Photosynthetic traits of Australian wild rice (Oryza australiensis) confer tolerance to extreme daytime temperatures

Key message A wild relative of rice from the Australian savannah was compared with cultivated rice, revealing thermotolerance in growth and photosynthetic processes and a more robust carbon economy in extreme heat. Abstract Above ~ 32 °C, impaired photosynthesis compromises the productivity of rice. We compared leaf tissues from heat-tolerant wild rice (Oryza australiensis) with temperate-adapted O. sativa after sustained exposure to heat, as well as diurnal heat shock. Leaf elongation and shoot biomass in O. australiensis were unimpaired at 45 °C, and soluble sugar concentrations trebled during 10 h of a 45 °C shock treatment. By contrast, 45 °C slowed growth strongly in O. sativa. Chloroplastic CO2 concentrations eliminated CO2 supply to chloroplasts as the basis of differential heat tolerance. This directed our attention to carboxylation and the abundance of the heat-sensitive chaperone Rubisco activase (Rca) in each species. Surprisingly, O. australiensis leaves at 45 °C had 50% less Rca per unit Rubisco, even though CO2 assimilation was faster than at 30 °C. By contrast, Rca per unit Rubisco doubled in O. sativa at 45 °C while CO2 assimilation was slower, reflecting its inferior Rca thermostability. Plants grown at 45 °C were simultaneously exposed to 700 ppm CO2 to enhance the CO2 supply to Rubisco. Growth at 45 °C responded to CO2 enrichment in O. australiensis but not O. sativa, reflecting more robust carboxylation capacity and thermal tolerance in the wild rice relative.

Oxidative regulation of chloroplast enzymes by thioredoxin and thioredoxin-like proteins in Arabidopsis thaliana

Thioredoxin (Trx) is a protein that mediates the reducing power transfer from the photosynthetic electron transport system to target enzymes in chloroplasts and regulates their activities. Redox regulation governed by Trx is a system that is central to the adaptation of various chloroplast functions to the ever-changing light environment. However, the factors involved in the opposite reaction (i.e., the oxidation of various enzymes) have yet to be revealed. Recently, it has been suggested that Trx and Trx-like proteins could oxidize Trx-targeted proteins in vitro. To elucidate the in vivo function of these proteins as oxidation factors, we generated mutant plant lines deficient in Trx or Trx-like proteins and studied how the proteins are involved in oxidative regulation in chloroplasts. We found that f-type Trx and two types of Trx-like proteins, Trx-like 2 and atypical Cys His-rich Trx (ACHT), seemed to serve as oxidation factors for Trx-targeted proteins, such as fructose-1,6-bisphosphatase, Rubisco activase, and the γ-subunit of ATP synthase. In addition, ACHT was found to be involved in regulating nonphotochemical quenching, which is the mechanism underlying the thermal dissipation of excess light energy. Overall, these results indicate that Trx and Trx-like proteins regulate chloroplast functions in concert by controlling the redox state of various photosynthesis-related proteins in vivo.

Enhancing crop yield by using Rubisco activase to improve photosynthesis under elevated temperatures

With the rapid growth of world population, it is essential to increase agricultural productivity to feed the growing population. Over the past decades, many methods have been used to increase crop yields. Despite the success in boosting the crop yield through these methods, global food production still needs to be increased to be on par with the increasing population and its dynamic consumption patterns. Additionally, given the prevailing environmental conditions pertaining to the global temperature increase, heat stress will likely be a critical factor that negatively affects plant biomass and crop yield. One of the key elements hindering photosynthesis and plant productivity under heat stress is the thermo-sensitivity of the Rubisco activase (RCA), a molecular chaperone that converts Rubisco back to active form after it becomes inactive. It would be an attractive and practical strategy to maintain photosynthetic activity under elevated temperatures by enhancing the thermo-stability of RCA. In this context, this review discusses the need to improve the thermo-tolerance of RCA under current climatic conditions and to further study RCA structure and regulation, and its limitations at elevated temperatures. This review summarizes successful results and provides a perspective on RCA research and its implication in improving crop yield under elevated temperature conditions in the future.

Salicylic Acid Is Involved in Rootstock–Scion Communication in Improving the Chilling Tolerance of Grafted Cucumber

Salicylic acid (SA) has been proven to be a multifunctional signaling molecule that participates in the response of plants to abiotic stresses. In this study, we used cold-sensitive cucumber and cold-tolerant pumpkin as experimental materials to examine the roles of SA in root–shoot communication responses to aerial or/and root-zone chilling stress in own-root and hetero-root grafted cucumber and pumpkin plants. The results showed that pumpkin (Cm) rootstock enhanced the chilling tolerance of grafted cucumber, as evidenced by the observed lower levels of electrolyte leakage (EL), malondialdehyde (MDA), and higher photosynthetic rate (Pn) and gene expression of Rubisco activase (RCA). However, cucumber (Cs) rootstock decreased the chilling tolerance of grafted pumpkins. Cs/Cm plants showed an increase in the mRNA expression of C-repeat-binding factor (CBF1), an inducer of CBF expression (ICE1), and cold-responsive (COR47) genes and CBF1 protein levels in leaves under 5/25 and 5/5°C stresses, or in roots under 25/5 and 5/5°C stresses, respectively, compared with the Cs/Cs. Chilling stress increased the endogenous SA content and the activity of phenylalanine ammonia-lyase (PAL), and the increase in SA content and activity of PAL in Cs/Cm plants was much higher than in Cs/Cs plants. Transcription profiling analysis revealed the key genes of SA biosynthesis, PAL, ICS, and SABP2 were upregulated, while SAMT, the key gene of SA degradation, was downregulated in Cs/Cm leaves, compared with Cs/Cs leaves under chilling stress. The accumulation of SA in the Cs/Cm leaves was mainly attributed to an increase in SA biosynthesis in leaves and that in transport from roots under aerial and root-zone chilling stress, respectively. In addition, exogenous SA significantly upregulated the expression level of cold-responsive (COR) genes, enhanced actual photochemical efficiency (ΦPSII), maximum photochemical efficiency (Fv/Fm), and Pn, while decreased EL, MDA, and CI in grafted cucumber. These results suggest that SA is involved in rootstock–scion communication and grafting-induced chilling tolerance by upregulating the expression of COR genes in cucumber plants under chilling stress.

Magnesium Application Promotes Rubisco Activation and Contributes to High-Temperature Stress Alleviation in Wheat During the Grain Filling

Inhibited photosynthesis caused by post-anthesis high-temperature stress (HTS) leads to decreased wheat grain yield. Magnesium (Mg) plays critical roles in photosynthesis; however, its function under HTS during wheat grain filling remains poorly understood. Therefore, in this study, we investigated the effects of Mg on the impact of HTS on photosynthesis during wheat grain filling by conducting pot experiments in controlled-climate chambers. Plants were subjected to a day/night temperature cycle of 32°C/22°C for 5 days during post-anthesis; the control temperature was set at 26°C/16°C. Mg was applied at the booting stage, with untreated plants used as a control. HTS reduced the yield and net photosynthetic rate (Pn) of wheat plants. The maximum carboxylation rate (VCmax), which is limited by Rubisco activity, decreased earlier than the light-saturated potential electron transport rate. This decrease in VCmax was caused by decreased Rubisco activation state under HTS. Mg application reduced yield loss by stabilizing Pn. Rubisco activation was enhanced by increasing Rubisco activase activity following Mg application, thereby stabilizing Pn. We conclude that Mg maintains Rubisco activation, thereby helping to stabilize Pn under HTS.

Carbon Dioxide Concentration Mechanisms in Natural Populations of Marine Diatoms: Insights From Tara Oceans

Marine diatoms, the most successful photoautotrophs in the ocean, efficiently sequester a significant part of atmospheric CO2 to the ocean interior through their participation in the biological carbon pump. However, it is poorly understood how marine diatoms fix such a considerable amount of CO2, which is vital information toward modeling their response to future CO2 levels. The Tara Oceans expeditions generated molecular data coupled with in situ biogeochemical measurements across the main ocean regions, and thus provides a framework to compare diatom genetic and transcriptional flexibility under natural CO2 variability. The current study investigates the interlink between the environmental variability of CO2 and other physicochemical parameters with the gene and transcript copy numbers of five key enzymes of diatom CO2 concentration mechanisms (CCMs): Rubisco activase and carbonic anhydrase (CA) as part of the physical pathway, together with phosphoenolpyruvate carboxylase, phosphoenolpyruvate carboxykinase, and malic enzyme as part of the potential C4 biochemical pathway. Toward this aim, we mined >200 metagenomes and >220 metatranscriptomes generated from samples of the surface layer of 66 globally distributed sampling sites and corresponding to the four main size fractions in which diatoms can be found: 0.8–5 μm, 5–20 μm, 20–180 μm, and 180–2,000 μm. Our analyses revealed that the transcripts for the enzymes of the putative C4 biochemical CCM did not in general display co-occurring profiles. The transcripts for CAs were the most abundant, with an order of magnitude higher values than the other enzymes, thus implying the importance of physical CCMs in diatom natural communities. Among the different classes of this enzyme, the most prevalent was the recently characterized iota class. Consequently, very little information is available from natural diatom assemblages about the distribution of this class. Biogeographic distributions for all the enzymes show different abundance hotspots according to the size fraction, pointing to the influence of cell size and aggregation in CCMs. Environmental correlations showed a complex pattern of responses to CO2 levels, total phytoplankton biomass, temperature, and nutrient concentrations. In conclusion, we propose that biophysical CCMs are prevalent in natural diatom communities.

Rubisco production in maize mesophyll cells through ectopic expression of subunits and chaperones

C4 plants, such as maize, strictly compartmentalize Rubisco to bundle sheath chloroplasts. The molecular basis for the restriction of Rubisco from the more abundant mesophyll chloroplasts is not fully understood. Mesophyll chloroplasts transcribe the Rubisco large subunit gene, and when normally quiescent transcription of the nuclear Rubisco small subunit gene family is overcome by ectopic expression, mesophyll chloroplasts still do not accumulate measurable Rubisco. Here we show that a combination of five ubiquitin promoter-driven nuclear transgenes expressed in maize leads to mesophyll accumulation of assembled Rubisco. These encode the Rubisco large and small subunits, Rubisco Assembly Factors 1 and 2, and the assembly factor Bundle Sheath Defective 2. In these plants Rubisco large subunit accumulates in mesophyll cells, and appears to be assembled into holoenzyme capable of binding the substrate analog CABP. Isotope discrimination assays suggest, however, that mesophyll Rubisco is not participating in carbon assimilation in these plants, most likely due to a lack of the substrate ribulose 1,5-bisphosphate and/or Rubisco activase. Overall, this work defines a minimal set of Rubisco assembly factors in planta and may help lead to methods of regulating the C4 pathway.

The relative abundance of wheat Rubisco activase isoforms is post-transcriptionally regulated

Diurnal rhythms and light availability affect transcription–translation feedback loops that regulate the synthesis of photosynthetic proteins. The CO2-fixing enzyme Rubisco is the most abundant protein in the leaves of major crop species and its activity depends on interaction with the molecular chaperone Rubisco activase (Rca). In Triticum aestivum L. (wheat), three Rca isoforms are present that differ in their regulatory properties. Here, we tested the hypothesis that the relative abundance of the redox-sensitive and redox-insensitive Rca isoforms could be differentially regulated throughout light–dark diel cycle in wheat. While TaRca1-β expression was consistently negligible throughout the day, transcript levels of both TaRca2-β and TaRca2-α were higher and increased at the start of the day, with peak levels occurring at the middle of the photoperiod. Abundance of TaRca-β protein was maximal 1.5 h after the peak in TaRca2-β expression, but the abundance of TaRca-α remained constant during the entire photoperiod. The redox-sensitive TaRca-α isoform was less abundant, representing 85% of the redox-insensitive TaRca-β at the transcript level and 12.5% at the protein level. Expression of Rubisco large and small subunit genes did not show a consistent pattern throughout the diel cycle, but the abundance of Rubisco decreased by up to 20% during the dark period in fully expanded wheat leaves. These results, combined with a lack of correlation between transcript and protein abundance for both Rca isoforms and Rubisco throughout the entire diel cycle, suggest that the abundance of these photosynthetic enzymes is post-transcriptionally regulated.