Wataru Yamori

Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation

Most plants show considerable capacity to adjust their photosynthetic characteristics to their growth temperatures (temperature acclimation). The most typical case is a shift in the optimum temperature for photosynthesis, which can maximize the photosynthetic rate at the growth temperature. These plastic adjustments can allow plants to photosynthesize more efficiently at their new growth temperatures. In this review article, we summarize the basic differences in photosynthetic reactions in C3, C4, and CAM plants. We review the current understanding of the temperature responses of C3, C4, and CAM photosynthesis, and then discuss the underlying physiological and biochemical mechanisms for temperature acclimation of photosynthesis in each photosynthetic type. Finally, we use the published data to evaluate the extent of photosynthetic temperature acclimation in higher plants, and analyze which plant groups (i.e., photosynthetic types and functional types) have a greater inherent ability for photosynthetic acclimation to temperature than others, since there have been reported interspecific variations in this ability. We found that the inherent ability for temperature acclimation of photosynthesis was different: (1) among C3, C4, and CAM species; and (2) among functional types within C3 plants. C3 plants generally had a greater ability for temperature acclimation of photosynthesis across a broad temperature range, CAM plants acclimated day and night photosynthetic process differentially to temperature, and C4 plants was adapted to warm environments. Moreover, within C3 species, evergreen woody plants and perennial herbaceous plants showed greater temperature homeostasis of photosynthesis (i.e., the photosynthetic rate at high-growth temperature divided by that at low-growth temperature was close to 1.0) than deciduous woody plants and annual herbaceous plants, indicating that photosynthetic acclimation would be particularly important in perennial, long-lived species that would experience a rise in growing season temperatures over their lifespan. Interestingly, across growth temperatures, the extent of temperature homeostasis of photosynthesis was maintained irrespective of the extent of the change in the optimum temperature for photosynthesis (Topt), indicating that some plants achieve greater photosynthesis at the growth temperature by shifting Topt, whereas others can also achieve greater photosynthesis at the growth temperature by changing the shape of the photosynthesis–temperature curve without shifting Topt. It is considered that these differences in the inherent stability of temperature acclimation of photosynthesis would be reflected by differences in the limiting steps of photosynthetic rate.

Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration

While interest in photosynthetic thermal acclimation has been stimulated by climate warming, comparing results across studies requires consistent terminology. We identify five types of photosynthetic adjustments in warming experiments: photosynthesis as measured at the high growth temperature, the growth temperature, and the thermal optimum; the photosynthetic thermal optimum; and leaf-level photosynthetic capacity. Adjustments of any one of these variables need not mean a concurrent adjustment in others, which may resolve apparently contradictory results in papers using different indicators of photosynthetic acclimation. We argue that photosynthetic thermal acclimation (i.e., that benefits a plant in its new growth environment) should include adjustments of both the photosynthetic thermal optimum (Topt) and photosynthetic rates at the growth temperature (Agrowth), a combination termed constructive adjustment. However, many species show reduced photosynthesis when grown at elevated temperatures, despite adjustment of some photosynthetic variables, a phenomenon we term detractive adjustment. An analysis of 70 studies on 103 species shows that adjustment of Topt and Agrowth are more common than adjustment of other photosynthetic variables, but only half of the data demonstrate constructive adjustment. No systematic differences in these patterns were found between different plant functional groups. We also discuss the importance of thermal acclimation of respiration for net photosynthesis measurements, as respiratory temperature acclimation can generate apparent acclimation of photosynthetic processes, even if photosynthesis is unaltered. We show that while dark respiration is often used to estimate light respiration, the ratio of light to dark respiration shifts in a non-predictable manner with a change in leaf temperature.

Phenotypic Plasticity in Photosynthetic Temperature Acclimation among Crop Species with Different Cold Tolerances

While interspecific variation in the temperature response of photosynthesis is well documented, the underlying physiological mechanisms remain unknown. Moreover, mechanisms related to species-dependent differences in photosynthetic temperature acclimation are unclear. We compared photosynthetic temperature acclimation in 11 crop species differing in their cold tolerance, which were grown at 15°C or 30°C. Cold-tolerant species exhibited a large decrease in optimum temperature for the photosynthetic rate at 360 μL L−1 CO2 concentration [Opt (A360)] when growth temperature decreased from 30°C to 15°C, whereas cold-sensitive species were less plastic in Opt (A360). Analysis using the C3 photosynthesis model shows that the limiting step of A360 at the optimum temperature differed between cold-tolerant and cold-sensitive species; ribulose 1,5-bisphosphate carboxylation rate was limiting in cold-tolerant species, while ribulose 1,5-bisphosphate regeneration rate was limiting in cold-sensitive species. Alterations in parameters related to photosynthetic temperature acclimation, including the limiting step of A360, leaf nitrogen, and Rubisco contents, were more plastic to growth temperature in cold-tolerant species than in cold-sensitive species. These plastic alterations contributed to the noted growth temperature-dependent changes in Opt (A360) in cold-tolerant species. Consequently, cold-tolerant species were able to maintain high A360 at 15°C or 30°C, whereas cold-sensitive species were not. We conclude that differences in the plasticity of photosynthetic parameters with respect to growth temperature were responsible for the noted interspecific differences in photosynthetic temperature acclimation between cold-tolerant and cold-sensitive species.

Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice

The role of NAD(P)H dehydrogenase (NDH)-dependent cyclic electron flow around photosystem I in photosynthetic regulation and plant growth at several temperatures was examined in rice (Oryza sativa) that is defective in CHLORORESPIRATORY REDUCTION 6 (CRR6), which is required for accumulation of sub-complex A of the chloroplast NDH complex (crr6). NdhK was not detected by Western blot analysis in crr6 mutants, resulting in lack of a transient post-illumination increase in chlorophyll fluorescence, and confirming that crr6 mutants lack NDH activity. When plants were grown at 28 or 35°C, all examined photosynthetic parameters, including the CO(2) assimilation rate and the electron transport rate around photosystems I and II, at each growth temperature at light intensities above growth light (i.e. 800 μmol photons m(-2) sec(-1)), were similar between crr6 mutants and control plants. However, when plants were grown at 20°C, all the examined photosynthetic parameters were significantly lower in crr6 mutants than control plants, and this effect on photosynthesis caused a corresponding reduction in plant biomass. The F(v)/F(m) ratio was only slightly lower in crr6 mutants than in control plants after short-term strong light treatment at 20°C. However, after long-term acclimation to the low temperature, impairment of cyclic electron flow suppressed non-photochemical quenching and promoted reduction of the plastoquinone pool in crr6 mutants. Taken together, our experiments show that NDH-dependent cyclic electron flow plays a significant physiological role in rice during photosynthesis and plant growth at low temperature.

The Solar Action Spectrum of Photosystem II Damage

The production of oxygen and the supply of energy for life on earth rely on the process of photosynthesis using sunlight. Paradoxically, sunlight damages the photosynthetic machinery, primarily photosystem II (PSII), leading to photoinhibition and loss of plant performance. However, there is uncertainty about which wavelengths are most damaging to PSII under sunlight. In this work we examined this in a simple experiment where Arabidopsis (Arabidopsis thaliana) leaves were exposed to different wavelengths of sunlight by dispersing the solar radiation across the surface of the leaf via a prism. To isolate only the process of photodamage, the repair of photodamaged PSII was inhibited by infiltration of chloramphenicol into the exposed leaves. The extent of photodamage was then measured as the decrease in the maximum quantum yield of PSII using an imaging pulse amplitude modulation fluorometer. Under the experimental light conditions, photodamage to PSII occurred most strongly in regions exposed to ultraviolet (UV) or yellow light. The extent of UV photodamage under incident sunlight would be greater than we observed when one corrects for the optical efficiency of our system. Our results suggest that photodamage to PSII under sunlight is primarily associated with UV rather than photosynthetically active light wavelengths.

Physiological Functions of Cyclic Electron Transport Around Photosystem I in Sustaining Photosynthesis and Plant Growth.

The light reactions in photosynthesis drive both linear and cyclic electron transport around photosystem I (PSI). Linear electron transport generates both ATP and NADPH, whereas PSI cyclic electron transport produces ATP without producing NADPH. PSI cyclic electron transport is thought to be essential for balancing the ATP/NADPH production ratio and for protecting both photosystems from damage caused by stromal overreduction. Two distinct pathways of cyclic electron transport have been proposed in angiosperms: a major pathway that depends on the PROTON GRADIENT REGULATION 5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE 1 (PGRL1) proteins, which are the target site of antimycin A, and a minor pathway mediated by the chloroplast NADH dehydrogenase-like (NDH) complex. Recently, the regulation of PSI cyclic electron transport has been recognized as essential for photosynthesis and plant growth. In this review, we summarize the possible functions and importance of the two pathways of PSI cyclic electron transport.

Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation rate in tobacco leaves

Effects of growth light intensity on the temperature dependence of CO(2) assimilation rate were studied in tobacco (Nicotiana tabacum) because growth light intensity alters nitrogen allocation between photosynthetic components. Leaf nitrogen, ribulose 1.5-bisphosphate carboxylase/oxygenase (Rubisco) and cytochrome f (cyt f) contents increased with increasing growth light intensity, but the cyt f/Rubisco ratio was unaltered. Mesophyll conductance to CO(2) diffusion (g(m)) measured with carbon isotope discrimination increased with growth light intensity but not with measuring light intensity. The responses of CO(2) assimilation rate to chloroplast CO(2) concentration (C(c)) at different light intensities and temperatures were used to estimate the maximum carboxylation rate of Rubisco (V(cmax)) and the chloroplast electron transport rate (J). Maximum electron transport rates were linearly related to cyt f content at any given temperature (e.g. 115 and 179 micromol electrons mol(-1) cyt f s(-1) at 25 and 40 degrees C, respectively). The chloroplast CO(2) concentration (C(trans)) at which the transition from RuBP carboxylation to RuBP regeneration limitation occurred increased with leaf temperature and was independent of growth light intensity, consistent with the constant ratio of cyt f/Rubisco. In tobacco, CO(2) assimilation rate at 380 micromol mol(-1) CO(2) concentration and high light was limited by RuBP carboxylation above 32 degrees C and by RuBP regeneration below 32 degrees C.

The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity

In C3 plants, CO2 assimilation is limited by ribulose 1,5-bisphosphate (RuBP) regeneration rate at high CO2. RuBP regeneration rate in turn is determined by either the chloroplast electron transport capacity to generate NADPH and ATP or the activity of Calvin cycle enzymes involved in regeneration of RuBP. Here, transgenic tobacco (Nicotiana tabacum ‘W38’) expressing an antisense gene directed at the transcript of either the Rieske iron-sulfur protein of the cytochrome (Cyt) b6/f complex or the δ-subunit of chloroplast ATP synthase have been used to investigate the effect of a reduction of these complexes on chloroplast electron transport rate (ETR). Reductions in δ-subunit of ATP synthase content did not alter chlorophyll, Cyt b6/f complex, or Rubisco content, but reduced ETR estimated either from measurements of chlorophyll fluorescence or CO2 assimilation rates at high CO2. Plants with low ATP synthase content exhibited higher nonphotochemical quenching and achieved higher ETR per ATP synthase than the wild type. The proportional increase in ETR per ATP synthase complex was greatest at 35°C, showing that the ATP synthase activity can vary in vivo. In comparison, there was no difference in the ETR per Cyt b6/f complex in plants with reduced Cyt b6/f content and the wild type. The ETR decreased more drastically with reductions in Cyt b6/f complex than ATP synthase content. This suggests that chloroplast ETR is more limited by Cyt b6/f than ATP synthase content and is a potential target for enhancing photosynthetic capacity in crops.

The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species

Effects of nitrogen (N) supply on the limiting step of CO(2) assimilation rate (A) at 380 µmol mol(-1) CO(2) concentration (A(380) ) at several leaf temperatures were studied in several crops, since N nutrition alters N allocation between photosynthetic components. Contents of leaf N, ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco) and cytochrome f (cyt f) increased with increasing N supply, but the cyt f/Rubisco ratio decreased. Large leaf N content was linked to a high stomatal (g(s) ) and mesophyll conductance (g(m) ), but resulted in a lower intercellular (C(i) ) and chloroplast CO(2) concentration (C(c) ) because the increase in g(s) and g(m) was insufficient to compensate for change in A(380) . The A-C(c) response was used to estimate the maximum rate of RuBP carboxylation (V(cmax) ) and chloroplast electron transport (J(max) ). The J(max) /V(cmax) ratio decreased with reductions in leaf N content, which was consistent with the results of the cyt f/Rubisco ratio. Analysis using the C(3) photosynthesis model indicated that A(380) tended to be limited by RuBP carboxylation in plants grown at low N concentration, whereas it was limited by RuBP regeneration in plants grown at high N concentration. We conclude that the limiting step of A(380) depends on leaf N content and is mainly determined by N partitioning between Rubisco and electron transport components.

Cold tolerant crop species have greater temperature homeostasis of leaf respiration and photosynthesis than cold sensitive species

Some plant species show constant rates of respiration and photosynthesis measured at their respective growth temperatures (temperature homeostasis), whereas others do not. However, it is unclear what species show such temperature homeostasis and what factors affect the temperature homeostasis. To analyze the inherent ability of plants to acclimate respiration and photosynthesis to different growth temperatures, we examined 11 herbace-ous crops with different cold tolerance. Leaf respiration (R(area)) and photosynthetic rate (P(area)) under high light at 360 microl l(-1) CO(2) concentrations were measured in plants grown at 15 and 30 degrees C. Cold-tolerant species showed a greater extent of temperature homeostasis of both R(area) and P(area) than cold-sensitive species. The underlying mechanisms which caused differences in the extent of temperature homeostasis were examined. The extent of temperature homeostasis of P(area) was not determined by differences in leaf mass and nitrogen content per leaf area, but by differences in photosynthetic nitrogen use efficiency (PNUE). Moreover, differences in PNUE were due to differences in the maximum catalytic rate of Rubisco, Rubisco contents and amounts of nitrogen invested in Rubisco. These findings indicated that the temperature homeostasis of photosynthesis was regulated by various parameters. On the other hand, the extent of temperature homeostasis of R(area) was unrelated to the maximum activity of the respiratory enzyme (NAD-malic enzyme). The R(area)/P(area) ratio was maintained irrespective of the growth temperatures in all the species, suggesting that the extent of temperature homeostasis of R(area) interacted with the photosynthetic rate and/or the homeostasis of photosynthesis.