Enabling sustainable crop protection with induced resistance in plants

Abstract

Induced resistance (IR), which enables plants to increase their resilience against insect pests and microbial pathogens by promoting their own immunity, has been recognized for its value in crop protection schemes. Despite promising applications, the use of IR in crop protection has remained marginal compared with pesticides and single resistance genes. This review aims to shed light on this disparity by examining the scientific milestones achieved over the past decades for both internal (immunological) and external (ecological) IR strategies. The multifaceted advantages of IR, particularly its ability to provide broad-spectrum protection and enhance the nutritional and nutraceutical value of certain crops, are also discussed. The various obstacles hindering the widespread adoption of IR strategies are then revealed. After considering recent scientific discoveries and insights, potential solutions are proposed, including leveraging epigenetic approaches to understand the mechanisms involved in IR. By acknowledging that the future sustainability of crop protection is irreconcilable with single-use technologies, this review proposes taking advantage of the latest insights regarding the adaptive nature of the plant immune system and its ecological interactions to safely integrate IR into existing crop protection schemes. By emphasizing the need for comprehensive and holistic approaches to basic and translational research, this review sets the stage for leveraging IR alongside other strategies to foster a resilient, environmentally friendly, and economically viable future, thereby ensuring the health of crops.

Key points

Introduction

Throughout history, plant pests and diseases have had a profound influence on human history, causing episodes of food insecurity and human suffering that have scarred our shared past. Devastating outbreaks, such as the Irish Potato Famine in the 19th century, have caused widespread hunger, economic turmoil, and mass migration with long-lasting historical consequences. Since the “green revolution” in the second half of the 20th century, our high-intensity food supply chain has become increasingly dependent on crop monocultures that are critically reliant on the excessive use of pesticides to protect against pests and diseases. However, this reliance is no longer deemed sustainable. In addition to concerns about non-target effects in the environment (1–4), the development of resistant pests, and concerns about the human health impacts of chemical residues in food products, the production and application of pesticides also generate a significant carbon footprint (5). Increasingly, such concerns have begun to influence agricultural policies globally. For example, the European Commission has proposed new policies with agricultural initiatives to reduce pesticides, such as the “European Green Deal” and “Farm to Fork Strategy” (6), which both propose a target of a 50% reduction in agrochemicals by 2030. Similar policies are being pursued in Japan, via the “Sustainable Food Systems Strategy MIDORI” (7), in the United States (8), and globally under the umbrella of the United Nations (9).

However, phasing out pesticides without replacing them with reliable alternatives can expose the food supply chain to risks that seriously affect regional food security and increase the volatility of the global food economy (10–13). Hence, there is an urgent need to identify and implement reliable alternatives to pesticides. One of the currently emerging crop protection practices identified by the European Commission is to harness strategies naturally employed by plants to resist pests and diseases (6). A plant’s immunity can be strengthened by stimulation with certain pathogens, pests, beneficial microbes, chemical agents, physical wounding, or herbivory (14). This phenomenon, known as induced resistance (IR), often provides broad-spectrum protection against a variety of pests and diseases (15, 16). IR allows plants to respond more quickly to biotic stressors (16) and can be combined with other crop protection strategies (15). IR is crucial for minimizing reliance on pesticides; moreover, in conjunction with our increasing knowledge of internal (immunological) and external (ecological) plant defense strategies (17), ample new opportunities exist to expand our current toolkit to ensure the sustainability of future plant health management. In turn, this contributes to achieving global food security and ensuring a sustainable food supply for a growing population.

How do plants defend themselves against pests and diseases?

Plants, much like all higher organisms, rely on several strategies to defend themselves against pests and pathogens (Figure 1). The first line of self-defense is controlled by the plant’s innate immune system, which operates according to a genetic blueprint that enables plants to detect signals and activate their inducible defense mechanisms. The innate immunity of plants has been studied extensively over recent decades and conceptually involves two separate layers (18, 19). The default layer, known as pattern-triggered immunity (PTI), responds to microbial molecular patterns such as flagellin, elongating factors, and danger signals and involves a variety of defense genes and mechanisms. This innate immune response provides a wide range of protection against different styles of attack. However, it has the disadvantage of being relatively weak against specialized attacks that involve PTI-suppressing virulence effectors (20). As an evolutionary response, plants can defend themselves via effector-triggered immunity (ETI), which is based on resistance (R) genes. R genes encode intracellular receptors that can activate the hypersensitivity immune response upon the direct or indirect recognition of immune-suppressive virulence effectors and are critical for so-called gene-for-gene, race-specific, or vertical resistance (21, 22). Despite the highly effective response of ETI to biotrophic parasites, its range of effectiveness is typically limited to a single species or even subspecies levels, such as pathovars. Moreover, the ongoing co-evolution by ETI-resistant attackers is selective for the emergence of new virulence effectors that are no longer recognized by existing R proteins, rendering ETI ineffective.

Figure 1

While PTI and ETI are important first layers of defense, plants require additional strategies to survive in hostile environments. When plants successfully repel initial assaults by pests or diseases they develop acquired or induced resistance through the activation of their own immunity. IR often involves a form of immunological stress memory referred to as “defense priming”—a phenomenon that conditions plants for enhanced stress resilience. Stress or defense response pathways are initially only weakly activated upon exposure to the priming agent but are then more strongly or rapidly induced when the plant is later challenged by an attacker (16, 23, 24). A classic example of defense priming is systemic acquired resistance (SAR), which occurs in response to localized pathogen attacks, triggering the release of long-distance defense signals that prime distal plant parts for the efficient activation of defenses upon later attacks, leading to enhanced resistance in a phenomenon similar to vaccination in humans (14). This phenomenon involves the finely tuned regulation of phytohormone signaling, elevated levels of pattern recognition receptors or dormant defense regulatory elements, and chromatin modifications (16, 25, 26). The priming effect can be long-lasting; it can even be transmitted to the next generations (27–32). There is mounting evidence that the long-term maintenance of priming is controlled by epigenetic changes, such as the reduced DNA methylation of transposons and the trimethylation of lysine 4 of histone subunit H3 (H3K4me3) at defense gene promoters, which have also been implicated in “poised” genes (genes in a “ready to be active” state) in animals [Box 1, (26)]. However, much remains to be discovered about the mechanisms through which stress-induced epigenetic changes prime stress-specific defense genes, how these epigenetic changes are maintained over cell division and sexual reproduction, and, ultimately, how they are erased in the absence of recurrent stress.

Plants also employ external ecological pathways to adapt to biotic stress; this is known as “indirect induced defense” or “plants crying out for help” (33). This mechanism allows plants to recruit other organisms to combat attackers. For example, the herbivore-induced emission of volatile organic compounds (VOCs) can attract predatory or parasitic insects that attack the impeding herbivore (34). Recently, similar interactions have been discovered above and below ground, where stressed plants alter their root exudation and headspace VOC chemistry to select and/or recruit a disease-suppressive microbiome. This also activates an immune response in neighboring plants, which protects the plant via a range of direct and indirect mechanisms, including induced systemic resistance (ISR) (35–37).

The current approach to crop protection still relies largely on pesticides and selective breeding for R genes, whereas strategies such as IR remain relatively underexploited. Unlike pesticides, IR is not curative and rarely provides complete protection against pests or microbial pathogens. Moreover, IR chemicals may have associated allocation fitness costs (trade-offs), such as reduced plant growth and yield or increased susceptibility to other stresses. These reasons may contribute to IR remaining underexploited. However, when applied in the correct context, IR offers numerous benefits. In addition to its broad-spectrum effectiveness, IR can help reduce pathogen loads, synergize with other management methods, and protect single R gene strategies from co-evolving pests and disease adaptations. This can help to decrease our reliance on unsustainable pesticides (38).

In this review, we explore the potential applications of IR and discuss how it can be integrated with the use of pesticides, other crop protection methods, and breeding strategies. By examining the costs and benefits of IR, we aim to establish a realistic framework for the safe exploitation of IR within current crop protection schemes.

Significant milestones in research into induced resistance

Reports on how IR combats plant pathogens date back to the 1930s (Figure 2). Initially, these reports were descriptive, presenting instances in which IR-like phenomena were observed [reviewed in Chester (39)]. In 1961, the term SAR was introduced by Frank Ross, who reported an experiment showing that inoculating a tobacco leaf with tobacco mosaic virus (TMV) led to resistance against the same virus in distal non-inoculated leaves 1 week after the first inoculation. In the 1960s, numerous studies on the biological induction of resistance were conducted in various plant species in which resistance was triggered by pathogens such as viruses, bacteria, and fungi (40).

Figure 2

A novel aspect of IR was described in a report by White (41): it showed that infiltration of the leaves of tobacco plants with salicylic acid (SA) led to SAR against TMV and induction of pathogenesis-related (PR) proteins. This is consistent with the later-described effects of endogenous SA during plant defense (42, 43). Ultimately, this discovery allowed screening programs that identified the functional analogs of SA as IR elicitors, which yielded products such as 2,6-dichloroisonicotinic acid (INA) and acibenzolar-S-methyl (ASM; an active ingredient of the commercial product Bion) (44, 45). As early as 1975, oryzimate was used as a resistance inducer in rice seedlings (46). Transgenic plants, such as SA-degrading NahG plants, which cannot accumulate SA (47), or the Nonexpressor of pathogenesis-related genes 1 (npr1) Arabidopsis mutant (48, 49), have helped to provide a deeper mechanistic understanding of IR signaling. Similarly, the discovery of jasmonic acid (JA) as an endogenous wound-inducible IR signal against insects and necrotrophic pathogens (50, 51) led to new research into the biosynthesis and response pathways of this IR-related hormone (52). Toward the end of the 2000s, researchers independently reported long-distance signals mediating systemic IR responses, such as methyl salicylate (53), azelaic acid (54), glycerol-3-phosphate (55), dehydroabietinal (56), and N-hydroxy pipecolic acid (57) for SAR, as well as electrical signals for the systemic IR response to wounding (58).

At approximately the same time, it was discovered that prolonged maintenance of IR-related defense priming involves epigenetic control (26) (Box 1), offering a plausible mechanism for the long-term (and sometimes transgenerational) durability of IR. More recently, it was shown that IR-related priming can be genetically engineered by fusing the NPR1 gene to a pathogen-responsive untranslated open reading frame (59) or epigenetically induced by the introgression of meiotically stable regions of reduced DNA methylation (60).

In the early 1990s, it was shown that IR was developed upon recovery from biotic stress, such as localized disease or herbivory, as well as being triggered by the root colonization of beneficial plant growth-promoting rhizobacteria (PGPR) (61–63).

ISR typically operates independently of SA but requires NPR1 and the intact jasmonate and ethylene (ET) signaling pathways (64–66). Subsequently, IR induction by beneficial fungi such as mycorrhizae (67) and even whole microbiota (68, 69) has been amply documented (Box 2).

Indirect induced defense by plants was initially described for plant–herbivore interactions, whereby the release of herbivore-induced plant volatiles (HIPVs) recruit natural enemies of the herbivore, such as predatory spider mites or parasitic wasps (94–96). The discovery of this “cry-for-help” led to follow-up studies showing that insect-derived elicitors, such as glucose oxidase and volicitin, boosted wound-induced volatiles (97) and that similar tritrophic interactions could occur below ground, allowing the recruitment of entomopathogenic nematodes (98). Based on enhanced knowledge of the genetic control of HIPVs, subsequent studies also provided proof of concept that the “cry-for-help” mechanism could be exploited in genetic strategies to improve crop protection (99, 100). In subsequent years, it became clear that both volatile and non-volatile metabolites in root exudates could recruit and/or select for disease-suppressive soil microbes (101–103). This precipitated more recent studies that have shown that the “cry-for-help” via root exudates conditions the soil for ISR-eliciting microbial consortia (104, 105). As for the internal epigenetic maintenance of IR (26), this “cry-for-help” in root exudates can protect plants across generations by conditioning the soil microbiome for disease-suppressive activity (17, 36), and it offers a plausible explanation for earlier reports about the development of disease-suppressive soils upon multiple cultivations with high disease incidence (e.g., take-all decline) (106).

Knowledge about microbe-, herbivore-, and damage-associated patterns triggering IR, such as cell wall components (e.g., oligogalacturonides from pectin; laminarin from algae; flagellin from bacteria; and Reynoutria extract, chitin, and chitosan from fungi and insects), as well as endogenous IR signals, such as β-aminobutyric acid (BABA), have allowed the development of commercial products in which microbes themselves or derived molecules constitute the active principle (Supplementary Table 1). Further development of such commercial products is ongoing: for example, there is a product based on the pheromone ascaroside 18 that is secreted by plant-parasitic nematodes (107, 108). Ascaroside 18 induces resistance in a variety of plant species to a broad spectrum of pathogens by activating both the SA-mediated and JA-mediated defense pathways, and its receptor has been identified recently (109). Ascaroside 18 is expected to be placed on the market in 2026 (D. Klessig, Boyce Thompson Institute, personal communication²).

Opportunities for induced resistance

Over six decades of research support IR as a potentially highly promising strategy to protect crops. IR is effective in protecting plants against a broad range of pathogens and pests. Although it may not provide 100% protection under high disease-pressure conditions, it offers an alternative to ETI-based strategies when the R gene repertoire is limited or unavailable, such as against necrotrophic pathogens and chewing herbivore pests (110, 111). Its multigenic (horizontal) character allows it to overcome resistance breakdown, and it can thus be used when resistance breakdown to pesticides or gene-for-gene strategies occurs (112). In the case of emerging diseases and pests, IR can provide faster solutions than traditional breeding. IR also offers an alternative in pathosystems for which no effective pesticides are available or where their use has been (or will be) banned and no gene-for-gene strategies are available. Because of its wide spectrum of effectiveness, IR can provide immediate protection against these challenges (Figure 3). Although the protection provided by IR may not necessarily be complete, it could still offer substantial benefits for farmers and protection against the devastating consequences of newly emerging pests and diseases.

Figure 3

Interestingly, the induction of plant defenses implies that plant secondary metabolism has been activated, which involves the biosynthesis of multiple bioactive compounds with health-promoting activities, such as polyphenols, carotenoids, flavonoids, phytoestrogens, and the activity of several antioxidant enzymes. Thus, the elicitation of IR, while stimulating plant defenses, frequently results in higher levels of these bioactive phytochemical compounds in fruits, vegetables, and herbs. Most of these metabolites have been investigated to assess their potential role in specific organoleptic properties of foods and show protective effects in human cells. Indeed, the application of biotic and abiotic elicitors and defense-related phytohormones during plant growth or the postharvest period has been used to enhance the production of secondary metabolites and produce high-quality and healthy fresh foods (113, 114). Beneficial plant symbionts triggering IR, such as mycorrhizal fungi and PGPR, can also improve the nutritional and nutraceutical value of fruits, as shown by the increased content of lycopene and beta carotene in tomato fruits, stronger anti-estrogenic activity (115–117) and higher concentrations of iridoids (oleuropein and secologanin) and flavonols in olive oil (118), and higher phenolics and anthocyanin content in berries (119).

Finally, therefore, IR in combination with low doses of chemical pesticides reduces the evolutionary pressure for pests and diseases to develop resistance against agrochemicals and may also complement R gene strategies by protecting available R genes against co-evolving pathogens (120–123). Under low- to moderate-pressure stress, IR is sufficient when stronger solutions are lacking or may function in complement or synergy with other plant protection methods. The current and emerging agri-tech solutions offer new opportunities to facilitate the incorporation of IR in common agricultural programs. In the next section, the limitations of IR, their potential solutions, and the application of IR in modern agriculture (Table 1) are discussed.

Factors limiting the adoption of induced resistance

Growth penalty caused by allocation fitness costs (trade-off)

Limitation

The activation of defense mechanisms requires energy and resources. Hence, the strong induction of IR can lead to a growth penalty, referred to as the allocation fitness cost. For example, negative effects on growth and development are typically more pronounced when plants are exposed to high concentrations of hormones or hormone-mimicking compounds as IR stimuli. These include methyl jasmonate (MeJA), SA, and SA-analogs such as benzothiadiazole (BTH) (124), BABA (125), acibenzolar-S-methyl (ASM) (126, 127), and INA (128, 129). This is unsurprising because an increase in defense hormone levels will result in the direct activation of defense pathways but cause a decrease in the effectiveness of defense priming, which is the more energy-efficient pillar of IR (16, 24). Moreover, defense hormones may perform antagonistic crosstalk with other developmental and environmental pathways and may even render plants more susceptible to other environmental stresses. For example, a recent study showed that treatment of Arabidopsis seedlings with JA results in long-lasting IR against herbivory but is associated with increased susceptibility to both necrotrophic and biotrophic pathogens (130). Therefore, caution is recommended when using hormone-mimicking compounds as IR agents, and the possibility of costs arising from reduced growth or increased susceptibility to other stresses must be considered. Overall, higher yield penalties are expected during IR compared with R gene strategies and pesticides (125). However, high pesticide doses may also lead to phytotoxic effects and have a negative impact on yield (131). Therefore, the adequate choice of IR stimuli, doses, and careful evaluation in the field may be essential before large-scale application. The innate plant immunity system comes with endogenous limitations. Internal feedback mechanisms and the interactions between primary and secondary metabolism engage to balance energy consumption. Consequently, only moderate levels of protection, typically ranging between 20% and 85% (132) and averaging around 40–60% (currently under study), can be achieved with IR. For farmers, the major goal of agriculture is economic benefit from yield. Therefore, yield reduction due to IR treatment can have a critical impact on agriculture, and farmers must consider the balance of cost and benefit when using IR to protect their crops.

Solution

A precise scientific assessment of fitness costs arising from the plants’ attempts to compensate for the growth penalty following IR must be established. Even if a growth penalty occurs, IR treatments can be adapted to avoid the reduction in benefit from economic loss caused by plant pathogens. However, should a growth penalty be expected in certain crops due to treatment with a specific elicitor, it could be countered and minimized by the concomitant application of other microbes or chemicals that promote crop growth.

Indeed, the induction of IR by well-selected bioactive compounds may also yield positive effects by increasing the photosynthesis and nutritional status of plants. For example, IR by natural compounds such as dehydroascorbic acid (DHA) and piperonylic acid (PA) positively affect plant growth and yield when applied in rice fields (133). Carboxylic acids have also been reported to induce resistance against fungal pathogens (134), and they also stimulate plant metabolism and photosynthesis (135) and promote the recruitment of beneficial microbiota (136). Similarly, the induction of IR by beneficial microbes is usually not associated with yield penalties, as microbes confer other benefits to the plant, such as improved nutrient acquisition and enhanced stress tolerance (Box 2). Indeed, numerous commercially available products categorized as biostimulants and biofertilizers, including diverse plant growth-promoting microorganisms, can trigger IR (Supplementary Table 1; Box 2).

Another strategy to improve overall efficacy and reduce the trade-off might be to combine multiple IR stimuli using different modes of action at subtoxic doses (137). Indeed, a combination of half-dose ASM and BABA exerted an additive effect, controlling Plasmopara viticola in grapevine (138). Similarly, a combination of MeJA and Trichoderma harzianum was more effective in controlling spot blotch than either treatment alone in bread wheat (139), and a combination of T. harzianum and ASM provided complete protection against gray mold in fava bean (140). Although these are examples of the use of multiple stimuli with additive or synergistic effects, careful selection of the compounds and doses is required to avoid growth penalties. For example, the drench application of BTH successfully protected pepper plants against Xanthomonas axonopodis pv. vesicatoria and cucumber mosaic virus but led to severe growth retardation and yield decrease. However, IR triggered by a combination of BTH and the PGPR strain Bacillus pumilus increased pepper IR capacity against both pathogens more effectively than individual treatments under field conditions and without any growth penalty (124).

Generating detailed insights into the mode of action of candidate IR stimuli is essential to support agricultural implementation and the design of adequate control strategies. Timing, dose, mode of application, and durability of the IR effect should be evaluated in laboratory experiments to allow adequate experimental design for field trials.

Inconsistency in induced resistance efficacy: external biotic/abiotic factors reduce induced resistance capacity

Limitation

The context-dependency of IR, namely the variability in IR efficacy relating to environmental and agronomic conditions, and phenological plant stages are limitations of IR that require further research.

Arguably, the most confounding factor in IR implementation in agronomy is the fact that environmental conditions can affect the general outcome of IR, leading to limited reproducibility of the resistance level achieved. For example, Walters et al. (141) showed that the efficacy of saccharin IR against Rhynchosporium secalis in barley depends on various parameters, including disease pressure. In addition, differences in effectiveness against different pathogen isolates have been reported (142), although the underlying reasons are not well understood.

IR is also dependent on the plant genotype. Several reports have shown that diverse cultivars of the same plant species can respond differently to IR stimuli. For example, the effects of induction treatment with INA or BTH differed among cucumber and soybean genotypes (143, 144). The efficiency of a combination of ASM, BABA, and cis-jasmonate in eliciting IR also varied among cultivars in barley against powdery mildew (Blumeria graminis) and leaf scald (Rhynchosporium secalis) in both controlled and field trials (145) and in tomato against Phytophthora (142). Similarly, some genotypes are more responsive to elicitation by beneficial microbes than others. Indeed, ISR has been shown to depend on the cultivar under laboratory and field conditions (146). Mycorrhiza-induced resistance (MIR) is also genotype-dependent and graft-transmissible, as reported for common bean and tomato (147), even though the mechanisms may differ depending on the plant genotype. For example, IR against powdery mildew was associated with epicuticular wax deposition and the overexpression of PR genes or with the accumulation of hormones and antimicrobial compounds in different grapevine cultivars (148).

The age of the treated plant also influences the efficacy of IR. As the growth season continues and the crop ages, plant defense mechanisms are expected to be induced by various natural stress factors to which the crop is inevitably exposed. This was contradicted by a study in potato showing that only approximately 30% of the field samples from Swedish wild and cultivated Solanum spp. expressed PR proteins (149). Indeed, the constitutive activation of plant defense is very energy-demanding for a plant and may reduce potential interactions with beneficial microbes. Nevertheless, young plants might benefit more from IR, as they lack age-related basal resistance. There is also evidence that the treatment of seedlings with IR agents can result in long-lasting IR, which is transmitted into newly formed leaves via epigenetic pathways (130, 150). Moreover, recent evidence has shown that the consistency and effect size of intergenerational acquired resistance (IAR) in Arabidopsis is higher upon induction treatment of young seedlings (151). Hence, the treatment of young plants under field conditions can be exploited as a preventive and durable method to enhance disease protection before pathogens can suppress immunity.

Biotic and abiotic contexts also contribute to the context dependency of IR under field conditions. Complex crosstalk occurs between abiotic and biotic stress signaling pathways in plants (152). For example, in Arabidopsis, elevated temperatures promote the expression of MYC2, a master positive regulator of JA signaling but a negative moderator of SA signaling (153). Thus, temperature is expected to modulate IR efficiency. Drought stress induces abscisic acid accumulation in multiple plants and is known to cause susceptibility to some pathogens (154, 155) but increase resistance to other pathogens (156). A thorough evaluation of how combined stresses affect plant immunity signaling and how defense signaling pathways interact and/or prioritize under realistic multi-stress conditions is needed, particularly in the current context of climate change (157).

Multiple lines of evidence indicate the effect of mineral nutrition on IR induction. Nutrient availability has been shown to affect plant susceptibility to pathogens, pests, and IR. For example, the enhanced resistance induced by mycorrhizal fungi in tomato against a fungal pathogen and a herbivorous insect was correlated with primed activation of defense genes, but this primed induction was dependent on the availability of nitrogen (158, 159) and phosphorus (160). Similarly, iron availability is also a key factor for IR (161). De Kesel et al. (32) demonstrated that diproline-induced IR is dependent on the iron supply in rice. Similar metabolites appear to accumulate in both IR and in the iron-deficient roots of dicots and monocots, and IR activation by soil-beneficial microbes requires some of the regulatory elements of iron-starvation responses [see (161) and the references therein, and (32)]. Similarly, BABA application and root colonization by some rhizosphere microbes not only led to broad-spectrum IR but also induced physiological and morphological root responses resembling those induced by iron deficiency [see (161) and references therein, and (162, 163)]. This apparent conserved convergence between nutrient deficiency responses and IR deserves further investigation; moreover, the information generated may provide the basis for fertilization recommendations to optimize MIR.

Solution

We propose combining immunological and ecological defense strategies by consolidating them within integrated pest management (IPM) programs. IPM has emerged in recent decades as an efficient and sustainable alternative to protect crops while minimizing environmental costs (164), and the IPM-framed combination of multiple methods can buffer the limitations imposed by the changing environmental conditions for IR (165).

Despite enormous research efforts into IPM, most approaches rely on the use of natural enemies to control pests; few studies have focused on the use of fungal or bacterial strains that inhibit parasites or compete for resources to control phytopathogenic microbes (166). The exploitation of plant immunity as a complementary strategy to be integrated with IPM remains unexplored. Moreover, IR can complement other biocontrol methods; for example, there are microbes that can directly antagonize pathogens, as in the case of the mycoparasitic fungi Trichoderma spp. and antibiotic-producing bacteria. In addition, these microbes can trigger IR, increasing the versatility and context stability of biocontrol inoculants (71). Recent studies suggest that plant immunity has the potential to strengthen IPM strategies in crops such as tomato (167, 168). The lack of research into the combination of IPM and IR is, in part, due to the complexity of studies analyzing the interplay between three or more interacting biological systems, i.e., the plant, the beneficial microorganism, and the pests (169). Research into dynamic multiway interactions revealed that plant immune responses are not fully conserved when interacting simultaneously with several organisms. Hence, studies in which IR is set in a multiway interaction context require a careful multifactorial design, which complicates the analysis and comprehension of the molecular mechanisms regulating plant immune responses.

Upon perceiving a herbivore attack, plants can release specific odors that attract natural enemies, helping them to get rid of the pest, a response referred to as a “cry-for-help” (170, 171). This is part of the immune response, known as indirect IR. Hence, a combination of evolutionarily acquired indirect resistance and the common release of natural enemies may exert synergistic benefits for the crop. Some recent studies have highlighted the potential of improving pest control using a combination of beneficial microbes and natural enemies. The inoculation of plants with beneficial fungi that trigger IR results in an enhanced attraction for natural enemies (172, 173). These results support the synergistic benefits of IR and IPM. Other studies illustrate even higher complexity, pointing to these interactions as additional valuable tools that contribute to crop protection. Groups of hemipteran insect families, such as Miridae and mites from the Phtyoseiidae family, can attack their prey as well as the host plant [zoophytophagous (173, 174)]. After the plant has been stimulated, it generates new waves of odors that complete additional layers of immunity, and the plant becomes more repellent. For example, plants with wounds induced by zoophytophagous mites are repellent to white fly pests (175), which is known as antixenosis.

Our understanding of how environmental factors negatively impact IR is substantially limited by a lack of research. The precise monitoring of the abiotic context and studies on their impact on IR can provide data to support mathematical modeling of the potential efficacy of IR in a given context.

Side effects and off-target effects of induced resistance

Limitation

Although the activation of IR can lead to broad-spectrum pest and disease resistance (176–178), increased susceptibility to IR has been observed in some studies. Walters et al. (145) reported that combinations of BTH, BABA, and cis-jasmone showed efficacy in the field for the control of barley infection by powdery mildew and leaf scald but enhanced barley susceptibility to Ramularia leaf spot. Similarly, although BTH induces resistance against Pseudomonas syringae in tomato, this was associated with increased susceptibility to Spodoptera exigua (179). In fields with multiple stress factors, this is an issue of concern.

Solution

The exploration of genetic variation may allow the selection of crop varieties expressing higher IR levels with minimal side effects on growth, interactions with beneficial organisms, and/or resistance to other biotic and abiotic stresses. They can be selected for conventional and genetic modification breeding schemes. The identification of key regulatory genes in model species allows their exploitation as breeding targets. For example, the discovery of the BABA receptor (IBI1) (150, 180, 181) and transporter (LHT1) (182) revealed that BABA-induced IR can be genetically uncoupled from the undesirable stress response to BABA, which relies on the protein kinase GCN2. As the IBI1, LHT1, and GCN2 genes are all highly conserved across taxonomically unrelated plant species, these genes can be used as breeding targets in crops to select varieties that require lower concentrations of BABA to reach economically satisfactory levels of disease protection with minimal side effects.

Unlocking the potential of induced resistance using epigenetics

The long-lasting effect of IR and its potential to be transmitted to subsequent generations is attributed to epigenetic reprogramming (Box 1). The role of epigenetic regulation in the plant response to pathogens is an emerging area recently used to elucidate plant immunity mechanisms (26). One of the most remarkable pieces of evidence linking epigenetic mechanisms with plant immunity can be demonstrated through the priming of the SA-dependent defense in Arabidopsis, where transcription-promoting modifications of the histone H3 tail in the promoters of SA-inducible defense genes are found (183, 184). These modifications facilitate the formation of open chromatin to allow for faster and/or stronger induction of defense genes (185). Dynamic and transient changes in genome-wide DNA methylation have also been observed upon the elicitation of IR in plants. DNA hypomethylation appears to be an early hallmark of plant defense activation during the onset of IR.

The descendants of IR-elicited plants exhibit IAR, in which plants remain less susceptible to pathogens (30, 32, 186). However, the mediators, target regions, and physiological consequences of the intergenerational maintenance of IR remain largely unknown. Although the exposure of epigenetically heritable IR phenomena to stress tends to be variable with relatively low effect sizes (31, 151), epigenetic modifications at the level of DNA methylation can provide almost complete disease protection that is metastable over multiple generations. The proof of concept for this approach comes from recent studies of epigenetic inbred lines (epiRILs) of Arabidopsis expressing disease resistance against virulent pathogens (60, 187). These epiRILs are genetically identical but vary in DNA methylation at transposable elements (188, 189). Moreover, the epigenetic quantitative trait loci mediating stably inherited resistance to downy mildew have been shown to act through the priming of pathogen-inducible defense genes without concomitant reductions in plant growth (60). Hence, the introduction of epigenetic variation into genetically identical crop inbred lines would facilitate the selection of meiotically stable IR phenotypes. Intriguingly, the loss of function of decrease in DNA methylation 1 (DDM1), a chromatin remodeler responsible for gene body methylation, was recently shown to lead to enhanced responsiveness to suboptimal doses of BABA (190). To advance the selection of epigenetically primed plant varieties, more precise and adjustable methods are required to introduce epigenetic variation into plant genomes. For example, the recent development of “reverse epigenetics” methods, such as the clustered regularly interspaced short palindromic repeats (CRISPR)-based multimodal targeting of chromatin remodelers, allows the precise modulation of IR-regulating epi-loci (191). Recently, an artificial zinc-finger fusion construct of various proteins involved in epigenetic regulation was demonstrated to direct gene silencing of specific target genes in Arabidopsis (22). Although translation to crop plants is still required, this could be of great value for the crop protection and breeding industry. This could also act as a valuable research tool to explore the complex mechanisms by which epigenetically altered genomes prime defense genes and mediate IR. Therefore, more detailed mechanistic studies are needed, not only to decipher the pathways by which plants acquire and maintain their epigenetic stress memory of IAR but also to understand how they erase these stressful memories. Insight into these epigenetic regulatory mechanisms will help improve the spectrum, effect size, and heritability of IR.

Concluding remarks

A series of hallmark events has accompanied the development of agriculture, from its infancy 12,000 years ago with continuous selection and breeding, through the improvement in yield using fertilizer and irrigation during the green revolution, the generation of crops with new attributes through transgenesis (GMOs), and the emergence of integrated pest management and crop improvements based on CRISPR-associated protein (CRISPR-Cas) technology, to utilizing IR to pathogens and pests, as presented in this review (Figure 4). IR offers a remarkable opportunity to support our agricultural system in an environment exposed to rapidly expanding challenges—not only those relating to climate change that favor the rapid spread of pests and emergence of new diseases but also in response to the rapidly changing socioeconomic environment. As scientists, we can investigate the mechanisms underlying IR, as outlined above, propose research, development, and technological advancements, and strive to obtain feedback from extension workers and farmers who are willing to try and implement IR technology.

Figure 4

Efforts should also be invested at the legislative level. Clear guidelines concerning the quality control and efficacy of marketed IR products must be established and harmonized across countries and continents. Implementing quality standards, for example, in terms of stability, inoculum quality in the case of microbes, efficacy, and shelf-life, is of utmost importance.

In the report, The future of crop protection in Europe (192), the European Union proposes IR as one of the options to support the sustainability of European farmers to work sustainably while securing food production, preserving biodiversity and the environment, and supporting farmers’ incomes. According to this report, the potential impacts of IR will be seen in crop yield, food security, and the competitiveness of EU farming. Similar initiatives are taking place in Asia and the United States (193).

Recently, it has also become apparent that there is a substantial added value for the application of IR technologies for improving the nutraceutical value of foods, which can confer medical or health benefits, for example, in obesity, metabolic syndrome, inflammation, diabetes, hypertension, cardiovascular diseases, and cancer, by increasing the levels of bioactive compounds in induced plants (115, 119, 194).

In summary, the elicitation of plant defenses can lead to the production of safe and high-quality food, which is an important societal issue facing high demand by both consumers and producers and, at the same time, reduce the possible negative effects of current agricultural practices on the environment.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fsci.2024.1407410/full#supplementary-material

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