What is the significance of electron transport in photochemical reactions of photosynthesis

A dilution series of WT proteins was loaded on gels to estimate the protein level in the mutant. Equal amounts of chlorophyll were loaded in each lane of a gel. How to cite this article : Yamori, W. Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light.

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Download PDF. Subjects C3 photosynthesis Photosystem I. This article has been updated. Abstract Cyclic electron transport around photosystem I PS I was discovered more than a half-century ago and two pathways have been identified in angiosperms.

Introduction Regulation of photosynthetic electron transport in the thylakoid membrane of chloroplasts is fundamental for the maximum photosynthetic yield and plant growth. Figure 1. Characterization of the crr6 mutant by Chl fluorescence analysis and immunoblot analysis. Full size image. Figure 2. Effect of the crr6 defect on plant biomass production. Table 1 Effect of growth light on leaf properties and photosynthetic components.

Full size table. Figure 3. Figure 4. Figure 5. Effect of the crr6 defect on alleviation of photoinhibition. Discussion The NDH-dependent cyclic electron transport has been proposed to prevent over-reduction of the stroma under severe stress conditions 1 , Analysis of gas exchange, chlorophyll fluorescence and P measurements Measurements of gas exchange, chlorophyll fluorescence and P redox state were performed simultaneously with a GFS and a Dual-PAM measuring system Walz, Effeltrich, Germany in uppermost, fully expanded new leaves of to days-old plants as described Sometimes the name is qualified to imply that it is inducible or regulated e.

Hendrickson et al. In the absence of stress, energy-dependent quenching qE is the dominant component of NPQ that develops at irradiances above light-limiting levels and it increases with irradiance.

The formation of qE depends on lumen acidification resulting from electron transport and upon the presence of the PsbS protein of PSII. Lumen acidification results in protonation of the PsbS protein, triggering qE formation Li et al. The formation of the xanthophyll pigment, zeaxanthin, is also induced by lumen acidification Kramer et al.

The binding of a fraction of the zeaxanthin pool to an as yet unknown protein not PsbS; Johnson and Ruban, also facilitates the quenching process induced by lumen acidification Ruban et al. Zeaxanthin accumulation results in enhanced quenching at higher although still acidic lumen pH values, consistent with earlier observations Noctor et al. Much uncertainty remains regarding the precise mechanism of the qE mechanism, and several models have been proposed Jahns and Holzwarth, ; Ruban et al.

While it is clear that pH changes, facilitated by the presence of zeaxanthin and PsbS, result in structural changes in PSII, it is still not certain how these changes result in the formation of quenching centres.

In this way, the rate of PSII electron transport, i. Although qE is the most commonly encountered form of PSII regulation, other mechanisms exist and are important under some circumstances Demmig-Adams and Adams, The responses of different plant species, such as Arabidopsis , soybean, maize, rice, and poplar, to growth with CO 2 enrichment has been extensively characterized over the last 30 years Miyazaki et al.

Growth with CO 2 enrichment has a positive effect on the plant growth, and yield of C 3 species by the stimulation of yield is often much smaller than expected in many crop species Long et al.

A stimulation of net photosynthesis can be observed even when plants are grown for long periods at high CO 2 Idso and Kimball, ; Gunderson et al. The acclimation of photosynthesis observed in C 3 plants grown for long periods at elevated CO 2 is related to a substantial re-programming of gene expression Fukayama et al.

When C 3 plants are grown for long periods under high CO 2 , they tend to become carbohydrate rich Delucia et al. Alterations of gene expression patterns in response to elevated CO 2 are at least in part related to altered sugar signalling because the expression of photosynthetic genes is rapidly inhibited when plants are supplied with exogenous sugars Krapp et al. Field studies have consistently confirmed that reduced or insufficient sink capacity leads to an increase in leaf carbohydrates and down-regulation of photosynthetic capacity.

While genetic factors play an important role in photosynthetic response to high CO 2 , the down-regulation of transcripts encoding Rubisco and other proteins associated with CO 2 fixation and an up-regulation of those encoding proteins involved in RuBP regeneration and starch synthesis is a common response to long-term growth with CO 2 enrichment Leakey et al.

The acclimation of photosynthesis to long-term growth with CO 2 enrichment is also related to enhanced nutrient demands, particularly for nitrogen and phosphorus. Nitrogen uptake and assimilation can fail to keep pace with the higher rates of photosynthesis and assimilate production.

Furthermore, growth at elevated CO 2 can inhibit shoot nitrate assimilation in C 3 plants if primary nitrate assimilation in the cytosol requires photorespiration for the provision of NADH Rachmilevitch et al. Long-term growth with CO 2 enrichment improves nitrogen use efficiency and favours higher rates of dark respiration Leakey et al. The acclimation of photosynthesis to elevated CO 2 observed in C 3 plants is largely absent from C 4 plants Prins et al.

Experiments conducted in free-air concentration enrichment FACE experiments have consistently shown that photosynthesis in C 4 plants such as maize is not changed when plants are grown at elevated CO 2 Leakey et al. Moreover, leaf transcriptome patterns are similar in leaves from plants at high CO 2 and those grown in air Kim et al. The expression of nuclear genes encoding photosynthetic proteins is influenced by a plethora of metabolic, developmental, and environmental triggers.

However, the unifying central feature of this control is that expression of photosynthetic proteins is highly responsive to chloroplast retrograde signals that reflect the metabolic state of the organelle Fey et al. The components of the photosynthetic electron transport chain are important sensors of light quantity and quality, over-reduction, overoxidation, or imbalances between components that trigger long- and short-term light acclimation processes that serve to optimize light harvesting and CO 2 fixation for growth and development Havaux and Niyogi, ; Karpinski et al.

Changes in photosynthetic energy metabolism are sensed by oxidative and reductive signalling pathways that regulate gene transcription and post-transcriptional processing Pfannschmidt and Liere, Metabolites and proteins that are exchanged between the chloroplasts, cytosol, and nucleus also make a key contribution to the coordination of gene expression in the nucleus and chloroplast Baier and Dietz, ; Weber and Fischer, Mitochondria are also important in cellular energy and redox metabolism, and it is therefore not surprising that they influence the transmission of retrograde chloroplast signals to the nucleus Pesaresi et al.

Light drives photosynthetic electron transport and is the most important factor in the control of photosynthetic gene expression Ma et al. The diurnal patterns of photosynthetic gene expression are fundamentally controlled by circadian clock regulators with input from photoreceptors such as phytochromes, crytochromes, phototropins, and Zeitlupe-like proteins Ma et al. Phototropins control light-induced movement responses that are considered to optimize photosynthesis.

Crytochromes are important in regulating plant responses to excess excitation energy responses Kleine et al. Excess excitation energy describes light energy that cannot be used to drive photosynthetic metabolism Karpinski et al. Exposure to high light causes rapid re-programming of gene transcription Pogson et al. The repression of LHC genes by high light is found in organisms as diverse as barley and Dunaliella Masuda et al.

ELIP2 is considered to be a sensor and negative regulator of chl biosynthesis Tzvetkova-Chevolleau et al. Responses to changing light intensity involve changes not only in photosynthesis but also in leaf water status and temperature that activate multiple signalling pathways including abscisic acid ABA , salicylic acid SA , and other hormone-mediated signal transduction systems Fryer et al. Light-induced changes in stomatal conductance result in a photorespiratory H 2 O 2 burst Mateo et al.

H 2 O 2 signalling from the peroxisome contributes to the information on the redox changes in the PET chain, particularly the PQ pool, that influence photosynthetic gene expression. High CO 2 is able to prevent many of these negative effects of exposure to high light by preventing over-reduction of the PET chain. The level of CO 2 can also influence photosystem composition.

Exposure to UV-B often decreases photosynthetic gene expression Mackerness et al. COP1 is inactivated by photoreceptor signalling in the light and participates in the inactivation of light-responsive genes in the dark Ma et al. HY5 is also important in photoreceptor signalling pathways Lee et al. Chl biosynthesis precursors porphyrins have long been known to play an important role in chloroplast to nucleus retrograde signalling pathways Johanningmeier and Howell, ; Nott et al.

The genomes uncoupled gun mutants, gun2 , 3 , 4 , and 5 , are affected in enzymes of porphyrin metabolism in Arabidopsis Mochizuki et al. The concept that Mg-protoporphyrin IX and its monomethylester are signals in retrograde signalling Oster et al. The recent characterization of a new Arabidopsis gun mutant gun 6 - 1D suggests a role for haem synthesized by the plastid ferrochelatase I as a regulator of photosynthesis-associated nuclear genes Woodson et al.

Changes in light quality can therefore lead to imbalances in light capture by the photosystems. It is not surprising, therefore, that the relative abundance of PSII and PSI is regulated by light quality to ensure optimal photosynthesis efficiency. In early studies, the electron transport inhibitors 3- 3,4-dichlorophenyl -1,1-dimethylurea DCMU and 2,5-dibromo methylisopropyl- p -benzoquinone DBMIB , which induce either oxidation or reduction of the PQ pool, respectively, were used extensively to study the effects of the reduction state of the PQ pool on chloroplast to nucleus retrograde signalling pathways Escoubas et al.

Accumulating evidence demonstrates that the redox state of the PQ pool modulates several independent redox signalling pathways that serve to regulate photosynthetic efficiency by the post-translational modification of existing light-harvesting and reaction centre proteins and by the activation of reaction centre gene transcription Allen et al. This process re-distributes absorbed excitation energy so that the relative rates of photochemical conversion and turnover in each reaction centre are balanced.

A second major target for redox-regulated protein phosphorylation is the chloroplast RNA polymerase complex called the plastid-encoded polymerase PEP. The signalling cascades triggered by reduction of the PQ pool interface with the other signalling pathways triggered by the PET chain and metabolism, particularly the singlet oxygen, H 2 O 2 , and glutathione pathways. Redox signalling pathways involving some of these components have been considered at length in other reviews and will therefore not be considered here in detail see, for example, Foyer and Noctor, ; Foyer and Shigeoka , ; Noctor et al.

Substantial re-programming of photosynthetic gene expression occurs when C 3 plants are grown under conditions where photorespiration is diminished or inhibited Miyazaki et al. In contrast, in comparisons of leaf transcriptomes of C 4 plants grown with CO 2 enrichment or with air, such changes in gene expression patterns are much less apparent Leakey et al.

Such observations are consistent with the absence of a high CO 2 -dependent stimulation of photosynthesis or growth in C 4 plants such as maize Leakey et al. However, growth with CO 2 enrichment alters stomatal opening and conductance in a similar manner in C 3 and C 4 plants.

For example, stomatal conductance values were significantly higher in leaves of maize plants grown under ambient CO 2 conditions compared with those from plants grown at high CO 2 Prins et al. Regardless of the CO 2 -dependent effects on whole plant water status, C 4 leaf transcriptome patterns are similar in plants unchanged by atmospheric CO 2 availability Kim et al.

Patterns of transcriptional changes occurring following the transition from growth at high CO 2 to air in C 3 leaves might therefore be used as an indicator of the influence of photorespiration on the photosynthetic control of gene expression Queval et al.

The published data sets for A. Of the probe sets 22 present on the A. A large number of genes involved in signalling, protein synthesis, and degradation or encoding transcription factors were modified following the transition from high CO 2 to photorespiratory conditions Table 2. Similar observations were made in rice Fukayama et al.

Taken together, available data show that CO 2 availability exerts a much greater major influence on the genes involved in signal transduction and protein metabolism in C 3 species than on those encoding proteins with functions in primary processes such as carbon, nitrogen, or lipid metabolism Ainsworth et al. Of the differentially expressed genes involved in photosynthesis, photorespiration, respiration, and carbon metabolism in A. Arabidopsis thaliana genes that respond to atmospheric CO 2 availability Queval et al.

The number of transcripts that were significantly induced or repressed in leaves 2 d and 4 d after transfer from high CO 2 growth conditions to air are listed according to Functional categories.

Transcripts encoding thylakoid electron transport chain components that were differentially expressed 2 d and 4 d after transfer from growth at high CO 2 to air. Grey bars, 2 d after transfer; white bars, 4 d after transfer. Transcripts encoding proteins associated with photorespiration, carbon fixation, and sucrose and starch synthesis that were differentially expressed 2 d and 4 d after transfer from growth at high CO 2 to air. A, carbon metabolism; B, nitrogen and sulphur metabolism.

The transcriptome comparisons of A. In contrast, LHCB2. Simplified scheme for the thylakoid electron transport chain showing the location of proteins encoded by genes whose expression is altered following the transfer from high CO 2 to air. Letters that are underlined indicate that the abundance of transcripts was lower in air relative to high CO 2 , while the absence of underlining indicates transcripts whose abundance was higher in air than in high CO 2.

This figure is available in colour at JXB online. As discussed above, a decrease in atmospheric CO 2 availability requires a change in the generation of ATP relative to NADPH by the PET chain in order to accommodate the alterations in chloroplast metabolism associated with enhanced flux through the photorespiration pathways.

One of the most striking features of the transcriptome signature of Arabidopsis leaves photosynthesizing in air compared with high CO 2 Queval et al. Of the genes encoding photosynthetic components that were induced after transfer to photorespiratory conditions Fig. The location of proteins encoded by these genes within the PET chain is indicated in Fig. The enhanced abundance of transcripts encoding components of the NDH complex and associated cyclic electron flow pathways Suorsa et al.

Moreover, the repression of VDE1 might suggest that photosynthetic control of gene expression operates to decrease NPQ in the face of the enhanced demand for protons to make ATP as illustrated in Fig. The second striking feature of the transcriptome signatures of Arabidopsis leaves in air compared with high CO 2 is the absence of large changes in transcripts encoding enzymes of carbon fixation or photorespiration Queval et al.

However, transcripts encoding two proteins involved in photosynthetic carbon metabolism were increased in expression in air relative to high CO 2 Fig. Only six genes encoding proteins involved in starch and sucrose synthesis Fig. These results are consistent with decreased starch production when CO 2 availability is low and photorespiration is increased Fig.

Simplified scheme showing the photosynthetic carbon reduction Calvin—Benson cycle and the photosynthetic carbon oxidation cycle and associated ammonia re-assimilation pathways. The figure indicates the location of proteins encoded by genes whose expression is altered following the transfer from high CO 2 to air. Gene lists for carbon fixation, nitrogen assimilation and photorespiration, were assembled as described in Fig.

Depiction of the pathways of sucrose synthesis in the cytosol and starch synthesis in the chloroplasts showing the location of proteins encoded by genes whose expression is altered following the transfer from high CO 2 to air. Gene lists for starch and sucrose metabolism were assembled as described in Fig.

Transcripts encoding proteins involved in nitrogen assimilation that were repressed under photorespiratory conditions in Arabidopsis leaves include NRT1. These data are consistent with the findings of other studies regarding the higher requirement for nitrogen and sulphur metabolites in plants grown with CO 2 enrichment Fig. A surprisingly large number of transcription factors were differentially expressed in response to photorespiration Table 2. Transcripts encoding the most photorespiration-repressed and photorespiration-induced transcription factors are shown in Fig.

Interestingly, of the photorespiration-induced transcription factors, eight belong to the dehydration-responsive element-binding DREB subfamily. This finding is consistent with the higher level of stomatal opening, transpiration, and water transport that accompanies the transfer of C 3 leaves from high CO 2 growth conditions to air.

None of the eight photorespiration-induced DREB transcription factors has yet been ascribed roles in the regulation of photosynthetic gene expression. Transcripts encoding the 10 most repressed or induced transcription factors 2 d and 4 d after transfer from growth at high CO 2 to air. The apetala2. C-repeat binding factors 1 and 3 CBF1 and CBF3 are involved in cold acclimation and they are regulated by a core component of the circadian clock Dong et al. Other transcription factors that were altered in expression following the transfer from high CO 2 growth conditions to air Fig.

These changes are consistent with recently described interactions between CO 2 and daylength in the control of gene expression Queval et al. Transcripts encoding the pseudo-response regulator 7 PRR7 that is an element involved in the feedback loop controlling circadian rhythms Nakamichi et al. In contrast, circadian 1 CIR1 is up-regulated by photorespiratory conditions.

The expression of CIR1 follows a circadian rhythm, and perturbations in its expression affect flowering time and the circadian regulation of several genes, including Lhcb Zhang et al. Transcripts encoding the LOB domain 41 LBD41 transcription factor, which is responsive to the oxygen level, were greatly decreased in abundance following the transfer to photorespiratory conditions Fig. Hypoxia induces the expression of LBD41 ; this transcription factor activates the promoter of an anaerobic gene [non-symbiotic haemoglobin 1 HB1 ; Licausi et al.

Since the ambient oxygen concentration was maintained constant at air levels in all conditions, it is of note that the expression of LBD41 is highly sensitive to the transfer from non-photorespiratory to photorespiratory conditions. Photosynthetic control operates at multiple levels in order to balance energy supply and energy demand and optimize photosynthetic efficiency, while minimizing potentially harmful back reactions.

This balancing act not only involves matching output assimilated carbon to input light and CO 2 within a fluctuating environment temperature, water status, and other potential stress factors but it also requires the production of ATP and reductant at appropriate ratios.

These ratios are responsive to metabolic factors, requiring flexibility in the relative rates of production. This flexibility is achieved through rapid, short-term modifications in post-translational controls and longer term regulation through effects on gene expression. The classical example of photosynthetic control of gene expression is the altered expression of genes that encode the core apoproteins of the photosystems that accompanies state transitions.

It is rarely applied to transcriptome changes associated with varying metabolic demands for ATP and reductant, such as occur when the rate of photorespiration is varied relative to photosynthesis. The evidence presented here demonstrates that appropriate transcriptional responses are triggered in A.

Moreover, transcripts associated with cyclic electron transport and NPQ respond in a way that is consistent with the expected alterations in supply and demand of ATP relative to reductant. The changes in transcriptome signatures that accompany alterations in atmospheric CO 2 availability are similar in different C 3 species, with the most impact on genes involved in signalling and protein turnover Ainsworth et al.

CO 2 enrichment also has an impact on the expression of genes encoding proteins involved in photosynthesis, such as light reaction components that tend to be decreased under CO 2 enrichment Li et al. The change in the transcription patterns of cyclic electron transport genes in A. Thus transient changes in photorespiration that may occur, for example, in response to changes in stomatal conductance could influence the expression of genes encoding cyclic pathway proteins.

C 4 grasses consistently exhibit lower maximum stomatal conductance to water than C 3 grasses, together with shifts towards smaller stomata at a given density Taylor et al. Carbonic anhydrases have been suggested to function early in the CO 2 signalling pathway that controls stomatal movement and hence gas exchange between plants and the atmosphere Hu et al.

The response of specific photosynthesis genes to changes in CO 2 concentration is accompanied by modified expression of specific transcription factors. As previously discussed Queval et al. Because patterns of CO 2 -regulated stomatal closure and hence associated signalling are similar in C 3 and C 4 plants, key questions remain concerning why C 3 and C 4 leaves do not show similar gene expression changes related to altered leaf water status as atmospheric CO 2 availability is changed Leakey et al.

A major difference between the two photosynthetic groups is the low level of photorespiration in C 4 plants and the absence of any effects of high CO 2 on photosynthesis in these species. One possibility is that the altered expression of transcription factors such as the DREB family members observed in the C 3 species, A.

Thus, changes associated with photorespiration and PET could be a proxy sensor for water status in C 3 plants, or at least act as a reinforcing signal that tones the response to changes in this status. This hypothesis requires further study to elucidate relationships of cause and effect. Considerable literature evidence supports the view that photosynthetic control is embedded not only within the whole cell physiology of the leaf but also in genome biology and control.

This is therefore an important point to consider when identifying potential targets for improving photosynthesis through selection or genetic modification. Models describing how metabolism and electron and proton transport activities interact are also an important tool in better understanding the integration of metabolism with electron transport and ATP synthesis e. Yin et al. They can thus establish some boundary conditions for chloroplast function. These models cannot, however, replace a direct experimental analysis of the regulation of electron transport in relation to metabolism.

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Sign In or Create an Account. Sign In. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Concepts of energy production and utilization.

Evidence for photosynthetic control of gene expression associated with photorespiration. Conclusions and perspectives. Photosynthetic control of electron transport and the regulation of gene expression. Foyer , Christine H. E-mail: c. Oxford Academic. Jenny Neukermans. Guillaume Queval. Graham Noctor. Jeremy Harbinson. Revision received:. Cite Cite Christine H.

Select Format Select format. Permissions Icon Permissions. Open in new tab Download slide. Table 1. Open in new tab. Table 2. Functional categories Number of genes Induced Repressed Protein metabolism 95 Transcription factors 94 Signalling 26 Stress response 38 68 Photosynthesis, photo respiration and carbon metabolism 34 70 Transport 30 68 DNA synthesis and repair 5 74 Development 26 49 Hormone metabolism 30 33 Secondary metabolism 28 20 Nitrogen and sulphur metabolism 9 26 Lipid metabolism 16 17 Cell wall metabolism 12 21 Cell cycle and division 0 32 Redox processes 17 10 Unknown function CO 2 concentration in the substomatal cavity.

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