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1.
Plant Physiol ; 194(2): 936-944, 2024 Jan 31.
Artigo em Inglês | MEDLINE | ID: mdl-37847042

RESUMO

Nonphotochemical quenching (NPQ) is the process that protects photosynthetic organisms from photodamage by dissipating the energy absorbed in excess as heat. In the model green alga Chlamydomonas reinhardtii, NPQ is abolished in the knock-out mutants of the pigment-protein complexes LHCSR3 and LHCBM1. However, while LHCSR3 is a pH sensor and switches to a quenched conformation at low pH, the role of LHCBM1 in NPQ has not been elucidated yet. In this work, we combined biochemical and physiological measurements to study short-term high-light acclimation of npq5, the mutant lacking LHCBM1. In low light in the absence of this complex, the antenna size of PSII was smaller than in its presence; this effect was marginal in high light (HL), implying that a reduction of the antenna was not responsible for the low NPQ. The mutant expressed LHCSR3 at the wild-type level in HL, indicating that the absence of this complex is also not the reason. Finally, NPQ remained low in the mutant even when the pH was artificially lowered to values that can switch LHCSR3 to the quenched conformation. We concluded that both LHCSR3 and LHCBM1 are required for the induction of NPQ and that LHCBM1 is the interacting partner of LHCSR3. This interaction can either enhance the quenching capacity of LHCSR3 or connect this complex with the PSII supercomplex.


Assuntos
Chlamydomonas reinhardtii , Chlamydomonas reinhardtii/genética , Chlamydomonas reinhardtii/metabolismo , Luz , Complexo de Proteína do Fotossistema II/metabolismo , Fotossíntese/fisiologia , Temperatura Alta , Complexos de Proteínas Captadores de Luz/genética , Complexos de Proteínas Captadores de Luz/metabolismo
2.
New Phytol ; 240(2): 663-675, 2023 10.
Artigo em Inglês | MEDLINE | ID: mdl-37530066

RESUMO

Drought is a major abiotic stress that impairs plant growth and development. Despite this, a comprehensive understanding of drought effects on the photosynthetic apparatus is lacking. In this work, we studied the consequences of 14-d drought treatment on Arabidopsis thaliana. We used biochemical and spectroscopic methods to examine photosynthetic membrane composition and functionality. Drought led to the disassembly of PSII supercomplexes and the degradation of PSII core. The light-harvesting complexes (LHCII) instead remain in the membrane but cannot act as an antenna for active PSII, thus representing a potential source of photodamage. This effect can also be observed during nonphotochemical quenching (NPQ) induction when even short pulses of saturating light can lead to photoinhibition. At a later stage, under severe drought stress, the PSI antenna size is also reduced and the PSI-LHCI supercomplexes disassemble. Surprisingly, although we did not observe changes in the PSI core protein content, the functionality of PSI is severely affected, suggesting the accumulation of nonfunctional PSI complexes. We conclude that drought affects both photosystems, although at a different stage, and that the operative quantum efficiency of PSII (ΦPSII ) is very sensitive to drought and can thus be used as a parameter for early detection of drought stress.


Assuntos
Arabidopsis , Arabidopsis/metabolismo , Complexo de Proteína do Fotossistema I/metabolismo , Secas , Complexo de Proteína do Fotossistema II/metabolismo , Fotossíntese/fisiologia , Complexos de Proteínas Captadores de Luz/metabolismo , Clorofila/metabolismo
3.
Nat Commun ; 14(1): 4207, 2023 07 14.
Artigo em Inglês | MEDLINE | ID: mdl-37452043

RESUMO

While photosynthesis transforms sunlight energy into sugar, aerobic and anaerobic respiration (fermentation) catabolizes sugars to fuel cellular activities. These processes take place within one cell across several compartments, however it remains largely unexplored how they interact with one another. Here we report that the weak acids produced during fermentation down-regulate both photosynthesis and aerobic respiration. This effect is mechanistically explained with an "ion trapping" model, in which the lipid bilayer selectively traps protons that effectively acidify subcellular compartments with smaller buffer capacities - such as the thylakoid lumen. Physiologically, we propose that under certain conditions, e.g., dim light at dawn, tuning down the photosynthetic light reaction could mitigate the pressure on its electron transport chains, while suppression of respiration could accelerate the net oxygen evolution, thus speeding up the recovery from hypoxia. Since we show that this effect is conserved across photosynthetic phyla, these results indicate that fermentation metabolites exert widespread feedback control over photosynthesis and aerobic respiration. This likely allows algae to better cope with changing environmental conditions.


Assuntos
Respiração Celular , Fotossíntese , Anaerobiose , Fermentação , Respiração
4.
Front Plant Sci ; 13: 833032, 2022.
Artigo em Inglês | MEDLINE | ID: mdl-35330875

RESUMO

Light absorbed by chlorophylls of Photosystems II and I drives oxygenic photosynthesis. Light-harvesting complexes increase the absorption cross-section of these photosystems. Furthermore, these complexes play a central role in photoprotection by dissipating the excess of absorbed light energy in an inducible and regulated fashion. In higher plants, the main light-harvesting complex is trimeric LHCII. In this work, we used CRISPR/Cas9 to knockout the five genes encoding LHCB1, which is the major component of LHCII. In absence of LHCB1, the accumulation of the other LHCII isoforms was only slightly increased, thereby resulting in chlorophyll loss, leading to a pale green phenotype and growth delay. The Photosystem II absorption cross-section was smaller, while the Photosystem I absorption cross-section was unaffected. This altered the chlorophyll repartition between the two photosystems, favoring Photosystem I excitation. The equilibrium of the photosynthetic electron transport was partially maintained by lower Photosystem I over Photosystem II reaction center ratio and by the dephosphorylation of LHCII and Photosystem II. Loss of LHCB1 altered the thylakoid structure, with less membrane layers per grana stack and reduced grana width. Stable LHCB1 knockout lines allow characterizing the role of this protein in light harvesting and acclimation and pave the way for future in vivo mutational analyses of LHCII.

5.
Sci Adv ; 7(52): eabj0055, 2021 Dec 24.
Artigo em Inglês | MEDLINE | ID: mdl-34936440

RESUMO

Photosynthesis fuels life on Earth using sunlight as energy source. However, light has a simultaneous detrimental effect on the enzyme triggering photosynthesis and producing oxygen, photosystem II (PSII). Photoinhibition, the light-dependent decrease of PSII activity, results in a major limitation to aquatic and land photosynthesis and occurs upon all environmental stress conditions. In this work, we investigated the molecular origins of photoinhibition focusing on the paradoxical energy dissipation process of unknown nature coinciding with PSII damage. Integrating spectroscopic, biochemical, and computational approaches, we demonstrate that the site of this quenching process is the PSII reaction center. We propose that the formation of quenching and the closure of PSII stem from the same event. We lastly reveal the heterogeneity of PSII upon photoinhibition using structure-function modeling of excitation energy transfer. This work unravels the functional details of the damage-induced energy dissipation at the heart of photosynthesis.

6.
Plant Cell Environ ; 44(9): 3002-3014, 2021 09.
Artigo em Inglês | MEDLINE | ID: mdl-33599977

RESUMO

Vascular plants use carotenoids and chlorophylls a and b to harvest solar energy in the visible region (400-700 nm), but they make little use of the far-red (FR) light. Instead, some cyanobacteria have developed the ability to use FR light by redesigning their photosynthetic apparatus and synthesizing red-shifted chlorophylls. Implementing this strategy in plants is considered promising to increase crop yield. To prepare for this, a characterization of the FR light-induced changes in plants is necessary. Here, we explore the behaviour of Arabidopsis thaliana upon exposure to FR light by following the changes in morphology, physiology and composition of the photosynthetic complexes. We found that after FR-light treatment, the ratio between the photosystems and their antenna size drastically readjust in an attempt to rebalance the energy input to support electron transfer. Despite a large increase in PSBS accumulation, these adjustments result in strong photoinhibition when FR-adapted plants are exposed to light again. Crucially, FR light-induced changes in the photosynthetic membrane are not the result of senescence, but are a response to the excitation imbalance between the photosystems. This indicates that an increase in the FR absorption by the photosystems should be sufficient for boosting photosynthetic activity in FR light.


Assuntos
Adaptação Fisiológica/efeitos da radiação , Arabidopsis/efeitos da radiação , Luz , Arabidopsis/fisiologia , Clorofila/metabolismo , Fluorescência , Complexos de Proteínas Captadores de Luz/efeitos da radiação , Fotossíntese/efeitos da radiação , Complexo de Proteína do Fotossistema I/efeitos da radiação , Complexo de Proteína do Fotossistema II/efeitos da radiação , Folhas de Planta/efeitos da radiação , Tilacoides/efeitos da radiação
7.
Plant Physiol ; 184(4): 2040-2051, 2020 12.
Artigo em Inglês | MEDLINE | ID: mdl-33051267

RESUMO

PSI is an essential component of the photosynthetic apparatus of oxygenic photosynthesis. While most of its subunits are conserved, recent data have shown that the arrangement of the light-harvesting complexes I (LHCIs) differs substantially in different organisms. Here we studied the PSI-LHCI supercomplex of Botryococccus braunii, a colonial green alga with potential for lipid and sugar production, using functional analysis and single-particle electron microscopy of the isolated PSI-LHCI supercomplexes complemented by time-resolved fluorescence spectroscopy in vivo. We established that the largest purified PSI-LHCI supercomplex contains 10 LHCIs (∼240 chlorophylls). However, electron microscopy showed heterogeneity in the particles and a total of 13 unique binding sites for the LHCIs around the PSI core. Time-resolved fluorescence spectroscopy indicated that the PSI antenna size in vivo is even larger than that of the purified complex. Based on the comparison of the known PSI structures, we propose that PSI in B. braunii can bind LHCIs at all known positions surrounding the core. This organization maximizes the antenna size while maintaining fast excitation energy transfer, and thus high trapping efficiency, within the complex.


Assuntos
Arabidopsis/química , Arabidopsis/ultraestrutura , Chlamydomonas reinhardtii/química , Chlamydomonas reinhardtii/ultraestrutura , Complexos de Proteínas Captadores de Luz/química , Complexos de Proteínas Captadores de Luz/ultraestrutura , Modelos Moleculares , Conformação Proteica , Subunidades Proteicas
8.
Elife ; 92020 09 25.
Artigo em Inglês | MEDLINE | ID: mdl-32975516

RESUMO

Carotenoids are essential in oxygenic photosynthesis: they stabilize the pigment-protein complexes, are active in harvesting sunlight and in photoprotection. In plants, they are present as carotenes and their oxygenated derivatives, xanthophylls. While mutant plants lacking xanthophylls are capable of photoautotrophic growth, no plants without carotenes in their photosystems have been reported so far, which has led to the common opinion that carotenes are essential for photosynthesis. Here, we report the first plant that grows photoautotrophically in the absence of carotenes: a tobacco plant containing only the xanthophyll astaxanthin. Surprisingly, both photosystems are fully functional despite their carotenoid-binding sites being occupied by astaxanthin instead of ß-carotene or remaining empty (i.e. are not occupied by carotenoids). These plants display non-photochemical quenching, despite the absence of both zeaxanthin and lutein and show that tobacco can regulate the ratio between the two photosystems in a very large dynamic range to optimize electron transport.


Most life on Earth depends on photosynthesis, the process used by plants and many other organisms to store energy from sunlight and produce oxygen. The first steps of photosynthesis, the capture and conversion of sunlight into chemical energy, happen in large assemblies of proteins containing many pigment molecules called photosystems. In plants, the pigments involved in photosynthesis are green chlorophylls and carotenoids. In addition to harvesting light, carotenoids have an important role in preventing damage caused by overexposure to sunlight There are over one thousand different carotenoids in living beings, but only one, ß-carotene, is present in every organism that performs the type of photosynthesis in which oxygen is released, and is thought to be essential for the process. However, this could never be proved because it is impossible to remove ß-carotene from cells using typical genetic approaches without affecting all other carotenoids. Xu et al. used genetic engineering to create tobacco plants that produced a pigment called astaxanthin in place of ß-carotene. Astaxanthin is a carotenoid from salmon and shrimp, not normally found in plants. These plants are the first living things known to perform photosynthesis without ß-carotene and demonstrate that this pigment is not essential for photosynthesis as long as other carotenoids are present. Xu et al. also show that the photosystems can adapt to using different carotenoids, and can even operate with a reduced number of them. Xu et al's findings show the high flexibility of photosynthesis in plants, which are able to incorporate non-native elements to the process. These results are also important in the context of increasing the photosynthetic efficiency, and thus the productivity of crops, since they show that a radical redesign of the photosynthetic machinery is feasible.


Assuntos
Fotossíntese , beta Caroteno/fisiologia , Plantas Geneticamente Modificadas/metabolismo , Plantas Geneticamente Modificadas/fisiologia , Nicotiana/metabolismo , Nicotiana/fisiologia , Xantofilas/metabolismo , beta Caroteno/metabolismo
9.
Plant Physiol ; 182(1): 472-479, 2020 01.
Artigo em Inglês | MEDLINE | ID: mdl-31653716

RESUMO

The photosynthetic apparatus must be able to withstand light conditions that exceed its capacity for carbon fixation. Photosynthetic organisms developed nonphotochemical quenching (NPQ), a process that dissipates excess absorbed light energy as heat and limits the production of reactive oxygen species and cellular damage. In the green alga Chlamydomonas reinhardtii, the LHCSR pigment-binding proteins are essential for NPQ. These complexes are not constitutively present in the thylakoid membranes; however, in laboratory conditions their expression depends on prior high light exposure of cells. To investigate the role of NPQ, we measured cells grown under a day-night cycle with a high light peak at mid-day. LHCSRs are present and NPQ is active consistently throughout the day, likely due to their slow degradation in vivo. This suggests that in physiologically relevant conditions, Chlamydomonas cells are prepared to immediately activate photoprotection, as is the case in vascular plants. We further reveal that state transitions are fully functional under these conditions and that PsbS is highly expressed throughout the day, suggesting it might have a more impactful role than previously thought.


Assuntos
Chlamydomonas reinhardtii/metabolismo , Complexos de Proteínas Captadores de Luz/metabolismo , Chlamydomonas/metabolismo , Chlamydomonas/efeitos da radiação , Chlamydomonas reinhardtii/efeitos da radiação , Luz , Fotossíntese/fisiologia
10.
Nat Plants ; 5(11): 1177-1183, 2019 11.
Artigo em Inglês | MEDLINE | ID: mdl-31659240

RESUMO

In nature, plants experience large fluctuations in light intensity and they need to balance the absorption and utilization of this energy appropriately. Non-photochemical quenching (NPQ) is a rapidly switchable mechanism that protects plants from photodamage caused by high light exposure by dissipating the excess absorbed energy as heat. It is triggered by the pH gradient across the thylakoid membrane and requires the protein PsbS and the xanthophyll zeaxanthin. However, the site and mechanism of the quencher(s) remain unknown. Here, we constructed a mutant of Arabidopsis thaliana that lacks light-harvesting complex II (LHCII), the main antenna complex of plants, to verify its contribution to NPQ. The mutant plant has normally stacked thylakoid membranes, displays no upregulation of other LHCs but shows a relative decrease in Photosystem I (PSI), which compensates for the decrease of the PSII antenna. The mutant plant exhibits a reduction in NPQ of about 60% and the remaining NPQ resembles that of mutant plants lacking chlorophyll (Chl) b, which lack all PSII peripheral antenna complexes. We thus report that PsbS-dependent NPQ occurs mainly in LHCII, but there is an additional quenching site in the PSII core.


Assuntos
Arabidopsis/metabolismo , Complexo de Proteína do Fotossistema II/fisiologia , Arabidopsis/genética , Mutação , Processos Fotoquímicos , Complexo de Proteína do Fotossistema II/genética , Tilacoides/metabolismo
11.
Proc Natl Acad Sci U S A ; 116(17): 8320-8325, 2019 04 23.
Artigo em Inglês | MEDLINE | ID: mdl-30962362

RESUMO

Sunlight drives photosynthesis but can also cause photodamage. To protect themselves, photosynthetic organisms dissipate the excess absorbed energy as heat, in a process known as nonphotochemical quenching (NPQ). In green algae, diatoms, and mosses, NPQ depends on the light-harvesting complex stress-related (LHCSR) proteins. Here we investigated NPQ in Chlamydomonas reinhardtii using an approach that maintains the cells in a stable quenched state. We show that in the presence of LHCSR3, all of the photosystem (PS) II complexes are quenched and the LHCs are the site of quenching, which occurs at a rate of ∼150 ps-1 and is not induced by LHCII aggregation. The effective light-harvesting capacity of PSII decreases upon NPQ, and the NPQ rate is independent of the redox state of the reaction center. Finally, we could measure the pH dependence of NPQ, showing that the luminal pH is always above 5.5 in vivo and highlighting the role of LHCSR3 as an ultrasensitive pH sensor.


Assuntos
Proteínas de Algas/fisiologia , Chlamydomonas , Concentração de Íons de Hidrogênio , Fotossíntese/fisiologia , Complexo de Proteína do Fotossistema II/fisiologia , Proteínas de Algas/metabolismo , Chlamydomonas/fisiologia , Chlamydomonas/efeitos da radiação , Cinética , Complexo de Proteína do Fotossistema II/metabolismo , Espectrometria de Fluorescência , Temperatura
12.
Sci Rep ; 9(1): 888, 2019 01 29.
Artigo em Inglês | MEDLINE | ID: mdl-30696875

RESUMO

Colon tumours are hierarchically organized and contain multipotent self-renewing cells, called Cancer Stem Cells (CSCs). We have previously shown that the Notch1 receptor is expressed in Intestinal Stem Cells (ISCs); given the critical role played by Notch signalling in promoting intestinal tumourigenesis, we explored Notch1 expression in tumours. Combining lineage tracing in two tumour models with transcriptomic analyses, we found that Notch1+ tumour cells are undifferentiated, proliferative and capable of indefinite self-renewal and of generating a heterogeneous clonal progeny. Molecularly, the transcriptional signature of Notch1+ tumour cells highly correlates with ISCs, suggestive of their origin from normal crypt cells. Surprisingly, Notch1+ expression labels a subset of CSCs that shows reduced levels of Lgr5, a reported CSCs marker. The existence of distinct stem cell populations within intestinal tumours highlights the necessity of better understanding their hierarchy and behaviour, to identify the correct cellular targets for therapy.


Assuntos
Linhagem da Célula/fisiologia , Células-Tronco Neoplásicas/metabolismo , Receptor Notch1/genética , Animais , Biomarcadores/metabolismo , Diferenciação Celular/fisiologia , Proliferação de Células/fisiologia , Autorrenovação Celular/fisiologia , Transformação Celular Neoplásica/metabolismo , Neoplasias do Colo/patologia , Perfilação da Expressão Gênica/métodos , Humanos , Mucosa Intestinal/metabolismo , Neoplasias Intestinais/patologia , Intestinos/patologia , Intestinos/fisiologia , Camundongos , Camundongos Transgênicos , Receptor Notch1/metabolismo , Receptores Acoplados a Proteínas G/genética , Receptores Acoplados a Proteínas G/metabolismo , Transdução de Sinais
13.
Plant Physiol ; 179(2): 630-639, 2019 02.
Artigo em Inglês | MEDLINE | ID: mdl-30498023

RESUMO

Whereas photosynthetic function under steady-state light conditions has been well characterized, little is known about its changes that occur in response to light fluctuations. Chlororespiration, a simplified respiratory chain, is widespread across all photosynthetic lineages, but its role remains elusive. Here, we show that chlororespiration plays a crucial role in intermittent-light conditions in the green alga Chlamydomonas reinhardtii Chlororespiration, which is localized in thylakoid membranes together with the photosynthetic electron transfer chain, involves plastoquinone reduction and plastoquinol oxidation by a Plastid Terminal Oxidase (PTOX). We show that PTOX activity is critical for growth under intermittent light, with severe growth defects being observed in a mutant lacking PTOX2, the major plastoquinol oxidase. We demonstrate that the hampered growth results from a major change in the kinetics of redox relaxation of the photosynthetic electron transfer chain during the dark periods. This change, in turn, has a dramatic effect on the physiology of photosynthesis during the light periods, notably stimulating cyclic electron flow at the expense of the linear electron flow.


Assuntos
Chlamydomonas reinhardtii/crescimento & desenvolvimento , Chlamydomonas reinhardtii/metabolismo , Oxirredutases/metabolismo , Proteínas de Plantas/metabolismo , Chlamydomonas reinhardtii/genética , Complexo Citocromos b6f/metabolismo , Escuridão , Transporte de Elétrons , Luz , Mutação , Oxirredução , Oxirredutases/genética , Fotossíntese/fisiologia , Complexo de Proteína do Fotossistema I/metabolismo , Proteínas de Plantas/genética , Plastoquinona/análogos & derivados , Plastoquinona/metabolismo , Tilacoides/metabolismo , Regulação para Cima
14.
Nat Plants ; 2: 16031, 2016 04 04.
Artigo em Inglês | MEDLINE | ID: mdl-27249564

RESUMO

Photosynthesis converts sunlight into biologically useful compounds, thus fuelling practically the entire biosphere. This process involves two photosystems acting in series powered by light harvesting complexes (LHCs) that dramatically increase the energy flux to the reaction centres. These complexes are the main targets of the regulatory processes that allow photosynthetic organisms to thrive across a broad range of light intensities. In microalgae, one mechanism for adjusting the flow of energy to the photosystems, state transitions, has a much larger amplitude than in terrestrial plants, whereas thermal dissipation of energy, the dominant regulatory mechanism in plants, only takes place after acclimation to high light. Here we show that, at variance with recent reports, microalgal state transitions do not dissipate light energy but redistribute it between the two photosystems, thereby allowing a well-balanced influx of excitation energy.


Assuntos
Chlamydomonas/metabolismo , Microalgas/metabolismo , Fotossíntese , Complexo de Proteína do Fotossistema I/metabolismo , Complexo de Proteína do Fotossistema II/metabolismo , Aclimatação , Luz
15.
Annu Rev Plant Biol ; 66: 49-74, 2015.
Artigo em Inglês | MEDLINE | ID: mdl-25580838

RESUMO

Plastids have retained from their cyanobacterial ancestor a fragment of the respiratory electron chain comprising an NADPH dehydrogenase and a diiron oxidase, which sustain the so-called chlororespiration pathway. Despite its very low turnover rates compared with photosynthetic electron flow, knocking out the plastid terminal oxidase (PTOX) in plants or microalgae leads to severe phenotypes that encompass developmental and growth defects together with increased photosensitivity. On the basis of a phylogenetic and structural analysis of the enzyme, we discuss its physiological contribution to chloroplast metabolism, with an emphasis on its critical function in setting the redox poise of the chloroplast stroma in darkness. The emerging picture of PTOX is that of an enzyme at the crossroads of a variety of metabolic processes, such as, among others, the regulation of cyclic electron transfer and carotenoid biosynthesis, which have in common their dependence on the redox state of the plastoquinone pool, set largely by the activity of PTOX in darkness.


Assuntos
Cloroplastos/fisiologia , Transporte de Elétrons , Oxirredutases/metabolismo , Fotossíntese , Proteínas de Plantas/metabolismo , Plantas/metabolismo , Cloroplastos/enzimologia , Cloroplastos/metabolismo , Oxirredução , Oxirredutases/genética , Filogenia
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