Chilling Sensitivity in Oryza sativa: The Role of Protein Phosphorylation in Protection against Photoinhibition

Thermal acclimation by Saxffraga cernua to low temperatures results in a change in the optimum temperature for gross photosynthetic activity and may directly involve the photosynthetic apparatus. In order to test this hypothesis photosynthetic electron transport activity of S. cernua thylakoids acclimated to growth temperatures of 200C and 10°C was measured in vitro. Both populations exhibited optimum temperatures for whole chain and PSII electron transport activity at temperatures close to those at which the plants were grown. Chlorophyll a fluorescence transients from 10°C-acclimated leaves showed higher rates in the rise and subsequent quenching of variable fluorescence at low measuring temperatures; 20°C-acclimated leaves showed higher rates of fluorescence rise at higher measuring temperatures. At these higher temperatures, fluorescence quenching rates were similar in both populations. The kinetics of State 1-State 2 transitions in 20°C-and 10°C-acclimated leaf discs were measured as changes in the magnitude of the fluorescence emission maxima measured at 77K. Leaves acclimated at 10°C showed a larger F730/F695 ratio at low temperatures, while at higher temperatures, 20°C-acclimated leaves showed a higher F730/F695 ratio after the establishment of State 2. High incubation temperatures also resulted in a decrease in the F695/F685 ratio for 10°C-acclimated leaves, suggesting a reduction in the excitation transfer from the light-harvesting complex of photosystem 11 to photosystem 11 reaction centers. The relative amounts of chlorophyllprotein complexes and thylakoid polypeptides separated electrophoretically were similar for both 20°C-and 10°C-acclimated leaves. Thus, photosynthetic acclimation to low temperatures by S. cernua is correlated with an increase in photosynthetic electron transport activity but does not appear to be accompanied by major structural changes or different relative amounts in thylakoid protein composition.Thermal acclimation of photosynthetic activity, usually measured as changes in the optimum temperature for photosynthesis resulting from a change in growth temperature, has been demonstrated in a number of species from diverse environments (for reviews, see Refs. 4 and 25). From an ecological viewpoint, the potential, or capacity for thermal acclimation is considered to be an important strategy for maximizing carbon fixation and seasonal net productivity, ' Supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada to WRC. 2Present address:

Section: Discussionsupporting

confidence: 71%

Thermal Acclimation of Photosynthetic Electron Transport Activity by Thylakoids of Saxifraga cernua

Mawson

Cummins²

1989

“…Phosphorylation of LHCII also provides protection against photoinhibition (15). However, low temperatures have been observed to inhibit the phosphorylation of LHCII in chilling-sensitive rice, though not in chilling-resistant barley (21,22). This probably makes rice PSII more susceptible to light-induced inhibition at chilling temperatures.…”

Section: Introductionmentioning

confidence: 99%

Distribution of Chlorophyll-Protein Complexes during Chilling in the Light Compared with Heat-Induced Modifications

Ovaska

Mäenpää²,

Nurmi³

et al. 1990

The effects of chilling in the light (4 days at 50C and 100-200 micromoles of photons per square meter per second) on the distribution of chlorophyll (Chi) protein complexes between appressed and nonappressed thylakoid regions of pumpkin (Cucurbita pepo L.) chloroplasts were studied and compared with the changes occurring during in vitro heat treatment (5 minutes at 400C) of isolated thylakoids. Both treatments induced an increase (18 and 65%, respectively) in the relative amount of the antenna Chi a protein complexes (CP47 + CP43) of photosystem 11 (PSII) in stroma lamellae vesicles. Freeze-fracture replicas of lightchilled material revealed an increase in the particle density on the exoplasmic fracture face of unstacked membrane regions. These two treatments differed markedly, however, in respect to comigration of the light-harvesting Chi a/b protein complex (LHCII) of PSII. The LHCII/PSII ratio in stroma lamellae vesicles remained fairly constant during chilling in the light, whereas it dropped during the heat treatment. Moreover thylakoid membrane (3). However, some PSII of smaller antenna size can be found in the PSI-rich thylakoid region, too (2). This PSII (PSII,6) does not seem to be functionally connected with PSI (20, 27). The segregation effected by the lateral heterogeneity is not rigid, but allows many acclimative reorganizations in response to environmental changes (1).A mechanism known to regulate the distribution of excitation energy is the light-induced phosphorylation of LHCII and subsequent migration of phospho-LHCII from the appressed to the nonappressed thylakoid regions (8). In this way, the allocation of excitation energy between PSII and PSI can be optimized in varying light conditions. Phosphorylation of LHCII also provides protection against photoinhibition (15). However, low temperatures have been observed to inhibit the phosphorylation of LHCII in chilling-sensitive rice, though not in chilling-resistant barley (21,22). This probably makes rice PSII more susceptible to light-induced inhibition at chilling temperatures.High, nonlethal temperatures are also known to cause changes in the lateral distribution of thylakoid components (24, 26). Heating of isolated thylakoids to temperatures above 30°C causes migration of PSII and an inner portion of its LHCII from the appressed to the nonappressed thylakoid regions. Concomitantly, there is conversion of PSIIa to PSII,,.The migration of PSII was postulated to play a role in preventing overexcitation and subsequent damage of PSII under photoinhibitory conditions (24). This suggestion is supported by the fact that PSII, is less sensitive to photoinhibition than PSILa (10,18

“…Photoinhibition is also believed to be a part of the damage caused by both water stress and cold stress (4,20). Understanding photoinhibition is thus a part of understanding the phenotypic and genotypic responses of the photosynthetic apparatus to its environment.…”

mentioning

confidence: 99%

Photoinhibition Resistance in the Red Alga Porphyra perforata

Herbert

1990

Photoinhibition resistance exhibited by the high intertidal red alga Porphyra perforate relative to its subtidal congener Porphyra nereocystis was examined using the protein synthesis inhibitor chloramphenicol to separate the damage and repair components of photoinhibition. Under photoinhibitory conditions, the rates of both damage to and replacement of photoinhibition-sensitive proteins was much higher in P. nereocystis than in P. perforate. Thus, photoinhibition resistance in P. perforate appears to be due to a reduced rate of photoinhibition damage rather than to an accelerated rate of photoinhibition repair. Reduction of photoinhibition damage in P. perforate may be by means of biophysical processes which increase the radiationless decay of excitation to heat in photosystem II. Alternatively, the photoinhibition-sensitive proteins in P. perforate may have slight structural alterations that improve their stability or they may be protected by enzyme systems that quench radicals formed by overexcitation of photosystem 11. Reduction of the damage component of photoinhibition is a reasonable way to limit photoinhibition in P. perforate during the severe desiccation and exposure to full sun that occur simultaneously during daily low tides, conditions under which the protein synthesis required for photoinhibition repair could not occur.Photoinhibition of photosynthesis by visible light has attracted the attention of a broad spectrum of plant scientists in the last decade. The appeal of photoinhibition is severalfold. At the biochemical level, the primary process of photoinhibition is a light-induced turnover ofone or more thylakoid membrane proteins in which the rate of degradation has exceeded the rates at which the degraded protein is identified and removed from the membrane and its replacement synthesized and reinserted in the membrane (2,15,16 acclimation and adaptation of the photosynthetic apparatus to its light environment (1). Photoinhibition is also believed to be a part of the damage caused by both water stress and cold stress (4, 20). Understanding photoinhibition is thus a part of understanding the phenotypic and genotypic responses of the photosynthetic apparatus to its environment.Plants endemic to high irradiance environments are resistant to photoinhibition by means of various adaptations of their photosynthetic apparatus, some of which are poorly understood. One such plant is the red alga Porphyra perforate J. Agardh, which persists naturally under extreme photoinhibitory conditions in the high-intertidal zone of the seashore experiencing severe desiccation under full sunlight on a daily basis during exposure by low tides. Relative to its shadeadapted, subtidal congener, Porphyra nereocystis Anderson, P. perforate exhibits a constitutive resistance to photoinhibition ( 11). The mechanisms conferring this resistance do not function either to reduce absorption of incident light or to decrease the amount of excess energy in PSII by using it in increased carbon fixation, photorespiration, or th...