Regulation of plant light harvesting by thermal dissipation of excess energy

2010 ◽  
Vol 38 (2) ◽  
pp. 651-660 ◽  
Author(s):  
Silvia de Bianchi ◽  
Matteo Ballottari ◽  
Luca Dall’Osto ◽  
Roberto Bassi
Keyword(s):  
Higher Plants ◽  
Current Knowledge ◽  
Protein Complexes ◽  
Thermal Dissipation ◽  
Photochemical Quenching ◽  
Knockout Mutants ◽  
Pigment Protein Complexes ◽  
Non Photochemical Quenching

Elucidating the molecular details of qE (energy quenching) induction in higher plants has proven to be a major challenge. Identification of qE mutants has provided initial information on functional elements involved in the qE mechanism; furthermore, investigations on isolated pigment–protein complexes and analysis in vivo and in vitro by sophisticated spectroscopic methods have been used for the elucidation of mechanisms involved. The aim of the present review is to summarize the current knowledge of the phenotype of npq (non-photochemical quenching)-knockout mutants, the role of gene products involved in the qE process and compare the molecular models proposed for this process.

scholarly journals Antenna Protein Clustering In Vitro Unveiled by Fluorescence Correlation Spectroscopy

2021 ◽  
Vol 22 (6) ◽  
pp. 2969
Author(s):  
Aurélie Crepin ◽  
Edel Cunill-Semanat ◽  
Eliška Kuthanová Trsková ◽  
Erica Belgio ◽  
Radek Kaňa
Keyword(s):  
Fluorescence Correlation Spectroscopy ◽  
Higher Plants ◽  
Fluorescence Emission ◽  
Correlation Spectroscopy ◽  
Photochemical Quenching ◽  
High Ph ◽  
Fluorescence Correlation ◽  
Non Photochemical Quenching

Antenna protein aggregation is one of the principal mechanisms considered effective in protecting phototrophs against high light damage. Commonly, it is induced, in vitro, by decreasing detergent concentration and pH of a solution of purified antennas; the resulting reduction in fluorescence emission is considered to be representative of non-photochemical quenching in vivo. However, little is known about the actual size and organization of antenna particles formed by this means, and hence the physiological relevance of this experimental approach is questionable. Here, a quasi-single molecule method, fluorescence correlation spectroscopy (FCS), was applied during in vitro quenching of LHCII trimers from higher plants for a parallel estimation of particle size, fluorescence, and antenna cluster homogeneity in a single measurement. FCS revealed that, below detergent critical micelle concentration, low pH promoted the formation of large protein oligomers of sizes up to micrometers, and therefore is apparently incompatible with thylakoid membranes. In contrast, LHCII clusters formed at high pH were smaller and homogenous, and yet still capable of efficient quenching. The results altogether set the physiological validity limits of in vitro quenching experiments. Our data also support the idea that the small, moderately quenching LHCII oligomers found at high pH could be relevant with respect to non-photochemical quenching in vivo.

The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions

2007 ◽  
Vol 34 (9) ◽  
pp. 759 ◽  
Author(s):  
Jose I. García-Plazaola ◽  
Shizue Matsubara ◽  
C. Barry Osmond
Keyword(s):  
Light Harvesting ◽  
Higher Plants ◽  
Protein Complexes ◽  
Light Exposure ◽  
Photosynthetic Pigment ◽  
In Vivo Studies ◽  
Photochemical Quenching ◽  
Strong Light

Several xanthophyll cycles have been described in photosynthetic organisms. Among them, only two are present in higher plants: the ubiquitous violaxanthin (V) cycle, and the taxonomically restricted lutein epoxide (Lx) cycle, whereas four cycles seem to occur in algae. Although V is synthesised through the β-branch of the carotenoid biosynthetic pathway and Lx is the product of the α-branch; both are co-located in the same sites of the photosynthetic pigment-protein complexes isolated from thylakoids. Both xanthophylls are also de-epoxidised upon light exposure by the same enzyme, violaxanthin de-epoxidase (VDE) leading to the formation of zeaxanthin (Z) and lutein (L) at comparable rates. In contrast with VDE, the reverse reaction presumably catalysed by zeaxanthin epoxidase (ZE), is much slower (or even inactive) with L than with antheraxanthin (A) or Z. Consequently many species lack Lx altogether, and although the presence of Lx shows an irregular taxonomical distribution in unrelated taxa, it has a high fidelity at family level. In those plants which accumulate Lx, variations in ZE activity in vivo mean that a complete Lx-cycle occurs in some (with Lx pools being restored overnight), whereas in others a truncated cycle is observed in which VDE converts Lx into L, but regeneration of Lx by ZE is extremely slow. Accumulation of Lx to high concentrations is found most commonly in old leaves in deeply shaded canopies, and the Lx cycle in these leaves is usually truncated. This seemingly anomalous situation presumably arises because ZE has a low but finite affinity for L, and because deeply shaded leaves are not often exposed to light intensities strong enough to activate VDE. Notably, both in vitro and in vivo studies have recently shown that accumulation of Lx can increase the light harvesting efficiency in the antennae of PSII. We propose a model for the truncated Lx cycle in strong light in which VDE converts Lx to L which then occupies sites L2 and V1 in the light-harvesting antenna complex of PSII (Lhcb), displacing V and Z. There is correlative evidence that this photoconverted L facilitates energy dissipation via non-photochemical quenching and thereby converts a highly efficient light harvesting system to an energy dissipating system with improved capacity to engage photoprotection. Operation of the α- and β-xanthophyll cycles with different L and Z epoxidation kinetics thus allows a combination of rapidly and slowly reversible modulation of light harvesting and photoprotection, with each cycle having distinct effects. Based on the patchy taxonomical distribution of Lx, we propose that the presence of Lx (and the Lx cycle) could be the result of a recurrent mutation in the epoxidase gene that increases its affinity for L, which is conserved whenever it confers an evolutionary advantage.

scholarly journals The role of LHCBM1 in non-photochemical quenching in Chlamydomonas reinhardtii

2022 ◽  
Author(s):  
Xin Liu ◽  
Wojciech J Nawrocki ◽  
Roberta Croce
Keyword(s):  
Chlamydomonas Reinhardtii ◽  
Protein Complexes ◽  
Ph Sensor ◽  
High Light ◽  
Photochemical Quenching ◽  
Knock Out ◽  
Photosynthetic Organisms ◽  
Pigment Protein Complexes ◽  
Non Photochemical Quenching

Non-photochemical 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 was abolished in the knock-out mutants of the pigment-protein complexes LHCSR3 and LHCBM1. However, while LHCSR3 was shown to be a pH sensor and switching to a quenched conformation at low pH, the role of LHCBM1 in NPQ has not been elucidated yet. In this work, we combine biochemical and physiological measurements to study short-term high light acclimation of npq5, the mutant lacking LHCBM1. We show that while in low light in the absence of this complex, the antenna size of PSII is smaller than in its presence, this effect is marginal in high light, implying that a reduction of the antenna is not responsible for the low NPQ. We also show that the mutant expresses LHCSR3 at the WT level in high light, indicating that the absence of this complex is also not the reason. Finally, NPQ remains low in the mutant even when the pH is artificially lowered to values that can switch LHCSR3 to the quenched conformation. It is concluded that both LHCSR3 and LHCBM1 need to be present 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.

scholarly journals Identification of parallel pH- and zeaxanthin-dependent quenching of excess energy in LHCSR3 in Chlamydomonas reinhardtii

2020 ◽  
Author(s):  
Julianne M. Troiano ◽  
Federico Perozeni ◽  
Raymundo Moya ◽  
Luca Zuliani ◽  
Kwangryul Baek ◽  
...  
Keyword(s):  
Chlamydomonas Reinhardtii ◽  
Light Harvesting ◽  
Complex Stress ◽  
Excess Energy ◽  
Photochemical Quenching ◽  
Light Harvesting Complexes ◽  
Light Harvesting Complex ◽  
Non Photochemical Quenching

AbstractUnder high light conditions, oxygenic photosynthetic organisms avoid photodamage by thermally dissipating excess absorbed energy, which is called non-photochemical quenching (NPQ). In green algae, a chlorophyll and carotenoid-binding protein, light-harvesting complex stress-related (LHCSR3), detects excess energy via pH and serves as a quenching site. However, the mechanisms by which LHCSR3 functions have not been determined. Using a combined in vivo and in vitro approach, we identify two parallel yet distinct quenching processes, individually controlled by pH and carotenoid composition, and their likely molecular origin within LHCSR3 from Chlamydomonas reinhardtii. The pH-controlled quenching is removed within a mutant LHCSR3 that lacks the protonable residues responsible for sensing pH. Constitutive quenching in zeaxanthin-enriched systems demonstrates zeaxanthin-controlled quenching, which may be shared with other light-harvesting complexes. We show that both quenching processes prevent the formation of damaging reactive oxygen species, and thus provide distinct timescales and mechanisms of protection in a changing environment.

scholarly journals From ecophysiology to phenomics: some implications of photoprotection and shade–sun acclimation in situ for dynamics of thylakoids in vitro

2012 ◽  
Vol 367 (1608) ◽  
pp. 3503-3514 ◽  
Author(s):  
Shizue Matsubara ◽  
Britta Förster ◽  
Melinda Waterman ◽  
Sharon A. Robinson ◽  
Barry J. Pogson ◽  
...  
Keyword(s):  
Membrane Dynamics ◽  
Persea Americana ◽  
Physiological Data ◽  
Photochemical Quenching ◽  
Shade Acclimation ◽  
Non Photochemical Quenching ◽  
Time Frames ◽  
Shade Leaves

Half a century of research into the physiology and biochemistry of sun–shade acclimation in diverse plants has provided reality checks for contemporary understanding of thylakoid membrane dynamics. This paper reviews recent insights into photosynthetic efficiency and photoprotection from studies of two xanthophyll cycles in old shade leaves from the inner canopy of the tropical trees Inga sapindoides and Persea americana (avocado). It then presents new physiological data from avocado on the time frames of the slow coordinated photosynthetic development of sink leaves in sunlight and on the slow renovation of photosynthetic properties in old leaves during sun to shade and shade to sun acclimation. In so doing, it grapples with issues in vivo that seem relevant to our increasingly sophisticated understanding of Δ pH-dependent, xanthophyll-pigment-stabilized non-photochemical quenching in the antenna of PSII in thylakoid membranes in vitro .

scholarly journals Photosynthesis without β-carotene

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Pengqi Xu ◽  
Volha U Chukhutsina ◽  
Wojciech J Nawrocki ◽  
Gert Schansker ◽  
Ludwik W Bielczynski ◽  
...  
Keyword(s):  
Dynamic Range ◽  
Protein Complexes ◽  
Tobacco Plant ◽  
Oxygenic Photosynthesis ◽  
Photochemical Quenching ◽  
Photoautotrophic Growth ◽  
Pigment Protein Complexes ◽  
Common Opinion ◽  
Non Photochemical Quenching ◽  
Β Carotene

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 β-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.

scholarly journals Allosteric regulation of the light-harvesting system of photosystem II

2000 ◽  
Vol 355 (1402) ◽  
pp. 1361-1370 ◽  
Author(s):  
Peter Horton ◽  
Alexander V. Ruban ◽  
Mark Wentworth
Keyword(s):  
Photosystem Ii ◽  
Xanthophyll Cycle ◽  
Light Harvesting ◽  
Allosteric Regulation ◽  
Photochemical Quenching ◽  
Protein Subunit ◽  
Ps Ii ◽  
Non Photochemical Quenching

Non–photochemical quenching of chlorophyll fluorescence (NPQ) is symptomatic of the regulation of energy dissipation by the light–harvesting antenna of photosystem II (PS II). The kinetics of NPQ in both leaves and isolated chloroplasts are determined by the transthylakoid ΔpH and the de–epoxidation state of the xanthophyll cycle. In order to understand the mechanism and regulation of NPQ we have adopted the approaches commonly used in the study of enzyme–catalysed reactions. Steady–state measurements suggest allosteric regulation of NPQ, involving control by the xanthophyll cycle carotenoids of a protonationdependent conformational change that transforms the PS II antenna from an unquenched to a quenched state. The features of this model were confirmed using isolated light–harvesting proteins. Analysis of the rate of induction of quenching both in vitro and in vivo indicated a bimolecular second–order reaction; it is suggested that quenching arises from the reaction between two fluorescent domains, possibly within a single protein subunit. A universal model for this transition is presented based on simple thermodynamic principles governing reaction kinetics.

scholarly journals Chlamydomonas reinhardtii LHCSR1 and LHCSR3 proteins involved in photoprotective non-photochemical quenching have different quenching efficiency and different carotenoid affinity

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Federico Perozeni ◽  
Giorgia Beghini ◽  
Stefano Cazzaniga ◽  
Matteo Ballottari
Keyword(s):  
Chlamydomonas Reinhardtii ◽  
Functional Properties ◽  
Carbon Fixation ◽  
Thermal Dissipation ◽  
Photochemical Quenching ◽  
High Sequence Identity ◽  
Pigment Analysis ◽  
Quenching Efficiency ◽  
Non Photochemical Quenching

AbstractMicroalgae are unicellular photosynthetic organisms considered as potential alternative sources for biomass, biofuels or high value products. However, their limited biomass productivity represents a bottleneck that needs to be overcome to meet the applicative potential of these organisms. One of the domestication targets for improving their productivity is the proper balance between photoprotection and light conversion for carbon fixation. In the model organism for green algae, Chlamydomonas reinhardtii, a photoprotective mechanism inducing thermal dissipation of absorbed light energy, called Non-photochemical quenching (NPQ), is activated even at relatively low irradiances, resulting in reduced photosynthetic efficiency. Two pigment binding proteins, LHCSR1 and LHCSR3, were previously reported as the main actors during NPQ induction in C. reinhardtii. While previous work characterized in detail the functional properties of LHCSR3, few information is available for the LHCSR1 subunit. Here, we investigated in vitro the functional properties of LHCSR1 and LHCSR3 subunits: despite high sequence identity, the latter resulted as a stronger quencher compared to the former, explaining its predominant role observed in vivo. Pigment analysis, deconvolution of absorption spectra and structural models of LHCSR1 and LHCR3 suggest that different quenching efficiency is related to a different occupancy of L2 carotenoid binding site.

scholarly journals Pre-purification of diatom pigment protein complexes provides insight into the heterogeneity of FCP complexes

2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Marcel Kansy ◽  
Daniela Volke ◽  
Line Sturm ◽  
Christian Wilhelm ◽  
Ralf Hoffmann ◽  
...  
Keyword(s):  
Spatial Organization ◽  
Higher Plants ◽  
Protein Complexes ◽  
Photosynthetic Apparatus ◽  
Thalassiosira Pseudonana ◽  
Photochemical Quenching ◽  
Complex Nature ◽  
Published Data ◽  
Core Complex ◽  
Pigment Protein Complexes

Abstract Background Although our knowledge about diatom photosynthesis has made huge progress over the last years, many aspects about their photosynthetic apparatus are still enigmatic. According to published data, the spatial organization as well as the biochemical composition of diatom thylakoid membranes is significantly different from that of higher plants. Results In this study the pigment protein complexes of the diatom Thalassiosira pseudonana were isolated by anion exchange chromatography. A step gradient was used for the elution process, yielding five well-separated pigment protein fractions which were characterized in detail. The isolation of photosystem (PS) core complex fractions, which contained fucoxanthin chlorophyll proteins (FCPs), enabled the differentiation between different FCP complexes: FCP complexes which were more closely associated with the PSI and PSII core complexes and FCP complexes which built-up the peripheral antenna. Analysis by mass spectrometry showed that the FCP complexes associated with the PSI and PSII core complexes contained various Lhcf proteins, including Lhcf1, Lhcf2, Lhcf4, Lhcf5, Lhcf6, Lhcf8 and Lhcf9 proteins, while the peripheral FCP complexes were exclusively composed of Lhcf8 and Lhcf9. Lhcr proteins, namely Lhcr1, Lhcr3 and Lhcr14, were identified in fractions containing subunits of the PSI core complex. Lhcx1, Lhcx2 and Lhcx5 proteins co-eluted with PSII protein subunits. The first fraction contained an additional Lhcx protein, Lhcx6_1, and was furthermore characterized by high concentrations of photoprotective xanthophyll cycle pigments. Conclusion The results of the present study corroborate existing data, like the observation of a PSI-specific antenna complex in diatoms composed of Lhcr proteins. They complement other data, like e.g. on the protein composition of the 21 kDa FCP band or the Lhcf composition of FCPa and FCPb complexes. They also provide interesting new information, like the presence of the enzyme diadinoxanthin de-epoxidase in the Lhcx-containing PSII fraction, which might be relevant for the process of non-photochemical quenching. Finally, the high negative charge of the main FCP fraction may play a role in the organization and structure of the native diatom thylakoid membrane. Thus, the results present an important contribution to our understanding of the complex nature of the diatom antenna system.

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