Adrianna Szczepaniec
Deborah Finke- 1Department of Entomology, Texas A&M AgriLife Research, Amarillo, TX, United States
- 2Division of Plant Sciences, University of Missouri, Columbia, MO, United States
Plants regularly encounter stress, and their responses to abiotic and biotic stressors have been a focus of research for decades. Stress caused by drought is one of the most often studied abiotic stresses owing to the increase in the incidence of drought driven by climate change. Severe drought has been shown to elicit a whole-plant response guided by key phytohormones, which not only respond to water stress but also play a critical role in the response of plants to biotic stress imposed by herbivores and pathogens. This is especially relevant for insect-transmitted pathogen systems, where plants, herbivores, and pathogens are linked in a web of direct and indirect interactions. Few studies have thus far explored the complex nature of drought-mediated tripartite interactions, however, and our ability to generalize and predict how plants respond to herbivore-transmitted pathogens while simultaneously countering the consequences of drought remains limited. The goal of this mini-review is to assess the current state of the field regarding the molecular mechanisms underlying plant responses to the combined effects of drought and simultaneous herbivory and pathogen transmission and their ecological consequences. We discuss plant responses to drought, herbivory, and pathogens as distinct and concurrent stresses, and highlight the implications of the tripartite interactions on insect vector and pathogen suppression in agroecosystems. This review provides a framework for future research linking generalized molecular responses in drought-stressed plants to tripartite species interactions and the ecology of insect-transmitted pathogens in the context of modern agriculture and water deficit driven by climate change.
Introduction
Climate change is driving an increase in incidence of drought at a global scale and extreme water deficiency is a significant impediment to plant fitness (Boyer, 1982, 2010; Bray et al., 2000). The impact of drought stress on plants extends beyond primary plant productivity, however, and results in profound changes in phytohormones and secondary metabolites involved in plant defenses (Asselbergh et al., 2008), the consequences of which for plant resistance to insects and pathogens are still poorly understood.
Plants commonly contend with multiple abiotic and biotic stresses simultaneously and must be capable of responding in a coordinated and dynamic fashion. This is particularly true for vector-borne plant pathogen systems where reciprocal direct and indirect feedback among plants, vectors, and pathogens results in changes in performance and behavior of the vectors and pathogens (Figure 1). Yet studies rarely measure the responses of plants to multiple stresses and even fewer studies have quantified the molecular mechanisms and ecological outcomes of tripartite plant-vector-pathogen interactions in the context of drought. However, the potential for non-additive effects of multiple stresses has contributed to a growing consensus that simplified investigations of pairwise interactions may not be sufficient (Mittler and Blumwald, 2010; Atkinson and Urwin, 2012; Atkinson et al., 2013; Prasch and Sonnewald, 2013; Bergès et al., 2018). Thus, the goal of this review is to outline the current state of the field and synthesize research on responses of drought-stressed plants to pathogen and herbivore attack. While reviews of the molecular mechanisms and consequences of single and multiple stresses have been assembled previously (e.g., Atkinson et al., 2015), this is the first synthesis of research focused specifically on the drought-mediated tripartite interactions among plants, insect vectors, and vector-borne pathogens. We highlight the general responses of plants to drought and biotic stress in order to contextualize the concepts of multi-stress responses. We examine the specific consequences of water deficit for plant interactions with pathogens and herbivores individually, and synthesize research on drought-mediated tripartite interactions. We also highlight the consequences of these responses for species interactions and for insect vector and pathogen suppression in agroecosystems. This mini-review aims to create a framework for linking key molecular mechanisms in plants under simultaneous drought and pathogen/vector attack to specific and predictable interactions among species.
Figure 1. Direct and indirect interactions among insect vectors, pathogens, and drought-stressed host plants, with examples of responding traits. Solid lines are direct effects, dashed lines are indirect effects. Arrows indicate the effect of one factor on another. Water deficit affects plant primary (differentiation) and secondary (defense) metabolism. These changes can alter reciprocal direct and indirect feedback among the plants, vectors, and pathogens and result in changes in performance and behavior of the vectors and pathogens.
Overview of General Molecular Responses of Plants to Biotic Stress and Drought
Plants utilize a diverse array of responses to attack by herbivores and pathogens. Metabolic responses are regulated by interconnected signaling pathways in which salicylic acid (SA) and jasmonic acid (JA) play a key role (Stout et al., 2006). The SA-mediated response pathway was originally implicated in plant resistance to pathogens (Kunkel and Brooks, 2002; Shah, 2003) and the JA-mediated pathway was thought to confer resistance to insects (Howe et al., 1996). We now know, however, that these pathways are intricate, interconnected (Walling, 2000; Koornneef and Pieterse, 2008; Thaler et al., 2010), and complicated by reciprocal down-regulation (i.e., “crosstalk”) (Thaler et al., 2002) that requires plants to integrate and prioritize their defenses (Bostock, 2005). Consequently, plant-mediated indirect interactions between pathogens and herbivores can lead to either induced resistance or induced susceptibility as a result of a multiple-enemy attack (Bostock, 2005).
The JA- and SA-mediated pathways overlap with the pathways that regulate plant responses to drought regulated by the hormone abscisic acid (ABA) (Ramanjulu and Bartels, 2002; Bartels and Sunkar, 2005; Urano et al., 2009; Harb et al., 2010). ABA modulates plants responses to drought stress, and its accumulation results in increases of reactive oxygen species, changes in cell turgor, and stomatal closure (Lee and Luan, 2012). ABA also prioritizes plant responses to biotic stress (Asselbergh et al., 2008), and interactions among ABA, JA, and SA have been extensively studied (Lee and Luan, 2012; Kazan, 2015; Nguyen et al., 2016).
Abscisic acid can dramatically re-shape interactions between JA and SA (Yasuda et al., 2008; Fan et al., 2009; Kazan, 2015; Muñoz-Espinoza et al., 2015; Guo et al., 2016; Wei et al., 2018), which illustrates that plant responses to biotic stress are frequently altered under drought. In general, accumulations of ABA are accompanied by a decrease in SA (Yasuda et al., 2008; Fan et al., 2009; Muñoz-Espinoza et al., 2015; Guo et al., 2016; Liu et al., 2016; Nachappa et al., 2016). However, an increase in ABA can also result in concomitant rise in SA (Audenaert et al., 2002; Anderson et al., 2004; Mauch-Mani and Mauch, 2005). Interactions between ABA and JA are equally variable, and ABA can have synergistic and antagonistic interactions with JA (Asselbergh et al., 2008). For example, changes in proteins involved in JA synthesis and accumulation were noted in a diversity of plants exposed to water deficit (Fan et al., 2009; Harb et al., 2010; Bonhomme et al., 2012; Ahmad et al., 2016; Haider et al., 2017), while other studies have indicated lack of JA induction in drought-stressed plants (Muñoz-Espinoza et al., 2015; Nachappa et al., 2016). The exact nature of interactions among the defensive responses of plants to biotic and abiotic stresses remains understudied, however, despite their importance to plant-pathogen, plant-insect, and plant-pathogen-vector interactions (Asselbergh et al., 2008; Erb et al., 2011; Davis et al., 2015b; Nachappa et al., 2016).
Pathogen-Plant Interactions in Water Deficit
In general, there is an inverse relationship between drought and resistance to pathogens driven by the negative cross talk between ABA and SA. For example, an ABA-mediated decrease in SA enhanced the susceptibility of Arabidopsis and tomato to Pseudomonas syringae (Mohr and Cahill, 2007) and tomato to Botrytis cinereal (Audenaert et al., 2002). Further, applications of exogenous ABA suppressed systemic acquired resistance (SAR) to pathogens, while induction of SAR decreased expression of ABA-biosynthesis genes, suggesting that the antagonistic interaction between these pathways is reciprocal (Yasuda et al., 2008). It is noteworthy that the crosstalk between ABA and SA can be accompanied by a synergism between ABA and JA in some (Fan et al., 2009), but not all cases (Anderson et al., 2004; Yasuda et al., 2008), emphasizing the complex and intricate links among these phytohormones.
There are instances, however, where ABA or drought stress in general promote enhanced plant resistance to pathogens. Stomatal closure induced by ABA to reduce transpiration can prevent pathogen entry (Melotto et al., 2006), and ABA signaling has been implicated in defense against necrotrophic pathogens, which induce JA-mediated defenses. This outcome suggests that instances of ABA-JA synergism can have positive outcomes for plant resistance and can vary across and within plant species (Asselbergh et al., 2008; Ramegowda and Senthil-Kumar, 2015).
Insect Vector-Plant Interactions in Water Deficit
Sap-feeding herbivores including insect vectors are predicted to respond positively to drought-stressed plants due to enhanced nutritional quality (Joern and Mole, 2005; Yan et al., 2015; Nachappa et al., 2016; Sconiers and Eubanks, 2017; Florencio-Ortiz et al., 2018). Specifically, physiological changes stemming from ABA-regulated osmotic adjustments that enable plants to maintain cell turgor by accumulating solutes (Ingram and Bartels, 1996; Harb et al., 2010) can benefit herbivores through increases in nitrogen and carbohydrate availability (Huberty and Denno, 2004). However, empirical support for this prediction is mixed.
Drought can have particularly complex and inconsistent effects on aphids, common vectors of phytopathogens. Aphids can respond positively (Tariq et al., 2012), negatively (Pons and Tatchell, 1995; Mcvean and Dixon, 2001; Hale et al., 2003; Simpson et al., 2012; Guo et al., 2016; Nachappa et al., 2016), or neutrally (Larsson and Björkman, 1993; Nachappa et al., 2016; Sconiers and Eubanks, 2017) to drought-stressed plants. The variable effects of drought on aphid fitness may be driven by the intensity of water deficit, whereby performance of a single aphid species increases under moderate stress but decreases under severe drought stress (Banfield-Zanin and Leather, 2015). Furthermore, aphids are highly susceptible to changes in osmotic pressure, which can constrain their ability to exploit elevated nutrients in drought-stressed plants, as was demonstrated in the lack of concomitant increase in performance of soybean aphids (Aphis glycines) exposed to soybean (Glycine max) under drought stress (Nachappa et al., 2016). Increased concentrations of JA-regulated glucosinolates have also been implicated in the lack of an enhanced aphid performance despite higher levels of nitrogen in stressed plants (Tariq et al., 2012).
Thrips and whiteflies are two other major insect vectors of phytopathogens, but few studies have explored the impact of drought on their fitness as vectors. Whiteflies, for example, were found to favor plants under low rates of irrigation (Paris et al., 1993; Skinner, 1996), while their oviposition was decreased by water deficit (Inbar et al., 2001). Similarly, thrips were more abundant on plants under water deficit and benefited from intermittent drought stress in cotton (Sconiers and Eubanks, 2017). Further, intense and severe drought was linked to outbreaks of Thrips tabaci in onion, which resulted in significant losses to crop productivity (Fournier et al., 1995).
The consequences of drought for vector fitness may also depend on its infection status. For instance, water deficit in tomato increased survival of Bactericera cockerelli (Hemiptera: Triozidae) infected with a bacterium Candidatus Liberibacter solanacearum, and resulted in a 60% increase in the number of adults (Huot and Tamborindeguy, 2017). Further, populations of infectious Rhopalosiphum padi aphids grew faster on wheat infected with Barley yellow dwarf virus compared to virus-free plants, and the effect was stronger when plants were under drought stress compared to unstressed plants (Davis et al., 2015a). This study did not explore how non-infected aphids responded to drought, which may further alter the outcome of plant-insect vector interactions (Hale et al., 2003). There is evidence that pathogens can lower the fitness of their insect vectors (Donaldson and Gratton, 2007; Nachappa et al., 2011; de Oliveira et al., 2014), and pathogen-mediated vector traits can interact with drought-mediated changes in plants. This was illustrated in the case of infectious soybean aphids, which unlike their virus-free counterparts, were unaffected by water status of the plants (Castle and Berger, 1993). Overall, water deficit exposure appears to have no effect or improve performance of non-infectious aphids, but further research is necessary to validate this effect.
Plant-Mediated Effects of Phytopathogens on Their Vectors
Increasing evidence documents that phytopathogens manipulate the performance and behavior of their insect vectors by altering the chemical or physical properties of their shared host plant (Casteel and Falk, 2016; Eigenbrode et al., 2018; Mauck et al., 2018). These phytopathogen-induced vector and host plant phenotypes are typically thought to be conducive to pathogen dissemination in the environment (Mauck et al., 2018). For example, pathogen-induced injury and altered volatile emissions can increase the attractiveness of infected plants to vectors (Eigenbrode et al., 2002; Jiménez-Martínez et al., 2004; Belliure et al., 2005; Bosque-Pérez and Eigenbrode, 2011; Hodge et al., 2011; Shapiro et al., 2012; Ogada et al., 2013). However, the exact nature of the interaction likely depends on the mechanism of pathogen transmission (Castle and Berger, 1993; Mauck et al., 2012; Eigenbrode et al., 2018). Pathogens that require long, uninterrupted feeding periods for efficient transmission may benefit by improving host plant quality and enhancing vector settling behavior (Belliure et al., 2005; Ogada et al., 2013). Alternatively, pathogens that require only a brief feeding probe for transmission may promote their own proliferation by inducing deceptive visual or chemical cues to attract vectors to unpalatable or low-quality plants from which vectors quickly emigrate after an initial feeding attempt (Purcell and Almeida, 2005; Mauck et al., 2010). While it is likely that drought will alter the plant-mediated effects of pathogens on their vectors, we currently lack the necessary understanding of the mechanistic basis of plant virus manipulation to predict these complicated multi-stress outcomes (Mauck et al., 2019).
Insect Transmission of Pathogens Under Drought Stress
The efficiency of pathogen transmission by insects is likely to be influenced by drought stress. Water deficit can directly affect plant resistance to pathogens and vectors via the overlap and crosstalk in the pathways regulated by the key phytohormones. However, water deficit can also affect plant infection risk indirectly by altering vector behaviors or preferences that are critical to transmission and are otherwise manipulated by vector-borne pathogens to their benefit in unstressed plants (reviewed in Mauck et al., 2016). For example, a loss in plant cell turgor pressure may alter feeding behaviors, such as the number of times a vector probes a plant (Krugner and Backus, 2014; Nachappa et al., 2016). Furthermore, low turgor pressure may enhance the plant-to-plant movement of vectors as they search for acceptable hosts, thereby increasing the number of plants contacted by individual vectors. These recent studies support the idea that drought may transiently and indirectly increase plant susceptibility to insect-transmitted pathogens, particularly if water deficit is severe and stimulates vector movement and probing frequency.
In fact, there is accumulating evidence to support the indirect effects of drought-stressed host plants on pathogen transmission. Drought stress increased aphid transmission of Cauliflower mosaic virus (CMV) and Turnip mosaic virus to Brassica rapa (van Munster et al., 2017). However, water deficit had the opposite effect on the aphid-transmitted Turnip yellow virus (TuYV) in Arabidopsis, whereby transmission of TuYV was significantly reduced due to lower viral accumulation in aphids feeding on drought-stressed plants (Yvon et al., 2017). Nachappa et al. (2016) found that incidence and transmission of the aphid-transmitted Soybean mosaic virus were also lower in soybean exposed to drought compared to well-watered plants, likely owing to a decrease in time required for the aphids to access phloem in the stressed plants. Further, drought affected aphid transmission of CMV across Arabidopsis accessions with varying fitness responses to water deficit, and the authors concluded that the consequences of drought for transmission and virulence were driven by the growth traits of the host plants (Bergès et al., 2018).
Thus, it appears that the effect of drought on vector feeding behavior and other fitness traits plays a key, albeit indirect, role in shaping the consequences of drought on transmission of vector-borne pathogens. It is also apparent that the interactions among the intensity and duration of drought, plant species, and vector and pathogen natural history traits are likely to be even more complex under field conditions.
Drought-Mediated Tripartite Interactions
Plants susceptible to insect-transmitted pathogens must contend simultaneously with the consequences of drought, herbivory, and pathogen infection and coordinate their defensive responses accordingly. Likewise, herbivores and pathogens employ strategies to overcome plant defenses and promote their own proliferation. The result is a complex web of direct and indirect effects among pathogens, vectors, and their shared host plants (Figure 1).
Predicting the outcomes of these complex interactions is a challenge as they are likely to be species-specific and driven by natural history traits and genetic diversity of each of the organisms. We speculate that changes in vector performance and behavior mediated by drought-induced modifications in plant primary and secondary metabolism are likely to increase plant disease risk. The overlap and crosstalk in the molecular responses of plants to biotic and abiotic stresses, however, will ultimately determine the outcome of tripartite interactions. Drought is likely to influence the overall number of vectors present in the environment and the likelihood that these vectors will encounter and feed upon host plants, which is the essential first-step in vector-borne pathogen transmission. However, the probability that an encounter between a vector and a host plant will result in infection is likely governed by the ability of the plant to mount a successful immune response while simultaneously countering the effects of herbivory and water limitation. Multiple comprehensive studies that integrate molecular, behavioral, and ecological studies within a single plant system are necessary in order to advance our understanding of the mechanisms and consequences of drought-mediated tripartite interactions.
Implications of Drought Stress for Suppression of Insect Vectors and Vector-Borne Pathogens
The tripartite interactions among plants, insect vectors, and pathogens take place within diverse communities, and the complex outcomes of these interactions can have broad implications for the management of agricultural systems. First, the ability to predict how deficit irrigation affects plant productivity, insect vectors, and the associated vector-borne pathogens will allow for effective exploitation of water as a means to suppress vectors and pathogens (Daane and Williams, 2003; Rousselin et al., 2017). Secondly, understanding the impact of drought stress on direct and indirect plant defenses will allow for predictions of the likelihood of pest outbreaks and proper remediation plans that incorporate irrigation as one of the pest management tactics. For example, drought may impair the competitive advantage of native herbivores during invasions by non-native herbivores, as was illustrated in wheat, where water deficit reduced the ability of the native aphid R. padi to inhibit the population growth of the invasive aphid, Metopolophium festucae Theobald subsp. cerealum (Foote et al., 2017). Incorporating irrigation to alter these interactions could lower the incidence and severity of outbreaks of non-native vectors and associated pathogens. Further, recruitment of natural enemies and their meaningful contribution to pest suppression can be affected by drought through altered attraction of predators to injured plants. The nearly universal drought-induced decrease in SA, which is important in indirect plant defenses, is likely to affect recruitment of predators through disrupted emission of volatiles (Martini and Stelinski, 2017).
Conclusions
Given the increases in incidence of drought across the globe, research exploring the mechanisms driving drought-mediated tripartite interactions on multiple levels of organization and across trophic levels is more critical than ever. Research should employ a species-specific approach to quantifying plant responses to multiple stresses and assessing their consequences from gene expression to the fitness and behavior of vectors, pathogens associated with them, and their natural enemies.
Author Contributions
AS and DF contributed equally to the conceptualization and composition of the manuscript.
Funding
This work was supported by the USDA NIFA TEX09638 to AS and USDA NIFA MO-HAPS0006 to DF.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Acknowledgments
The authors thank Punya Nachappa and Priya Voothuluru for discussion that inspired an earlier draft of this review.
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Keywords: herbivory, pathogen transmission, plant-insect interactions, plant-pathogen interactions, water deficiency, climate change
Citation: Szczepaniec A and Finke D (2019) Plant-Vector-Pathogen Interactions in the Context of Drought Stress. Front. Ecol. Evol. 7:262. doi: 10.3389/fevo.2019.00262
Received: 28 March 2019; Accepted: 24 June 2019;
Published: 09 July 2019.
Edited by:
Lora A. Richards, University of Nevada, Reno, United StatesReviewed by:
Muthappa Senthil-Kumar, National Institute of Plant Genome Research (NIPGR), IndiaKarsten Mody, Darmstadt University of Technology, Germany
Copyright © 2019 Szczepaniec and Finke. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Adrianna Szczepaniec, YXN6Y3plcGFuaWVjJiN4MDAwNDA7dGFtdS5lZHU=