WRKY48 negatively regulates plant acclimation to a combination of high light and heat stress.

Plants growing under natural conditions experience high light (HL) intensities that are often accompanied by elevated temperatures. These conditions could affect photosynthesis, reduce yield, and negatively impact agricultural productivity. The combination of different abiotic challenges creates a new type of stress for plants by generating complex environmental conditions that often exceed the impact of their individual parts. Transcription factors (TFs) play a key role in integrating the different molecular signals generated by multiple stress conditions, orchestrating the acclimation response of plants to stress. In this study, we show that the TF WRKY48 negatively controls the acclimation of Arabidopsis thaliana plants to a combination of HL and heat stress (HL + HS), and its expression is attenuated by jasmonic acid under HL + HS conditions. Using comparative physiological and transcriptomic analyses between wild-type and wrky48 mutants, we further demonstrate that under control conditions, WRKY48 represses the expression of a set of transcripts that are specifically required for the acclimation of plants to HL + HS, hence its suppression during the HL + HS stress combination contributes to plant survival under these conditions. Accordingly, mutants that lack WRKY48 are more resistant to HL + HS, and transgenic plants that overexpress WRKY48 are more sensitive to it. Taken together, our findings reveal that WRKY48 is a negative regulator of the transcriptomic response of Arabidopsis to HL + HS and provide new insights into the complex regulatory networks of plant acclimation to stress combination.

The impact of multifactorial stress combination on reproductive tissues and grain yield of a crop plant.

Global warming, climate change, and industrial pollution are altering our environment subjecting plants, microbiomes, and ecosystems to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. These conditions, termed, "multifactorial stress combination" (MFSC), can cause a significant decline in plant growth and survival. However, the impacts of MFSC on reproductive tissues and yield of major crop plants are largely unknown. We subjected soybean (Glycine max) plants to a MFSC of up to five different stresses (water deficit, salinity, low phosphate, acidity, and cadmium), in an increasing level of complexity, and conducted integrative transcriptomic-phenotypic analysis of their reproductive and vegetative tissues. We reveal that MFSC has a negative cumulative effect on soybean yield, that each set of MFSC condition elicits a unique transcriptomic response (that is different between flowers and leaves), and that selected genes expressed in leaves or flowers of soybean are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. Our study identified networks and pathways associated with reactive oxygen species, ascorbic acid and aldarate, and iron/copper signaling/metabolism as promising targets for future biotechnological efforts to augment the resilience of reproductive tissues of major crop plants to MFSC. In addition, we provide unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.

The impact of multifactorial stress combination on plants, crops, and ecosystems: how should we prepare for what comes next?

The complexity of environmental conditions encountered by plants in the field, or in nature, is gradually increasing due to anthropogenic activities that promote global warming, climate change, and increased levels of pollutants. While in the past it seemed sufficient to study how plants acclimate to one or even two different stresses affecting them simultaneously, the complex conditions developing on our planet necessitate a new approach of studying stress in plants: Acclimation to multiple stress conditions occurring concurrently or consecutively (termed, multifactorial stress combination [MFSC]). In an initial study of the plant response to MFSC, conducted with Arabidopsis thaliana seedlings subjected to an MFSC of six different abiotic stresses, it was found that with the increase in the number and complexity of different stresses simultaneously impacting a plant, plant growth and survival declined, even if the effects of each stress involved in such MFSC on the plant was minimal or insignificant. In three recent studies, conducted with different crop plants, MFSC was found to have similar effects on a commercial rice cultivar, a maize hybrid, tomato, and soybean, causing significant reductions in growth, biomass, physiological parameters, and/or yield traits. As the environmental conditions on our planet are gradually worsening, as well as becoming more complex, addressing MFSC and its effects on agriculture and ecosystems worldwide becomes a high priority. In this review, we address the effects of MFSC on plants, crops, agriculture, and different ecosystems worldwide, and highlight potential avenues to enhance the resilience of crops to MFSC.

The effects of multifactorial stress combination on rice and maize.

The complexity of environmental factors affecting crops in the field is gradually increasing due to climate change-associated weather events, such as droughts or floods combined with heat waves, coupled with the accumulation of different environmental and agricultural pollutants. The impact of multiple stress conditions on plants was recently termed "multifactorial stress combination" (MFSC) and defined as the occurrence of 3 or more stressors that impact plants simultaneously or sequentially. We recently reported that with the increased number and complexity of different MFSC stressors, the growth and survival of Arabidopsis (Arabidopsis thaliana) seedlings declines, even if the level of each individual stress is low enough to have no significant effect on plants. However, whether MFSC would impact commercial crop cultivars is largely unknown. Here, we reveal that a MFSC of 5 different low-level abiotic stresses (salinity, heat, the herbicide paraquat, phosphorus deficiency, and the heavy metal cadmium), applied in an increasing level of complexity, has a significant negative impact on the growth and biomass of a commercial rice (Oryza sativa) cultivar and a maize (Zea mays) hybrid. Proteomics, element content, and mixOmics analyses of MFSC in rice identified proteins that correlate with the impact of MFSC on rice seedlings, and analysis of 42 different rice genotypes subjected to MFSC revealed substantial genetic variability in responses to this unique state of stress combination. Taken together, our findings reveal that the impacts of MFSC on 2 different crop species are severe and that MFSC may substantially affect agricultural productivity.

Comparison of metabolomic reconfiguration between Columbia and Landsberg ecotypes subjected to the combination of high salinity and increased irradiance.

BACKGROUND: Plants growing in the field are subjected to combinations of abiotic stresses. These conditions pose a devastating threat to crops, decreasing their yield and causing a negative economic impact on agricultural production. Metabolic responses play a key role in plant acclimation to stress and natural variation for these metabolic changes could be key for plant adaptation to fluctuating environmental conditions. RESULTS: Here we studied the metabolomic response of two Arabidopsis ecotypes (Columbia-0 [Col] and Landsberg erecta-0 [Ler]), widely used as genetic background for Arabidopsis mutant collections, subjected to the combination of high salinity and increased irradiance. Our findings demonstrate that this stress combination results in a specific metabolic response, different than that of the individual stresses. Although both ecotypes displayed reduced growth and quantum yield of photosystem II, as well as increased foliar damage and malondialdehyde accumulation, different mechanisms to tolerate the stress combination were observed. These included a relocation of amino acids and sugars to act as potential osmoprotectants, and the accumulation of different stress-protective compounds such as polyamines or secondary metabolites. CONCLUSIONS: Our findings reflect an initial identification of metabolic pathways that differentially change under stress combination that could be considered in studies of stress combination of Arabidopsis mutants that include Col or Ler as genetic backgrounds.

Exogenous spermine alleviates the negative effects of combined salinity and paraquat in tomato plants by decreasing stress-induced oxidative damage.

Plants are frequently exposed to different combinations of soil constraints including salinity and different herbicides. These abiotic conditions negatively affect photosynthesis, growth and plant development resulting in limitations in agriculture production. To respond to these conditions, plants accumulate different metabolites that restore cellular homeostasis and are key for stress acclimation processes. In this work, we analyzed the role of exogenous spermine (Spm), a polyamine involved in plant tolerance to abiotic stress, in tomato responses to the combination of salinity (S) and the herbicide paraquat (PQ). Our findings showed that application of Spm reduced leaf damage and enhanced survival, growth, photosystem II function and photosynthetic rate of tomato plants subjected to the combination of S and PQ. In addition, we revealed that exogenous Spm reduced H2O2 and malondialdehyde (MDA) accumulation in plants subjected to S+PQ, suggesting that the role of exogenous Spm in alleviating the negative effects of this stress combination could be attributed to a decrease in stress-induced oxidative damage in tomato plants. Taken together, our results identify a key role for Spm in improving plant tolerance to combined stress.

Climate change-associated multifactorial stress combination: A present challenge for our ecosystems.

Humans negatively influence Earth ecosystems and biodiversity causing global warming, climate change as well as man-made pollution. Recently, the number of different stress factors have increased, and when impacting simultaneously, the multiple stress conditions cause dramatic declines in plant and ecosystem health. Although much is known about how plants and ecosystems are affected by each individual stress, recent research efforts have diverted into how these biological systems respond to several of these stress conditions applied together. Studies of such "multifactorial stress combination" concept have reported a severe decrease in plant survival and microbiome biodiversity along the increasing number of factors in a consistent directional trend. In addition, these results are in concert with studies about how ecosystems and microbiota are affected by natural conditions imposed by climate change. Therefore, all this evidence should serve as an important warning in order to decrease pollutants, create strategies to deal with global warming, and increase the tolerance of plants to multiple stressful factors in combination. Here we review recent studies focused on the impact of abiotic stresses on plants, agrosystems and different ecosystems including forests and microecosystems. In addition, different strategies to mitigate the impact of climate change in ecosystems are discussed.