The goal of this work is to assess the mechanistic bases of natural genetic variations in plant responses of photosynthesis to stress. To achieve this goal, we devised the Linkage Integration Hypothesis Testing (LIgHT) approach, comparing chromosomal locations of quantitative trait loci (QTLs) for multiple phenotypes to distinguish between hypothetical mechanisms. As a use case, we explored genetic variations in photosynthesis-related processes under chilling stress in recombinant inbred lines of cowpea (Vigna unguiculata L. Walp.). We focused on photosynthesis-related parameters measurable in high throughput and indicative of proposed chilling responses, including the states of PSI and PSII, photoprotective non-photochemical quenching, PSII photodamage, and nyctinastic leaf movements (NLMs). The patterns of QTL linkages indicated that chilling stress tolerance is genetically controlled by avoiding PSII photodamage rather than PSI damage or NLMs. This model was validated in a separate experiment measuring the rates of PSII photodamage and repair. Additional linkages suggest that chilling-induced damage to PSII is controlled by the thylakoid proton motive force and redox state of PSII. This regulation appears to be modulated by thylakoid fatty acid composition, previously associated with the same genetic loci and now supported by broader mechanistic evidence. We propose that the LIgHT approach can be broadly applied to test mechanisms underlying genetic variations.

Chloroplasts play a central role in plant responses to environmental stress. Little is known, however, about how chloroplast homeostasis is maintained during stress responses that place high metabolic and bioenergetic demands on the cell. As a chloroplast-derived retrograde signal, jasmonate (JA) promotes broad-spectrum immunity by triggering the degradation of JAZ transcriptional repressors that act in the nucleus to control chloroplast metabolism. Here, we manipulated JAZ abundance to investigate how chloroplast integrity and function is maintained at high levels of defense. A jaz decuple mutant (jazD) lacking 10 of 13 JAZs exhibited strong growth-defense antagonism without loss of photosynthetic efficiency. Treatment of jazD with the JA-receptor agonist coronatine triggered rapid loss of chlorophyll and the turnover of chloroplast proteins and lipids, leading to the collapse of photosynthetic activity and cell death. These findings were supported by global transcript and metabolite profiling over a time course of coronatine treatment. Genetic screens identified MYC2 and the JAZ-destabilizing F-box protein, COI1, as positive regulators of coronatine-induced chloroplast dismantling in jazD plants. These results demonstrate how the progressive loss of JAZ repression drives a continuum of MYC2-dependent growth-defense tradeoffs, including disassembly of the photosynthetic apparatus as a terminal response. In highlighting the critical role for JAZ proteins in maintaining chloroplast integrity at high levels of defense, our results provide insight into the general mechanism by which jasmonate governs chloroplast metabolism to balance growth and stress responses.

Recent studies have shown a linear relationship between solar-induced Chl fluorescence (SIF) and gross primary productivity (GPP) at large scales. However, this relationship diverges at finer leaf scales, particularly in tropical forests with complex canopy structures. To address this issue, we assessed seasonal and intracanopy variations in leaf energy partitioning in central Amazonian forests with extensive in-canopy sampling and pulse-amplitude-modulated Chl fluorescence measurements. We explored the pathways of photon utilization for photochemistry (ΦPSII), heat dissipation (ΦNPQ), and nonregulated quenching (ΦNO) of fluorescence. We found consistent increases in ΦNPQ and decreases in ΦPSII and ΦNO with increasing canopy height, primarily driven by changes in photosynthetically active radiation. During the dry season, a triphasic relationship between ΦNO and ΦPSII was detected, alternating between positive and negative relationships across leaf irradiance levels, highlighting stress-induced physiological responses. Interspecific variation and vapor pressure deficit also played significant roles in modulating ΦNO, emphasizing the complex interaction between environmental factors, species composition, and energy dissipation across canopy strata. These insights into leaf-level fluorescence and energy dynamics show the complex mediation of ΦNPQ-ΦNO-ΦPSII relationships, offering implications for enhancing SIF-GPP relationships and understanding tropical forest responses to climate change.

Understanding how environmental drivers affect tree functioning is essential to improve predictions of tropical forests' response to climate change. While functional traits directly influence tree performance, our understanding of how canopy environments shape their coordination and variation along the vertical forest profile remains limited. We quantified annual growth rates in terms of above‐ground biomass (AGB), the maximum efficiency of photosystem II (Fv/Fm) and six tree functional traits related to water transport (xylem density and Huber value), leaf morphology (leaf size, angle and stomatal density) and photosynthesis (specific leaf area) along the vertical forest profile in an old‐growth central Amazonian forest. To investigate the influence of canopy environments and ontogenetic stages on the variation of these traits, we divided the forest into three vertical strata defined by height from the ground (S1: 0–20 m; S2: 20–40 m; S3: >40 m). We sampled 162 branches and 486 leaves from 54 trees of 10 species, encompassing at least five of the most abundant species per stratum. Path analysis and correlation matrices were used to explore the links between canopy environments, traits and the ‘fast–slow’ plant economics spectrum. We found significant effects of height on relative tree growth, leaf size and specific leaf area. Trait correlations varied across strata suggesting an ecological stratification of canopy functional niches. Trait–growth correlations increased in number and strength with increasing height, suggesting greater trait‐mediated growth control in large trees. Our results reveal how traits and strategies on the ‘fast–slow’ plant economics spectrum are vertically distributed and coordinated along the forest profile. Our findings highlight important interactions between species and canopy environments in determining plant traits, with emergent species showing adaptive strategies at different stages of their development. Read the free Plain Language Summary for this article on the Journal blog.

Diffusion of electrons over distances on the order of 100 μm has been observed in crystals of a small tetraheme cytochrome (STC) from Shewanella oneidensis [J. Huang et al. J. Am. Chem. Soc. 142, 10459–10467 (2020)]. Electron transfer between hemes in adjacent subunits of the crystal is slower and more strongly dependent on temperature than had been expected based on semiclassical electron-transfer theory. We here explore explanations for these findings by molecular-dynamics simulations of crystalline and monomeric STC. New procedures are developed for including time-dependent quantum mechanical energy differences in the gap between the energies of the reactant and product states and for evaluating fluctuations of the electronic-interaction matrix element that couples the two hemes. Rate constants for electron transfer are calculated from the time- and temperature-dependent energy gaps, coupling factors, and Franck–Condon-weighted densities of states using an expression with no freely adjustable parameters. Back reactions are considered, as are the effects of various protonation states of the carboxyl groups on the heme side chains. Interactions with water are found to dominate the fluctuations of the energy gap between the reactant and product states. The calculated rate constant for electron transfer from heme IV to heme Ib in a neighboring subunit at 300 K agrees well with the measured value. However, the calculated activation energy of the reaction in the crystal is considerably smaller than observed. We suggest two possible explanations for this discrepancy. The calculated rate constant for transfer from heme I to II within the same subunit of the crystal is about one-third that for monomeric STC in solution.

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Efforts to improve photosynthetic performance are increasingly employing natural genetic variation. However, genetic variation in the organellar genomes (plasmotypes) is often disregarded due to the difficulty of studying the plasmotypes and the lack of evidence that this is a worthwhile investment. Here, we systematically phenotyped plasmotype diversity using Arabidopsis thaliana as a model species. A reanalysis of whole-genome resequencing data of 1,541 representative accessions shows that the genetic diversity among the mitochondrial genomes is eight times lower than among the chloroplast genomes. Plasmotype diversity of the accessions divides the species into two major phylogenetic clusters, within which highly divergent subclusters are distinguished. We combined plasmotypes from 60 A. thaliana accessions with the nuclear genomes (nucleotypes) of four A. thaliana accessions to create a panel of 232 cytonuclear genotypes (cybrids). The cybrid plants were grown in a range of different light and temperature conditions and phenotyped using high-throughput phenotyping platforms. Analysis of the phenotypes showed that several plasmotypes alone or in interaction with the nucleotypes have significant effects on photosynthesis and that the effects are highly dependent on the environment. Moreover, we introduce Plasmotype Association Studies (PAS) as a method to reveal plasmotypic effects. Within A. thaliana, several organellar variants can influence photosynthetic phenotypes, which emphasizes the valuable role this variation has on improving photosynthetic performance. The increasing feasibility of producing cybrids in various species calls for further research into how these phenotypes may support breeding goals in crop species.

Spring plant regrowth can be impacted by overwintering stresses such as ice encasement and winter desiccation. The photosynthetic ramifications of these two stresses and whether chlorophyll fluorescence-based parameters during spring recovery may be efficient at differentiating winter survival of winter wheat (Triticum aestivum) is not well known. A panel of 10 winter wheat genotypes from various origins were exposed to surface ice encasement (2.54 cm deep) or winter desiccation in a low-temperature growth chamber and were transferred to a growth chamber containing high throughput photosynthetic imagers, which measured photosynthetic efficiency and non-photochemical quenching (NPQ) associated parameters. Antioxidant enzyme activity and lipid peroxidation were also measured but were only significant in response to treatment duration. Low-temperature dormancy or prolonged effects of each winter stress caused a decline in Fv/Fm, but Fv/Fm was not different in response to genotype. The NPQ parameters revealed dynamic stress responses and were better at distinguishing responses to each stress and between genotypes compared to Fv/Fm. Most NPQ parameters were recovered to control levels after 24 to 50 h of recovery. Measurements of qI and qE were effective for screening winter wheat genotypes for surface ice encasement. The Phi II values were slower to recover for winter desiccated plants compared to the surface ice-treated plants, indicating that this parameter may be a good indicator of soil moisture-associated stress during winter. Detailed photosynthetic health assessments including NPQ parameters are valuable for detecting overwintering stresses to overwintering crop species such as winter wheat.

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Galactolipids comprise the majority of chloroplast membranes in plants, and their biosynthesis requires dephosphorylation of phosphatidic acid at the chloroplast envelope membranes. In Arabidopsis (Arabidopsis thaliana), the lipid phosphate phosphatases LPPγ, LPPε1, and LPPε2 have been previously implicated in chloroplast lipid assembly, with LPPγ being essential, as null mutants were reported to exhibit embryo lethality. Here, we show that lppγ mutants are in fact viable and that LPPγ, LPPε1, and LPPε2 do not appear to have central roles in the plastid pathway of membrane lipid biosynthesis. Redundant LPPγ and LPPε1 activity at the outer envelope membrane is important for plant development, and the respective lppγ lppε1 double mutant exhibits reduced flux through the ER pathway of galactolipid synthesis. While LPPε2 is imported and associated with interior chloroplast membranes, its role remains elusive and does not include basal nor phosphate limitation-induced biosynthesis of glycolipids. The specific physiological roles of LPPγ, LPPε1, and LPPε2 are yet to be uncovered, as does the identity of the phosphatidic acid phosphatase required for plastid galactolipid biosynthesis.

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Kentucky bluegrass (Poa pratensis L.; drought resistant) and perennial ryegrass (Lolium perenne L.; drought sensitive) are economically important grass species contrasting in drought stress resistance. This study determined the optimal chlorophyll fluorescence parameters to indicate drought incidence and whether the parameters differentiate intra- and interspecies variations in drought stress. For each species, nine cultivars were exposed to well-watered or drought (water withheld) conditions in growth chambers containing high-throughput photosynthetic imagers to track real-time responses of maximum quantum efficiency of photosystem II (Fv/Fm), quantum yield of photosystem II (phi II), non-photochemical quenching (NPQ), energy-dependent quenching (qE), and photoinhibition-associated quenching (qI). Soil moisture content and relative water content of leaf tissues were evaluated. Due to drought, Fv/Fm and phi II decreased for cultivars of both species but earlier for perennial ryegrass compared to Kentucky bluegrass. The NPQ, qI, and qE values exhibited more dynamic and earlier changes due to drought compared to Fv/Fm and phi II and allowed for early, mid, and late drought responses to be illustrated. Drought induced an increase in NPQ, qI, and qE values, which corresponded to activation of photoprotection mechanisms, and was exhibited earlier for perennial ryegrass compared to Kentucky bluegrass. As the drought treatment progressed, a decrease or stabilization of low values of NPQ, qI, and qE was observed, and the lowest values were associated with the most drought-sensitive cultivars. These results indicate important stress tolerance protection mechanisms for grass species and will broadly impact basic and applied grass research as a nondestructive phenotyping tool. Kentucky bluegrass and perennial ryegrass contrast in drought resistance.Chlorophyll fluorescence parameters during drought responses reveal novel insight into resistance mechanisms.Plant non-photochemical protection strategies were activated by drought stress in both grass species.Measurements of non-photochemical quenching parameters indicated drought responses earlier than quantum efficiency.Non-photochemical parameters are good, early indicators of drought stress incidence in grass species.

In plant genomic experiments, correlations among various biological traits (phenotypes) give new insights into how genetic diversity may have tuned biological processes to enhance fitness under diverse conditions. Consequently, knowing how the correlations are affected by genetic (G) and environmental (E) factors helps develop climate-resilient plants. However, the current literature lacks any method for assessing the effect of predictors on pairwise correlations among multiple phenotypes together with easily interpretable model parameters. To address this need, we propose to model pairwise correlations directly in terms of G and E and develop a computationally efficient inference procedure. Two major novelties in our methodology are (1) the use of a composite pairwise likelihood method to avoid the positive definiteness restriction on the correlation matrix and (2) the use of a novel Minorize–Maximize (MM) algorithm for the efficient estimation of a large number of parameters. The proposed method shows excellent numerical performance on synthetic datasets. The analysis of the motivating data on cowpea reveals that the rates of solar energy storage by photosynthesis (the aggregate trait) are differentially affected by different genetic loci through two distinct processes: “photoinhibition” which results from photodamage caused by excess light, and “photoprotection” which protects plants from photodamage but also results in energy loss. Supplementary material to this paper is provided online.

The concentration of inorganic phosphate (Pi) in the chloroplast stroma must be maintained within narrow limits to sustain photosynthesis and to direct the partitioning of fixed carbon. However, it is unknown if these limits or the underlying contributions of different chloroplastic Pi transporters vary throughout the photoperiod or between chloroplasts in different leaf tissues. To address these questions, we applied live Pi imaging to Arabidopsis (Arabidopsis thaliana) wild-type plants and 2 loss-of-function transporter mutants: triose phosphate/phosphate translocator (tpt), phosphate transporter 2;1 (pht2;1), and tpt pht2;1. Our analyses revealed that stromal Pi varies spatially and temporally, and that TPT and PHT2;1 contribute to Pi import with overlapping tissue specificities. Further, the series of progressively diminished steady-state stromal Pi levels in these mutants provided the means to examine the effects of Pi on photosynthetic efficiency without imposing nutritional deprivation. Phi PSII and nonphotochemical quenching (NPQ) correlated with stromal Pi levels. However, the proton efflux activity of the ATP synthase (gH+) and the thylakoid proton motive force (pmf) were unaltered under growth conditions, but were suppressed transiently after a dark to light transition with return to wild-type levels within 2 min. These results argue against a simple substrate-level limitation of ATP synthase by depletion of stromal Pi, favoring more integrated regulatory models, which include rapid acclimation of thylakoid ATP synthase activity to reduced Pi levels. Mutational manipulation of chloroplast stromal phosphate content implicates integrated regulation of ATP synthase activity and photoprotective mechanisms.

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AbstractUnderstanding the regulation of photosynthetic light harvesting and electron transfer is of great importance to efforts to improve the ability of the electron transport chain to supply downstream metabolism. A central regulator of the electron transport chain is ATP synthase, the molecular motor that harnesses the chemiosmotic potential generated from proton-coupled electron transport to synthesize ATP. ATP synthase is regulated both thermodynamically and post-translationally, with proposed phosphorylation sites on multiple subunits. In this study we focused on two N-terminal serines on the catalytic subunit β in tobacco (Nicotiana tabacum), previously proposed to be important for dark inactivation of the complex to avoid ATP hydrolysis at night. Here we show that there is no clear role for phosphorylation in the dark inactivation of ATP synthase. Instead, mutation of one of the two phosphorylated serine residues to aspartate to mimic constitutive phosphorylation strongly decreased ATP synthase abundance. We propose that the loss of N-terminal phosphorylation of ATPβ may be involved in proper ATP synthase accumulation during complex assembly.

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Photorespiration consumes substantial amounts of energy in the forms of adenosine triphosphate (ATP) and reductant making the pathway an important component in leaf energetics. Because of this high reductant demand, photorespiration is proposed to act as a photoprotective electron sink. However, photorespiration consumes more ATP relative to reductant than the C3 cycle meaning increased flux disproportionally increases ATP demand relative to reductant. Here we explore how energetic consumption from photorespiration impacts the flexibility of the light reactions in nicotiana tabacum. Specifically, we demonstrate that decreased photosynthetic efficiency (ϕII ) at low photorespiratory flux was related to feedback regulation at the chloroplast ATP synthase. Additionally, decreased ϕII at high photorespiratory flux resulted in the accumulation of photoinhibition at photosystem II centers. These results are contrary to the proposed role of photorespiration as a photoprotective electron sink. Instead, our results suggest a novel role of ATP consumption from photorespiration in maintaining ATP synthase activity, with implications for maintaining energy balance and preventing photodamage that will be critical for plant engineering strategies.