Multiple roles of oxygen in the photoinactivation and dynamic repair of Photosystem II in spinach leaves (original) (raw)
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INTRODUCTION The Photoinactivation of Photosystem II in Leaves: A Personal Perspective
2001
A paradox of photosynthesis is that light is both required for the process and detrimental to the photosynthetic apparatus. In C 3 photosynthesis under light-limiting conditions, about 9 to 10 photons are sufficient for the evolution of one O 2 molecule Photosystem II components plastoquinone pool cytochrome b/f complex plastocyanin photosystem I components NADP + Photosystem (PS) II is the pigment-protein complex responsible for the photooxidation of water molecules. It has to generate oxidants that are sufficiently strong to oxidise water. Because of its role in forming such strong oxidants, PS II is highly susceptible to damage by the strong oxidants themselves, particularly in strong light. For example, a leaf exposed to full sun of 2000 µmol photons m -2 s -1 absorbs about 1700 µmol photons m -2 s -1 . If the light-saturated rate of photosynthesis corresponds to the evolution of 40 µmol O 2 m -2 s -1 , and the evolution of each O 2 molecule requires 10 photons, then 400 µmol ph...
Photoinactivation of Photosystem II in leaves
Photosynthesis Research, 2005
Photoinactivation of Photosystem II (PS II), the light-induced loss of ability to evolve oxygen, inevitably occurs under any light environment in nature, counteracted by repair. Under certain conditions, the extent of photoinactivation of PS II depends on the photon exposure (light dosage, x), rather than the irradiance or duration of illumination per se, thus obeying the law of reciprocity of irradiance and duration of illumination, namely, that equal photon exposure produces an equal effect. If the probability of photoinactivation (p) of PS II is directly proportional to an increment in photon exposure (p=kDx, where k is the probability per unit photon exposure), it can be deduced that the number of active PS II complexes decreases exponentially as a function of photon exposure: N=N o exp()kx). Further, since a photon exposure is usually achieved by varying the illumination time (t) at constant irradiance (I), N=N o exp()kI t), i.e., N decreases exponentially with time, with a rate coefficient of photoinactivation kI, where the product kI is obviously directly proportional to I. Given that N=N o exp()kx), the quantum yield of photoinactivation of PS II can be defined as )dN/dx=kN, which varies with the number of active PS II complexes remaining. Typically, the quantum yield of photoinactivation of PS II is ca. 0.1 lmol PS II per mol photons at low photon exposure when repair is inhibited. That is, when about 10 7 photons have been received by leaf tissue, one PS II complex is inactivated. Some species such as grapevine have a much lower quantum yield of photoinactivation of PS II, even at a chilling temperature. Examination of the longer-term time course of photoinactivation of PS II in capsicum leaves reveals that the decrease in N deviates from a single-exponential decay when the majority of the PS II complexes are inactivated in the absence of repair. This can be attributed to the formation of strong quenchers in severely photoinactivated PS II complexes which are able to dissipate excitation energy efficiently and to protect the remaining active neighbours against damage by light.
Photosynthesis Research, 2012
When visible light is excess, the photosynthetic machinery is photoinhibited. The extent of net photoinhibition of photosystem II (PSII) is determined by a balance between the rate of photodamage to D1 and some other PSII proteins and the rate of the turnover cycle of these proteins. It is widely believed that the protein turnover requires much energy cost. The aims of this study are to (1) evaluate the energy cost of PSII repair, (2) measure the benefit in terms of photosynthetic gain realized by the repairing of the photodamaged PSII, and (3) know whether acclimation of photosynthesis to growth light affects the rates of the photodamage and repair. We grew spinach in high-light (HL) and low-light (LL) and measured the rates of D1 photodamage and repair in these leaves. We determined the rate constants of photodamage (k pi ) and repair (k rec ) by the PAM fluorometry in the presence or in the absence of lincomycin, an inhibitor of 70S protein synthesis. HL leaves showed smaller k pi and greater k rec than LL leaves. The energy cost of the repairing of the photodamaged D1 protein was \0.5 % of ATP produced by photophosphorylation at PPFDs ranging from 400 to 1600 lmol m -2 s -1 and was greater in HL leaves than in LL leaves. The benefits brought about by the repair were more than from 35 to 270 times the cost at PPFDs ranging from 400 to 1600 lmol m -2 s -1 . The benefits of HL leaves were greater than those of LL leaves because of the higher photosynthesis rates in HL leaves. Running a simple simulation of daily photosynthesis using the parameters obtained in this study, we discuss why the plants need to pay the cost of D1 protein turnover to repair the photodamaged PSII.
The time course of photoinactivation of photosystem II in leaves revisited
Photosynthesis Research, 2012
Since photosystem II (PS II) performs the demanding function of water oxidation using light energy, it is susceptible to photoinactivation during photosynthesis. The time course of photoinactivation of PS II yields useful information about the process. Depending on how PS II function is assayed, however, the time course seems to differ. Here, we revisit this problem by using two additional assays: (1) the quantum yield of oxygen evolution in limiting, continuous light and (2) the flash-induced cumulative delivery of PS II electrons to the oxidized primary donor (P700 ? ) in PS
The photoinactivation of photosystem II in leaves: A personal perspective
2001
a, a parameter that describes how effectively photoinactivated PS II units protect their functional neighbours; Car, carotenoids; pH, transthylakoid pH difference; D1 protein, psbA gene product in the PS II reaction centre; f, functional fraction of PS II; F v /F m , the ratio of variable to maximum chlorophyll a fluorescence; k d , rate coefficient for degradation of D1 protein; k i and k r , rate coefficient for photoinactivation and repair of PS II, respectively; NADP + , oxidized nicotinamide adenine dinucleotide phosphate; P680, the primary electron donor in the PS II reaction centre; Ph, pheophytin; PS, photosystem; Q A , first quinone acceptor of an electron in PS II; R s , the gross rate of D1 protein synthesis.
Physiologia Plantarum, 2011
Photosystem II (PS II) is photoinactivated during photosynthesis, requiring repair to maintain full function during the day. What is the mechanism(s) of the initial events that lead to photoinactivation of PS II? Two hypotheses have been put forward. The 'excess-energy hypothesis' states that excess energy absorbed by chlorophyll (Chl), neither utilized in photosynthesis nor dissipated harmlessly in non-photochemical quenching, leads to PS II photoinactivation; the 'Mn hypothesis' (also termed the two-step hypothesis) states that light absorption by the Mn cluster in PS II is the primary effect that leads to dissociation of Mn, followed by damage to the reaction centre by light absorption by Chl. Observations from various studies support one or the other hypothesis, but each hypothesis alone cannot explain all the observations. We propose that both mechanisms operate in the leaf, with the relative contribution from each mechanism depending on growth conditions or plant species. Indeed, in a single system, namely, the interior of a leaf, we could observe one or the other mechanism at work, depending on the location within the tissue. There is no reason to expect the two mechanisms to be mutually exclusive.
Oxygen-evolution patterns from spinach Photosystem II preparations
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1983
Patterns of O 2 evolution resulting from sequences of short flashes are reported for Photosystem (PS) II preparations isolated from spinach and containing an active, O2-evolving system. The results can be interpreted in terms of the S-state model developed to explain the process of photosynthetic water splitting in chloroplasts and algae. The PS II samples display damped, oscillating patterns of 02 evolution with a period of four flashes. Unlike chloroplasts, the flash yields of the preparations decay with increasing flash number due to the limited plastoquinone acceptor pool on the reducing side of PS II. The optimal pH for 0 2 evolution in this system (pH 5.5-6.5) is more acidic than in chloroplasts (pH 6.5-8.0). The O2-evolution , inactivation half-time of dark-adapted preparations was 91 min (on the rate electrode) at room temperature. Dark-inactivation half-times of 14 h were observed ff the samples were aged off the electrode at room temperature. Under our conditions (experimental conditions can influence flash-sequence results), deactivation of S 3 was first order with a half-time of 105 s while that of S 2 was biphasic. The half-times for the first-order rapid phase were 17 s (one preflash) and 23 s (two preflashes). The longer S 2 phase deactivated very slowly (the minimum half-time observed was 265 s). These results indicate that deactivation from S 3-, S 2 ~ St, thought to be the dominant pathway in chloroplasts, is not the case for PS II preparations. Finally, it was demonstrated that the ratio of S~ to S o can be set by previously developed techniques, that S o is formed mostly from activated S 3 ($4), and that both S o and S t are stable in the dark.
Photosynthesis Research, 1996
Photoinactivation of Photosystem (PS) II in vivo was investigated by cumulative exposure of pea, rice and spinach leaves to light pulses of variable duration from 2 to 100 s, separated by dark intervals of 30 min. During each light pulse, photosynthetic induction occurred to an extent depending on the time of illumination, but steady-state photosynthesis had not been achieved. During photosynthetic induction, it is clearly demonstrated that reciprocity of irradiance and duration of illumination did not hold: hence the same cumulative photon exposure (mol m -2) does not necessarily give the same extent of photoinactivation of PS II. This contrasts with the situation of steady-state photosynthesis where the photoinactivation of PS II exhibited reciprocity of irradiance and duration of illumination (Park et al. (1995) Planta 196:401-411). We suggest that, for reciprocity to hold between irradiance and duration of illumination, there must be a balance between photochemical (qP) and non-photochemical (NPQ) quenching at all irradiances. The index of susceptibility to light stress, which represents an intrinsic ability of PS II to balance photochemical and non-photochemical quenching, is defined by the quotient (1 -qP)/NPQ. Although constant in steady-state photosynthesis under a wide range of irradiance (Park et al. (1995). Plant Cell Physiol 36:1163-1169), this index of susceptibility for spinach leaves declined extremely rapidly during photosynthetic induction at a given irradiance, and, at a given cumulative photon exposure, was dependent on irradiance. During photosynthetic induction, only limited photoprotective strategies are developed: while the transthylakoid pH gradient conferred some degree of photoprotection, neither D1 protein turnover nor the xanthophyll cycle was operative. Thus, PS II is more easily photoinactivated during photosynthetic induction, a phenomenon that may have relevance for understorey leaves experiencing infrequent, short sunflecks.
Physiologia Plantarum, 2006
Photosystem II (PSII) complexes, which split water into oxygen, protons and electrons in photosynthesis, require light but are also inactivated by it. Recovery of PSII from photoinactivation requires de novo protein synthesis. PSII in capsicum leaf segments were photoinactivated in the absence of chloroplast-encoded protein synthesis. At large photon exposures and despite the absence of repair, a residual fraction of PSII remained functional, being ca 0.08-0.2 depending on the ease of gas exchange in the tissue. This study revealed that the residual functional PSII was photoprotected by both (1) reaction-center quenching of excitation energy by photoinactivated PSII even when little or no PSII activity was permitted, and (2) antenna quenching, which was dependent on a trans-thylakoid pH gradient sustained mainly by linear electron transport and facilitated by the residual functional PSII complexes themselves. Significantly, little or no contribution to photoprotection of PSII was observed from cyclic electron flow around PSI. Further, the small residual functional PSII population was critical for recovery of the photoinactivated PSII complexes. Thus, photoinactivated and residual functional PSII complexes in leaves play a mutually beneficial role in each other's ultimate survival.
The rate coefficient of repair of photosystem II after photoinactivation
Physiologia Plantarum, 2003
During photosynthesis, photoinactivation and repair of photosystem II (PSII) occur simultaneously, resulting in a net loss of functional PSII under a given irradiance. This study determines the rate coefficients for the partial processes, allowing the calculation of the partial rates at any concentration of functional/non-functional PSII. The rate coefficient of photoinactivation was obtained from the onset of photoinactivation of PSII in leaf segments of Capsicum annuum L. in the absence of repair, and was in turn used to obtain the rate coefficient (k r ) of repair of PSII when repair was occurring.