Abstract
Climate change has led to an increased number of abiotic and biotic stresses, and the plants experience these stresses simultaneously. Abiotic stresses like drought, heat, and salinity greatly influence plant-pathogen interaction when co-occurring with the biotic stressors. Recent studies have shown that combined stresses induce unique physiological and molecular responses, which involve rewiring of the hormonal pathways, accumulation of various metabolites and induction or suppression of immunity genes in plants. The net impact of the interaction, which depends on a multitude of factors, thus, modulates the effect of biotic stressors on plants by either increasing or decreasing plants susceptibility towards them. The present review aims to provide an overview of the current knowledge on the biotic and abiotic stress interactions in plants. We have discussed the role of drought, salt, and heat stress in influencing pathogen infection in plants in brief. Plants responses to the three types of combined stresses are compared to decipher the common and unique plant responses to these stresses.
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Introduction
Global warming pose increasing threats to plants as it leads to the evolution of complex environmental conditions involving several abiotic and biotic stressors. Many abiotic stress conditions like high and low temperatures, drought, and salinity affect the survival, dispersal, and virulence of many biotic stressors. For instance, high temperature plays a vital role in the increased occurrence of diseases caused by Ralstonia solanacearum, Acidovorax avenae, and Burkholderia glumea (Kudela 2009). Moreover, increase in temperature during winters (warmer winters) ease the survival of aphids thus spreading Barley yellow dwarf virus (BYDV) and also increase viruses of potato and sugar beet (Thomas 1989; Mackerron et al. 1993).
The role of environmental factors in influencing the occurrence and progression of plant diseases has been earlier identified and represented as ‘disease triangle’. Abiotic stresses like high temperature, salinity, and drought along with affecting plant growth also modulate the response of plants towards pathogen infection by either affecting the pathogen per se or enhancing or suppressing the defense response of plants to the pathogens (Fig. 1A). Pathogens are equipped with constantly evolving virulence mechanism that helps them to successfully invade their hosts. The tug of war between the plants and pathogens is widely affected by these abiotic stresses which modulate plant defense as well as pathogen multiplication, virulence, motility and survival in the endosphere, phyllosphere and the rhizosphere (Fig. 1B). It is the interaction between plants and pathogens at these levels (endo-, phyllo- and rhizosphere) that influences the net impact of the combined stresses on plants. Recent studies have thrown light on the transcriptional, physiological, and metabolic changes occurring during combined stresses and unique responses characteristic to combined stresses have been observed in plants. Modulation of highly complex and intertwined hormone signaling has been observed in all combined stresses (Prasch and Sonnewald 2013).
This review highlights the ways by which heat, salinity, and drought stress affect pathogen infections in plants. Both negative and positive effects of these three abiotic stresses on pathogen infection are briefly discussed, and new avenues for further understanding the interaction between the two stresses are highlighted (Fig. 2).
Effect of heat stress on pathogen infection
Heat stress has varied effects on pathogens and plant-pathogen interaction depending upon the type of pathogen, host plant, geographic location and season (Elad and Pertot 2014; Velásquez et al. 2018) Warmer winters facilitate the survival and virulence of pathogens evolved under cooler climates thereby increasing the risk of diseases caused by them (Deutsch et al. 2008). For example, increase in temperature during winters resulted in early outbreak of phoma stem canker of oilseed rape (caused by Leptosphaeria maculans) in southern United Kingdom (Sun et al. 2000). An increase in annual mean temperature by 0.8–1.0 °C led to early onset of Cercospora leaf spot of sugar beet (Richerzhagen et al. 2011). Increase in temperature modulates life cycle of pathogens by affecting their survival, multiplication, and dissemination by vectors. Among all the abiotic factors temperature is the most crucial parameter that affects the life cycle and density of viral vectors thereby affecting the occurrence of viral diseases (Bale et al. 2002).
Plants transcriptome and metabolome undergoes extensive changes to cope with the effect of high temperature. This not only affects plants physiology and growth but also their ability to fight with pathogens and pests. Heat stress may either increase or decrease the susceptibility of plants to a pathogen depending on the tolerance capacity of host and pathogen to the elevated temperature. In general, pathogen infection is aggravated when the host plant is more adversely affected by the increased temperature than the pathogen. Heat stress basically affects plant pathogen interaction by either modulating the expression of host resistance genes or modifying the pathogen virulence. Heat stress impairs both the basal and R gene-mediated resistance (Table S1). For example, high temperature not only modulates the inoculum density of L. maculans (Huang et al. 2005), it also impairs the Rlm6-mediated resistance to pathogen in Brassica napus (Huang et al. 2006). Contrarily, higher temperatures (25–35 °C) enhance Yr36 mediated resistance to Puccinia striiformis in Triticum aestivum (Uauy et al. 2005) and Xa7 mediated resistance to X. oryzae in O. sativa (Webb et al. 2010). Moreover, high temperature (30 °C) triggers more efficient RNA silencing-mediated plant defense thus enhancing the resistance of plants to some geminiviruses like Cassava geminivirus and Cotton leaf crinkle virus (Chellappan et al. 2005; Tuttle et al. 2008). High temperature also modulates plant pathogen interaction by modulating virulence strategies of pathogens. In Pseudomonas syringae-Arabidopsis thaliana pathosystem, elevated temperature (30 °C) caused increased translocation of bacterial T3E effector proteins into the plant cell thereby facilitating bacterial growth in plants (Fig. 2) (Huot et al. 2017). High temperature (26 °C) enhances the replication of Turnip crinkle virus (TCV) in A. thaliana (Zhang et al. 2012), Peanut stunt virus in Nicotiana benthamiana (Obrepalska-Steplowska et al. 2015) and spread of Tobacco mosaic virus in Nicotiana tabacum (Király et al. 2008). High temperature (35 °C) also enhances expression of cell wall degrading enzymes of Pectobacterium atrosepticum leading to increased virulence (Hasegawa et al. 2005). Contrastingly, high temperature is known to suppress production of bacterial toxins in P. syringae pv. glycinea (causal agent of bacterial blight in soybean) (Hockett et al. 2013).
To better understand the impact of heat stress on pathogen infection, studies have been performed wherein the effects of both individual and combined heat and pathogen infection on plants have been studied and compared. Prasch and Sonnewald (2013) showed heat stress co-occurring with Turnip mosaic virus infection modifies viral specific signaling leading to impairment of defence responses and increased susceptibility to the virus. Transcriptome studies in Oryza sativa plants exposed to combined heat and Xanthomonas oryzae infection have indicated the role of genes involved in ABA biosynthesis, metabolism and signaling in Xa7 mediated resistance to Xanthomonas oryzae (Cohen et al. 2017). ABA biosynthetic genes were upregulated under both individual and combined heat and X. oryzae infection at all time points indicating their role in modifying plant pathogen interaction under high temperature conditions. Heat stress also represses SA signalling which is otherwise induced under Pseudomonas syringae pv. tomato DC3000 infection in A. thaliana leading to increased susceptibility to the pathogen (Huot et al. 2017).
Effect of salinity stress on pathogen infection
The effect of salinity stress on pathogen infection in plants also depends on several factors, namely, type of pathogen, the intensity of salt stress imposed, etc. Whereas viral infection under salinity stress is majorly seen to aggravate infection (Elsheikh and Osman 2002; Cui et al. 2015; Li et al. 2018), fungal infection under salinity stress is either enhanced or suppressed depending on the intensity of salt stress (Wiese et al. 2004; Triky-Dotan et al. 2005; DiLeo et al. 2010). For instance, at low concentration, salt stress suppressed S. lycopersicum defense against Oidium neolycopersi (causal agent of powdery mildew), high salt concentration provided resistance against the pathogen (Kissoudis et al. 2016). A high concentration of salt inhibits fungal growth, and this can be attributed to increased resistance conferred at a higher concentration of salt. Low concentration of salts, seemingly tolerated by the fungi, may induce ABA signaling which interferes with SA mediated defense, thereby enhancing the susceptibility. Salt stress also increases the intensity of infection caused by P. syringae pv. tomato in S. lycopersicum. The enhanced susceptibility was attributed to salinity induced ABA accumulation in roots, which suppressed SA mediated defense (Pye et al. 2013). In another study, it was found that combined salinity stress and P. syringae pv. lachrymans infection had a more detrimental impact on water status and stomatal functioning of Cucumis sativus than the individual stresses (Chojak-Koźniewska et al. 2017). The increased disease severity was correlated with increased bacterial population due to increased nutrient leakage caused by salinity induced membrane damage, thus, rendering the apoplastic environment more favorable for pathogen growth. Enhanced infection in combined stress plants also corresponded with increased ABA/SA ratio and decreased Pathogenesis-related 1 gene (PR1). Moreover, combined stress-specific reactive oxygen species production and scavenging were also seen. Combined stressed plants exhibited an increased production of ROS followed by upregulation of Iron superoxide dismutase (FeSOD) enzyme activity (Chojak-Koźniewska et al. 2017).
Effect of drought stress on pathogen infection
Drought stress causes various physiological changes in plants including stomatal closure, reduction in photosynthesis, inhibition of leaf growth and changes in root/shoot ratio. In some cases, drought also impairs production of plant defense substances, favouring the progress of the pathogen. Conversely, several diseases are less severe when the availability of moisture is limited (Achuo et al. 2006). The effect of drought on plants less susceptibility to a pathogen largely depends on the nature of pathogen and occurrence and intensity of drought (Gupta et al. 2016; Ramegowda and Senthil-Kumar 2015; El Aou-ouad et al. 2016). Although most studies till date have focussed on the effect of drought on plants responses towards pathogen infection, a few have also highlighted the direct impact of drought on pathogen growth inside the plant (Gupta et al. 2016; Sinha et al. 2016). The interaction between drought-induced responses and pathogen infection inside the plants can be positive, negative, or neutral. In cases of positive interaction, both stresses may have additive damaging effects on plants as indicated by enhanced damage incurred by Beet yellows virus and Maize dwarf mosaic virus under drought stress (Olsen et al. 1990). Prasch and Sonnewald (2013) showed that combined virus and drought stress caused more reduction in plant biomass as compared with plants treated with either virus or drought alone. Drought stress may also exacerbate the damage caused by xylem invading pathogens as indicated by Xyllela fastidiosa infection in drought stressed Vitis vinifera wherein the combined stress caused more severe disease symptoms and greater reductions in physiological parameters like total photosynthetic activity and stomatal conductance (Choi et al. 2013). Drought-induced changes in plant architecture or physiology can also suppress pathogen infection as well as growth in plants. For example, drought stress induced reduction in root lengths decrease the chances of soil borne pathogens to reach the roots thereby causing suppression of infection (Huisman 1982). Inside the plant interface, drought stress can also supress pathogen growth as indicated by reduced P. syringae growth in A. thaliana (Gupta et al. 2017) and decreased multiplication of R. solanacearum in Cicer arietinum under drought stress (Sinha et al. 2016). In cases of neutral interaction, both the stresses though cast negative effects on plants, there is no interaction between the two stressors inside the plant. For instance, combined drought and GLRaV-3 infection in V. vinifera did not cause any additive damage to the plants. However, both the individual drought, virus infection and combined stress reduced the net photosynthetic rate, stomatal conductance, leaf transpiration and hydraulic conductance in plants (El Aou-Ouad et al. 2016, 2017).
The interaction between drought stress and viral diseases is much more intricate, as shown by Davis et al. (2015) in the study that involved the application of simulated drought stress on wheat plants infected with Barley yellow dwarf virus (BYDV). Under well-watered conditions, BYDV infection led to reduced plant growth. Drought stress (chronic) did not have any significant effect on plant growth; however, acute water deprivation had a positive effect on BYDV infected plants making the plants more tolerant to BYDV infection. However, there is a possibility that drought conditions enhance the build-up of the vector population and the spread of the virus (Davis et al. 2015).
The effect of drought on plant-pathogen interaction can be attributed to the cross-talk between the drought stress-induced the ABA pathway and pathogen-induced SA and JA pathway (Lievens et al. 2017). The LC–MS based profiling of the three hormones in A. thaliana exposed to combined drought and P. syringae infection, drought being the first stressor, revealed repression of ABA, concomitant induction of SA and JA and reduced bacterial growth in the plants. However, when the pathogen was the first stressor, accumulation of ABA, SA, JA levels, and unaltered bacterial growth as compared to individually stressed plants (pathogen-infected) was observed. Thus, repression of ABA synthesis seems to be responsible for the observed resistance in combined stressed plants. Furthermore, it was found that prolonged duration of drought leads to suppression of plant defense, mainly SA and ET signaling leading to the susceptibility of plants to the bacteria (Gupta et al. 2017). Interestingly, secondary cell wall modifications are also differentially affected by the severity of drought in R. solanacearum infected plants. Early drought led to up-regulation of lignin biosynthesis and prolonged drought-induced cellulose biosynthesis which was correlated with enhanced susceptibility (Sinha et al. 2017).
Avenues for improving plant resistance under combined abiotic and biotic stresses
Although the role of abiotic stress on pathogen infection was observed and documented long ago in terms of disease triangle, extensive molecular studies to understand the molecular changes under combined stress have just begun. The effect of heat, salt and drought on pathogen infection and plant pathogen interaction is complicated and cannot be generalized. Greenhouses and plant growth chambers must be designed in such a way that they mimic field conditions and wherever possible filed studies should be performed to assess the role of abiotic factors on plant diseases. Predictive climatic models and simulation studies have been developed for a few plant-pathosystems, like phoma stem canker (L. maculans) of oilseed rape in the United Kingdom (Evans et al. 2008). To predict the future severity of epidemics, weather-based models were combined with climate change models. The result of the study showed the increased severity of the disease and also that the area affected by the canker disease will extend to areas which are currently not affected by the disease, Similar predictive climatic models have been developed for downy mildew (caused by Plasmopara viticola) (Salinari et al. 2006), and powdery mildew (caused by Erysiphe necator) (Caffarra et al. 2012) of grapevine and Cercospora leaf spot (caused by Cercospora beticola) of sugar beet (Richerzhagen et al. 2011). There is a need to develop many more such predictive climatic models to understand the effect of abiotic factors on plant diseases. Carefully designed experiments under controlled conditions can help in further uncovering the molecular intricacies of plant patho-systems under heat, salt or drought stress. The knowledge gained from advances in transcriptomics, metabolomics and phenomics on the effect of abiotic factors on plant-pathogen interaction can be coupled with agronomic practices, like crop rotation, tillage, fertilization, irrigation, use of resistant/tolerant varieties, to reduce the risk of increased infection under combined abiotic and biotic stresses. (Juroszek and von Tiedemann 2011).
Conclusion and future perspectives
In an environment where plants are exposed to multiple stresses, the consequences of the interaction between the different stresses inside and outside the plant interface can be diverse and complicated. Abiotic stresses have been known to impact the disease cycle of pathogens and predispose plants to various pathogens (Bostock et al. 2014). Abiotic stresses interfere with the strategy used by pathogen for infection. Different factors drive the response of plants to combined abiotic and biotic stresses. The suppression or accumulation of phytohormones mainly ABA and SA are some of the common responses observed under all abiotic and biotic stress combination. The other important target affected by combined stresses is R gene-mediated immunity genes (Fig. 1). Apart from affecting plant defense responses, abiotic stresses induced changes like altered water potential and or ionic concentration may interfere with pathogen virulence at plant interface. Thus, the pathogen effectors might also be affected by the abiotic stressors. However, studies in this direction are not available. Analysis of the plant-pathogen interactome at the site of infection during combined stress may reveal the mechanism behind the altered defense under combined stress. Another major stage of plant-pathogen interaction vulnerable to abiotic stress is the root and leaf interface. Plants secrete anti-microbial metabolites as a part of defense mechanism against a wide variety of pathogens. Analysis of metabolites at the root and leaf interface under combined stress conditions can also shed light on the effect of abiotic stress on the establishment of infection.
The transcriptomic data generated has opened up new areas of research in combined stress. RNA silencing is an important defense arsenal of plants and being targeted by combined heat and pathogen stress, stands as an important area to be probed under other abiotic, biotic stress combinations. It would be quite interesting to see the regulation of small RNA under combined stresses. Moreover, analysis of stress modulated metabolome and secretome of both plant and pathogen can shed light on newly evolved defense strategies of plants. The effect of abiotic stresses on pathogens post-infection remains unknown, and it will be interesting to study if abiotic stresses affect pathogens capability to hijack plants defense for successful infection. Since each plant-pathogen interaction is unique, and the effect of abiotic stresses on plant-pathogen interaction is furthermore specific, studying the effect of combined stress on crop plants is important. Effective designing of experiments mimicking the environmental conditions prevailing at the time of infection in fields should be undertaken. This further warrants the role of wide-scale field studies to analyze the weather conditions at the time of infections and carefully understand the correlation, if any, between environmental conditions and plant’s susceptibility to diseases. Although the combined stress research is still in its infancy, it is rapidly unfolding the intricate mechanisms of plant defense and providing avenues for the further improvement of crops under current climatic conditions.
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Acknowledgements
Combined stress tolerance related projects at MS-K lab were supported by DBT-innovative young biotechnologist award (BT/09/IYBA/2015/07). PP acknowledges financial support from SERB young scientist (SB/YS/LS-71/2014) scheme. We acknowledge DBT-eLibrary Consortium (DeLCON) and NIPGR library for providing access to e-resources. We also thank Dr. Mahesh Patil for critical reading of the manuscript.
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1. List of studies on the effect of abiotic factors on pathogens and the known modes of interaction between the two stresses in plants. (DOCX 22 kb)
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Pandey, P., Senthil-Kumar, M. Plant-pathogen interaction in the presence of abiotic stress: What do we know about plant responses?. Plant Physiol. Rep. 24, 541–549 (2019). https://doi.org/10.1007/s40502-019-00483-7
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DOI: https://doi.org/10.1007/s40502-019-00483-7