The induction of pyrenoid synthesis by hyperoxia and its implications for the natural diversity of photosynthetic responses in Chlamydomonas

In algae, it is well established that the pyrenoid, a component of the carbon-concentrating mechanism (CCM), is essential for efficient photosynthesis at low CO2. However, the signal that triggers the formation of the pyrenoid has remained elusive. Here, we show that, in Chlamydomonas reinhardtii, the pyrenoid is strongly induced by hyperoxia, even at high CO2 or bicarbonate levels. These results suggest that the pyrenoid can be induced by a common product of photosynthesis specific to low CO2 or hyperoxia. Consistent with this view, the photorespiratory by-product, H2O2, induced the pyrenoid, suggesting that it acts as a signal. Finally, we show evidence for linkages between genetic variations in hyperoxia tolerance, H2O2 signaling, and pyrenoid morphologies.

Discrepancy in photosynthetic responses of the red alga Pyropia yezoensis to dehydration stresses under exposure to desiccation, high salinity, and high mannitol concentration

Macroalgae that inhabit intertidal zones are exposed to the air for several hours during low tide and must endure desiccation and high variations in temperature, light intensity, and salinity. Pyropia yezoensis (Rhodophyta, Bangiales), a typical intertidal red macroalga that is commercially cultivated in the northwestern Pacific Ocean, was investigated under different dehydration stresses of desiccation, high salinity, and high mannitol concentration. Using chlorophyll fluorescence imaging, photosynthetic activities of P. yezoensis thalli were analyzed using six parameters derived from quenching curves and rapid light curves. A distinct discrepancy was revealed in photosynthetic responses to different dehydration stresses. Dehydration caused by exposure to air resulted in rapid decreases in photosynthetic activities, which were always lower than two other stresses at the same water loss (WL) level. High salinity only reduced photosynthesis significantly at its maximum WL of 40% but maintained a relatively stable maximum quantum yield of photosystem II (PSII) (Fv/Fm). High mannitol concentration induced maximum WL of 20% for a longer time (60 min) than the other two treatments and caused no adverse influences on the six parameters at different WL except for a significant decrease in non-photochemical quenching (NPQ) at 20% WL. Illustrated by chlorophyll fluorescence images, severe spatial heterogeneities were induced by desiccation with lower values in the upper parts than the middle or basal parts of the thalli. The NPQ and rETRmax (maximum relative electron transport rate) demonstrated clear distinctions for evaluating photosynthetic responses, indicating their sensitivity and applicability. The findings of this study indicated that the natural dehydration of exposure to air results in stronger and more heterogeneous effects than those of high salinity or high mannitol concentration.

Genetically-determined variations in photosynthesis indicate roles for specific fatty acid species in chilling responses

Using a population of recombinant inbred lines (RILs) cowpea (Vigna unguiculata. L. Walp), we tested for co-linkages between lipid contents and chilling responses of photosynthesis. Under low temperature conditions (19°C/13°C, day/night), we observed co-linkages between quantitative trait loci (QTL) intervals for photosynthetic light reactions and specific fatty acids, most strikingly, the thylakoid-specific fatty acid 16:1 found exclusively in phosphatidylglycerol (PG 16:1t). By contrast, we did not observe co-associations with bulk polyunsaturated fatty acids or high-melting-point-PG (sum of PG 16:0, PG 18:0 PG 16:1t) previously thought to be involved in chilling sensitivity. These results suggest that in cowpea, chilling sensitivity is modulated by specific lipid interactions rather than bulk properties. We were able to recapitulate the predicted impact of PG 16:1t levels on photosynthetic responses at low temperature using mutants and transgenic Arabidopsis lines. Because PG 16:1t synthesis requires the activity of peroxiredoxin-Q, which is activated by HO and known to be involved in redox signaling, we hypothesize that the accumulation of PG 16:1t occurs as a result of upstream effects on photosynthesis that alter redox status and production of reactive oxygen species.

Genetic Variation in Photosynthetic Responses to Chilling Modulates Proton Motive Force, Cyclic Electron Flow and Photosystem II Photoinhibition

The work demonstrates the use of detailed, high-throughput phenotyping to generate and test mechanistic models to explain the genetic diversity of photosynthetic responses to abiotic stress. We assessed a population of recombinant inbred lines (RILs) of cowpea (Vigna unguiculata. (L.) Walp.) with significant differences in a range of photosynthetic responses to chilling. We found well-defined, colocalized (overlapping) QTL intervals for photosynthetic parameters, suggesting linkages among the redox states of Q, the thylakoid pmf, through effects on cyclic electron flow and photodamage to PSII. We propose that these genetic variations optimize photosynthesis in the tolerant lines under low temperatures, preventing recombination reactions within Photosystem II that can lead to deleterious O production. By contrast, we did not observe linkages to PSI redox state, PSI photodamage or ATP synthase activity, or nyctinastic (diurnally controlled) leaf movements, likely indicating that several proposed models likely do not contribute to the genetic control of photosynthesis at low temperature in our mapping panel. The identified QTL intervals include a range of potential causative genetic components, with direct applications to breeding of photosynthesis for more climate-resilient productivity.

Differential Impact of an Eclipse on Photosynthetic Performance of Trees with Different Degrees of Shade Tolerance

Solar eclipses represent a natural and unexpected event for plants that can potentially affect photosynthetic performance at the individual level. This effect, however, has seldom been evaluated. Here, we measured the impact of a total solar eclipse on the photosynthetic rate of different tree species—located in the Bosque Fray Jorge National Park, Chile—with varying degrees of shade tolerance. Specifically, we assessed whether the rapid and progressive light limitation facilitated by a solar eclipse would negatively impact the photosynthetic responses of these tree species and whether their photosynthetic performance would have a greater decrease when the percentage of eclipse shadow was higher, particularly in the less shade-tolerant species. To accomplish this, we compared daily changes in the photosynthetic rates of three tree species during a control (non-eclipse) vs. an eclipse day that occurred on 2 July 2019. Overall, tree species showed differences between a non-eclipse and eclipse day in the daily dynamics of their photosynthetic performance, with this trend being most evident at the peak of the solar eclipse. Additionally, each species showed a different pattern of de-epoxidation in accordance with its degree of shade tolerance. Our results suggest that solar eclipses negatively affect the photosynthesis of the studied Chilean tree species, which may be related to energy dissipation capacity via the de-epoxidation of xanthophyll pigments. This effect was more evident in shade-intolerant species, indicating that eclipses can present different consequences for the overall performance of various plant species.

Morphological, Physiological and Photophysiological Responses of Critically Endangered Acer catalpifolium to Acid Stress

Acid rain deposition (AR) has long-lasting implications for the community stability and biodiversity conservation in southwest China. Acer catalpifolium is a critically endangered species in the rain zone of Western China where AR occurs frequently. To understand the effects of AR on the morphology and physiology of A. catalpifolium, we conducted an acid stress simulation experiment for 1.5 years. The morphological, physiological, and photosynthetic responses of A. catalpifolium to the acidity, composition, and deposition pattern of acid stress was observed. The results showed that simulated acid stress can promote the growth of A. catalpifolium via the soil application mode. The growth improvement of A. catalpifolium under nitric-balanced acid rain via the soil application mode was greater than that of sulfuric-dominated acid rain via the soil application mode. On the contrary, the growth of A. catalpifolium was significantly inhibited by acid stress and the inhibition increased with the acidity of acid stress applied via leaf spraying. The inhibitory impacts of nitric-balanced acid rain via the leaf spraying of A. catalpifolium were greater than that of sulfur-dominant acid rain via leaf spraying. The observations presented in this work can be utilized for considering potential population restoration plans for A. catalpifolium, as well as the forests in southwest China.

Sensitivity of Photosynthesis to Warming in Two Similar Species of the Aquatic Angiosperm Ruppia from Tropical and Temperate Habitats

Climate change-related events, such as marine heatwaves, are increasing seawater temperatures, thereby putting pressure on marine biota. The cosmopolitan distribution and significant contribution to marine primary production by the genus Ruppia makes them interesting organisms to study thermal tolerance and local adaptation. In this study, we investigated the photosynthetic responses in Ruppia to the predicted future warming in two contrasting bioregions, temperate Sweden and tropical Thailand. Through DNA barcoding, specimens were determined to Ruppia cirrhosa for Sweden and Ruppia maritima for Thailand. Photosynthetic responses were assessed using pulse amplitude-modulated fluorometry, firstly in short time incubations at 18, 23, 28, and 33 °C in the Swedish set-up and 28, 33, 38, and 43 °C in the Thai set-up. Subsequent experiments were conducted to compare the short time effects to longer, five-day incubations in 28 °C for Swedish plants and 40 °C for Thai plants. Swedish R. cirrhosa displayed minor response, while Thai R. maritima was more sensitive to both direct and prolonged temperature stress with a drastic decrease in the photosynthetic parameters leading to mortality. The results indicate that in predicted warming scenarios, Swedish R. cirrhosa may sustain an efficient photosynthesis and potentially outcompete more heat-sensitive species. However, populations of the similar R. maritima in tropical environments may suffer a decline as their productivity will be highly reduced.