Photoinhibition
Encyclopedia
Photosynthesis
Photosynthesis is a chemical process that converts carbon dioxide into organic compounds, especially sugars, using the energy from sunlight. Photosynthesis occurs in plants, algae, and many species of bacteria, but not in archaea. Photosynthetic organisms are called photoautotrophs, since they can...
capacity of a plant
Plant
Plants are living organisms belonging to the kingdom Plantae. Precise definitions of the kingdom vary, but as the term is used here, plants include familiar organisms such as trees, flowers, herbs, bushes, grasses, vines, ferns, mosses, and green algae. The group is also called green plants or...
, alga
Algae
Algae are a large and diverse group of simple, typically autotrophic organisms, ranging from unicellular to multicellular forms, such as the giant kelps that grow to 65 meters in length. They are photosynthetic like plants, and "simple" because their tissues are not organized into the many...
, or cyanobacterium. Photosystem II
Photosystem II
Photosystem II is the first protein complex in the Light-dependent reactions. It is located in the thylakoid membrane of plants, algae, and cyanobacteria. The enzyme uses photons of light to energize electrons that are then transferred through a variety of coenzymes and cofactors to reduce...
(PSII) is more sensitive to light than the rest of the photosynthetic machinery, and most researchers define the term as light-induced damage to PSII. In living organisms, photoinhibited PSII centres are continuously repaired via degradation and synthesis of the D1 protein of the photosynthetic reaction center of PSII. Photoinhibition is also used in a wider sense, as dynamic photoinhibition, to describe all reactions that decrease the efficiency of photosynthesis when plants are exposed to light.
History
The first measurements of photoinhibition were published in 1956 by Bessel Kok. Even in the very first studies, it was obvious that plants have a repair mechanism that continuously repairs photoinhibitory damage. In 1966, Jones and Kok measured the action spectrum of photoinhibition and found that ultraviolet light is highly photoinhibitory. The visible-light part of the action spectrum was found to have a peak in the red-light region, suggesting that chlorophylls act as photoreceptors of photoinhibition. In the 1980s, photoinhibition became a popular topic in photosynthesis research, and the concept of a damaging reaction counteracted by a repair process was re-invented. Research was stimulated by a paper by Kyle, Ohad and Arntzen in 1984, showing that photoinhibition is accompanied by selective loss of a 32-kDa protein, later identified as the PSII reaction center protein D1. The photosensitivity of PSII from which the oxygen evolving complex had been inactivated with chemical treatment was studied in the 1980s and early 1990s. A paper by Imre Vass and coworkers in 1992 described the acceptor-side mechanism of photoinhibition. Measurements of production of singlet oxygenSinglet oxygen
Singlet oxygen is the common name used for the diamagnetic form of molecular oxygen , which is less stable than the normal triplet oxygen. Because of its unusual properties, singlet oxygen can persist for over an hour at room temperature, depending on the environment...
by photoinhibited PSII provided further evidence for an acceptor-side-type mechanism. The concept of a repair cycle that continuously repairs photoinhibitory damage, evolved and was reviewed by Aro et al. in 1993. Many details of the repair cycle, including the finding that the FtsH protease
Protease
A protease is any enzyme that conducts proteolysis, that is, begins protein catabolism by hydrolysis of the peptide bonds that link amino acids together in the polypeptide chain forming the protein....
plays an important role in the degradation of the D1 protein, have been discovered since. In 1996, a paper by Tyystjärvi and Aro showed that the rate constant of photoinhibition is directly proportional to light intensity, a result that opposed the former assumption that photoinhibition is caused by the fraction of light energy that exceeds the maximum capability of photosynthesis. The following year, laser pulse photoinhibition experiments done by Itzhak Ohad's group led to the suggestion that charge recombination reactions may be damaging because they can lead to production of singlet oxygen. The molecular mechanism(s) of photoinhibition are constantly under discussion. The newest candidate is the manganese
Manganese
Manganese is a chemical element, designated by the symbol Mn. It has the atomic number 25. It is found as a free element in nature , and in many minerals...
mechanism suggested 2005 by the group of Esa Tyystjärvi. A similar mechanism was suggested by the group of Norio Murata, also in 2005.
What is inhibited
Photoinhibition occurs in all organisms capable of oxygenic photosynthesis, from vascular plants to cyanobacteria. In both plants and cyanobacteria, blue light causes photoinhibition more efficiently than other wavelengths of visible light, and all wavelengths of ultraviolet light are more efficient than wavelengths of visible light. Photoinhibition is a series of reactions that inhibit different activities of PSII, but there is no consensus on what these steps are. The activity of the oxygen-evolving complex of PSII is often found to be lost before the rest of the reaction centre loses activity. However, inhibition of PSII membranes under anaerobic conditions leads primarily to inhibition of electron transfer on the acceptor side of PSII. Ultraviolet light causes inhibition of the oxygen-evolving complex before the rest of PSII becomes inhibited. Photosystem IPhotosystem I
Photosystem I is the second photosystem in the photosynthetic light reactions of algae, plants, and some bacteria. Photosystem I is so named because it was discovered before photosystem II. Aspects of PS I were discovered in the 1950s, but the significances of these discoveries was not yet known...
(PSI) is less susceptible to light-induced damage than PSII, but slow inhibition of this photosystem has been observed. Photoinhibition of PSI occurs in chilling-sensitive plants and the reaction depends on electron flow from PSII to PSI.
How often does damage occur?
Photosystem II is damaged by light irrespective of light intensity. The quantum yieldQuantum yield
The quantum yield of a radiation-induced process is the number of times that a defined event occurs per photon absorbed by the system. The "event" may represent a chemical reaction, for example the decomposition of a reactant molecule:...
of the damaging reaction in typical leaves of higher plants exposed to visible light, as well as in isolated thylakoid
Thylakoid
A thylakoid is a membrane-bound compartment inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thylakoids frequently form stacks of disks referred to as...
membrane preparations, is in the range of 10−8 to 10−7 and independent of the intensity of light. This means that one PSII complex is damaged for every 10-100 million photon
Photon
In physics, a photon is an elementary particle, the quantum of the electromagnetic interaction and the basic unit of light and all other forms of electromagnetic radiation. It is also the force carrier for the electromagnetic force...
s that are intercepted. Therefore, photoinhibition occurs at all light intensities and the rate constant of photoinhibition is directly proportional to light intensity. Some measurements suggest that dim light causes damage more efficiently than strong light.
Molecular mechanism(s)
The mechanism(s) of photoinhibition are under debate, several mechanisms have been suggested. Reactive oxygen speciesReactive oxygen species
Reactive oxygen species are chemically reactive molecules containing oxygen. Examples include oxygen ions and peroxides. Reactive oxygen species are highly reactive due to the presence of unpaired valence shell electrons....
, especially singlet oxygen, have a role in the acceptor-side, singlet oxygen and low-light mechanisms. In the manganese mechanism and the donor side mechanism, reactive oxygen species do not play a direct role. Photoinhibited PSII produces singlet oxygen, and reactive oxygen species inhibit the repair cycle of PSII by inhibiting protein synthesis in the chloroplast.
Acceptor-side photoinhibition
Strong light causes the reduction of the plastoquinonePlastoquinone
Plastoquinone is a quinone molecule involved in the electron transport chain in the light-dependent reactions of photosynthesis. Plastoquinone is reduced , forming plastoquinol...
pool, which leads to protonation and double reduction (and double protonation) of the QA electron acceptor of Photosystem II. The protonated and double-reduced forms of QA do not function in electron transport. Furthermore, charge recombination reactions in inhibited Photosystem II are expected to lead to the triplet state of the primary donor (P680) more probably than same reactions in active PSII. Triplet P680 may react with oxygen to produce harmful singlet oxygen.
Donor-side photoinhibition
If the oxygen-evolving complex is chemically inactivated, then the remaining electron transfer activity of PSII becomes very sensitive to light. It has been suggested that even in a healthy leaf, the oxygen-evolving complex does not always function in all PSII centers, and those ones are prone to rapid irreversible photoinhibition.Manganese mechanism
A photon absorbed by the manganese ions of the oxygen-evolving complex triggers inactivation of the oxygen-evolving complex. Further inhibition of the remaining electron transport reactions occurs like in the donor-side mechanism. The mechanism is supported by the action spectrum of photoinhibition.Singlet oxygen mechanisms
Inhibition of PSII is caused by singlet oxygen produced either by weakly coupled chlorophyll molecules or by cytochromeCytochrome
Cytochromes are, in general, membrane-bound hemoproteins that contain heme groups and carry out electron transport.They are found either as monomeric proteins or as subunits of bigger enzymatic complexes that catalyze redox reactions....
s or iron-sulfur
Iron-sulfur protein
Iron-sulfur proteins are proteins characterized by the presence of iron-sulfur clusters containing sulfide-linked di-, tri-, and tetrairon centers in variable oxidation states...
centers.
Low-light mechanism
Charge recombination reactions of PSII cause the production of triplet P680 and, as a consequence, singlet oxygen. Charge recombination is more probable under dim light than under higher light intensities.Kinetics and action spectrum
Photoinhibition follows simple first-order kinetics if measured from a lincomycinLincomycin
Lincomycin is a lincosamide antibiotic that comes from the actinomyces Streptomyces lincolnensis. It has been structurally modified by thionyl chloride to its more commonly known 7-chloro-7-deoxy derivative, clindamycin...
-treated leaf, cyanobacterial or algal cells, or isolated thylakoid membranes in which concurrent repair does not disturb the kinetics. Data from the group of W. S. Chow indicate that in leaves of pepper (Capsicum annuum
Capsicum annuum
Capsicum annuum is a domesticated species of the plant genus Capsicum native to southern North America and northern South America. The three species C. annuum, C. frutescens and C. chinense all evolved from a single common ancestor located somewhere in the northwest Brazil - Colombia area...
), the first-order pattern is replaced by a pseudo-equilibrium even if the repair reaction is blocked. The deviation has been explained by assuming that photoinhibited PSII centers protect the remaining active ones.
Both visible and ultraviolet light cause photoinhibition, ultraviolet wavelengths being much more damaging. Some researchers consider ultraviolet and visible light induced photoinhibition as a two different reactions, while others stress the similarities between the inhibition reactions occurring under different wavelength ranges.
PSII repair cycle
Photoinhibition occurs continuously when plants or cyanobacteria are exposed to light, and the photosynthesizing organism must, therefore, continuously repair the damage. The PSII repair cycle, occurring in chloroplasts and in cyanobacteria, consists of degradation and synthesis of the D1 protein of the PSII reaction centre, followed by activation of the reaction center. Due to the rapid repair, most PSII reaction centers are not photoinhibited even if a plant is grown in strong light. However, environmental stresses, for example, extreme temperatures, salinitySalinity
Salinity is the saltiness or dissolved salt content of a body of water. It is a general term used to describe the levels of different salts such as sodium chloride, magnesium and calcium sulfates, and bicarbonates...
, and drought, limit the supply of carbon dioxide
Carbon dioxide
Carbon dioxide is a naturally occurring chemical compound composed of two oxygen atoms covalently bonded to a single carbon atom...
for use in carbon fixation
Carbon fixation
In biology, carbon fixation is the reduction of carbon dioxide to organic compounds by living organisms. The obvious example is photosynthesis. Carbon fixation requires both a source of energy such as sunlight, and an electron donor such as water. All life depends on fixed carbon. Organisms that...
, which decreases the rate of repair of PSII.
In photoinhibition studies, repair is often stopped by applying an antibiotic (lincomycin or chloramphenicol
Chloramphenicol
Chloramphenicol is a bacteriostatic antimicrobial that became available in 1949. It is considered a prototypical broad-spectrum antibiotic, alongside the tetracyclines, and as it is both cheap and easy to manufacture it is frequently found as a drug of choice in the third world.Chloramphenicol is...
) to plants or cyanobacteria, which blocks protein synthesis in the chloroplast
Chloroplast
Chloroplasts are organelles found in plant cells and other eukaryotic organisms that conduct photosynthesis. Chloroplasts capture light energy to conserve free energy in the form of ATP and reduce NADP to NADPH through a complex set of processes called photosynthesis.Chloroplasts are green...
. Protein synthesis occurs only in an intact sample, so lincomycin is not needed when photoinhibition is measured from isolated membranes. The repair cycle of PSII recirculates other subunits of PSII (except for the D1 protein) from the inhibited unit to the repaired one.
Protective mechanisms
Plants have mechanisms that protect against adverse effects of strong light. The most studied biochemical protective mechanism is non-photochemical quenchingNon-photochemical quenching
Non-photochemical quenching is a mechanism employed by plants and algae to protect themselves from the adverse effects of high light intensity. It involves the quenching of singlet excited state chlorophylls via enhanced internal conversion to the ground state , thus harmlessly dissipating...
of excitation energy. Visible-light-induced photoinhibition is ~25% faster in an Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana is a small flowering plant native to Europe, Asia, and northwestern Africa. A spring annual with a relatively short life cycle, arabidopsis is popular as a model organism in plant biology and genetics...
mutant lacking non-photochemical quenching than in the wild type
Wild type
Wild type refers to the phenotype of the typical form of a species as it occurs in nature. Originally, the wild type was conceptualized as a product of the standard, "normal" allele at a locus, in contrast to that produced by a non-standard, "mutant" allele...
. It is also apparent that turning or folding of leaves, as occurs, e.g., in Oxalis
Oxalis
Oxalis is by far the largest genus in the wood-sorrel family Oxalidaceae: of the approximately 900 known species in the Oxalidaceae, 800 belong here...
species in response to exposure to high light, protects against photoinhibition.
Measurement
Thylakoid
A thylakoid is a membrane-bound compartment inside chloroplasts and cyanobacteria. They are the site of the light-dependent reactions of photosynthesis. Thylakoids consist of a thylakoid membrane surrounding a thylakoid lumen. Chloroplast thylakoids frequently form stacks of disks referred to as...
membranes or their subfractions, or from intact cyanobacterial cells by measuring the light-saturated rate of oxygen evolution in the presence of an artificial electron acceptor (quinone
Quinone
A quinone is a class of organic compounds that are formally "derived from aromatic compounds [such as benzene or naphthalene] by conversion of an even number of –CH= groups into –C– groups with any necessary rearrangement of double bonds," resulting in "a fully conjugated cyclic dione structure."...
s and dichlorophenol-indophenol have been used).
The degree of photoinhibition in intact leaves can be measured using a fluorimeter to measure the ratio of variable to maximum value of chlorophyll a fluorescence (FV/FM). This ratio can be used as a proxy of photoinhibition because more energy is emitted as fluorescence from Chlorophyll a when many excited electrons from PSII are not captured by the acceptor and decay back to their ground state.
When measuring FV/FM, the leaf must be incubated in the dark for at least 10 minutes, preferably longer, before the measurement, in order to let non-photochemical quenching relax.
Flashing light
Photoinhibition can also be induced with short flashes of light using either a pulsed laserLaser
A laser is a device that emits light through a process of optical amplification based on the stimulated emission of photons. The term "laser" originated as an acronym for Light Amplification by Stimulated Emission of Radiation...
or a xenon flash lamp
Flashtube
A flashtube, also called a flashlamp, is an electric arc lamp designed to produce extremely intense, incoherent, full-spectrum white light for very short durations. Flashtubes are made of a length of glass tubing with electrodes at either end and are filled with a gas that, when triggered, ionizes...
. When very short flashes are used, the photoinhibitory efficiency of the flashes depends on the time difference between the flashes. This dependence has been interpreted to indicate that the flashes cause photoinhibition by inducing recombination reactions in PSII, with subsequent production of singlet oxygen. The interpretation has been criticized by noting that the photoinhibitory efficiency of xenon flashes depends on the energy of the flashes even if such strong flashes are used that they would saturate the formation of the substrate of the recombination reactions.
Dynamic photoinhibition
Some researchers prefer to define the term “photoinhibition” so that it contains all reactions that lower the quantum yield of photosynthesis when a plant is exposed to light. In this case, the term "dynamic photoinhibition" comprises phenomena that reversibly down-regulate photosynthesis in the light and the term "photodamage" or "irreversible photoinhibition" covers the concept of photoinhibition used by other researchers. The main mechanism of dynamic photoinhibition is non-photochemical quenchingNon-photochemical quenching
Non-photochemical quenching is a mechanism employed by plants and algae to protect themselves from the adverse effects of high light intensity. It involves the quenching of singlet excited state chlorophylls via enhanced internal conversion to the ground state , thus harmlessly dissipating...
of excitation energy absorbed by PSII. Dynamic photoinhibition is acclimation to strong light rather than light-induced damage, and therefore "dynamic photoinhibition" may actually protect the plant against "photoinhibition".
See also
- AnthocyaninAnthocyaninAnthocyanins are water-soluble vacuolar pigments that may appear red, purple, or blue according to pH...
- ChlorophyllChlorophyllChlorophyll is a green pigment found in almost all plants, algae, and cyanobacteria. Its name is derived from the Greek words χλωρος, chloros and φύλλον, phyllon . Chlorophyll is an extremely important biomolecule, critical in photosynthesis, which allows plants to obtain energy from light...
- Kautsky effectKautsky effectKautsky effect is a phenomenon consisting on a typical variation on the behavior of a plant fluorescence when is exposed to light. It was discovered in 1931 by H. Kautsky and A...
- Light reaction
- Photosynthetic reaction centrePhotosynthetic reaction centreA photosynthetic reaction center is a complex of several proteins, pigments and other co-factors assembled together to execute the primary energy conversion reactions of photosynthesis...
- PhotosynthesisPhotosynthesisPhotosynthesis is a chemical process that converts carbon dioxide into organic compounds, especially sugars, using the energy from sunlight. Photosynthesis occurs in plants, algae, and many species of bacteria, but not in archaea. Photosynthetic organisms are called photoautotrophs, since they can...