induced by osmotic water fluxes. This control coordinates with variations in stomatal conductance and the turgor of guard cells, which act like an accordion's air button. Thylakoid ultrastructural dynamics regulate macromolecular blocking/collision probability, direct diffusional pathlengths, division of function of Cytochrome b6 f complex between linear and cyclic electron transport, luminal pH via osmotic water fluxes, and the separation of pH dynamics between granal and lamellar lumens in response to environmental variations. With the two functionally asymmetrical photosystems located distantly from each other, the ultrastructural control, nonphotochemical quenching, and carbon-reaction feedbacks maximally cooperate to balance electron transport with gas exchange, provide homeostasis in fluctuating light environments, and protect photosystems in drought. Grana stacks represent a dry/high irradiance adaptation of photosynthetic machinery to improve fitness in challenging land environments. Our theory unifies many well-known but seemingly unconnected phenomena of thylakoid structure and function in higher plants.

The physiological basis for estimating photosynthesis from Chla fluorescence.

Solar-induced Chl fluorescence (SIF) offers the potential to curb large uncertainties in the estimation of photosynthesis across biomes and climates, and at different spatiotemporal scales. However, it remains unclear how SIF should be used to mechanistically estimate photosynthesis. In this study, we built a quantitative framework for the estimation of photosynthesis, based on a mechanistic light reaction model with the Chla fluorescence of Photosystem II (SIFPSII ) as an input (MLR-SIF). Utilizing 29 C3 and C4 plant species that are representative of major plant biomes across the globe, we confirmed the validity of this framework at the leaf level. The MLR-SIF model is capable of accurately reproducing photosynthesis for all C3 and C4 species under diverse light, temperature, and CO2 conditions. We further tested the robustness of the MLR-SIF model using Monte Carlo simulations, and found that photosynthesis estimates were much less sensitive to parameter uncertainties relative to the conventional Farquhar, von Caemmerer, Berry (FvCB) model because of the additional independent information contained in SIFPSII . Once inferred from direct observables of SIF, SIFPSII provides 'parameter savings' to the MLR-SIF model, compared to the mechanistically equivalent FvCB model, and thus avoids the uncertainties arising as a result of imperfect model parameterization. Our findings set the stage for future efforts to employ SIF mechanistically to improve photosynthesis estimates across a variety of scales, functional groups, and environmental conditions.

Inference of photosynthetic capacity parameters from chlorophyll a fluorescence is affected by redox state of PSII reaction centers.

Solar-induced chlorophyll fluorescence (SIF) has been used to infer photosynthetic capacity parameters (e.g., the maximum carboxylation rate Vcmax , and the maximum electron transport rate Jmax ). However, the precise mechanism and practical utility of such approach under dynamic environments remain unclear. We used the balance between the light and carbon reactions to derive theoretical equations relating chlorophyll a fluorescence (ChlF) emission and photosynthetic capacity parameters, and formulated testable hypotheses regarding the dynamic relationships between the true total ChlF emitted from PSII (SIFPSII ) and Vcmax and Jmax . We employed concurrent measurements of gas exchanges and ChlF parameters for 15 species from six biomes to test the formulated hypotheses across species, temperatures, and limitation state of carboxylation. Our results revealed that SIFPSII alone is incapable of informing the variations in Vcmax and Jmax across species, even when SIFPSII is determined under the same environmental conditions. In contrast, the product of SIFPSII and the fraction of open PSII reactions qL , which indicates the redox state of PSII, is a strong predictor of both Vcmax and Jmax , although their precise relationships vary somewhat with environmental conditions. Our findings suggest the redox state of PSII strongly influences the relationship between SIFPSII and Vcmax and Jmax .

The roles of photochemical and non-photochemical quenching in regulating photosynthesis depend on the phases of fluctuating light conditions.

The induction and relaxation of photochemistry and non-photochemical quenching (NPQ) are not instantaneous and require time to respond to fluctuating environments. There is a lack of integrated understanding on how photochemistry and NPQ influence photosynthesis in fluctuating environments. We measured the induction and relaxation of chlorophyll a fluorescence and gas exchange in poplar and cotton at varying temperatures under saturating and fluctuating lights. When the light shifted from dark to high, the fraction of open reaction centers in photosystem II (qL) gradually increased while NPQ increased suddenly and then remained stable. Temperature significantly changed the response of qL but not that of NPQ during the dark to high light transition. Increased qL led to higher photosynthesis but their precise relationship was affected by NPQ and temperature. qL was significantly related to biochemical capacity. Thus, qL appears to be a strong indicator of the activation of carboxylase, leading to the similar dynamics between qL and photosynthesis. When the light shifted from high to low intensity, NPQ is still engaged at a high level, causing a stronger decline in photosynthesis. Our finding suggests that the dynamic effects of photochemistry and NPQ on photosynthesis depend on the phases of environmental fluctuations and interactive effects of light and temperature. Across the full spectra of light fluctuation, the slow induction of qL is a more important limiting factor than the slow relaxation of NPQ for photosynthesis in typical ranges of temperature for photosynthesis. The findings provided a new perspective to improve photosynthetic productivity with molecular biology under natural fluctuating environments.

Comparisons of photosynthetic and anatomical traits between wild and domesticated cotton.

Mesophyll conductance (gm) is a crucial leaf trait contributing to the photosynthetic rate (AN). Plant domestication typically leads to an enhancement of AN that is often associated with profound anatomical modifications, but it is unclear which of these structural alterations influence gm. We analyzed the implication of domestication on leaf anatomy and its effect on gm in 26 wild and 31 domesticated cotton genotypes (Gossypium sp.) grown under field conditions. We found that domesticated genotypes had higher AN but similar gm to wild genotypes. Consistent with this, domestication did not translate into significant differences in the fraction of mesophyll occupied by intercellular air spaces (fias) or mesophyll and chloroplast surface area exposed to intercellular air space (Sm/S and Sc/S, respectively). However, leaves of domesticated genotypes were significantly thicker, with larger but fewer mesophyll cells with thinner cell walls. Moreover, domesticated genotypes had higher cell wall conductance (gcw) but smaller cytoplasmic conductance (gcyt) than wild genotypes. It appears that domestication in cotton has not generally led to significant improvement in gm, in part because their thinner mesophyll cell walls (increasing gcw) compensate for their lower gcyt, itself due to larger distance between plasmalemma and chloroplast envelopes.

Improve Plant Photosynthesis by a New Slow-Release Carbon Dioxide Gas Fertilizer.

In the natural state, the concentration of carbon dioxide in the atmosphere is about 300 µmol mol-1. Plants need a suitable balance of CO2 to achieve optimal growth. The optimum CO2 content corresponding to a high photosynthesis rate is between 0.1 and 1.0% by volume. However, air has only a CO2 content of 0.03% by volume, so plants cannot use all of their growth potential. The use of fertilizer to assist in the supply of CO2 increases the rate of photosynthesis. In this work, a slow-release CO2 gas fertilizer inspired by polyphenol chemistry was prepared to provide sustainable CO2 that could improve plant photosynthetic capacity and get a higher crop yield. The core-shell structure was designed to confer gas fertilizers slow-release property. Micron-sized calcium carbonate particles with uniform particle size and regularity morphology, as carbon sources for plant photosynthesis, was a core, and tannic acid was coated on it as a shell via oxidative oligomerization and cross-linked by polyetherimide. The structure and morphology of fertilizers were characterized by scanning electron microscopy, X-ray energy dispersive spectroscopy, transmission electron microscopy, X-ray photoelectron spectroscopy, and thermogravimetric analysis. In vitro experiments, the prepared fertilizers were proved to have slow-release properties. And then through net photosynthesis rate, chlorophyll fluorescence parameters, chlorophyll content, leaf area, leaf mass per area, and dry matter to study the effects of slow-release CO2 gas fertilizers on plant physiology of Brassica chinensis. The results revealed that the slow-release CO2 gas fertilizers not only had good slow-release properties but also can well improve plant photosynthesis.

Sun-induced Chl fluorescence and its importance for biophysical modeling of photosynthesis based on light reactions.

Recent progress in observing sun-induced Chl fluorescence (SIF) provides an unprecedented opportunity to advance photosynthesis research in natural environments. However, we still lack an analytical framework to guide SIF studies and integration with the well-developed active fluorescence approaches. Here, we derive a set of coupled fundamental equations to describe the dynamics of SIF and its relationship with C3 and C4 photosynthesis. These equations show that, although SIF is dynamically as complex as photosynthesis, the measured SIF simplifies photosynthetic modeling from the perspective of light reactions by integrating over the dynamic complexities of photosynthesis. Specifically, the measured SIF contains direct information about the actual electron transport from photosystem II to photosystem I, giving a quantifiable link between light and dark reactions. With much-reduced requirements on inputs and parameters, the light-reactions-centric, SIF-based biophysical model complements the traditional, dark-reactions-centric biochemical model of photosynthesis. The SIF-photosynthesis relationship, however, is nonlinear. This is because photosynthesis saturates at high light whereas SIF has a stronger tendency to keep increasing, as fluorescence quantum yield has a relatively muted sensitivity to light levels. Successful applications of the SIF-based model of photosynthesis will depend on a predictive understanding of several previously underexplored physiological and biophysical processes. Advances can be facilitated by coordinated efforts in plant physiology, remote sensing, and eddy covariance flux observations.

Drought-introduced variability of mesophyll conductance in Gossypium and its relationship with leaf anatomy.

Mesophyll conductance (gm ) is one of the major determinants of photosynthetic rate, for which it has an impact on crop yield. However, the regulatory mechanisms behind the decline in gm of cotton (Gossypium. spp) by drought are unclear. An upland cotton (Gossypium hirsutum) genotype and a pima cotton (Gossypium barbadense) genotype were used to determine the gas exchange parameters, leaf anatomical structure as well as aquaporin and carbonic anhydrase gene expression under well-watered and drought treatment conditions. In this study, the decrease of net photosynthetic rate (AN ) under drought conditions was related to a decline in gm and in stomatal conductance (gs ). gm and gs coordinate with each other to ensure optimum state of CO2 diffusion and achieve the balance of water and CO2 demand in the process of photosynthesis. Meanwhile, mesophyll limitations to photosynthesis are equally important to the stomatal limitations. Considering gm , its decline in cotton leaves under drought was mostly regulated by the chloroplast surface area exposed to leaf intercellular air spaces per leaf area (Sc /S) and might also be regulated by the expression of leaf CARBONIC ANHYDRASE (CA1). Meanwhile, cotton leaves can minimize the decrease in gm under drought by maintaining cell wall thickness (Tcw ). Our results indicated that modification of chloroplasts might be a target trait in future attempts to improve cotton drought tolerance.

Mesophyll conductance in cotton bracts: anatomically determined internal CO2 diffusion constraints on photosynthesis.

Mesophyll conductance (gm) has been shown to affect photosynthetic capacity and thus the estimates of terrestrial carbon balance. While there have been some attempts to model gm at the leaf and larger scales, the potential contribution of gm to the photosynthesis of non-leaf green organs has not been studied. Here, we investigated the influence of gm on photosynthesis of cotton bracts and how it in turn is influenced by anatomical structures, by comparing leaf palisade and spongy mesophyll with bract tissue. Our results showed that photosynthetic capacity in bracts is much lower than in leaves, and that gm is a limiting factor for bract photosynthesis to a similar extent to stomatal conductance. Bract and the spongy tissue of leaves have lower mesophyll conductance than leaf palisade tissue due to the greater volume fraction of intercellular air spaces, smaller chloroplasts, lower surface area of mesophyll cells and chloroplasts exposed to leaf intercellular air spaces and, perhaps, lower membrane permeability. Comparing bracts with leaf spongy tissue, although bracts have a larger cell wall thickness, they have a similar gm estimated from anatomical characteristics, likely due to the cumulative compensatory effects of subtle differences in each subcellular component, especially chloroplast traits. These results provide the first evidence for anatomical constraints on gm and photosynthesis in non-leaf green organs.

Changes in activities of both photosystems and the regulatory effect of cyclic electron flow in field-grown cotton (Gossypium hirsutum L) under water deficit.

To clarify the influence of water deficit on the functionality of the photosynthetic apparatus of cotton plants, leaf gas exchange, chlorophyll a fluorescence, and P700 redox state were examined in field-grown cotton Gossypium hirsutum L. cv. Xinluzao 45. In addition, we measured changes in the P515 signal and analyzed the activity of ATP synthase and the trans-thylakoid proton gradient (ΔpH). With increasing water deficit, the net CO2 assimilation rate (AN) and stomatal conductance (gs) significantly decreased, but the maximum quantum efficiency of PSII photochemistry (Fv/Fm) did not change. The photochemical activity of photosystem II (PSII) was reflected by the photochemical quenching coefficient (qP), quantum efficiency of photosystem II [Y(II)], and electron transport rate through PSII [ETR(II)], while the activity of photosystem I (PSI) was reflected by the quantum efficiency of photosystem I [Y(I)] and the electron transport rate through PSI [ETR(I)]. Both activities were maintained under mild water deficit, but were slightly decreased under moderate water deficit. Under moderate water deficit, cyclic electron flow (CEF), the fraction of absorbed light dissipated thermally via the ΔpH- and xanthophyll-regulated process [Y(NPQ)], and the fraction of P700 oxidized under a given set of conditions [Y(ND)] increased. Our results suggest that the activities of both photosystems are stable under mild water deficit and decrease only slightly under moderate water deficit. Moderate water deficit stimulates CEF, and the stimulation of CEF is essential for protecting PSI and PSII against photoinhibition.

Variability of mesophyll conductance and its relationship with water use efficiency in cotton leaves under drought pretreatment.

Drought slows net photosynthetic rate (AN) but increases water use efficiency (WUE). Farmers give an artificial drought pretreatment to some crops in the early growth stage and find that yield increases accompanying with the improvement of WUE. We conducted well-watered, non-drought, mild drought and moderate drought pretreatments of potted cotton cultivars. The aims of the present study were to analyse the importance of mesophyll conductance (gm) as a factor that may simultaneously improve AN and WUE under drought pretreatment conditions, and to analyse the role of anatomical structure and biochemical mechanism in the variability of gm. Our results showed that significant variability of gm estimated by gas exchange and chlorophyll fluorescence was observed between non-drought pretreatment and drought pretreatment associated with change in AN and WUE. There was great difference in anatomical structure and expression of aquaporins (GhAQP1) among all the treatments. In addition, expression of carbonic anhydrase (CA) may not be important in the regulation of gm under drought pretreatment conditions. We concluded that the variability of gm offers a potential target for improving leaf AN and WUE simultaneously by the regulation of anatomical structure and GhAQP1.