Global Warming, Climate Change, and Environmental Pollution: Recipe for a Multifactorial Stress Combination Disaster

A multifactorial stress combination occurs when more than two to three abiotic and/or biotic stress factors simultaneously impact a plant.Global warming, climate change, and industrial pollution could result in an increase in the frequency, complexity, and intensity of multifactorial stress combinations impacting plants, soils, and microbial communities.With the increase in the number of factors simultaneously impacting plants, the survival and growth of plants declines, even if the levels of each of these individual stresses is very low.The response of plants to a multifactorial stress combination is unique and involves many transcripts and genes that are not altered in response to each of the different stresses applied individually.The harmful effects of a multifactorial stress combination on the survival and growth of plants, different soil properties, and diversity of microbial communities should serve as a dire warning to our society and prompt us to act drastically to reduce the different sources of multifactorial stresses in our environment. Global warming, climate change, and environmental pollution present plants with unique combinations of different abiotic and biotic stresses. Although much is known about how plants acclimate to each of these individual stresses, little is known about how they respond to a combination of many of these stress factors occurring together, namely a multifactorial stress combination. Recent studies revealed that increasing the number of different co-occurring multifactorial stress factors causes a severe decline in plant growth and survival, as well as in the microbiome biodiversity that plants depend upon. This effect should serve as a dire warning to our society and prompt us to decisively act to reduce pollutants, fight global warming, and augment the tolerance of crops to multifactorial stress combinations. Global warming, climate change, and environmental pollution present plants with unique combinations of different abiotic and biotic stresses. Although much is known about how plants acclimate to each of these individual stresses, little is known about how they respond to a combination of many of these stress factors occurring together, namely a multifactorial stress combination. Recent studies revealed that increasing the number of different co-occurring multifactorial stress factors causes a severe decline in plant growth and survival, as well as in the microbiome biodiversity that plants depend upon. This effect should serve as a dire warning to our society and prompt us to decisively act to reduce pollutants, fight global warming, and augment the tolerance of crops to multifactorial stress combinations. The accumulated impact of human life on our planet over the past several decades, and in particular the industrial revolution, resulted in a constant increase in greenhouse gas production (mainly CO2) caused by the burning of fossil fuels (Figure 1A ; www.ipcc.ch/) [1.Sala O.E. et al.Global biodiversity scenarios for the year 2100.Science. 2000; 287: 1770-1774Crossref PubMed Scopus (5873) Google Scholar, 2.Mazdiyasni O. AghaKouchak A. Substantial increase in concurrent droughts and heatwaves in the United States.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11484-11489Crossref PubMed Scopus (242) Google Scholar, 3.Lehmann J. Rillig M. Distinguishing variability from uncertainty.Nat. Clim. Chang. 2014; 4: 153Crossref Scopus (21) Google Scholar, 4.Bigot S. et al.Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change.Glob. Chang. 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The accumulation of CO2 in the atmosphere traps the IR radiation emitted from the surface of the Earth following absorption of sunlight and heats our planet, driving an alarming trend of continual increase in global surface and ocean temperatures, termed global warming (Figure 1A; www.ipcc.ch/, https://ourworldindata.org/owid-grapher, www.eea.europa.eu/) [1.Sala O.E. et al.Global biodiversity scenarios for the year 2100.Science. 2000; 287: 1770-1774Crossref PubMed Scopus (5873) Google Scholar, 2.Mazdiyasni O. AghaKouchak A. Substantial increase in concurrent droughts and heatwaves in the United States.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11484-11489Crossref PubMed Scopus (242) Google Scholar, 3.Lehmann J. Rillig M. Distinguishing variability from uncertainty.Nat. Clim. Chang. 2014; 4: 153Crossref Scopus (21) Google Scholar, 4.Bigot S. et al.Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change.Glob. Chang. 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Global warming in turn drives a drastic change in our climate, termed climate change, that is accompanied by an increase in the frequency and intensity of droughts and heat waves (Figure 1B), as well as of other abiotic stress conditions such as flooding, salinity, and freezing stresses (www.ipcc.ch/, www.ncdc.noaa.gov/, https://ourworldindata.org/owid-grapher, www.eea.europa.eu/, www.epa.gov/) [1.Sala O.E. et al.Global biodiversity scenarios for the year 2100.Science. 2000; 287: 1770-1774Crossref PubMed Scopus (5873) Google Scholar, 2.Mazdiyasni O. AghaKouchak A. Substantial increase in concurrent droughts and heatwaves in the United States.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11484-11489Crossref PubMed Scopus (242) Google Scholar, 3.Lehmann J. Rillig M. Distinguishing variability from uncertainty.Nat. Clim. 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As a result, the quality of water used to irrigate crops (e.g., its pH, salinity levels, and content of different contaminants) is declining [7.Bailey-Serres J. et al.Genetic strategies for improving crop yields.Nature. 2019; 575: 109-118Crossref PubMed Scopus (193) Google Scholar,12.Mittler R. Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives.Annu. Rev. Plant Biol. 2010; 61: 443-462Crossref PubMed Scopus (618) Google Scholar,13.Lobell D.B. Gourdji S.M. The influence of climate change on global crop productivity.Plant Physiol. 2012; 160: 1686-1697Crossref PubMed Scopus (502) Google Scholar]. In addition to the gradual increase in day and night temperatures [14.Slattery R.A. Ort D.R. Carbon assimilation in crops at high temperatures.Plant Cell Environ. 2019; 42: 2750-2758Crossref PubMed Scopus (25) Google Scholar, 15.Grinevich D.O. et al.Novel transcriptional responses to heat revealed by turning up the heat at night.Plant Mol. 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A. 2015; 112: 11484-11489Crossref PubMed Scopus (242) Google Scholar, 3.Lehmann J. Rillig M. Distinguishing variability from uncertainty.Nat. Clim. Chang. 2014; 4: 153Crossref Scopus (21) Google Scholar]). Such increases would further threaten global food production and security, potentially destabilizing different areas on our planet, leading to unrest, hunger, and even wars [27.Challinor A.J. et al.A meta-analysis of crop yield under climate change and adaptation.Nat. Clim. Chang. 2014; 4: 287-291Crossref Scopus (898) Google Scholar, 28.Savary S. Willocquet L. Modeling the impact of crop diseases on global food security.Annu. Rev. Phytopathol. 2020; 58: 313-341Crossref PubMed Scopus (9) Google Scholar, 29.Mourtzinis S. et al.Climate-induced reduction in US-wide soybean yields underpinned by region-and in-season-specific responses.Nat. Plants. 2015; 114026Crossref PubMed Scopus (52) Google Scholar]. In addition, the geographical growth areas of many important crops are expected to shift as temperatures climb and conditions worsen (Figure 1F) (www.eea.europa.eu/) [7.Bailey-Serres J. et al.Genetic strategies for improving crop yields.Nature. 2019; 575: 109-118Crossref PubMed Scopus (193) Google Scholar,8.Cline W.R. Global Warming and Agriculture: Impact Estimates by Country. Peterson Institute for International Economics, 2007Google Scholar,12.Mittler R. Blumwald E. Genetic engineering for modern agriculture: challenges and perspectives.Annu. Rev. Plant Biol. 2010; 61: 443-462Crossref PubMed Scopus (618) Google Scholar]. Although not expected to impact plants all at once, different combinations of the environmental factors, stressors, pollutants, pathogens, and pests, as described in the previous text, are likely to affect plants, crops, and trees growing in different areas of our planet. Furthermore, owing to the continual increase in many of the processes that drive these factors (Figure 1A–E) (www.ipcc.ch/), the likelihood that plants will be subjected to a multifactorial stress combination (Box 1) of several co-occurring stressors is gradually increasing [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar,31.Zandalinas S.I. et al.The impact of multifactorial stress combination on plant growth and survival.New Phytol. 2021; (Published online January 26, 2021. https://doi.org/10.1111/nph.17232)Crossref PubMed Scopus (15) Google Scholar].Box 1The Definition of a Multifactorial Stress CombinationWe define a multifactorial stress combination as a combination of three or more (n ≥ 3) stress factors simultaneously impacting plants. This definition takes the concept of a simple combination of two or at most three different stresses (e.g., drought and heat, salt and heat, drought, salinity and heat, or drought, heat and virus infection; e.g., [42.Sewelam N. et al.Molecular plant responses to combined abiotic stresses put a spotlight on unknown and abundant genes.J. Exp. Bot. 2020; 71: 5098-5112Crossref PubMed Scopus (11) Google Scholar,44.Rizhsky L. et al.When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress.Plant Physiol. 2004; 134: 1683-1696Crossref PubMed Scopus (1044) Google Scholar,48.Prasch C.M. Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks.Plant Physiol. 2013; 162: 1849-1866Crossref PubMed Scopus (261) Google Scholar,50.Shaar-Moshe L. et al.Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat.Plant Physiol. 2017; 174: 421-434Crossref PubMed Scopus (48) Google Scholar]) and extends it to a combination of multiple factors. As depicted in the model presented in Figure I, the multiple stress factors that could simultaneously impact plants can be of biotic (e.g., virus, bacteria, insect), abiotic climate-driven (e.g., flooding, drought, heat), abiotic man-made anthropogenic (e.g., pesticides, antibiotics, heavy metals), or biotic/abiotic soil-associated (e.g., nutrient deficiency, salinity, decreased microbial diversity) origin. Any combination of three or more such factors, impacting plants simultaneously, is therefore defined as a multifactorial stress combination. We define a multifactorial stress combination as a combination of three or more (n ≥ 3) stress factors simultaneously impacting plants. This definition takes the concept of a simple combination of two or at most three different stresses (e.g., drought and heat, salt and heat, drought, salinity and heat, or drought, heat and virus infection; e.g., [42.Sewelam N. et al.Molecular plant responses to combined abiotic stresses put a spotlight on unknown and abundant genes.J. Exp. Bot. 2020; 71: 5098-5112Crossref PubMed Scopus (11) Google Scholar,44.Rizhsky L. et al.When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress.Plant Physiol. 2004; 134: 1683-1696Crossref PubMed Scopus (1044) Google Scholar,48.Prasch C.M. Sonnewald U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks.Plant Physiol. 2013; 162: 1849-1866Crossref PubMed Scopus (261) Google Scholar,50.Shaar-Moshe L. et al.Unique physiological and transcriptional shifts under combinations of salinity, drought, and heat.Plant Physiol. 2017; 174: 421-434Crossref PubMed Scopus (48) Google Scholar]) and extends it to a combination of multiple factors. As depicted in the model presented in Figure I, the multiple stress factors that could simultaneously impact plants can be of biotic (e.g., virus, bacteria, insect), abiotic climate-driven (e.g., flooding, drought, heat), abiotic man-made anthropogenic (e.g., pesticides, antibiotics, heavy metals), or biotic/abiotic soil-associated (e.g., nutrient deficiency, salinity, decreased microbial diversity) origin. Any combination of three or more such factors, impacting plants simultaneously, is therefore defined as a multifactorial stress combination. At least two recent studies addressed the potential effects of a multifactorial stress combination on plants, soils, and different microbial populations. Rillig et al. [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar] examined the impact of multifactorial stress combination on soil properties and microbial populations. The effects of ten different stress factors associated with global warming, climate change, and environmental pollution were studied on soils, using different combinations of drought, low nitrogen, temperature, microplastics, glyphosate, antibiotics, fungicides, copper, salinity, and insecticides. It was found that an increase in the number of factors constituting a multifactorial stress combination (selected sets of one, two, five, eight, and ten stress factors) was accompanied by a decrease in the diversity of the soil microbiome, soil respiration, and other soil properties such as water-stable soil aggregates and decomposition rate (Figure 2A ). Although previous studies proposed that such an effect would occur, Rillig et al. [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar] were the first to demonstrate the negative effects of multifactorial stress combination on soil properties and microbial communities. Examining the impact of a multifactorial stress combination on plants, Zandalinas et al. [31.Zandalinas S.I. et al.The impact of multifactorial stress combination on plant growth and survival.New Phytol. 2021; (Published online January 26, 2021. https://doi.org/10.1111/nph.17232)Crossref PubMed Scopus (15) Google Scholar] subjected arabidopsis (Arabidopsis thaliana) seedlings to a combination of six different stresses, including heat, salt, high light, cadmium, acidity, and the herbicide paraquat (Figure 2B,C). In addition to studying the impact of multifactorial stress combination on plant growth and survival, this study also conducted a transcriptomic analysis of a selected set of multifactorial stress combinations and examined the impact of multifactorial stresses on the survival of different mutants impaired in reactive oxygen species (ROS) metabolism, as well as other metabolic processes and hormonal signaling pathways. Perhaps the most important finding of this study was that, although each of the different stresses, applied individually to plants, had a negligible effect on their growth and survival, the accumulated impact of multifactorial stress combination on plants was detrimental (Figure 2B,C). This finding is important because it demonstrates that different stresses can interact to negatively impact plant health and performance, even if the effect of each stress applied individually is negligible. Multifactorial stress combination could therefore impact agricultural areas or ecosystems in ways that we may not be able to predict. For example, we may not be able to observe a clear decline in crop yields or ecosystems because of a low level of a single stress factor; however, once additional factors are introduced, even at low levels, they could negatively interact with each other and lead to dramatic decreases in agricultural productivity, as well as push ecosystems towards a rapid decline. Together with the pioneering study of Rillig et al. [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar], the results reported by Zandalinas et al. [31.Zandalinas S.I. et al.The impact of multifactorial stress combination on plant growth and survival.New Phytol. 2021; (Published online January 26, 2021. https://doi.org/10.1111/nph.17232)Crossref PubMed Scopus (15) Google Scholar] therefore suggest that, with the increasing number of simultaneously occurring environmental stress factors in our environment, plant life, microbiomes, and soils are likely to deteriorate further (Figure 2). The similar trends observed in these two studies should serve as a dire warning to our society. Further altering our climate and polluting our environment could result in even higher complexities of multifactorial stress combinations that in turn would drive a crucial decline in plant growth, soil conditions, and overall agricultural productivity [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar,31.Zandalinas S.I. et al.The impact of multifactorial stress combination on plant growth and survival.New Phytol. 2021; (Published online January 26, 2021. https://doi.org/10.1111/nph.17232)Crossref PubMed Scopus (15) Google Scholar]. While the study of Rillig et al. [30.Rillig M.C. et al.The role of multiple global change factors in driving soil functions and microbial biodiversity.Science. 2019; 366: 886-890Crossref PubMed Scopus (121) Google Scholar] demonstrated that multifactorial stress combinations degrade soils (Figure 2A), Zandalinas et al. [31.Zandalinas S.I. et al.The impact of multifactorial stress combination on plant growth and survival.New Phytol. 2021; (Published online January 26, 2021. https://doi.org/10.1111/nph.17232)Crossref PubMed Scopus (15) Google Scholar] demonstrated that the impact of multifactorial stress combination on plants is similar between plants growing in peat soil (Figure 2C) or on agar plates (Figure 2B). Plants growing in