Recent history and future trends in host–plant resistance

Abstract

Host–plant resistance (HPR) is a subdiscipline in entomology that aims to understand, develop, and deploy crop varieties resistant to arthropod herbivores. The seminal figure in HPR was Reginald Painter, whose 1951 monograph Insect Resistance in Crop Plants established a conceptual framework and methodological approach for applied research on plant resistance. In the 75 years since the publication of this book, the empirical and multidisciplinary approach established by Painter has led to the development and use of hundreds of arthropod-resistant crop varieties. Much of the success of HPR research has been, and will continue to be, tied to advances in scientific disciplines related to HPR, such as plant breeding and genetics, analytical chemistry, and plant–insect interactions. However, given the challenges facing agriculture and pest management over the coming decades, increased attention will need to be given to the deployment of resistant varieties and the integration of resistant varieties into integrated pest management (IPM) programs. Recent advances in our understanding of fundamental aspects of the interactions between plants and herbivores provide insights that can facilitate the increased use of plant resistance in IPM programs, and the diverse membership of the Entomological Society of America can play a critical role by increasing communication between scientists interested in applied and fundamental aspects of plant resistance to insects.

Introduction

Seed-producing plants and the herbivorous arthropods that feed on them comprise approximately half of all terrestrial macroscopic species (Schoonhoven et al. 2005), and the interactions between plants and herbivorous arthropods are critical for structuring terrestrial ecosystems (e.g., Wimp et al. 2005, Visakorpi et al. 2019). Arthropod herbivores are important in agricultural systems because their activities often constrain agricultural productivity. It has long been recognized that different genotypes of cultivated plants (e.g., cultivars, landraces) differ in their resistance to arthropod herbivores—that is, in their inherent capacity to avoid or reduce the damage (yield loss) caused by herbivores (Painter 1951, Kennedy and Barbour 1992). Host–plant resistance (HPR) is an important subdiscipline in entomology that aims to understand, develop, and deploy crop varieties resistant to arthropod herbivores. Historically, the Entomological Society of America (ESA) has been the most important scientific society for practitioners of HPR (Wiseman 1999). Within the ESA, HPR was recognized as a separate subsection (Subsection Fa, within Section F: Crop and Urban Pest Management) until 2007, when subject-matter subsections were reorganized and HPR was subsumed under the Plant-Insect Ecosystems (P-IE) section (Hutchins and Steffey 2006).

The purpose of this review is to provide a brief overview of HPR and assess trends in HPR over the past several decades. We then provide some thoughts on how the subdiscipline is likely to advance in the future. Because HPR is a highly interdisciplinary field of study, progress in HPR has been and will continue to be linked to developments in allied disciplines, such as plant breeding, genetics, and analytical chemistry. Furthermore, the subdiscipline of HPR has developed in parallel with the study of the ecology and evolution of plant–-insect interactions, but exchanges of ideas across these 2 subdisciplines have not been as extensive or productive as might be expected (Kogan 1986, Stout 2013). We will argue that a reassessment of the subdiscipline of HPR in light of recent advances in our understanding of the ecology and evolution of plant–insect interactions will be needed to increase the integration of resistant varieties into integrated pest management (IPM) programs, and that ecologists and IPM practitioners in the ESA can be instrumental in making this reassessment.

A Brief Overview of HPR

The scientific study of crop varieties resistant to arthropod pests dates to at least the latter part of the 18th century, with reports of wheat varieties resistant to infestation by Hessian fly, Mayetiola destructor (Say) (Smith 2005). Other early successes in the use of resistant crop varieties include varieties of apples resistant to wooly apple aphid and grape rootstock resistant to phylloxera. Painter (1951) in the seminal monograph of the subdiscipline, Insect Resistance in Crop Plants, collated existing knowledge about plant resistance in major crops and outlined an approach to studying plant resistance that would prove highly influential over the succeeding 7 decades. The approach to studying plant resistance outlined by Painter consisted of 3 steps: the evaluation, or screening, of crop germplasm resources to identify genotypes possessing resistance to the pest of interest; breeding, with the purpose of introgressing (incorporating) genes responsible for resistance into agronomically acceptable backgrounds; and the integration of resistant varieties into pest management programs. This approach has proven highly successful: over 500 crop genotypes with resistance to arthropod herbivores have been developed using this approach, with a value exceeding $2 billion US annually (Smith and Clement 2012). Wiseman (1999) and Stout and Davis (2009) provide several case studies of crops in which plant resistance has been critical to the development of successful IPM programs.

In addition to defining an approach to the study of plant resistance, Painter (1951) introduced 3 terms to ‘divide’ the phenomenon of plant resistance into ‘bases or mechanisms’. As defined by Painter, non-preference comprises plant traits or plant genotypes that affect herbivore behavior in ways that reduce the probability a potential host plant is located or chosen for food, shelter, or oviposition; nonpreference was later renamed antixenosis by Kogan and Ortman (1978), and this term is used more widely today. Antibiosis refers to negative effects of resistant plants or plant traits on insect fitness (e.g., growth, development, survival, or fecundity). Finally, tolerance denotes the ability of a plant to recover from or compensate for herbivory in such a way as to minimize the fitness or yield consequences of herbivory (Stout 2019). This framework for categorizing plant resistance has remained largely unchanged since Painter (1951) but has been criticized on various grounds (Painter 1951, Stout 2013, Erb 2018). Antibiosis and antixenosis are poorly delineated in the HPR literature, are difficult to separate experimentally, and often share common causal bases (Stenberg and Muola 2017). Moreover, the trichotomous scheme does not accommodate the full range of plant traits now known to contribute to plant resistance (e.g., plant volatiles that attract natural enemies of herbivores or physiological traits that result in temporal asynchrony between plant and pest populations) (Stout 2013). Despite the weaknesses of Painter’s framework for studying plant resistance, no widely accepted alternative framework has been proposed in the applied literature.

The subdiscipline of HPR is characterized by its practical and empirical nature. HPR is strongly directed toward the pragmatic end of increasing the profitability of agricultural production through the development of high-yielding crop varieties with enhanced resistance to arthropod pests. Historically, the subdiscipline of HPR was only incidentally concerned with understanding the mechanisms underlying the phenomenon of plant resistance; according to Painter (1951), ‘…experimenters have been able to utilize insect resistance in crop improvement and insect control without complete knowledge of the reasons why the plants are resistant … a number of causes or mechanisms … result in resistance rather than a single factor, and in attempting to breed resistant varieties a knowledge of these mechanisms may sometimes be of little use’ (Painter 1951, 24–25). This is not to say that fine mechanistic work has not sometimes been conducted by HPR researchers (e.g., 1,4-benzoxazinones in maize; Klun and Robinson 1969), only that it is not integral to the subdiscipline. Furthermore, unlike the study of plant resistance carried on by scientists interested in the ecology and evolutionary biology of plant–insect interactions (see below), the HPR subdiscipline lacks an elaborate conceptual or theoretical foundation through which hypotheses explaining patterns of variation are generated.

A second distinctive of the subdiscipline of HPR is its interdisciplinary and collaborative character (Fig. 1): ‘[t]he plant breeder, agronomist or horticulturist, and entomologist, are the basic members [of an HPR research team], but for an understanding of the mechanism of resistance, plant and insect physiologists and biochemists should also be members of the team. This will necessitate cooperation between these groups…’ (Painter 1951, 13). The role of the entomologist is critical for the development and execution of appropriate protocols for assessing the resistance of crop genotypes, and entomologists have incorporated plant resistance as a tactic into the larger discipline of IPM in both theory and practice (e.g., Pedigo and Rice 2006). Expertise in plant breeding and genetics is required to incorporate genes responsible for resistance into high-yielding, agronomically acceptable backgrounds, particularly since most plant resistance is polygenic and high levels of resistance are often found only in unimproved germplasm (Kennedy and Barbour 1992). Knowledge of agronomy is essential because the goal of an HPR program is the use of resistant varieties in commercial production systems, and because much resistance is sensitive to the cultural (agronomic) conditions under which a crop is grown. In cases in which an understanding of the causal basis of plant traits is desired, expertise in plant and insect physiology, biochemistry, molecular biology, and/or natural product chemistry is often needed to identify and quantify putative resistance-related traits and determine causal relationships between plant traits and resistance. One consequence of the strong interdisciplinary nature of HPR is that advances in HPR are often tied to progress in allied disciplines.

Figure 1.

Scientific subdisciplines and areas of research allied with host-plant resistance. The X-axis depicts an approximate timeline of the development of the subdisciplines.

Importantly, the subdiscipline of HPR has developed in parallel with a body of fundamental literature concerned with the ecology and evolution of plant–insect interactions (see Kogan 1986 for a more detailed discussion of the parallel development of these fields). The seminal articles in the study of the ecology and evolution of natural plant–insect interactions (e.g., Fraenkel 1959, Ehrlich and Raven 1964, Hairston et al. 1960) were published shortly after Painter’s (1951) monograph on crop resistance, and the field of plant–insect interactions has since emerged as one of the most vigorous and productive subdisciplines in ecology (Fritz and Simms 1992, Erb and Reymond 2019, Barbero and Maffei 2023). The goals and approaches of researchers in HPR and plant–insect interactions differ considerably despite the overlap in subject matter. In contrast to the practical goals of HPR researchers, researchers in plant–insect interactions are typically interested in understanding the ecological factors that regulate populations of herbivores and in providing explanations for observed patterns of diversity and host use in herbivores and of allocation to plant defenses within and among plant species (Strauss and Zangerl 2002). The ecological and evolutionary literature on plant–insect interactions is rife with theories and hypotheses to explain these patterns (Stamp 2003). In addition, the early emphasis on secondary metabolism as the primary driver of plant–insect interactions and reciprocal evolution has led to a strong mechanistic strain in which researchers attempt to elucidate the causal bases of plant resistance to herbivores (Erb and Reymond 2019). Despite the obvious potential benefits of intellectual interchange and cooperation among researchers in HPR and plant–insect interactions, such collaboration has often been somewhat limited (Kogan 1986, Stout 2013).

Critical Assessment of State of the Subdiscipline of HPR

A critical assessment of changes in the subdiscipline of HPR must begin by acknowledging the enduring legacy of Painter’s approach in the subdiscipline. Almost one third of papers published in the ‘Plant Resistance’ section of the Journal of Economic Entomology (JEE) from 2005 to 2023 were germplasm screening studies—evaluations of large numbers (>10) of genotypes to identify genotypes possessing resistance (Fig. 2). A roughly equal number of studies involved detailed characterizations of the effects of resistant varieties on herbivores or the effects of herbivory on resistant and susceptible varieties. This latter group of articles almost always involved fewer genotypes than screening studies and often sought to characterize resistance as antixenosis, antibiosis, and tolerance. Thus, the approach and framework developed by Painter remain paradigmatic for the subdiscipline of HPR.

Figure 2.

Qualitative analysis of the content of articles published in the ‘Plant Resistance’ section of the Journal of Economic Entomology, 2005–2023 (n = 340). Articles were placed into 7 categories based on their Abstracts. ‘Screening’ articles describe studies in which a large number of crop genotypes were evaluated for resistance in an attempt to discover genotypes possessing resistance to insect pests; also included in this category were articles that documented resistant biotypes of insect pests. ‘Biology’ articles described detailed studies of the effects of resistant plants on herbivore pests or the effects of herbivorous pests on plant biology. ‘Biology’ articles usually involved fewer genotypes than ‘Screening’ studies, and often the resistance of these genotypes had been previously characterized. Both ‘Screening’ and ‘Biology’ articles often utilized Painter’s trichotomous categorization scheme. ‘Mechanism’ articles investigated plant traits or genes underlying (causing) resistance. Articles in the ‘Bt’ category comprised studies of Bt-mediated resistance in maize, cotton, rice, and soybean. ‘Induced resistance’ articles investigated herbivore-induced responses or resistance. ‘Implementation’ studies included studies of interactions of resistant varieties with other management tactics, quantification of the economic benefits of plant resistance, or development of variety-specific economic thresholds.

The ongoing influence of Painter aside, progress in HPR over the past few decades has been partly driven by advances in related disciplines. Perhaps most importantly, advances in the ability to manipulate genetic material and transfer genes across species has led to the development and widespread deployment, beginning in 1996, of transgenic maize, cotton, and (recently) soybean varieties containing genes for insecticidal proteins from Bacillus thuringiensis (Bt crops). Over 100 million hectares are planted to Bt crops annually, with very high levels of efficacy, and diverse Bt crops are under development against a range of target pests (Douglas 2018, Tabashnik et al. 2023). Unlike natural plant resistance, which is usually polygenic (Smith and Clement 2012), the genetic basis of Bt-mediated resistance is simple (one or, in the case of pyramided varieties, a few genes). The phenotypic basis of resistance in Bt crops is also simple, dependent as it is on the expression of one or a few proteins. It is therefore debatable whether Bt crops should be considered a type of plant resistance or an efficient method for insecticide delivery, although the JEE includes papers on Bt resistance in its ‘Plant Resistance’ section (Fig. 2; studies of Bt crops represented almost 10% of studies published in the ‘Plant Resistance’ section of JEE from 2005 to 2023), and Bt crops are included in many reviews of plant resistance (Douglas 2018, Smith 2021). The simple genetic and phenotypic basis of resistance in Bt crops has led, quite predictably, to the evolution of Bt resistance in target herbivores, and much of the current effort in this field is centered on developing approaches to increase the sustainability of transgenic insecticidal crops (Tabashnik et al. 2023).

HPR has also been affected by advances in omics techniques and analytical tools such as liquid and gas chromatography and mass spectrometry. Progress in these areas has made it increasingly practical to identify and quantify genes, secondary metabolites, and other plant traits potentially responsible for resistance. As one notable example, it is now almost routine to collect and characterize volatile chemicals emitted by plants following injury by herbivores (e.g., van Doan et al. 2021). Another important example is the increasing availability of metabolomic techniques, which allow a more comprehensive picture of phytochemical diversity in a plant (Wetzel and Whitehead 2020). Improvements in analytical chemistry and instrumentation, coupled with the availability of genome sequences for many crop plants and methods for monitoring gene expression, have vastly increased the capacity to determine mechanisms of plant resistance—that is, to identify specific plant traits and genes responsible for differences in resistance to pest arthropods. Thus, the limitations on discerning cause and effect relationships in plant resistance noted by Painter (1951) are being overcome. While still not common, studies that attempt to identify plant traits or genes causally responsible for resistance are not unusual in the applied literature (e.g., almost 1 in 5 studies in the ‘Plant Resistance’ section of the JEE over the past 20 years were investigations of mechanisms of plant resistance [Fig. 2]).

The advent of molecular breeding has also influenced HPR. Marker-assisted selection has for the past several decades allowed breeders to use statistical associations between variation in traits governed by many genes (e.g., most plant resistance) and genetic markers (quantitative trait loci, QTL) to facilitate the selection process (Desta and Ortiz 2014). More recently, sophisticated genotyping techniques and data-driven approaches such as genomic selection have been used to increase genetic gain per unit time for complex traits (Ahmed et al. 2020, Smith 2021). The use of genotyping-by-sequencing and association mapping to identify QTLs associated with resistance to pea aphid (Acyrthosiphon pisum [Harris]) in lentils is one recent example of the application of these techniques to HPR (Das et al. 2022). At the same time, the development of high-throughput phenotyping techniques, which involve nondestructive sampling, mechanization of data collection, and analysis of large datasets, has enabled more rapid and quantitative measurements of plant traits associated with resistance and plant injury (Goggin et al. 2015, Crossa et al. 2021). High-throughput phenotyping is particularly important in breeding for plant resistance, because screening for variation in plant resistance or tolerance in large populations of plants is often the most important bottleneck in breeding for resistance to insects (Goggin et al. 2015, Peterson et al. 2017).

Continued advances in disciplines allied to HPR can be expected to strongly impact HPR over the coming decades. Increased incorporation of high-throughput phenotyping, genomic selection, and other molecular breeding techniques into conventional breeding programs promises to increase the number of breeding programs for which the development of insect-resistant varieties is an attainable goal (Smith 2021). Increasing adoption of these techniques will also increase the feasibility of breeding for tolerance, a notoriously difficult trait for which to breed (Peterson et al. 2017). Innovations in plant biotechnology will include the introduction of novel Bt and other proteinaceous toxins with unique activities and effectiveness against new target pests. As one recent example, ThryvOn cotton, introduced in 2023 across the southern United States, contains a Bt toxin effective against tobacco thrips (Frankliniella fusca) and tarnished plant bugs (Lygus lineolaris); unlike most other Bt crops, the mechanism by which ThryvOn cotton controls pests involves antixenotic effects and nonlethal antibiotic effects (Huseth et al. 2020). RNAi technology and (especially) gene editing will expand the opportunities for designing insecticidal crop plants with novel modes of action (Douglas 2018, Tyagi et al. 2020). Although applications of gene editing to increase crop resistance to herbivores are limited to this point, the recent enhancement of soybean (Glycine max) resistance to lepidopteran pests via the CRISPR/Cas9-mediated alteration of flavonoid biosynthesis provides an example of the potential of this approach (Zhang et al. 2022). Finally, advances in analytical instrumentation, genomics, transcriptomics, and metabolomics will make it easier to elucidate the causal basis of plant resistance, which will in turn provide novel targets for gene editing and molecular breeding.

Despite the significant progress in HPR and related disciplines described above, plant resistance still plays a smaller role in IPM programs than it should (Stout and Davis 2009, Smith and Clement 2012, Smith 2021). There are many reasons for the underutilization of plant resistance in IPM, among them a lack of funding support for research in HPR and a continued overreliance on insecticides in pest management (Smith and Clement 2012, Smith 2021). Perhaps the most significant factor contributing to the underutilization of plant resistance, however, is the lack of research focused on deploying resistant varieties in multitactic management programs. In fact, of 340 articles published in the ‘Plant Resistance’ section of the JEE over the last 20 years, only about 3% dealt explicitly with the integration of resistant varieties in IPM by, for example, investigating interactions with other management tactics, quantifying the economic benefits of plant resistance, or developing variety-specific economic thresholds (Fig. 2). We argue in the next section that the fundamental literature on plant–insect interactions provides key insights that can be used to increase the implementation of plant resistance as a component of multitactic management programs.

Incorporating Insights From the Ecological Literature to Increase the Use of Plant Resistance

The fundamental literature on the ecology and evolution of plant–insect interactions addresses a range of questions and topics potentially relevant to the integration of plant resistance into IPM programs. At a general level, one central question of historical importance concerns the relative roles of plant resistance (‘bottom-up’ forces) and predation and parasitism (‘top-down’ forces) in regulating populations of herbivores (Hairston et al. 1960); this question bears directly on the integration of plant resistance and biological control. Another general area on which the ecological literature has placed a greater emphasis is the sources and implications of phenotypic plasticity in plant resistance (Kant et al. 2015); an understanding of phenotypic plasticity in plant resistance is important for understanding, among other things, the effects of environmental factors and cultural practices such as soil fertility on the expression of resistance in plants. In the following paragraphs, we summarize areas of current interest in the ecological and evolutionary literature and suggest ways that discoveries in these areas relate to the use of plant resistance in IPM.

Herbivore-Induced Resistance

Plants can respond to herbivory by rapidly initiating comprehensive transcriptomic and metabolomic changes that confer resistance or tolerance to subsequent herbivory (Kant et al. 2015). This induced resistance can affect herbivores directly by reducing growth or increasing mortality or indirectly by attracting natural enemies of the herbivore or by warning other plants of herbivore presence (Heil 2014, Marmolejo et al. 2021). This phenomenon of induced resistance is nearly ubiquitous in plants and has been the subject of intense interest from ecologists and plant biologists over the past several decades. Tremendous progress has been made in our understanding of many aspects of induced resistance, including perception of attack, signaling and phytohormonal mediation of resistance, and induced changes in primary and secondary metabolism responsible for induced resistance. Despite this progress, however, the implications of induced resistance to IPM remain largely unexplored (Poelman et al. 2023). Most phenotyping protocols used in traditional screenings for plant resistance probably conflate constitutive and induced resistance—that is, by merely measuring differences among plant genotypes in injury or pest populations at specific time points during the growing season, most screening studies provide no information about whether differences among genotypes in these measures derive from constitutive resistance or induced responses, or about the relative importance of these 2 dimensions of resistance. One way that induced resistance may be manifested in field crops is as an increase in resistance to late-season herbivores in plants subjected to herbivory earlier in the season. Studies have demonstrated that early season herbivory can alter the size, composition, or impact of subsequent herbivore populations (Poelman et al. 2023), with some evidence that plants may tailor responses in ‘anticipation’ of common patterns of herbivore infestation (Mertens et al. 2021). Such plant-mediated interactions among temporally separated herbivores may involve direct induced resistance, indirect induced resistance, or both. (Kessler and Baldwin 2004), for example, found that experimental infestation of wild tobacco (Nicotiana attenuata) with a mirid bug (Tupiocoris notatus) increased the direct resistance of the plants to subsequent Manduca quinquemaculata and also increased the attractiveness of the plants to a generalist geocorid predator. However, the practical implications of plant-mediated interactions for scouting, economic thresholds, biological control, or other aspects of IPM have rarely been studied in agroecosystems.

Another frequently suggested possibility for increasing the use of induced resistance in IPM is breeding crop plants for increased inducibility (Poelman et al. 2023). Examples of genotypic differences in inducibility have been reported in the literature (e.g., Rasmann et al. 2005 reported varietal differences in inducibility of caryophyllene in maize), but to date there are no examples of varieties intentionally bred for heightened responsiveness to herbivory. Finally, chemical elicitors of induced resistance to insects have been discovered. They are widely used to experimentally manipulate plant resistance to arthropod herbivores in greenhouse and field studies (Xin et al. 2012, Sobhy et al. 2014) and could conceivably be used to stimulate crop resistance at appropriate times during a growing season. Elicitors of plant resistance to pathogenic microorganisms are used commercially to a limited degree (Yang et al. 2022) but to this point, applications of elicitors have not been incorporated into IPM programs for herbivorous insects in any crop.

Role of Phytochemical Diversity in Plant Resistance

The remarkable diversity of secondary metabolites produced by plants was one of the patterns that served as an impetus for the modern subdiscipline of plant–insect interactions (Fraenkel 1959, Ehrlich and Raven 1964). Only recently, however, have ecologists begun to consider the significance of phytochemical diversity per se in plant–insect interactions (Wetzel and Whitehead 2020). These efforts have been facilitated by the development of metabolomic approaches. Several competing hypotheses have been forwarded to explain the importance of phytochemical diversity, both within and among plants, in plant resistance: phytochemical diversity may be the consequence of selective pressure over evolutionary time from diverse enemies (herbivores, pathogens) and mutualists; variability in plant quality (as determined by nutrients and phytochemicals) may itself represent a challenge for herbivore physiology and performance; synergies in the biological activities of phytochemicals may make mixtures more effective than single compounds; herbivores may adapt more slowly to mixtures of phytochemicals than to single compounds (Wetzel et al. 2016, Wetzel and Whitehead 2020). Because crop plants are more genetically uniform than plants in unmanaged systems, phytochemical diversity may be less important in crop resistance to herbivore pests. However, there are other drivers of phytochemical diversity within and among plants, including soil fertility, abiotic stress, and prior interactions with biotic stressors (e.g., Lindroth et al. 2023). Moreover, there are ways of increasing genetic diversity in managed systems, such as varietal mixtures (Snyder et al. 2020). Thus, it may be possible to manipulate phytochemical diversity in crops to increase effectiveness of plant resistance in IPM.

Indirect Defense and Tritrophic Interactions

In response to insect herbivory, plants produce a variety of volatile organic compounds that serve as cues for natural enemies of herbivores to locate their prey (Das et al. 2013). These volatile cues can also be perceived by herbivores themselves, that can either be attracted or repelled to herbivore-infested plants (De Moraes et al. 2001, Zakir et al. 2013, Knolhoff and Heckel 2014). Furthermore, volatile signals emitted by herbivore-infested plants may be perceived by other plants and serve to alert them of close herbivore presence (Baldwin and Schultz 1983). The compositions of these volatile blends tend to be very specific to the plant and herbivore species, making them reliable cues in a complex environment (Arimura et al. 2009). Research in this area started in the late 1980s and early 1990s with the discovery that plant volatile blends change in response to insect herbivory and that insect natural enemies are more attracted to plants fed on by their herbivore host (Dicke and Sabelis 1987, Turlings et al. 1990). Since then, studies have focused on various aspects, including the chemistry, evolutionary context, and transcriptional regulation of volatile compounds, variation in volatile induction in plants infested with different herbivore species, identification of compounds that elicit responses in natural enemies, effects of abiotic factors on volatile emissions, and mechanisms of uptake and perception of volatiles by plants. Research in this field has opened promising possibilities for IPM that include selection of cultivars that emit stronger volatile blends, exogenous application of plant volatile inducers, release of synthetic plant volatiles induced by herbivory, modification of agronomic landscapes including crop mixtures or companion plants that increase diversity in induced defenses, and use of volatile compounds in push–pull systems (Peñaflor and Bento 2013, Poelman et al. 2023).

There is natural intraspecific variation in the synthesis and emission of plant volatiles, making it possible to select plant genotypes that produce more attractive volatile compounds through conventional breeding or genetic engineering techniques (Peñaflor and Bento 2013). However, a drawback of this approach is that natural enemies could become acclimated to volatile cues that do not reliably indicate the presence of herbivore prey, ultimately decreasing attraction of natural enemies (Rodriguez-Saona et al. 2012). Perhaps a better strategy would be to engineer plants to respond more strongly in the presence of herbivore attack, reducing the metabolic cost of constitutive volatile production (Rodriguez-Saona et al. 2012). A field study using cultivars of Brassica oleracea with naturally varying induced volatile profiles found differential attraction of the parasitoid Cotesia glomerata to plants infested with Pieris rapae caterpillars (Poelman et al. 2009). This study suggests that the selection of plant genotypes that are more attractive to natural enemies following herbivory enhances the biological control of insect pests.

Production of herbivore-induced plant volatiles can also be artificially induced by exposing plants to phytohormones, their derivatives, or volatiles emitted by plants exposed to herbivory (Patt et al. 2018). For example, treatment of lima bean and tomato plants with the plant hormone jasmonic acid increased herbivore-induced volatile emissions, reduced herbivory, and increased herbivore parasitism by natural enemies under field conditions (Thaler 1999, Heil 2004). Alternatively, plant treatment or dispensers containing synthetic volatile compounds normally released by herbivore-exposed plants can also increase attraction of herbivore natural enemies under field conditions (James 2003, Yu et al. 2010, Uefune et al. 2012). A common compound in plant volatile blends induced by insect herbivory is methyl salicylate, which attracts parasitoids and insect predators of various herbivore species (Rodriguez-Saona et al. 2011, Martini et al. 2014). This compound is commercially available in slow-release dispensers for its use in agriculture to increase biological control (Rodriguez-Saona et al. 2011).

Pest control by natural enemies is also enhanced by plant diversification in agricultural fields. A diverse landscape can improve diversity and abundance of natural enemies by providing food resources and shelter that may not always be available in monocultures (Rodriguez-Saona et al. 2012). The combination of herbivore-induced plant volatiles to attract natural enemies and companion flowering plants that provide food resources for those natural enemies is referred to as the ‘attract and reward’ approach (Simpson et al. 2011). Implementation of this approach under field conditions increased the number of natural enemies and reduced pest herbivores in corn, broccoli and grape combined with buckwheat (Simpson et al. 2011). Plant diversity could be increased in monocultures by using cover crops, intercropping, or by planting wild species in strips and crop borders. An increase in plant diversity not only favors faunal diversification but also improves soil health (Rodriguez-Saona et al. 2012). A well-known successful strategy that integrates the use of crop mixtures and induced plant resistance is the push–pull system that consists of repelling (‘pushing’) herbivore pests from the main crop while attracting them to trap crops where they can be controlled (Khan et al. 1997). This strategy has been successful for the control of stem borers in cereal crops in Africa and may be effective for controlling other crop pests. However, due to the specificity of herbivore–plant interactions, push–pull systems need to be developed for each particular crop–herbivore system (Khan and Pickett 2004).

The Role of Soil Health in Plant Resistance and Pest Management

Advances in methods for assessing soil health are providing new insights into the ecology of interactions between soil organisms, plants, and the above- or below-ground arthropod herbivores (Muramoto et al. 2022). The general concept of soil health relates to the capacity of soil to serve as a living ecosystem that sustains plants, animals, and humans (Lehmann et al. 2020). Furthermore, healthy soils in agroecosystems promote complex biological communities of soil-borne organisms that support crops more resilient to external perturbations and therefore herbivory (Alyokhin et al. 2020). Management practices for soil health may reduce erosion, increase nutrient use efficiency, improve soil structure, and sustain or increase yields, but, historically, the relationship between soil health and pest management has rarely been considered in production recommendations (Atwood et al. 2022). Soil health can be influenced by the microbial composition of the soil, such as the presence of arbuscular mycorrhizae and soil nematodes, which, in turn, can increase plant resistance or tolerance against insect pests (Brito et al. 2021, Topalović and Geisen 2023). For example, studies on the impact of arbuscular mycorrhizae on plant resistance have demonstrated that, in some cases, they may help increase plant defenses against insect feeding through improved nutrient uptake (Gange and West 1994) and activation of defense signaling pathways (Hause et al. 2007). As another example, free-living soil nematodes in the rhizosphere have been shown to enhance plant resistance to diseases by promoting a more favorable ratio of plant-beneficial microorganisms to plant-pathogenic microorganisms, thereby improving plant performance and complementing varietal resistance (Topalović and Geisen 2023). Certain agricultural practices, such as reduced tillage, use of mulch, and cover crops have been reported to increase free-living nematode communities and to decrease plant disease-producing organisms in rice fields (Masson et al. 2022). However, despite the important role soil health plays in agroecosystems, the effects of native arbuscular mycorrhizal communities and soil nematodes on practical aspects of pest management are under-studied.

The Role of Insect Saliva, Oral Secretions, and Insect-Associated Microorganisms in Induced Plant Resistance

Research in this area has focused on the study of plant responses to insect attack as well as the identification of herbivore-associated molecules that induce (elicitors) or suppress (effectors) herbivore-induced defenses. For chewing insects, the mechanical damage caused by feeding induces the production of plant elicitor peptides that activate defense responses. These responses are further modified by herbivore-associated molecules that may originate from the insect, from the plant itself, or from microorganisms harbored by the insect. During feeding, insect herbivores release oral secretions coming from their foreguts and saliva coming from their salivary glands; they also secrete waste products such as frass, honeydew, and oviposition fluids. These insect secretions contain molecules that, upon perception by plants, modulate defense responses that can affect herbivores, associated microorganisms and natural enemies. Turlings et al. (1990) first discovered that wounded maize plants treated with beet armyworm oral secretions release a volatile blend similar to the blend emitted by caterpillar-infested plants, and that those volatiles were used by parasitic wasps to locate their herbivore host. However, perception of herbivore-associated molecules does not always benefit the plant; for example, the salivary enzyme glucose oxidase from Helicoverpa zea caterpillars reduces nicotine concentration in tobacco and improves insect growth (Musser et al. 2002). Some herbivores elicit defenses that are often triggered by pathogens and that are antagonistic to those responses against insects. Further research has demonstrated that the composition of herbivore secretions and the responses triggered after plant perception are specific to the plant–herbivore system (reviewed by Acevedo et al. 2015).

After the initial discovery of the active roles of insect secretions in plant immunity, research focused on the identification of specific elicitors and effectors, elucidation of downstream plant responses and mechanisms of perception, and documentation of the composition of secretions from various insect species and their activity in different host plants. More recently, it has been demonstrated that insect natural enemies and associated microbes can modulate herbivore-induced defenses in plants. Poelman et al. (2011) found that parasitoids modified the composition of oral secretions in parasitized herbivores and, as a result, modified induction of plant defense-related genes. Later, Tan et al. (2018) found that H. zea caterpillars parasitized by the braconid wasp Microplitis croceipes induced lower levels of defense responses in tomato plants than nonparasitized caterpillars. The researchers further showed that the differential plant responses were associated with lower activity of the salivary enzyme glucose oxidase resulting from polydnavirus injected by the wasps. The reduction in plant defense responses upon caterpillar feeding resulted in increased wasp fitness. Similar results were also identified in a different lab with other study systems (Cusumano et al. 2018). Likewise, insect-associated microbes can directly and indirectly modify plant defense responses. Chung et al. (2013) found that the oral secretions of Colorado potato beetles (Leptinotarsa decemlineata) contain bacteria that downregulate herbivore-induced responses in tomato plants, increasing insect performance. In another study, it was found that H. zea caterpillars containing the bacterium Enterobacter ludwigii secreted more glucose oxidase in their saliva and induced higher defense responses in tomato plants than those without the bacterium (Wang et al. 2017).

Altogether, this basic research has engendered a deeper understanding of the complexity of insect–plant interactions shaped by millions of years of coevolution. At the same time, this research has provided critical information that should be considered in the implementation of induced resistance in pest management programs. Plant elicitors could be exploited for pest management with a better understanding of their perception by plants and the development of feasible ways to deliver them into crop systems. Alternatively, instead of treating plants with elicitor molecules, plants could be treated with herbivores that produce only mild damage but induce resistance against later, more damaging herbivores. Such ‘plant vaccination’ has been documented in tobacco initially damaged by mirid bugs that increased plant resistance to subsequent herbivory by tobacco hornworm (Kessler and Baldwin 2004) and in grapes using Willamette mites (Eotetranychus willamettei) to increase plant resistance to Pacific mites (Tetranychus pacificus) (Karban et al. 1997). Other approaches include breeding or engineering of plants that are highly inducible or that express higher levels of defense responses upon insect damage. An area that has attracted significant attention has been the utilization of herbivore-associated microbes for insect management. An immediate application could be the knockdown of essential insect symbionts by the use of natural or engineered antimicrobial compounds (Dandekar et al. 2012, Li et al. 2015). Another option could be the use of microbes to deliver double-stranded (ds) RNA molecules to knock down essential herbivore genes (Douglas 2018). Yet another option could be the introduction of symbiont strains that either enhance plant-induced resistance or increase insect susceptibility to natural or synthetic compounds. Some bacterial strains present in the gut of fall armyworm caterpillars enhance insect mortality when fed on resistant maize plants, suggesting that efficacy of plant resistance could be enhanced by transient herbivore gut bacteria (Mason et al. 2019). To our knowledge, this knowledge has not yet been applied to IPM, but as research progresses, it could become a source for novel and sustainable pest management strategies.

Plant Defense Priming

Priming is a physiological state in which plants are better prepared to respond to biotic or abiotic stressors (Frost et al. 2008). Primed plants exhibit enhanced resistance to stressful events such as herbivory or pathogen attack (Conrath et al. 2006). Scientists have identified a number of products that induce plant defense priming, including soil amendments, synthetic plant hormones and microorganisms (Pereira et al. 2021). The use of plant defense inducers that effectively enhance plant resistance before herbivory occurs is a promising pest management strategy but is still not commonly used in agriculture. For example, the use of arbuscular mycorrhizal fungi, plant growth-promoting rhizobacteria, and silicon can not only induce priming of antiherbivore defenses but also improve plant nutrition and resistance to abiotic stress (Pieterse et al. 2001, Pineda et al. 2010, Song et al. 2013, Singh et al. 2020). More recently, scientists have demonstrated that entomopathogenic fungi can grow as endophytes in plants, thereby conferring protection against herbivores (Vega 2018, Ahmad et al. 2020, Cachapa et al. 2021). An attractive characteristic of some plant-defense inducers is that they could be applied as seed treatments to enhance resistance in the germinated plants (Worrall et al. 2012). However, the resistance conferred by defense inducers could affect plants and herbivore systems differently; in some cases, they could confer protection to some herbivores but susceptibility to others feeding on the same plant species (Hartley and Gange 2009). Therefore, integration of knowledge from the field of plant–insect interactions could help design recipes that would be more fitted to a particular crop and its more damaging herbivores.

Plant Tolerance

Plant responses to herbivore antagonists often include changes in traits related to tolerance—that is, the ability of the plant to recover from or compensate for the injury caused by insect pests (Painter 1951, Smith 2005). Expression of tolerance traits by a plant typically does not have deleterious effects on herbivore fitness and hence does not place selective pressure on herbivore populations to evolve countermeasures, potentially making tolerance a more sustainable pest management strategy. Despite the benefits of plant tolerance in IPM, entomologists have focused more attention on insect pest biology than on plant biology (Erb 2018). This is because phenotyping for plant resistance is difficult and because the mechanisms and genetic basis of tolerance are poorly understood (Peterson et al. 2017).

Tolerance to herbivore injury has been identified in a variety of crops, including maize, potato, and rice (Robert et al. 2015, Poveda et al. 2018, Villegas et al. 2021). In rice, tolerance of root feeding by the rice water weevil, Lissorhoptrus oryzophilus, appears to be greater in hybrid rice varieties than in inbred varieties (Villegas et al. 2021). In addition, the susceptibility of certain rice varieties to rice water weevil is dependent on symbiotic associations with arbuscular mycorrhizae; despite higher densities of weevil larvae in rice plants inoculated with arbuscular mycorrhizae in field studies, mycorrhizae-inoculated plants showed higher tolerance to root damage as evidenced by increased plant biomass and yield (Bernaola and Stout 2021). This suggests microbial soil organisms could potentially be a sustainable tool in IPM as a soil amendment or seed treatment. However, the mechanisms underlying tolerance in crop plants are not well understood. One possible tolerance mechanism involves upregulation of detoxicative mechanisms for reactive oxygen species (ROS), to counteract the deleterious effects of hemipteran herbivory (Koch et al. 2016). The initial response to herbivory injury is generation of ROS and the activation of induced responses within the plant; this leads to changes in plant hormones that eventually trigger ROS mitigation. This ROS mitigation appears to be linked to the resumption of growth and therefore may underpin the tolerance phenotype (Koch et al. 2016). However, identification of tolerance mechanisms is complicated because factors such as herbivore specialization and feeding guild, symbiotic relationships (e.g., arbuscular mycorrhizae), and environmental conditions influence expression of tolerance (Foyer et al. 2015, Zhou et al. 2015, Tao et al. 2016). Thus, to gain a holistic understanding of tolerance mechanisms in crop systems, cooperation among multiple disciplines (plant physiology, entomology, agronomy, and ecology) is needed to improve research at the applied and fundamental levels (Peterson et al. 2017).

Influence of Domestication on Plant Resistance

Plant-feeding insects have coevolved with their host plants for millions of years under natural conditions, but the domestication of plants by humans has changed this equilibrium. Plant domestication started about 10,000 years ago with the cultivation of grasses like wheat and barley (Purugganan and Fuller 2009). Since then, humans have selected plants with desirable traits such as larger fruits, higher yields, shorter maturity, appropriate plant architecture, disease resistance, and adaptation to varying environmental conditions. The reduction of genetic diversity in modern crops has probably led to increased pest susceptibility (Chaudhary 2013). Insects can adapt quickly to chemistries and other plant traits to which they are constantly exposed. Furthermore, in wild conditions, plants are under specific selective pressures that have resulted in varying intrinsic resistance to herbivores, but in domesticated crops the selective pressures are different and often decrease herbivore resistance. To ameliorate this situation, humans spray pesticides, the indiscriminate use of which has also led to the development of insect resistance to insecticide molecules with associated environmental and human health risks.

A number of studies support the hypothesis that domesticated plants are often less resistant to herbivores than their wild ancestors (Whitehead et al. 2017). Studies in cabbage found lower performance of herbivores and associated parasitoids in wild cultivars; this was correlated with constitutively higher levels of glucosinolates when compared to domesticated types (Gols et al. 2008). Similarly, wild tomato plants were less preferred by Manduca sexta moths for oviposition while natural enemies were more attracted to herbivore-induced volatiles from wild cultivars than to those from cultivated types (Li et al. 2018). These and other studies suggest that herbivore-resistance of wild plants is both constitutive and induced. However, a metaanalysis failed to show association between the concentration of constitutive nonvolatile secondary metabolites and herbivore resistance (Whitehead et al. 2017). Likely, herbivores adapt more easily to constitutively expressed defenses than to induced ones. Research in plant–insect interactions has uncovered basic mechanisms of plant responses to herbivore attack and has suggested ways to integrate this knowledge in agricultural landscapes to reduce insect herbivory (Rodriguez-Saona et al. 2012). However, there is little adoption of these methods. Perhaps economic studies that evaluate the effect of new methods in reducing costs and increasing profit associated with new pest management programs could improve adoption. Also, there is a need for more studies in field conditions where plants are exposed to a more complex environment than what they encounter in greenhouses.

Conclusions

The use of resistant varieties is, in many ways, an ideal IPM tactic. Resistant varieties are usually simple and cost-effective to use, have cumulative impacts over space and time, are generally compatible with other management tactics, and have a lower impact on non-target organisms and the environment than alternative tactics (Smith 2021). Progress in biotechnology, molecular breeding, analytical tools, and omics techniques have increased the feasibility and efficiency of the approach to plant resistance pioneered by Painter (1951). However, it is clear that strengthening communication between researchers in various disciplines will be needed to achieve a greater understanding of plant resistance and increase its use in IPM. One potential barrier to such interdisciplinary communication is the lack of formal coursework in HPR at US universities. An informal survey of course offerings at over 20 US universities indicates that HPR content is typically relegated to a few lectures in broader IPM courses, with fewer than 20% of entomology departments offering specific courses in HPR (a few more universities offer courses specifically in plant-insect interactions). The lack of formal HPR coursework may also be an indication that few faculty specializing in HPR are being hired at US universities.

Furthermore, we contend that the important step of integrating resistant varieties into management programs is under-researched and would greatly benefit from increased interactions among applied entomologists and ecologists who study fundamental aspects of plant-insect interactions. Collaboration among these 2 groups of scientists should facilitate the development of novel strategies for integrating plant resistance into management programs. One of the strengths of the ESA is the diversity in scientific backgrounds and interests of its members, and the ESA counts among its membership not only applied entomologists interested in the development and use of resistant varieties in crop management programs, but also many ecologists, evolutionary biologists, and physiologists who study fundamental aspects of plant-insect interactions. By encouraging interactions between these groups of scientists, and by focusing the attention of ecologists and evolutionary biologists on the importance of resistant varieties in IPM, the ESA can play a critical role in increasing the utilization of this tactic.

Acknowledgments

The authors thank David Onstad for the invitation to write this review.

Author Contributions

Michael Stout (Conceptualization [Equal], Data curation [Lead], Investigation [Equal], Project administration [Lead], Writing—original draft [Lead], Writing—review & editing [Lead]), Lina Bernaola (Conceptualization [Supporting], Writing—original draft [Supporting], Writing—review & editing [Supporting]), and Flor Acevedo (Conceptualization [Equal], Project administration [Supporting], Writing—original draft [Supporting], Writing—review & editing [Equal])