Modifications to the photosynthetic apparatus of higher plants in response to changes in the light environment

A brief review of the photosynthetic apparatus of higher plants is given, followed by a consideration of the modifications induced in this apparatus by changes in light intensity and light quality. Possible strategies by which plants may optimize photosynthetic activity by both long- and short-term modifications of their photosynthetic apparatus in response to changing light regimes are discussed.     

Changes in the photosynthetic apparatus of maize in response to simulated natural temperature fluctuations

The response of the photosynthetic apparatus to low temperature periods differed among three hybrids of maize (Zea mays L.) grown in a phytotron. Light-saturated photosynthetic rates, leaf chlorophyll content, and mesophyll cell photosynthetic unit density all declined with increasing duration of low temperature. No single metabolic or physiological parameter appeared to control the response of the three hybrids to low temperature stress. Among all temperature treatments, net photosynthetic rate on a leaf area basis was more closely correlated with leaf chlorophyll content than with any other measured parameter. Final shoot dry weight was most highly correlated with stomatal conductance to CO₂.     

Acclimation of the photosynthetic apparatus to low light in a thermophilic Synechococcus sp. strain

Depending upon their growth responses to high and low irradiance, respectively, thermophilic Synechococcus sp. isolates from microbial mats associated with the effluent channels of Mushroom Spring, an alkaline siliceous hot spring in Yellowstone National Park, can be described as either high-light (HL) or low-light (LL) ecotypes. Strains isolated from the bottom of the photic zone grow more rapidly at low irradiance compared to strains isolated from the uppermost layer of the mat, which conversely grow better at high irradiance. The LL-ecotypes develop far-red absorbance and fluorescence emission features after growth in LL. These isolates have a unique gene cluster that encodes a putative cyanobacteriochrome denoted LcyA, a putative sensor histidine kinase; an allophycocyanin (FRL-AP; ApcD4-ApcB3) that absorbs far-red light; and a putative chlorophyll a-binding protein, denoted IsiX, which is homologous to IsiA. The emergence of FRL absorbance in LL-adapted cells of Synechococcus sp. strain A1463 was analyzed in cultures responding to differences in light intensity. The far-red absorbance phenotype arises from expression of a novel antenna complex containing the FRL-AP, ApcD4-ApcB3, which is produced when cells were grown at very low irradiance. Additionally, the two GAF domains of LcyA were shown to bind phycocyanobilin and a [4Fe-4S] cluster, respectively. These ligands potentially enable this photoreceptor to respond to a variety of environmental factors including irradiance, redox potential, and/or oxygen concentration. The products of the gene clusters specific to LL-ecotypes likely facilitate growth in low-light environments through a process called Low-Light Photoacclimation.

     

Acclimation of Arabidopsis thaliana to the light environment: Changes in composition of the photosynthetic apparatus

Acclimation to changes in the light environment was investigated in Arabidopsis thaliana (L.) Heynh. cv. Landsberg erecta. Plants grown under four light regimes showed differences in their development, morphology, photosynthetic performance and in the composition of the photosynthetic apparatus. Plants grown under high light showed higher maximum rates of oxygen evolution and lower levels of light-harvesting complexes than their low light-grown counterparts; plants transferred to low light showed rapid changes in maximum photosynthetic rate and chlorophyll-a/b ratio as they became acclimated to the new environment. In contrast, plants grown under lights of differing spectral quality showed significant differences in the ratio of photosystem II to photosystem I. These changes are consistent with a model in which photosynthetic metabolism provides signals which regulate the composition of the thylakoid membrane.Abbreviations Aac1 gene encoding actin - Chl chlorophyll - F far-red-enriched light (R:FR = 0.72) - FR far-red light - H high light (400 mol · m^–2 · s^–1) - L low light (100 ml · m^–2 · s^–1) - LHCII light-harvesting complex of PSII - Lhcb genes encoding the proteins of LHCII - R red light - Rbcs genes encoding the small subunit of Rubisco - Rubisco ribulose-1,5-bisphosphate carboxylase/oxygenase - W white light (R:FR = 1.40) This work was supported by Natural Environment Research Council Grant No. GR3/7571A. We would like to thank H. Smith (Botany Department, University of Leicester) and E. Murchie (University of Sheffield) for helpful discussions.     

Rearrangement of light harvesting bacteriochlorophyll homologues as a response of green sulfur bacteria to low light intensities

The pigment composition of two species of green-colored BChl c-containing green sulfur bacteria (Chlorobium limicola and C. chlorovibrioides) and two species of brown-colored BChl e-containing ones (C. phaeobacteroides and C. phaeovibrioides) incubated at different light intensities have been studied. All species responded to the reduction of light intensity from 50 to 1 Einstein(E) m^–2 s^–1 by an increase in the specific content of light harvesting pigments, bacteriochlorophylls and carotenoids. At critical light intensities (0.5 to 0.1 E m^–2 s^–1) only brown-colored chlorobia were able to grow, though at low specific rates (0.002 days^–1 mg prot^–1). High variations in the relative content of farnesyl-bacteriochlorophyll homologues were found, in particular BChl e ₁ and BChl e ₄, which were tentatively identified as [M, E] and [I, E] BChl_F e, respectively. The former was almost completely lost upon reduction of light intensity from 50 to 0.1 E m^–2 s^–1, whereas the latter increased from 7.2 to 38.4% and from 13.6 to 42.0% in C. phaeobacteroides and C. phaeovibrioides, respectively. This increase in the content of highly alkylated pigment molecules inside the chlorosomes of brown species is interpreted as a physiological mechanism to improve the efficiency of energy transfer towards the reaction center. This study provides some clues for understanding the physiological basis of the adaptation of brown species to extremely low light intensities.Abbreviations BChl bacteriochlorophyll - [M, E] BChl_F e 8-methyl, 12-ethyl BChl e, esterified with farnesol (F). Analogously: I - isobutyl - Pr propyl - Car carotenoids - Chlb chlorobactene - HPLC high performance liquid chromatography - Isr isorenieratene - LHP light harvesting pigments - PDA photodiode array detector - RC reaction center - RCH relative content of homologues     

Changes in the cyanobacterial photosynthetic apparatus during acclimation to macronutrient deprivation

When the cyanobacterium Synechococcus sp. Strain PCC 7942 is deprived of an essential macronutrient such as nitrogen, sulfur or phosphorus, cellular phycobiliprotein and chlorophyll contents decline. The level of -carotene declines proportionately to chlorophyll, but the level of zeaxanthin increases relative to chlorophyll. In nitrogen- or sulfur-deprived cells there is a net degradation of phycobiliproteins. Otherwise, the declines in cellular pigmentation are due largely to the diluting effect of continued cell division after new pigment synthesis ceases and not to net pigment degradation. There was also a rapid decrease in O₂ evolution when Synechococcus sp. Strain PCC 7942 was deprived of macronutrients. The rate of O₂ evolution declined by more than 90% in nitrogen- or sulfur-deprived cells, and by approximately 40% in phosphorus-deprived cells. In addition, in all three cases the fluorescence emissions from Photosystem II and its antennae were reduced relative to that of Photosystem I and the remaining phycobilisomes. Furthermore, state transitions were not observed in cells deprived of sulfur or nitrogen and were greatly reduced in cells deprived of phosphorus. Photoacoustic measurements of the energy storage capacity of photosynthesis also showed that Photosystem II activity declined in nutrient-deprived cells. In contrast, energy storage by Photosystem I was unaffected, suggesting that Photosystem I-driven cyclic electron flow persisted in nutrient-deprived cells. These results indicate that in the modified photosynthetic apparatus of nutrient-deprived cells, a much larger fraction of the photosynthetic activity is driven by Photosystem I than in nutrient-replete cells.Abbreviations ES energy storage - N nitrogen - P phosphorus - PBS phycobilisomes - S sulfur     

Photochemical activities and organization of photosynthetic apparatus of C3 and C4 plants grown under different light intensities

Changes in the photochemical activities, influenced by variation in the growth light intensity, were followed in typical C₃ (Phaseolus, Ipomoea) and C₄ (Amaranthus, Sorghum) plants. Progressive decrease in the growth light intensity accelerated the O-P fluorescence induction in whole leaves. Such acceleration of the fluorescence kinetics was found to be not due to enhanced photosystem II activity but possibly a result of reduced rate of electron flow between the two photosystems. This is supported by 4 lines of evidence: (1) by the Hill activity determined in the presence of electron acceptors functioning before and after plastoquinone; (2) the photosynthetic unit size determined after flash excitation showing variations that were apparently too small to account for the changes observed fluorescence induction; (3) modification of the kinetics of second-range light-induced absorbance changes at 520 nm; and (4) absence of significant changes in the ratio of P₇₀₀/total chlorophyll ratio. The P₇₀₀/cytochrome f ratio, however, increased from the usual 1–1.5 to 3–4 in plants grown under 9% sunlight. Increase in the P₇₀₀/cytochrome f ratio was found to be due to a decrease in the cytochrome f/chlorophyll ratio, and this was due to perhaps to a simultaneous increase in chlorophyll and decrease in cytochrome content.     

Photochemical activities and organization of photosynthetic apparatus of C3 and C4 plants grown under different light intensities

Changes in the photochemical activities, influenced by variation in the growth light intensity, were followed in typical C₃ (Phaseolus, Ipomoea) and C₄ (Amaranthus, Sorghum) plants. Progressive decrease in the growth light intensity accelerated the O-P fluorescence induction in whole leaves. Such acceleration of the fluorescence kinetics was found to be not due to enhanced photosystem II activity but possibly a result of reduced rate of electron flow between the two photosystems. This is supported by 4 lines of evidence: (1) by the Hill activity determined in the presence of electron acceptors functioning before and after plastoquinone; (2) the photosynthetic unit size determined after flash excitation showing variations that were apparently too small to account for the changes observed fluorescence induction; (3) modification of the kinetics of secondrange light-induced absorbance changes at 520 nm; and (4) absence of significant changes in the ratio of P₇₀₀/total chlorophyll ratio. The P₇₀₀/cytochrome f ratio, however, increased from the usual 1–1.5 to 3–4 in plants grown under 9% sunlight. Increase in the P₇₀₀/cytochrome f ratio was found to be due to a decrease in the cytochrome f/chlorophyll ratio, and this was due to perhaps to a simultaneous increase in chlorophyll and decrease in cytochrome content.     

Regulation of the photosynthetic apparatus under fluctuating growth light

Safe and efficient conversion of solar energy to metabolic energy by plants is based on tightly inter-regulated transfer of excitation energy, electrons and protons in the photosynthetic machinery according to the availability of light energy, as well as the needs and restrictions of metabolism itself. Plants have mechanisms to enhance the capture of energy when light is limited for growth and development. Also, when energy is in excess, the photosynthetic machinery slows down the electron transfer reactions in order to prevent the production of reactive oxygen species and the consequent damage of the photosynthetic machinery. In this opinion paper, we present a partially hypothetical scheme describing how the photosynthetic machinery controls the flow of energy and electrons in order to enable the maintenance of photosynthetic activity in nature under continual fluctuations in white light intensity. We discuss the roles of light-harvesting II protein phosphorylation, thermal dissipation of excess energy and the control of electron transfer by cytochrome b₆f, and the role of dynamically regulated turnover of photosystem II in the maintenance of the photosynthetic machinery. We present a new hypothesis suggesting that most of the regulation in the thylakoid membrane occurs in order to prevent oxidative damage of photosystem I.     

Nonstomatal inhibition of photosynthesis in sunflower at low leaf water potentials and high light intensities

The inhibition of photosynthesis at low leaf water potentials was studied in soil-grown sunflower to determine the degree to which photosynthesis under high light was affected by stomatal and nonstomatal factors. Below leaf water potentials of −11 to −12 bars, rates of photosynthesis at high light intensities were insensitive to external concentrations of CO₂ between 200 and 400 microliters per liter. Photosynthesis also was largely insensitive to leaf temperature between 10 and 30 C. Changes in CO₂ concentration and temperature had negligible effect on leaf diffusive resistance. The lack of CO₂ and temperature response for both photosynthesis and leaf diffuse resistance indicates that rates of photosynthesis were not limited by either CO₂ diffusion or a photosynthetic enzyme. It was concluded that photosynthesis under high light was probably limited by reduced photochemical activity of the leaves at water potentials below −11 to −12 bars.     

Long-term acclimation of barley photosynthetic apparatus to narrow-band red and blue light

Chloroplasts of barley plants grown under red light (RL, 660 nm) dramatically differed from the chloroplasts of plants raised under blue light (BL, 450 nm) or control plants (white light). The chloroplasts under RL had an extensive membrane system with high stacking degree and disordered irregular shaped stacks (shaggy-formed grana). After 5 h in darkness, dynamic rearrangements of chloroplast architecture in RL- and especially BL-grown plants were restricted compared with control plants. The light spectral quality affected the content and proportions of photosynthetic pigments. The leaves of RL-grown plants had the increased ratio of low-temperature fluorescence bands, F₇₄₁/F₆₈₃, corresponding to emission of PSI and PSII, respectively. This increase can be related to specific architecture of chloroplasts in RL-treated plants, providing close spacing between the two photosystems, which enhances energy transfer from PSII to PSI and facilitates the movement of LHCII toward PSI.     

Changes in the photosynthetic apparatus during fusarium wilt of tomato

Development of fusarium wilt was studied in 4-to 6-month-old tomato plants (Lycopersicon esculentum L., cv. Kunera). It was shown that the development of this disease could follow two patterns. When the wilt developed slowly (type I disease), the mycelium of Fusarium oxysporum fungus partly blocked the xylem and grew extensively within parenchyma. When the wilt developed fast (type II syndrome), the occlusion of both xylem and phloem was observed; the xylem sap circulation was suppressed and, consequently, tomato plant tissues were dehydrated. The development of type I and type II diseases led to suppression of photosynthetic activity in plants. In the case of slow wilt (type I), both light and dark stages of photosynthesis were damaged. This was evident from the decrease in the effectiveness of light harvesting and charge separations in the reaction centers of photosystem II (PSII), suppression of electron transport at the acceptor side of PSII, and the decrease in activity of Rubisco. In the case of fast wilt (type II), the Rubisco activity did not change, and photochemical activity of chloroplasts was suppressed to a smaller degree than during type I fusarium wilt. The decrease in the rate of linear electron transport in tomato leaves was mostly due to inhibition of electron flow at the acceptor side of PSII. The data obtained suggest that photosynthetic activity in tomato plants is suppressed by different mechanisms depending on the developmental pattern of fusarium wilt.     

Influence of high frequency light/dark fluctuations on photosynthetic characteristics of microalgae photoacclimated to different light intensities and implications for mass algal cultivation

Oxygen evolution from aScenedesmus obliquus dominated outdoor culture was followed in a small volume chamber, irradiated either by continuous white light or under light/dark frequencies between 0.05 to 5000 Hz, using arrays of high intensity red light emitting diodes (LED's). By placing neutral density filters in the path of the white light, light saturation curves of the oxygen evolution (P/I curves) were measured using diluted aliquots of algal cultures. The results clearly showed that photosynthetic rates increased exponentially with increasing light/dark frequencies, that a longer dark period in relation to the light period does not necessarily lead to higher photosynthetic rates (efficiencies), and that algae do not acclimate to a specific light/dark frequency. One of the most important factors that influenced photosynthetic rates, either under continuous illumination or intermittent, was whether the algae were dark or light acclimated. Low light/dark frequencies were perceived by the algae as low light conditions, whilst the opposite was true for high frequencies. The light utilisation efficiency in a fluctuating light/dark environment depended on the acclimated state of the algae, the specific frequency of the fluctuations and the duration of the exposure. Since the frequencies determined the perceived quantities of light, dark reactions played an important role in determining the average photosynthetic efficiencies. These results have important implications for algal biotechnology.     

Changes of fluorescence and xanthophyll pigments during dehydration in the resurrection plantSelaginella lepidophylla in low and medium light intensities

The changes in photosynthetic efficiency and photosynthetic pigments during dehydration of the resurrection plantSelaginella lepidophylla (from the Chiuhahuan desert, S.W. Texas, USA) were examined under different light conditions. Changes in the photosynthetic efficiency were deduced from chlorophyll a fluorescence measurements (F_o, F_m, and F_v) and pigment changes were measured by HPLC analysis. A small decrease in F_v/F_m was seen in hydrated stems in high light (650 μmol photons·m⁻²·s⁻¹) but not in low light (50 μmol photons·m⁻²·s⁻¹). However, a pronounced decline in F_v/F_m was observed during dehydration in both light treatments, after one to two hours of dehydration. A rise in F_o was observed only after six to ten hours of dehydration. Concomitant with the decrease in photosynthetic efficiency during dehydration a rise in the xanthophyll zeaxanthin was observed, even in low-light treatments. The increase in zeaxanthin can be related to previously observed photoprotective non-photochemical quenching of fluorescence in dehydrating stems ofS. lepidophylla. We hypothesize that under dehydrating conditions even low light levels become excessive and zeaxanthin-related photoprotection is engaged. We speculate that these processes, as well as stem curling and self shading (Eickmeier et al. 1992), serve to minimize photoinhibitory damage toS. lepidophylla during the process of dehydration.     

Changes of the photosynthetic apparatus in Spirulina cyanobacterium by sodium stress

Spirulina platensis trichomes grown in Zarrouks medium having total Na+ concentration as 0.14 M when transferred to fresh Zarrouks medium containing enhanced level of Na+ ions equal to 0.86 M showed 30% more accumulation of Na+ intracellularly as compared to the control. An inhibition of photosystem II activity to almost 66% was observed. Also due to this exposure to high Na+, the room temperature absorption characteristics of Spirulina trichomes and the thylakoid membrane preparations were altered indicating changes in the chromophore protein interactions and alterations in the phycocyanin/allophycocyanin ratio; there by affecting the energy harvest and energy transfer processes. An increase in the carotenoid absorption was two fold over the control in the treated sample. Similarly, room temperature and low temperature (77 K) fluorescence emission spectra collectively suggested alterations in the chlorophyll a emissions, F 726 of photosystem I reflecting changes in the lipid protein environment of the thylakoid. Our results indicate that in Spirulina the enhanced Na+ level alters the energy harvest and transfer processes. It also affected the emission characteristics of chlorophyll a of photosystem I.