Impact of Climate Change on Soil Carbon Exchange, Ecosystem Dynamics, and Plant–Microbe Interactions

CHAPTER 15

Impact of Climate Change on Soil Carbon Exchange, Ecosystem Dynamics, and Plant Microbe Interactions Mohd Aamir1, Krishna Kumar Rai1,2, Manish Kumar Dubey1, Andleeb Zehra1, Yashoda Nandan Tripathi1, Kumari Divyanshu1, Swarnmala Samal1 and R.S. Upadhyay1 1

Laboratory of Mycopathology and Microbial Technology, Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, India 2 Division of Crop Improvement and Biotechnology, Indian Institute of Vegetable Research, Indian Council of Agricultural Research (ICAR), Varanasi, India

Contents 15.1 Introduction 15.2 Climate Change, Plant Diseases, and Host Pathogen Interaction 15.3 Climate Change: Impact on Carbon Exchange and Microbial Activities 15.4 Microbial Response Mechanism to Climate Change 15.5 Impact of Climatic Change on Plant Microbe Interactions 15.6 Climate Change and Abiotic Stress: Microbe-Mediated Stress Alleviation 15.7 Microbial Attenuation of Abiotic Stress 15.8 Mechanism of Microbe-Mediated Stress Tolerance 15.9 Conclusion Acknowledgments Author Contributions Statement Conflict of Interest References Further Reading

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15.1 INTRODUCTION Global climate change is a matter of debate among researchers, scientists, and environmentalists. The changing climate in different regions has affected many natural phenomena including weather patterns and sea levels, as well as modulating the lifestyles and biogeography of flora and Climate Change and Agricultural Ecosystems DOI: https://doi.org/10.1016/B978-0-12-816483-9.00020-7

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fauna. The Intergovernmental Panel on Climate Change (IPCC) estimated that in order to limit global warming to 1.5°C above preindustrial levels, CO2 emissions must be reduced by approximately 45% from 2010 levels by 2030, and reach net zero around 2050 (Weigmann, 2019). Furthermore, according to one report, it was projected that the temperature and CO2 concentration may increase by 3.4°C and 1250 ppm by 2095, respectively (Savary et al., 2012), which would cause more variabilities in climatic conditions and adverse weather events (Pachauri and Reisinger, 2007) affecting agriculture, forest, flora, fauna, and their existing co-interactions drastically (Pathak et al., 2018). The IPCC predicted that, by 2100, the resilience of the majority of the natural ecosystem would be likely to be exceeded by the combinations of climate change, and the associated disturbances including high temperature, drought, salinity, flooding, wildfire, ocean acidification, insects, and other factors regulating the global climate change such as deforestation, habitat destruction, overexploitation of resources, land use change and pollution. Several natural causes that have been reported for changed climatic conditions including modification in solar activity, ice cap distribution, volcanic eruption, and waves. In contrast, the artificial causes include various anthropogenic activities, such as CO2 emissions from various industrial areas, deforestation, acid rain, depletion of the ozone layer, and increased evolution of greenhouse gases (GHGs) (Presidential Advisory Council on Education, Science, and Technology: PACEST, 2007). However, since the mid-20th century, the main causes of global warming and climate change have been the unrestrained release of GHGs, particularly atmospheric CO2 (Serrano et al., 2019). The greenhouse effect on the Earth is mainly contributed to by deforestation, burning of fossil fuels, and intensification of agriculture sector. Past reports have predicted that about 20% 35% of total GHGs emission are contributed by agriculture (Thangarajan et al., 2013; Zhou et al., 2016). According to one report, during 2010 13 about 12,000 tons of CO2 was released mainly from deforestation, management of nutrients, soil emission, and livestock production (IPCC, 2014). The continuum change in climatic conditions is the result of changes in the carbon flux distributed between the land, oceans, and atmosphere. Climate change affects the soil microbial activities in both a direct and indirect manner. Therefore, the soil microbiota reactions to GHGs in the atmosphere play an important role in global warming. Some indispensable climatic parameters including temperature, humidity, precipitation, solar radiation, and air motion are directly or indirectly involved

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in the regulation of energy and water balance in a geographical region. However, the cumulative effects of these variables cannot be avoided as there is considerable potential for mutual interactions between these variables that may cause additive or antagonistic effects on soil microbiota and, therefore, activities engaged in the production of GHGs (Shaw et al., 2002; Mikkelsen et al., 2008). The most speculated on and direct effects of climate change include the warming effects or increase in temperature, extreme climatic episodes, and precipitation changes, whereas indirect effects include complexities observed in the diversity of the microbial population in the soil that alter the physiochemical conditions of soil and thereby affect plant productivity (Bardgett et al., 2008). Additionally, the fluctuations observed in climatic trends are also affected by carbon allocation to the microbial community which overall affects the community structures and dynamics of the microbial system, playing a crucial role in the decomposition of organic matter. Moreover, the biological mechanisms responsible for regulating this exchange and distribution of carbon between interdependent community systems affects climate change through climate-ecosystem feedback and could augment or the longlasting effects of regional or global climate (Heimann and Reichstein, 2008). The distribution and circulation of carbon between the terrestrial ecosystems function as a global carbon sink through C (carbon) accumulation in the living vegetations, microbial biomass, and in soil (including litter, detritus, and humic components), while releasing and absorbing GHGs such as methane, nitrous oxide, and CO2, and thereby regulating global climate feedback trends. The natural processes and anthropogenic disturbances of modern industrialization including increased deforestation, habitat destruction, GHG emissions, burning of fossil fuels, release of ozone-depleting substances, N2 enrichment (Beedlow et al., 2004), and sulfur deposition (Monteith et al., 2007) have been reported to cause a major impact on the sink activity of the terrestrial ecosystem (Bardgett et al., 2008). Since CO2 is a primary substrate utilized as metabolic fuel by plants, atmospheric CO2 affects the allocation of carbon below the ground level and also influences root exudation chemistry. All these changes potentially affect the rhizospheric interaction of plants with beneficial microbes (Williams et al., 2018). In all cases, the overall carbon budget of the ecosystem under the influence of fluctuating climatic conditions is determined through the balance between respiration and photosynthesis. The diversity and productivity of plants of a particular region are well established and determined through interactions with rhizospheric

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microbiota and decomposers, thereby the circulating the carbon flux that overall affect the climatic conditions is dependent on complex interactions and feedback between the biotic and abiotic components, including freeliving heterotrophic microbes, and symbiotic and nonsymbiotic associative partners which overall influence and determine the quality and quantity of carbon flux within the ecosystem. In a natural ecosystem, the community compositions and structures are highly dependent on multiple parameters that include the type of organisms, life history traits, different thermal tolerances, and most importantly their dispersal abilities. Moreover, the community dynamics are decided by interactions occurring between the species (interspecific) or among the species (intraspecific) and are well determined by the complexity and diversity of occupying species in terms of different attributes and parameters, as mentioned above. The complexities observed in natural communities are highly dependent on interaction types and mechanisms that could be positive, negative, or have no functional roles. Moreover, the changed climatic conditions have also altered the distribution of species and therefore, their possible existing interactions (Wookey et al., 2009; Vander Putten, 2012). The rise in atmospheric concentration of GHGs, in particular CO2, has been reported as a major component triggering a rise in global average temperature and consequently affecting the distribution of rain and climatic conditions worldwide (Vasskog et al., 2015; Castello and Macedo, 2016; Worm and Paine, 2016; Runting et al., 2017). Due to the changed climatic conditions, crop plants suffer from adverse environmental conditions such as high temperature (or temperature changes from freezing to scorching), drought (water stress), variable light conditions that affect photomorphogenetic responses, and nutrient deprivation in soil, which directly influence the growth, morphology, physiology, and developmental aspects of plants (Aamir et al., 2017). The most detrimental effects of the increased CO2 level in the atmosphere on plants are the altered photosynthetic rate, and disturbed metabolism (Jia and Zhou, 2012; Philippot et al., 2013), which ultimately cause changed physiological processes in plants. Higher biomass accumulation and differential patterns of occurrences of pests and diseases are also challenging issues (Mendes et al., 2013). Furthermore, the distribution of assimilated carbon to decomposers is an important component of the ecosystem’s function. The altered physiological mechanism due to climate change disturbs this partition of assimilated carbon to microbial entities associated with rhizospheric soils and, therefore, affects the relationships between plants and microbes.

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15.2 CLIMATE CHANGE, PLANT DISEASES, AND HOST PATHOGEN INTERACTION The climatic parameters allow interpretation of physical processes in upper soil layers and the lower atmospheric region plays a crucial role in determining the climate for the local or regional biosphere (Monteith and Unsworth, 2007). It has been suggested that precipitation changes and rising temperature due to changing climate have resulted into the increased occurrence of the plant diseases which could be attributed to the increased use of pesticides (Chen and McCarl, 2001). It is also conceivable that the rising temperature, change in rainfall duration, and changes in relative humidity have not only affected agricultural productivity but also have a significant impact on the severity of plant diseases (Chakraborty and Newton, 2011). Furthermore, it has been found that climatic change could have severe repercussions on developmental stages and processes of pathogens, affecting host development, changes in the morphophysiological processes of plants, and therefore, affecting the host pathogen interaction (Coakley et al., 1999). Moreover, host susceptibility toward diseases caused by pathogens is also influenced in a stressed environments (Gassmann et al., 2016). Host susceptibility is determined through a plethora of molecular processes and signaling mechanisms including reactive oxygen signaling (ROS)-mediated defense signaling (Baxter et al., 2013), hormonal-induced cell signaling (Nguyen et al., 2016), calcium sensors (Ranty et al., 2016), and molecular priming (Thevenet et al., 2017), all of which modify the transcriptional processes, cellular mechanisms, and physiological responses. Agricultural productivity is largely determined by the presence of pathogens and the status of plant diseases in any environment. In changing environments, the condition of occurring diseases in crop plants is boosted due to a change in distribution pattern, an evolution of the new races and pathotypes, and epidemic development (Yáñez-López et al., 2012). Furthermore, the rapidly fluctuating environment has influenced many inoffensive pests to become more virulent, resulting in a greater number of pest occurrences. Nevertheless, the disease severity of plants is significantly influenced by increased temperature and its exposure duration to the plants, as it was suggested that epidemics of plant diseases are highly dependent on temperature variations (Elad, 2009) and stability of plants in a particular environment (Evans et al., 2008). Temperature changes, particularly optimum temperatures, influence the development of hosts,

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physiological attributes of microbial pathogens, and therefore determine the incidence of disease development (Suzuki et al., 2014; Ashoub et al., 2015). In addition, alterations observed in the biology of hosts and pathogens due to their temperature dependences corresponds to a difficult and complex nature of disease prediction outcomes. Microbial populations with short life cycles adapt the re-occurring changes in the environment with faster reproductive processes and dispersal mechanisms (Coakley et al., 1999) and become more complicated in physiological attributes in a stressed environment developed through changed climatic events (Sturrock et al., 2011). The prolonged effect of climate change results in divergence in the geographical distribution of hosts and pathogens, and altered crop losses, and therefore, difficulty in managing plant diseases. Chakraborty et al. (2012) have emphasized that climate change affects both the flora and fauna with their multitrophic interactions. It has been documented that both abiotic and biotic stresses effectuated from the changed climatic condition have influenced the host pathogen interaction in multiple ways (Vandenkoornhuyse et al., 2015). The interactions between soil microbes and plants assist in the regulation and maintenance of ecosystem properties (Classen et al., 2015). In a changed environment, the interaction networks between species are altered and, therefore, change the dynamical aspects of ecosystem properties. Moreover, altered the host pathogen relationship complicates the relation required for predicting the risk of disease development. However, disease prediction depends on several factors that include the shifting of the pathogenic races or change in host abundances in an altered environment. Mounting amount of research conducted over the last few years has demonstrated the shifting of species interactions in changing climate which has altered the function of the ecosystem, and affected the biodiversity (Walther et al., 2002; Gottfried et al., 2012; Langley and Hungate, 2014). In fact, the interactions between the microbial populations of soil, and their interactions with plants determine the composition, abundance, distribution, and diversity of the species as well as the landscape patterns of animals and plants (Berg et al., 2010; Vander Putten et al., 2013). The impact of climate change on plant pathogen interactions and diseases is an interesting and challenging research field among researchers, but the information on the topic is scanty. In recent years, the ongoing research in the field has shifted the direction of study to evaluate the effect of a single meteorological variable such as elevated concentration of atmospheric CO2, temperature, and precipitation on the life cycle of the host,

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pathogens, and the effect of interactions occurring between these variables on host cell physiology, pathogen response, and disease epidemiology in a controlled environment. The climate induced increased CO2 concentration and rising temperature levels could affect the sensing and response mechanisms of microbial communities existing in soil as well as the behavioral responses of plants (Ainsworth and Rogers, 2007; Chakraborty et al., 2012) and therefore, will definitely modulate the plant pathogen interaction (Ferrocino et al., 2013). It has been reported that under the conditions of the rising CO2 levels and temperatures the morphophysiological attributes and the metabolic performances will be influenced and, therefore, affect agricultural productivity. The continual changes in climate have affected plant microbe interactions under the extremities of abiotic stress condition. Therefore, it is imperative to understand the role beneficial microbes in the alleviation of stress response that has been resulted from the changed climatic condition, and its translation to enhanced agricultural production.

15.3 CLIMATE CHANGE: IMPACT ON CARBON EXCHANGE AND MICROBIAL ACTIVITIES Due to their vast diversity, complexity, and extreme genetic potential, microbes affect the global exchange of carbon (C) between land and atmosphere and the C cycle-climate feedback in many ways. However, one could measure their metabolic activities either in the form of atmospheric carbon gain or carbon loss from the soil ecosystem (Bardgett et al., 2008). The increased human interferences for the release of GHGs and other global changes have affected climatic conditions and, thereby, affected the exchange of C between the land and the atmosphere. The changed climatic conditions affected the microbial activities for the breakdown of organic matter. The microbial system plays an indispensable role in regulating the C flux between land and atmosphere. The direct impact of climate change on the microbial system and their functions have been well evidenced (Blankinship et al., 2011; Henry, 2013; Manzoni et al., 2012; A’Bear et al., 2014). The disturbed C flux in the changed climatic scenario has also affected the microbial response and mechanisms for circulating C and, therefore, explicit consideration of both positive and negative roles of the microbial system in the C cycle which explain both the positive and negative impacts of global climate change on microbial physiology, C transfer, and assimilation in a terrestrial ecosystem. In the

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majority, the C gain could be assessed from the uptake of C in the form of CO2 and methane (methanogens) from the atmosphere, whereas the C loss could be analyzed through the C loss from the soil via respiration and methanogenesis (methanogens) processes. The temperature-dependent microbial processes directly affect the microbial soil respiration rates. Furthermore, the rise in warming temperature has influenced microbial metabolism and received considerable attention in the last few years (Bradford, 2013; Frey et al., 2013; Hagerty et al., 2014; Karhu et al., 2014). Moreover, previous research has indicated that the microbial activity in feeding back GHG to the atmosphere causes the actual warming effect (Bardgett et al., 2008). The direct effect of climate change on microbial activities, response mechanisms, and their functional profile could be interpreted from the relative abundances and diversity of microbial communities in soil. Furthermore, the differential behavior could be explained based on their different growth rates, temperature sensitivity, and other physiological attributes (Castro et al., 2010; Gray et al., 2011; Lennon et al., 2012; Whitaker et al., 2014; Briones et al., 2014; DelgadoBaquerizo et al., 2014). In contrast, the indirect effects include the change in the physiochemical profile of soil that alters the diversity of microbial populations and overall affect the productivity of crop plants. The influx of C to soil affects the activity and dynamics of microbial communities, as reflected from microbial respiration, decomposition processes, and release of C from the soil. One of the most important contributions of the soil microbiota is the decomposition of organic matter and an increased warming effect that definitely increases microbial activity for organic matter decomposition. The structure of microbial communities is also affected by prolonged drought conditions (Evans and Wallenstein, 2012), which might result in decreased efficiency for C uptake and its utilization (Göransson et al., 2013), decoupling microbial growth and respiration (Meisner et al., 2013a), or might have positive or negative feedbacks to plant communities (Meisner et al., 2013b). Explicitly,the increased decomposition would generate a large amounts of GHGs and, therefore, have increased efflux of CO2 to the atmosphere and export of the dissolved organic C by the process of hydrologic leaching (Jenkinson et al., 1991; Davidson and Janssens, 2006). It is noteworthy that the since soil microbes play a crucial role in soil C cycling and other ecosystem processes, a comprehensive study is required to understand the biological processes and mechanisms involved in microbial processing of organic matter to the release of the atmospheric CO2 and other GHGs under the

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scenario of future climatic changes. When environmental conditions are disturbed by climate change-induced events it will affect the microbial processes through observed changes in activities like soil respiration, enzyme activities, and decomposition of litter (Keitt et al., 2016). Under the effect of changed environment, microbial activities will be influenced as reflected from observed changes in functions like microbial enzymic activity, soil respiration, and decomposition of litter. However, the exact mechanism through which these changes occurred is not known. Further, it has been reported that whole soil, aggregate functional responses result from the individual activities of a diverse community of soil microbes may involve different mechanism working simultaneously to create the observed function. The most common response mechanism includes microbial physiology, evolution, community composition, and feedbacks (Keitt et al., 2016) as microbial traits that correlate physiological attributes with environmental performances and fitness of microbial species that lead to sorting of species and compositional change over gradients (Leibold et al., 2004). This could be interpreted as mean annual air temperatures, and mean annual precipitation could be positively correlated with the rate of soil respiration (Raich and Schlesinger, 1992). Moreover, the mean annual net primary productivity of the ecosystem shows strong correlations with mean annual respiration rates, as reported the soil respiration rate is found to be 24% higher than the mean annual NPP (Keitt et al., 2016). However, the temperature dependence and strong response of soil respiration rates over productivity (Jenkinson et al., 1991; Schimel et al., 1994) may result in a net transfer of carbon from land to the atmosphere, which would generate positive feedback on climate change. In contrast, on increasing temperature, the effect on heterotrophic microbial respiration (during temperature-dependent microbial decomposition of substrates) and its potential feedback to climate change is uncertain (Davidson and Janssens, 2006; Trumbore, 2006). This uncertainty may be due to the chemical complexity and diversity of the substrates that would affect the temperature-dependent biochemical decomposition of organic matter by heterotrophic organisms (Davidson and Janssens, 2006). Furthermore, other parameters that decide the microbial response to contribute to global warming include the decomposition of organic materials. In some cases, the decomposition rate is either hindered by the type of material (recalcitrant or susceptible to microbial attack) or has some physical or chemical barrier (for preventing microbial action), therefore the decomposition process is relatively very slow. The indirect feedback of climate

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change on the microbial system affects the potential abilities and functioning of microbes through their impact on plant growth and composition of vegetation. The indirect effects of climate change to the microbial system are regulated through different feedback loops that incorporate plant microbe interactions, microbe microbe interactions, soil mineralization events, plant chemistry, and plant composition, and the most likely shifting in other ecosystem interactions that mediate the other functions of the ecosystem (Gilman et al., 2010; Adler et al., 2012; Steinauer et al., 2015). The increased concentration of atmospheric CO2 causes an increased rate of photosynthesis, production of food products, and the transfer of photosynthate C to heterotrophic microbes and symbiotic mycorrhizal fungi (Bardgett, 2005; Johnson et al., 2005). C is distributed through the secretion of sugar-rich exudates, amino acids, and organic acids (Diaz et al., 1993; Zak et al., 1993). The results of increased carbon flux from vegetation to the soil and the microbial biomass is unpredictable due to its dependence on multiple factors such as the status of the soil health and properties, soil food web interactions, and other ecosystem functions. However, the most accurate outcome of such C transfer is the loss of C from the soil through microbial respiration and its dissolution in water bodies due to stimulation of microbial activities and enhanced mineralization of soil organic carbon. Furthermore, other possible results include stimulation of microbial biomass and immobilization of soil nitrogen, thereby delimiting the N availability to plants, creating negative feedback that constrains future increases in plant growth and carbon transfer to the soil (Diaz et al., 1993). Moreover, a deficiency in the soil N content could result in increased competition between microbes and plants to obtain soil N. The deficient condition for soil N in microbes affects the microbial decomposition, and therefore causes enhanced accumulation of soil C.

15.4 MICROBIAL RESPONSE MECHANISM TO CLIMATE CHANGE It has been reported that microbial contributions to the warming effect are further dependent on the microbial response mechanism and are decided by a plethora of mechanisms including microbial physiology, community compositions, feedback, and evolution. The microbial physiology and susceptibility for varying environmental conditions may lead to the sorting of species and compositional changes over gradients

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(Leibold et al., 2004). In many cases, it has been reported that that under the climate extremes such as freezing and drought have explicated greater changes in microbial activities compared to overall changes in temperature and precipitation as well as functional plasticity observed during the shortterm changes in this entire process. Furthermore, the community compositions are decided by differential abilities of the microbial systems to perform well in a changed environment either through adopting the particular niche by relatively abundant taxa or through dispersal of new taxa, which ultimately results in the directional selection of species in changing environmental conditions. It was reported that shifting in the composition of microbial communities could be directly linked to altered ecosystem functioning when soil organisms differ in their functional traits or control a rate-limiting or fate-controlling step (Schimel and Schaeffer, 2012). To better understand this phenomenon, we can assume that under the effect of climate change the relative abundances of the microbial population is affected and therefore, the crucial ecological functions such as nitrogen fixation, nitrification and de-nitrification and methanogenesis associated with them are also disturbed (Bakken et al., 2012; Salles et al., 2012; Bodelier et al., 2000). The positive feedback of the microbial community under the effect of climate change is attributed by the initial resistance to change followed by a rapid shift or collapse as the extent of change progresses. However, the microbial communities existing in microbial consortia under the effect of changed climate initially show resistance to the change, resulting in frequency-dependent selection but finally leading to resilience when an abrupt state shifting occurs.

15.5 IMPACT OF CLIMATIC CHANGE ON PLANT MICROBE INTERACTIONS Climate adversities like the elevated levels of atmospheric CO2, the rise in global temperature, drought have affected the ecology and physiology of both plants and microbes. Since plants distribute some the assimilated carbon to feed microbial populations associated with them, the interruption in the C assimilation pathway under the effect of climate change would definitely influence plant microbial interactions (Jia and Zhou, 2012). It has been reported that microbial diversity and abundances are highly susceptible to climate change events (Maestre et al., 2015a,b). The beneficial microbes associated with plants have a large impact on host cell physiology and protect their host from disease and various abiotic stress factors.

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Changed climatic events have altered the interactions and dynamics of the plant microbe response and affected the microbial communities associated with plants, and therefore, altered their establishment and performances to regulate the soil N and C dynamics. Further, under the effect of increased temperature, the species are moving to higher altitudes and latitudes. The reproductive physiology of the host plant under the warming effect has been found to be changed by early leafing and flowering time in the growing season (Wolkovich et al., 2012). This has resulted into an alteration in the functional traits of plants (Hudson et al., 2011; Verheijen et al., 2015) and therefore affected the multiple properties of the ecosystem (Valencia et al., 2016; Butler et al., 2017). The rise in temperature has affected the community structures and dynamics, with the conversion of grasses and forbs with shrubs which disturb the ecosystem functions and processes through the large impact on carbon exchange between land and atmosphere (Lawrence and Swenson, 2011; Pearson et al., 2013). The elevated CO2 level in the changed climatic scenario has affected the biomass accumulated by C3 and C4 plants (Poorter and Navas, 2003). Differences in the C allocation pattern and host physiology under the warming effect caused maximum accumulation of biomass above ground level (45%) by C3 plants compared to C4 (12%) plants. The differences observed in the biomass accumulation level could be interlinked with the association of the host with beneficial microbes, particularly arbuscular mycorrhiza (AM) fungi. C4 plants allocate more C to AM fungi to gain benefits from these fungi and therefore selection force favors the growth of AM fungi in the case of C4 plants rather than the accumulation of biomass by C3 species. Overtly, these results explain how warming resulted in the beneficial association of the host with the AM fungi. The association of Glomus intraradices and Glomus mossae with the host under the effect of increased temperature has been experimentally demonstrated (Baon et al., 1994; Monz et al., 1994). Under the effect of rising drought the plant growth was affected (both roots and shoots) and therefore there was an interruption in the allocation of photosynthetic food products to the rhizospheric microbes and AM fungi. However, the density of ectomycorrhizal fungi is not disturbed during prolonged drought conditions. The consequences of climate change on plant microbe, microbe microbe, and ecosystem functions are not fully understood. One of the major limitations in this context is that to date the effect of global climate change on plant microbe interactions has been considered with a focused

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approach on a single trophic level (either a specific plant or microbe), ignoring the interactive aspects of plant microbe and microbe microbe interactions occurring at different or the same trophic levels observed for aboveground or belowground organisms in a natural ecosystem. This limitation has generated a gap in our understanding of the direct and indirect impacts of changes in climate and biodiversity on the terrestrial ecosystem and therefore an accurate prediction for ecological consequences of global change.

15.6 CLIMATE CHANGE AND ABIOTIC STRESS: MICROBEMEDIATED STRESS ALLEVIATION Global warming may result in an increase in average global temperature, severe droughts, increased CO2 level, extreme rainfall, floods, cyclones, etc. All these factors will together cause a detrimental effect on crop growth and yields and will also impose severe pressure on land and water resources. According to one report, it was predicted that the climatic conditions will undergo drastic changes in the 21st century and will affect various parameters such as increased global mean surface temperature that may result in an unbalanced and disturbed rainfall in a particular regime, and therefore, will agricultural productivity will be affected (Shah and Srivastava, 2017). The sector which is considered to be most vulnerable to climate change is agriculture. Global productivity has been severely affected under the changed climatic events which have influenced plant susceptibility to diseases (Prasch and Sonnewald, 2013; Narsai et al., 2013; Atkinson et al., 2013; Suzuki et al., 2014; Ramegowda and Senthil-Kumar, 2015; Pandey et al., 2015; Mahalingam, 2015) and a large number of epidemics have occurred around the world, providing sufficient evidence for highlighting the global effects of climate change events (Nazir et al., 2018). One of the most crucial subjects for discussion under the changed climatic scenario is how to raise agricultural productivity for future demands. Abiotic stresses such as salinity, heat, and drought are the major limiting factors for agricultural productivity (Meena et al., 2017). Current attempts toward attenuation of the abiotic stressor(s) under the changed climatic conditions have met with limited success. However, microbe-mediated stress signaling has gained considerable attention, particularly in the context of sustainable agriculture that promotes an indigenous mechanism for maintaining a clean and green environment (Sorty et al., 2018). Further, alleviation of stress by employing microbial species has been

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evidenced to have a long history (de Zélicourt et al., 2018; Nadeem et al., 2014; Souza et al., 2015). The microbes have eminent genetic and metabolic capabilities to cope with harsh environmental conditions for stress mitigation in plants (Gopalakrishnan et al., 2015). It has been reported that microbial interactions with plants result in a plethora of local and systemic responses that improve the metabolic capabilities of plants to tolerate harsh environmental conditions (Nguyen et al., 2016). Moreover, the interactions of plants with beneficial microbes cause metabolic reprogramming that results in the accumulation of defense-related compounds to counteract the effects of harsh environmental conditions. In recent years, with the invention of new tools and sophisticated technologies it has now become possible to explore the entire genetic machinery of microbes. In addition, with the advent of next-generation sequencing tools, researchers have extended their attention to retrieving information and data collection from metagenomics studies for those uncultivable microbial samples which were previously inaccessible from other conventional strategies and therefore characterized the microbial communities for their functional exploitation (Bulgarelli et al., 2012; Igiehon and Babalola, 2018). Further, a collection of samples from specialized habitats including rhizospheric soil, degraded and depleted soils, disturbed fertility status, endophytic communities, and other unexplored sites may come up with positive results for unidentified microbial populations or obligate endophytes inhabiting plant tissues to decipher multiphasic functions associated with stress tolerance. Research studies done so far at molecular, biochemical, and physiological levels on plant microbe interactions have shed light on the facts that microbial associations with plants predominantly result in their protection from various abiotic and biotic stresses (Farrar et al., 2014). The molecular response of plant microbe interactions measured at different levels generated a great deal of biological data when analyzed at multi-omics-based platforms for comprehensive knowledge of microbe-mediated defense mechanisms and plant responses at a deeper level (Kissoudis et al., 2014). Moreover, the investigation of a particular pathway for stress mitigation in plants may assist in identification of novel signaling molecules, proteins, genes, and gene cascades to connect with other gene networks and pathways for their functional correlation with the help of highly advanced and sophisticated tools and technologies. This technological advancement has explored the route of microbial physiological mechanisms at genetic and molecular levels through RNAi-based gene silencing, gene-editing

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systems, genetic mutant-based studies, and different omics-based approaches like genomics, proteomics, interactomics, secretomics, and metabolomics, for a better understanding of microbe-mediated stress avoidance in plants (Yin et al., 2014; Luan et al., 2015). Additionally, meta-omics-based tools including metagenomics, metatranscriptomics, and metaproteomics have been found to be useful as emerging tools for assessing functional aspects of microbial communities at a deeper level (de Castro et al., 2013).

15.7 MICROBIAL ATTENUATION OF ABIOTIC STRESS The mitigation of various abiotic stresses such as high temperature, drought, salinity, etc. is a useful approach, where microbes associated with rhizosphere, phyllosphere, and endophytic communities and/or microbes in a symbiotic relationship with plants have been used for the alleviation of stress responses and promotion of plant growth and development. The most common mechanisms through which these microbes alleviate the stress response includes secretion of beneficial plant growth-promoting compounds, antioxidants and osmolytes, plant nutrient acquisition, modulation of plant growth-related hormones, and regulation through fine-tuning of stress-related genes. Rhizospheric microorganisms including genera that belong to Pseudomonas (Ali et al., 2009; Sorty et al., 2016; Rajkumar et al., 2017), Azotobacter (Sahoo et al., 2014a,b), Bacillus (Tiwari et al., 2011; Bacon et al., 2015; Sorty et al., 2016), Endobacter medicaginis, Micromonospora spp., Microbacterium trichothecenolyticumn, and Brevibacillus choshinensis (Trujillo et al., 2010; Ramírez-Bahena et al., 2013), Trichoderma (Ahmad et al., 2015; Zaidi et al., 2018; Guo et al., 2018), Bradyrhizobium (Swaine et al., 2007; Tittabutr et al., 2013), Methylobacterium (Madhaiyan et al., 2007; Meena et al., 2012), Enterobacter (Sorty et al., 2016) have been well documented to alleviate the stress response during plant-microbe interaction. Beside the classical mycorrhizal fungi, PGPR, and the microbes associated with the rhizosphere, overall it was found that the the endophytic fungi play a crucial role in plant growth promotion against abiotic stresses (Egamberdieva et al., 2013; Berg et al., 2013; Hameed et al., 2014). However, to date the information on the effect of multiple abiotic stresses and their cumulative influence on plant microbe interactions is not fully explored. To alleviate plants under stress conditions it is highly recommended to enrich and supplement plants with microbial inoculation. However, the molecular mechanism used by these microbes and their interactions and responses with

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plants are crucial for understanding the behavior of microbes under stressed environments. Generally, inoculation of beneficial microbes in plants results in an increased expression of the defense-related genes. Recently, many stress-responsive genes in plants have been identified using individual experimentation when done under abiotic and biotic stress conditions (Narsai et al., 2013; Shaik and Ramakrishna, 2013, 2014). In many cases, early colonization of plants with beneficial microbial symbiosis is accompanied by suppression of the plant immune response to allow their growth. For example, Brotman et al. (2013) reported that colonization of Trichoderma asperelloides 203 in Arabidopsis roots resulted in massive transcriptional reprogramming of stress-responsive genes as analyzed through microarray analysis and validated through qRT-PCR experiments. The colonization process involves massive transcriptional reprogramming of stress-responsive genes and transcription factors (Brotman et al., 2013). Apart from this, the association of plants with symbiotic fungi also leads through transcriptional regulation of host gene expression incited by fungal lipochitooligosaccharides (Czaja et al., 2012).

15.8 MECHANISM OF MICROBE-MEDIATED STRESS TOLERANCE The microbial populations found in rhizospheric soil are modulated by the secretion of root exudates. The selection force operated by plants regulates the abundance of microbes to occupy that specialized niche called the “rhizosphere” in the soil (Qiao et al., 2017). It has been reported that the secretion of the root exudates of the plant allocates the nutrient and carbon in the form of low-molecular-weight compounds such as sugars, amino acids, organic acids, and polymerized sugar (mucilage) in soil, affecting the microbial activities and community assemblages (Drigo et al., 2010; Jiang et al., 2017). The beneficial microorganisms colonize the rhizosphere/endorhizosphere of plants and have been found to impart abiotic stress (drought) tolerance by producing exopolysaccharides (EPS), phytohormones, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, volatile compounds, inducing accumulation of the osmolytes (such as K1, glutamate, trehalose, proline, glycine betaine, proline betaine, ectoine, etc.), antioxidants, upregulation or downregulation of stress-responsive genes, and alteration in the root morphology in acquisition of the drought

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Figure 15.1 General mechanism of plant growth promotion and stress tolerance by rhizospheric microorganisms.

tolerance (Vurukonda et al., 2016) (Fig. 15.1). The most common approaches through which plant growth-promoting rhizobacteria (PGPR) promote plant growth and development include the availability of mineral nutrients through increased atmospheric nitrogen fixation and phosphate solubilization (Pereira and Castro, 2014; Wang et al., 2017), promoting growth and development of roots through release of phytohormones and secondary metabolites to the rhizosphere such as indole acetic acid (IAA) and other signaling molecules like nitric oxide (NO) (Cassán et al., 2014), siderophore production (Sayyed et al., 2013), and decreased ethylene production through increased ACC-deaminase activity (Vacheron et al., 2013; Singh et al., 2015; Nadeem et al., 2016). In this sense, trehalose metabolism in rhizobia is a key for signaling plant growth, yield and adaptation to abiotic stress. Figueiredo et al. (2008) reported increased plant growth, N content and nodulation of Phaseolus vulgaris L. under drought stress when these plants were inoculated with Rhizobium etli overexpressing trehalose-6-phosphate synthase gene. PGPR improves plant health (increased root length, root surface area and the number of root tips, leading to enhanced uptake of nutrients) in stressed environments by producing indole acetic acid, gibberellins and some unknown determinants (Egamberdieva and Kucharova, 2009). PGPR inoculation favors the

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humid environment around roots, which prevents entry of pathogens or toxic metal ions inside the roots (Wang et al., 2017). Further, PGPR incorporation improves the physiological mechanism for water use efficiency, modulating transpiration and stomatal conductance, and decreasing ROS production (Vejan et al., 2016). The different mechanisms employed by different bacterial species are shown in Table 15.1. However, the mechanism of plant growth promotion is highly dependent on plant type, bacteria, and putative interaction aspects. In contrast to bacteria, rhizocompetent fungal genera, such as Trichoderma have been used widely in commercial formulations as biofertilizers and biocontrol agents. It has been reported that inoculation of Trichoderma with plants results in the stimulation of plant growth promotion as well as mitigation of stress against a wide range of environmental stress conditions. Brotman et al. (2013) reported the increased expression of genes related to osmoprotection and general oxidative stress in both roots and leaves of host plants following treatment of plants with Trichoderma. Furthermore, improved germination of the seeds of Arabidopsis and cucumber was reported prior to imposition of salt stress (Brotman et al., 2013). Trichoderma inoculation enhances the tolerance of plants to stress conditions such as drought and salinity (Mastouri et al., 2010; Shoresh and Harman, 2010), through enhanced root growth, nutritional uptake, and protection from oxidative damage. Mastouri et al. (2012) reported that Trichoderma harzianum T22 colonization is mainly attributed to the higher capacity for scavenging ROS and recycling of partly higher capacity to scavenge ROS oxidized ascorbate and glutathione, a mechanism that is expected to enhance tolerance to abiotic stresses. Likewise, in rice, stress mitigation by T. harzianum resulted in the upregulation of aquaporin, dehydrin, and malondialdehyde genes (Pandey et al., 2016). Moreover, the endophytic symbionts mitigate abiotic stress by two general mechanisms, including activation of a host defense response and another including accumulation of antistress-related biochemicals. During stress response, symbiotic plants maintain their osmolyte concentration either low or high compared to nonstressed controls. Further osmotic adjustment is effected by the accumulation of proline or glycine betaine. The symbiotic association of plants with beneficial microbes scavenges the ROS generated against stress conditions through activation of antioxidant defense machinery that includes many defense enzymes like SOD, CAT, GPX, DHAR, and MDHAR. The symbiotic associations also help plants

Table 15.1 Different mechanisms of stress tolerance in plants by rhizospheric microbial species in different crop species Organism Crop Mechanism

Burkholderia phytofirmans Pseudomonas fluorescens

Grapevine Groundnut

Synthesis of ACC-deaminase Synthesis of ACC-deaminase

Pseudomonas putida P. putida KT2440 P. polymyxa and Rhizobium tropici Pseudomonas sp. AMK-P6

Canola Citrus Common bean Sorghum

Synthesis of ACC-deaminase Inhibition of root chloride and proline accumulation Change in hormone balance and stomatal conductance

Pseudomonas sp. AMK-P7

Sorghum

P. putida P45 Bacillus megaterium and Glomus sp. Piriformospora indica P. putida GAP-P45

Sunflower Trifolium

P. fluorescens

Maize

Bacillus thuringiensis

Lavandula dentate

Bacillus polymyxa

Lycopersicon esculentum

Barley Maize

References

Barka et al. (2006) Saravanakumar and Samiyappan (2007) Chang et al. (2007) Vives-Peris et al. (2018) Figueiredo et al. (2008)

Induction of heat shock proteins and improved plant biochemical status Induction of heat shock proteins and improved plant biochemical status Improved soil aggregation due to EPS production IAA and proline production

Ali et al. (2009)

Antioxidant production Accumulation of proline improved plant biomass, relative water content, and leaf water potential Increased proline, abscisic acid, auxin, gibberellin, and cytokinin content improved plant growth IAA induced higher proline and K-content, improved nutritional, physiological, and metabolic activities, and decreased glutathione reductase (GR) and ascorbate peroxidase (APX) activity Proline accumulation improved the physiological and biochemical parameters of plants

Baltruschat et al. (2008) Sandhya et al. (2010)

Ali et al. (2009) Sandhya et al. (2009a,b) Marulanda et al. (2007)

Ansary et al. (2012) Armada et al. (2014)

Shintu and Jayaram (2015) (Continued)

Table 15.1 (Continued) Organism

Crop

Mechanism

References

Microbial consortia employing P. jessenii R62, P. synxantha R81, and A. nitroguajacolicus strain YB3, Arthobacter nitroguajacolicus strain YB5 Azospirillum lipoferum

Rice

Accumulation of proline maintained osmotic adjustment and improved plant growth

Gusain et al. (2015)

Maize

Bano et al. (2013)

Klebsiella variicola F2, P. fluorescens YX2, and Raoultella planticola YL2 Azoapirillum brasilense Az39

Maize

Improved plant growth through accumulation of free amino acids and soluble sugars Accumulation of choline and GB and improved leaf RWC and DMW

Cassan et al. (2009)

Bacillus subtilis GB03

Arabidopsis

Azospirillum sp.

Wheat

P. putida H-2 3 B. thuringiensis AZP2 Novosphingobium sp.

Soybean Wheat Citrus

Cadaverine production by PGPR improved root growth and mitigated osmotic stress Expression of PEAMT gene resulted in elevated metabolic level of choline together with GB in osmotically stressed plants and improved leaf RWC and dry DMW IAA enhanced root growth, lateral root formation, and increased uptake of water and nutrients under drought stress Secretion of gibberellins by P. putida improved plant growth Reduction of volatile emissions and higher photosynthesis Decreased transpiration (E) and stomatal conductance (gs)

Rice

Gou et al. (2015)

Zhang et al. (2010)

Arzanesh et al. (2011) Kang et al. (2014) Timmusk et al. (2014) Vives-Peris et al. (2018)

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Figure 15.2 General mechanism proposed for endophytic-mediated plant growth promotion and stress mitigation in associated plants.

to improve the rate of photosynthesis through increased chlorophyll content (Fig. 15.2). Under drought stress, Capsicum annum shows higher chlorophyll content as it is associated with a higher photosynthesis rate when colonized with endophytes including Chaetomium globosum (Khan et al., 2012) and Penicillium resedanum (Khan et al., 2014). Besides rhizospheric bacteria the symbiotic association with host plants with some AM fungi like Glomus mosseae, G. etunicatum, G. intraradices, G. fasciculatum, G. macrocarpum, G. coronatum, etc., improves the plant resistance to water deficit and drought stress through the alteration of plant physiology and expression of plant genes. Wu and Xia (2006) reported that AM fungi improve osmotic adjustment and drought tolerance of mycorrhizal citrus grafting seedlings by decreasing the leaf content of malondialdehyde and soluble protein and by enhancing superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) activity. Different microbial species employed as a microbial symbiont in different plants against different types of stresses are shown in Table 15.2. In comparison to drought stress, AM symbiosis has frequently been observed to show plasticity of host plants toward salinity stress. In maize, mung bean, and clover, salt resistance was improved by AM colonization due to improved osmoregulation or proline accumulation (Ben Khaled et al., 2003).

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Table 15.2 List of beneficial fungal endophytes, host plants, and type of stress response where their roles have been demonstrated in stress mitigation Endophyte

Abiotic stress

Host plant

References

Glomus mossae

Salinity

Giri et al. (2007)

Bradyrhizobium sp.

Drought

Piriformis indica Curvularia proteuberate

Salinity Heat

Trichoderma harzianum

Cold, heat, salt

Acacia nilotica Solanum lycopersicum Cajanus cajan Chamaecrista fasciculata Oryza sativa Dicanthelium lanuginosum Lycopersicum esculentum L. esculentum

Neotyphodium spp.

Drought

Festuca spp.

Fusarium culmorum

Drought, heat, and salt Drought Drought

L. esculentum O. sativa Tall fescue Watermelon Triticum aestivum L. esculentum Dichanthelium lanuginosum Ocimum basilicum Medicago truncatula Arabidopsis thaliana Zea mays

Acremonium sp. Curvularia proteuberate (Cp4666D) C. protuberate (CpMH206)

Drought

Glomus clarum Piriformospora indica

Salinity Salinity

Piriformospora pseudoalcaligenes Rhizophagus irregularis EEZ 58 Cladosporium cladosporioides E162 Epichloë bromicola

Salinity

P. pseudoalcaligenes

Salinity

T. harzianum TH-56 Bacillus cereus Pb25

Drought Salinity

Drought

Pain et al. (2018) Jogawat et al. (2016) Rodriguez et al. (2008)

Matsouri et al. (2010) Hamilton et al. (2012) Rodriguez and Redman (2008) White et al. (1992) Rodriguez et al. (2008) Rodriguez et al. (2008) Elhindi et al. (2016) Li et al. (2017) Abdelaziz et al. (2017) Quiroga et al. (2017)

Drought

Nicotiana benthamiana

Dastogeer et al. (2017)

Drought

Hordeum brevisubulatum A. thaliana

Chen et al. (2018)

O. sativa Vigna radiata (mung bean)

Abdelaziz et al. (2017) Pandey et al. (2016) Islam et al. (2016)

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15.9 CONCLUSION This chapter has discussed the effect of climate change on ecosystem functional aspects and dynamic responses. Soil microorganisms play a crucial role in stress alleviation and regulating the multifunctionality response and mechanisms while occupying a multitrophic level. Climate changes have both direct and indirect effects on both plant communities and soil microbes. The phenotypic plasticity and genetic flexibility of microbes provide them with outstanding potential to tolerate stress conditions, and therefore their interactions with plants help them to cope with harsh environments under a changed climate scenario. Changes in the composition of microbial communities determine the ecosystem functional aspects and dynamics either through rate-limiting or fate-controlling steps. Keeping the importance of soil microbes in mind we need to characterize the functional interactions between them. The modern omics approaches, including genomics, transcriptomics, proteomics, secretomics, and phenomics, have attempted to explore the hidden genetic potentials of existing unknown and known microbial diversity and their possible complexities and interactions with the environment.

ACKNOWLEDGMENTS MA is thankful to the Indian Council of Medical Research (ICMR), New Delhi, for research facilities in the form of an ICMR-Junior Research Fellowship and ICMR-SRF. The authors acknowledge Head, Department of Botany, BHU, for providing technical help and facilities required during this work.

AUTHOR CONTRIBUTIONS STATEMENT MA conceived the idea and decided to write on this topic. MA wrote and reviewed the entire chapter. KKR, MKD, AZ, YNT, KD, and SS all contributed equally in their assistance in writing the manuscript. RSU supervised the whole work. All authors finally approved the manuscript for publication.

CONFLICT OF INTEREST None of the authors involved in this manuscript has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of this report.

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FURTHER READING Atkinson, N.J., Urwin, P.E., 2012. The interaction of plant biotic and abiotic stresses: from genes to the field. J. Exp. Bot. 63, 3523 3543.

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