Photosynthesis in newly developed leaves of heat-tolerant wheat acclimates to long-term nocturnal warming.

We examined photosynthetic traits of pre-existing and newly developed flag leaves of four wheat genotypes grown in controlled-environment experiments. In newly developed leaves, acclimation of the maximum rate of net CO2 assimilation (An) to warm nights (i.e. increased An) was associated with increased capacity of Rubisco carboxylation and photosynthetic electron transport, with Rubisco activation state probably contributing to increased Rubisco activity. Metabolite profiling linked acclimation of An to greater accumulation of monosaccharides and saturated fatty acids in leaves; these changes suggest roles for osmotic adjustment of leaf turgor pressure and maintenance of cell membrane integrity. By contrast, where An decreased under warm nights, the decline was related to lower stomatal conductance and rates of photosynthetic electron transport. Decreases in An occurred despite higher basal PSII thermal stability in all genotypes exposed to warm nights: Tcrit of 45-46.5 °C in non-acclimated versus 43.8-45 °C in acclimated leaves. Pre-existing leaves showed no change in An-temperature response curves, except for an elite heat-tolerant genotype. These findings illustrate the impact of night-time warming on the ability of wheat plants to photosynthesize during the day, thereby contributing to explain the impact of global warming on crop productivity.

Wheat photosystem II heat tolerance: evidence for genotype-by-environment interactions.

High temperature stress inhibits photosynthesis and threatens wheat production. One measure of photosynthetic heat tolerance is Tcrit - the critical temperature at which incipient damage to photosystem II (PSII) occurs. This trait could be improved in wheat by exploiting genetic variation and genotype-by-environment interactions (GEI). Flag leaf Tcrit of 54 wheat genotypes was evaluated in 12 thermal environments over 3 years in Australia, and analysed using linear mixed models to assess GEI effects. Nine of the 12 environments had significant genetic effects and highly variable broad-sense heritability (H2 ranged from 0.15 to 0.75). Tcrit GEI was variable, with 55.6% of the genetic variance across environments accounted for by the factor analytic model. Mean daily growth temperature in the month preceding anthesis was the most influential environmental driver of Tcrit GEI, suggesting biochemical, physiological and structural adjustments to temperature requiring different durations to manifest. These changes help protect or repair PSII upon exposure to heat stress, and may improve carbon assimilation under high temperature. To support breeding efforts to improve wheat performance under high temperature, we identified genotypes superior to commercial cultivars commonly grown by farmers, and demonstrated potential for developing genotypes with greater photosynthetic heat tolerance.

Wheat photosystem II heat tolerance responds dynamically to short- and long-term warming.

Wheat photosynthetic heat tolerance can be characterized using minimal chlorophyll fluorescence to quantify the critical temperature (Tcrit) above which incipient damage to the photosynthetic machinery occurs. We investigated intraspecies variation and plasticity of wheat Tcrit under elevated temperature in field and controlled-environment experiments, and assessed whether intraspecies variation mirrored interspecific patterns of global heat tolerance. In the field, wheat Tcrit varied diurnally-declining from noon through to sunrise-and increased with phenological development. Under controlled conditions, heat stress (36 °C) drove a rapid (within 2 h) rise in Tcrit that peaked after 3-4 d. The peak in Tcrit indicated an upper limit to PSII heat tolerance. A global dataset [comprising 183 Triticum and wild wheat (Aegilops) species] generated from the current study and a systematic literature review showed that wheat leaf Tcrit varied by up to 20 °C (roughly two-thirds of reported global plant interspecies variation). However, unlike global patterns of interspecies Tcrit variation that have been linked to latitude of genotype origin, intraspecific variation in wheat Tcrit was unrelated to that. Overall, the observed genotypic variation and plasticity of wheat Tcrit suggest that this trait could be useful in high-throughput phenotyping of wheat photosynthetic heat tolerance.

Wheat respiratory O2 consumption falls with night warming alongside greater respiratory CO2 loss and reduced biomass.

Warming nights are correlated with declining wheat growth and yield. As a key determinant of plant biomass, respiration consumes O2 as it produces ATP and releases CO2 and is typically reduced under warming to maintain metabolic efficiency. We compared the response of respiratory O2 and CO2 flux to multiple night and day warming treatments in wheat leaves and roots, using one commercial (Mace) and one breeding cultivar grown in controlled environments. We also examined the effect of night warming and a day heatwave on the capacity of the ATP-uncoupled alternative oxidase (AOX) pathway. Under warm nights, plant biomass fell, respiratory CO2 release measured at a common temperature was unchanged (indicating higher rates of CO2 release at prevailing growth temperature), respiratory O2 consumption at a common temperature declined, and AOX pathway capacity increased. The uncoupling of CO2 and O2 exchange and enhanced AOX pathway capacity suggest a reduction in plant energy demand under warm nights (lower O2 consumption), alongside higher rates of CO2 release under prevailing growth temperature (due to a lack of down-regulation of respiratory CO2 release). Less efficient ATP synthesis, teamed with sustained CO2 flux, could thus be driving observed biomass declines under warm nights.

The thermal tolerance of photosynthetic tissues: a global systematic review and agenda for future research.

Understanding plant thermal tolerance is fundamental to predicting impacts of extreme temperature events that are increasing in frequency and intensity across the globe. Extremes, not averages, drive species evolution, determine survival and increase crop performance. To better prioritize agricultural and natural systems research, it is crucial to evaluate how researchers are assessing the capacity of plants to tolerate extreme events. We conducted a systematic review to determine how plant thermal tolerance research is distributed across wild and domesticated plants, growth forms and biomes, and to identify crucial knowledge gaps. Our review shows that most thermal tolerance research examines cold tolerance of cultivated species; c. 5% of articles consider both heat and cold tolerance. Plants of extreme environments are understudied, and techniques widely applied in cultivated systems are largely unused in natural systems. Lastly, we find that lack of standardized methods and metrics compromises the potential for mechanistic insight. Our review provides an entry point for those new to the methods used in plant thermal tolerance research and bridges often disparate ecological and agricultural perspectives for the more experienced. We present a considered agenda of thermal tolerance research priorities to stimulate efficient, reliable and repeatable research across the spectrum of plant thermal tolerance.

Responses of leaf respiration to heatwaves.

Mitochondrial respiration (R) is central to plant physiology and responds dynamically to daily short-term temperature changes. In the longer-term, changes in energy demand and membrane fluidity can decrease leaf R at a common temperature and increase the temperature at which leaf R peaks (Tmax ). However, leaf R functionality is more susceptible to short-term heatwaves. Catalysis increases with rising leaf temperature, driving faster metabolism and leaf R demand, despite declines in photosynthesis restricting assimilate supply and growth. Proteins denature as temperatures increase further, adding to maintenance costs. Excessive heat also inactivates respiratory enzymes, with a concomitant limitation on the capacity of the R system. These competing push-and-pull factors are responsible for the diminishing acceleration in leaf R rate as temperature rises. Under extreme heat, membranes become overly fluid, and enzymes such as the cytochrome c oxidase are impaired. Such changes can lead to over-reduction of the energy system culminating in reactive oxygen species production. This ultimately leads to the total breakdown of leaf R, setting the limit of leaf survival. Understanding the heat stress responses of leaf R is imperative, given the continued rise in frequency and intensity of heatwaves and the importance of R for plant fitness and survival.

Acclimation of leaf photosynthesis and respiration to warming in field-grown wheat.

Climate change and future warming will significantly affect crop yield. The capacity of crops to dynamically adjust physiological processes (i.e., acclimate) to warming might improve overall performance. Understanding and quantifying the degree of acclimation in field crops could ensure better parameterization of crop and Earth System models and predictions of crop performance. We hypothesized that for field-grown wheat, when measured at a common temperature (25°C), crops grown under warmer conditions would exhibit acclimation, leading to enhanced crop performance and yield. Acclimation was defined as (a) decreased rates of net photosynthesis at 25°C (A25 ) coupled with lower maximum carboxylation capacity (Vcmax25 ), (b) reduced leaf dark respiration at 25°C (both in terms of O2 consumption Rdark _O225 and CO2 efflux Rdark _CO225 ) and (c) lower Rdark _CO225 to Vcmax25 ratio. Field experiments were conducted over two seasons with 20 wheat genotypes, sown at three different planting dates, to test these hypotheses. Leaf-level CO2 -based traits (A25 , Rdark _CO225 and Vcmax25 ) did not show the classic acclimation responses that we hypothesized; by contrast, the hypothesized changes in Rdark_ O2 were observed. These findings have implications for predictive crop models that assume similar temperature response among these physiological processes and for predictions of crop performance in a future warmer world.

Predicting dark respiration rates of wheat leaves from hyperspectral reflectance.

Greater availability of leaf dark respiration (Rdark ) data could facilitate breeding efforts to raise crop yield and improve global carbon cycle modelling. However, the availability of Rdark data is limited because it is cumbersome, time consuming, or destructive to measure. We report a non-destructive and high-throughput method of estimating Rdark from leaf hyperspectral reflectance data that was derived from leaf Rdark measured by a destructive high-throughput oxygen consumption technique. We generated a large dataset of leaf Rdark for wheat (1380 samples) from 90 genotypes, multiple growth stages, and growth conditions to generate models for Rdark . Leaf Rdark (per unit leaf area, fresh mass, dry mass or nitrogen, N) varied 7- to 15-fold among individual plants, whereas traits known to scale with Rdark , leaf N, and leaf mass per area (LMA) only varied twofold to fivefold. Our models predicted leaf Rdark , N, and LMA with r2 values of 0.50-0.63, 0.91, and 0.75, respectively, and relative bias of 17-18% for Rdark and 7-12% for N and LMA. Our results suggest that hyperspectral model prediction of wheat leaf Rdark is largely independent of leaf N and LMA. Potential drivers of hyperspectral signatures of Rdark are discussed.

Exploring high temperature responses of photosynthesis and respiration to improve heat tolerance in wheat.

High temperatures account for major wheat yield losses annually and, as the climate continues to warm, these losses will probably increase. Both photosynthesis and respiration are the main determinants of carbon balance and growth in wheat, and both are sensitive to high temperature. Wheat is able to acclimate photosynthesis and respiration to high temperature, and thus reduce the negative affects on growth. The capacity to adjust these processes to better suit warmer conditions stands as a potential avenue toward reducing heat-induced yield losses in the future. However, much remains to be learnt about such phenomena. Here, we review what is known of high temperature tolerance in wheat, focusing predominantly on the high temperature responses of photosynthesis and respiration. We also identify the many unknowns that surround this area, particularly with respect to the high temperature response of wheat respiration and the consequences of this for growth and yield. It is concluded that further investigation into the response of photosynthesis and respiration to high temperature could present several methods of improving wheat high temperature tolerance. Extending our knowledge in this area could also lead to more immediate benefits, such as the enhancement of current crop models.

Resilience of rice (Oryza spp.) pollen germination and tube growth to temperature stress.

Resilience of rice cropping systems to potential global climate change will partly depend on the temperature tolerance of pollen germination (PG) and tube growth (PTG). Pollen germination of high temperature-susceptible Oryza glaberrima Steud. (cv. CG14) and Oryza sativa L. ssp. indica (cv. IR64) and high temperature-tolerant O. sativa ssp. aus (cv. N22), was assessed on a 5.6-45.4 °C temperature gradient system. Mean maximum PG was 85% at 27 °C with 1488 µm PTG at 25 °C. The hypothesis that in each pollen grain, the minimum temperature requirements (Tn ) and maximum temperature limits (Tx ) for germination operate independently was accepted by comparing multiplicative and subtractive probability models. The maximum temperature limit for PG in 50% of grains (Tx(50) ) was the lowest (29.8 °C) in IR64 compared with CG14 (34.3 °C) and N22 (35.6 °C). Standard deviation (sx ) of Tx was also low in IR64 (2.3 °C) suggesting that the mechanism of IR64's susceptibility to high temperatures may relate to PG. Optimum germination temperatures and thermal times for 1 mm PTG were not linked to tolerating high temperatures at anthesis. However, the parameters Tx(50) and sx in the germination model define new pragmatic criteria for successful and resilient PG, preferable to the more traditional cardinal (maximum and minimum) temperatures.

High night temperature induces contrasting responses for spikelet fertility, spikelet tissue temperature, flowering characteristics and grain quality in rice.

Climate change is increasing night temperature (NT) more than day temperature (DT) in rice-growing areas. Effects of combinations of NT (24-35°C) from microsporogenesis to anthesis at one or more DT (30 or 35°C) at anthesis on rice spikelet fertility, temperature within spikelets, flowering pattern, grain weight per panicle, amylose content and gel consistency were investigated in contrasting rice cultivars under controlled environments. Cultivars differed in spikelet fertility response to high NT, with higher fertility associated with cooler spikelets (P<0.01). Flowering dynamics were altered by high NT and a novel high temperature tolerance complementary mechanism, shorter flower open duration in cv. N22, was identified. High NT reduced spikelet fertility, grain weight per panicle, amylose content and gel consistency, whereas high DT reduced only gel consistency. Night temperature >27°C was estimated to reduce grain weight. Generally, high NT was more damaging to grain weight and selected grain quality traits than high DT, with little or no interaction between them. The critical tolerance and escape traits identified, i.e. spikelet cooling, relatively high spikelet fertility, earlier start and peak time of anthesis and shorter spikelet anthesis duration can aid plant breeding programs targeting resilience in warmer climates.