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Plant Resistance Inducers (Pris): Perspectives for Future Disease Management in the Field

Plant Resistance Inducers (Pris): Perspectives for Future Disease Management in the Field

CAB Reviews 2020 15, No. 001

Plant resistance inducers (PRIs): perspectives for future disease management in the field

M. Sandroni1, E. Liljeroth1, T. Mulugeta2 and E. Alexandersson1*

Address: 1 Department of Protection Biology, Swedish University of Agricultural Sciences, P.O. Box 102, 23053 Alnarp, Sweden. 2 Department of Biology, Kotebe Metropolitan University, 31248 Addis Ababa, Ethiopia.

*Correspondence: E. Alexandersson. Email: [email protected]

Received: 14 September 2019 Accepted: 4 November 2019 doi: 10.1079/PAVSNNR202015001

The electronic version of this article is the definitive one. It is located here: http://www.cabi.org/cabreviews

© CAB International 2020 (Online ISSN 1749-8848)

Abstract

Plants are confronted with numerous biotic stresses that may affect productivity. Besides their constitutive defence, can activate specific metabolic processes to enhance resistance upon stress detection. These defence mechanisms can also be activated through the recognition of plant resistance inducers (PRIs). This review highlights some of the current challenges that prevent the adoption of PRIs in agriculture, and explore research topics and knowledge gaps to be addressed for bringing PRIs closer to practice. First, we present studies on the variance of induced defence responses and examine the possibility of employing inducibility in breeding strategies as well as the possible role of epigenetics. We also discuss the efficiency of PRIs in future climate and knowledge gaps on this subject. Remote sensing, high-throughput phenotyping and modelling in combination with PRIs as part of decision support systems and integrated pest management are further possibilities to advance the use of PRIs. Finally, we discuss the challenges which need to be addressed to make PRIs available for small-scale farmers in low-income countries. Although PRIs have successfully presented significant rates of disease prevention under controlled conditions, converting these findings into field application still depends on more studies, e.g. on how they can be integrated into disease management programmes. Better mechanistic understanding of IR together with the coupling of PRIs to new disease monitoring and protection strategies can give PRIs a stronger role in future agricultural practice.

Keywords: Induced resistance (IR), Plant resistance inducers (PRIs), Inducibility, Plant breeding, Integrated pest management (IPM), Climate change

Review Methodology: We searched the following databases: CAB Abstracts, PubMed and Google Scholar. In addition, we used the references from the articles obtained by this method to check for additional relevant material.

Introduction defence against further attacks by a wide range of viruses, bacteria, fungi and [3], a process also known as Plants are constantly confronted with numerous biotic induced resistance (IR). IR is most commonly divided into stresses. In agriculture, pests and lead to systemic acquired resistance (SAR) and induced systemic crop losses between 20 and 30% annually [1]. To prevent resistance (ISR), and they mainly differ by the signalling infection, plants have developed an elaborate defence pathways and molecules through which local and systemic system that is activated upon the recognition of patho- defence are acquired. As signalling compounds and path- gen-associated molecular patterns (PAMPs) or ways may differ depending on the inducing agent, IR is often effectors, leading to PAMP-triggered immunity (PTI) classified more specifically, e.g. as wound-induced resist- and effector-triggered immunity (ETI), respectively [2]. ance [4], mycorrhiza-induced resistance [5–7] and Through PTI and ETI, plants can enhance their innate volatile-induced resistance [8–10].

http://www.cabi.org/cabreviews 2 CAB Reviews Plant resistance can also be induced through the we stress the importance of studying the efficiency of PRIs application of plant resistance inducers (PRIs), which can in future climate and a wider range of agricultural settings. be either chemical agents, extracts from plants or microbes The latter could be a step of introducing the use of PRIs by [11], or non-pathogenic microbes, including mycorrhizal small-scale farmers in low-income countries, the challenges fungi, plant growth-promoting rhizobacteria or fungi, of which we also discuss. These are all areas where more and other microbes used as biopesticides [12]. Moreover, scientific studies can help bring PRIs closer to agricultural IR may lead to the priming of cells, usually defined as practice, as shown in Figure 2. a memory state in which plants are capable of responding to post-challenge stresses more rapidly, and even in distal parts from the original stress. Among chemical PRIs, pota- Incorporating PRIs in Breeding Programmes ssium phosphite (Phi) and acibenzolar-S-methyl (ASM, also called benzothiadiazole or BTH) have been widely studied The possibility of breeding for improved IR response is a in controlled environments and, in fewer cases, in the field. recurrent topic [12], as it is clear now that responsiveness Phi has also a direct effect against mainly patho- to PRIs is dependent on many factors and varies according gens. For example, the use of Phi in combination with lower to the plant genotype. In a 3-year study using a combination doses of fungicides in fields lead to the same level of ASM, BABA and Cis-, showed of control of the full recommended dose of the same differences in IR against Rhynchosporium secalis and Blumeria fungicide against potato late blight over 4 years of study graminis f. sp. hordei in controlled environment and field [13]. BABA-IR is the elicited systemic defence triggered by conditions [28]. Inducibility may also depend on the patho- β-aminobutyric acid (BABA). It has been known to induce gen strain. When applying BABA on accessions, resistance since 1963, but mostly studied and applied as inducibility varied significantly not only among genotypes a chemical inducer in the past two decades [14]. BABA but also depended on the isolate of was recently found to be produced endogenously in used [29], which adds to the complexity of conducting plants [15], but as a plant metabolite, it was shown to be these studies. This will be a definite challenge if IR will be tissue-specific and accumulate locally [16]. included as a future target in breeding programmes. Numerous studies and reviews are available on the The stimulation of defence responses has been observed use of PRIs for inducing and priming resistance in plants not only in crops and model species, but also in wild [12, 17–22]. The use of resistance inducers, however, is not relatives [30], and domestication resulted in the loss of sufficient for full control of plant diseases as their efficacy both basal and IR in some crops. The effects of ASM on wild depends on several factors [11], which also regularly and commercial accessions of common beans (Phaseolus lead to inconsistent results under field conditions [17]. vulgaris) against pv. syringae and Nonetheless, recent ‘-omics’ approaches are generating Enterobacter sp. strain FCB1 showed that wild accessions data on the effects of PRIs on plant proteome, transcrip- had a higher basal defence and IR when compared to the tome and metabolome [11, 21], elucidating, piece by piece, commercial cultivars [31]. Moreover, ASM treatment the complex signalling network behind IR. For example, increased the susceptibility against Enterobacter sp. strain recent studies demonstrated that Phi altered the abundance FCB1 on the commercial genotypes. Another concern is of 60 metabolites in potato [23] and ASM significantly how to screen and select for higher inducibility as there is a reprogramed transcriptome towards resistance to lack of standardized procedures. The possibility of using the aphid Dysaphis plantaginea [24]. ASM and chitosan were transcript markers has been lifted and apple cultivars were responsible for the differential expression of 5062 and 5210 monitored for their varying ability to respond to PRIs [32]. genes in strawberry [25], respectively, and BABA affected Breeding for a targeted defence response pathway could the transcriptome and increased the abundance of many be an alternative. For example, Arabidopsis overexpressing defence-secreted proteins in potato [26]. Primed plants the defence gene NIM1 encoding the signalling protein may have little energetic trade-offs and subtle changes in NPR1, presented higher responsiveness to the application the phenotype as defence signalling is not expressed con- of ASM [33]. stitutively. Inside the plant, however, significant reprogram- The advance of epigenetics provides the possibility ming to elicit defence responses is observed. of tailoring and developing stable and, Although some experiments conducted under field perhaps, heritable plant material with no change in the conditions presented enhanced resistance, further studies genetic composition [34]. In a laboratory and greenhouse are needed to better explain the molecular mechanisms study on the Brassica napus– pathosystem, behind IR in a multi-factor environment. In Table 1, we list epilines with reduced sensitivity to (SA) field studies conducted with PRIs during the last 10 years, were developed and successfully increased resistance which complements the previous list published in 2007 against B. cinerea [35]. SA pathway induces a hypersensitive [27]. The focus of this review is to provide an overview response that favours infection and interacts antagonisti- of challenges that currently prevent a broader use of PRIs cally with JA pathway, responsible for controlling this in breeding and IPM strategies, and to summarize their necrotrophic pathogen. The possibility of developing lines advantages and future applications (Figure 1). Furthermore, with altered expression of genes of specific defence

http://www.cabi.org/cabreviews Table 1 List of plant resistance inducers (PRIs) tested in the field in the past 10 years including comments on their effects Crop PRI Effects/results References Apple Acibenzolar-S-methyl A light IPM strategy involving ASM and application allowed some control of caused by [32] Venturia inaequalis at the end of primary contamination, which reduced the incidence of the disease at harvest. It reduced the number of pesticide applications when compared to regular IPM strategy. Phosphite Reduced apple scab (V. inaequalis) for all PRIs, increased leaf chlorophyll content and fruit yield for all PRIs. [63] Salicylic acid derivative Results were not as positive as a conventional pesticide used (Penconazole). Harpin protein Acibenzolar-S-methyl Reduction of blossom and shoot blight symptoms caused by Erwinia amylovora. Trunk injection of ASM and [64] phosphite KPhi induced PR-1, PR-2, and PR-8, and defence compounds were synthetized and accumulated in the canopy. Barley Acibenzolar-S-methyl Control of Rhynchosporium secalis and f. sp. Hordei by a combination of PRIs depended on [28] β-aminobutyric acid the , and cultivar inconsistency observed between years. PRIs had no effect on grain yield in most Cis-jasmone cases. Analysis of a defence-related enzyme suggested plants were already induced. Acibenzolar-S-methyl Partially effective or ineffective control of B. graminis f. sp. Hordei and Rhynchosporium commune by a [65] β-aminobutyric acid combination of PRIs. Effective and consistent control of co-application of PRIs and fungicide, but almost no Cis-jasmone difference from fungicide alone. Citrus β-aminobutyric acid Reduced disease severity of citrus Huanglongbing caused by Candidatus Liberibacter spp., and reduced [66]

http://www.cabi.org/cabreviews Acibenzolar-S-methyl bacterial population growth. 2,6-dichloroisonicotinic acid Common bean Acibenzolar-S-methyl Reduction of the number of lesions caused by Pseudomonas syringae pv. syringae in one wild accession and [31] one landrace. Higher resistance against Enterobacter FCB1 in wild accessions, but increased susceptibility in cultivars. Cotton Acibenzolar-S-methyl Salicylic acid Different combinations of PRIs and biological control agents (BCA) reduced the incidence of Fusarium [67] oxysporum and debaryanum, increased the rate of seed germination compared to infected control, and increased phenolic content. Grapevine Chitosan Increased plant recovery from yellows caused by the phytoplasma Flavescence dorée (FD) and Bois noir (BN), [68] 3 Alexandersson E. Mulugeta, T. Liljeroth, E. Sandroni, M. Phosetyl-Al and decreased the incidence of symptomatic plants by the end of the two-year field experiment. Glutathione + Oligosaccharines Acibenzolar-S-methyl Oilseed rape Acibenzolar-S-methyl PRIs combination significantly controlled light leaf spot caused by Pyrenopeziza brassicae. Equally or more [69] β-aminobutyric acid effective than fungicides in the first year, but equally or less effective than fungicide in the second. No Cis-jasmone significant effect on yield in both years. Pear Phosphite Reduced pear scab (Venturia pirina) severity for all PRIs, increased leaf chlorophyll content and fruit yield for all [63] Salicylic acid derivative PRIs. Results were not as positive as a conventional pesticide used (Penconazole). Harpin protein Pepper Acibenzolar-S-methyl ASM induced resistance against axonopodis pv. vesicatoria and primed the gene CaPR4 for 20 [70] days. Treated plants also presented less symptoms of naturally occurring Cucumber Mosaic Virus (CMV). Acibenzolar-S-methyl Combined treatment of PRI and the plant growth promoting rhizobacteria (PGPR) Bacillus pumilus INR7 had an [71] Bacillus pumilus INR7 additive effect against X. axonopodis pv. Vesicatoria, increased expression of defence marker genes CaPR1, CaTin1, and CaPR4, and showed no growth repressing effect from ASM. Potato β-aminobutyric acid Lower dose of fungicide with BABA showed similar control of P. infestans as recommended fungicide dose. [72] Reduced fungicide dose alone did not present the same efficiency. Potassium phosphite Co-application of potassium phosphite and lower dose of fungicide reduced the severity of late blight [13] (P. infestans) at leaves and tubers at similar levels to recommended fungicides. Phosphite Reduced around 50% of the lesion size on tubers caused by Phytophthora infestans, Fusarium solani and [73] Erwinia carotovora.ForP. infestans, increased levels of , , peroxidase (POD) and oxidase (PPO) activity. Increased tuber yield only in the first year. Potassium phosphite Application to seed tuber and foliage increased defence responses against Fusarium solani: higher pectin [74] content in tuber tissues, higher activity and content of polygalacturonase and proteinase inhibitor, and new isoform of chitinase found. 4 CAB Reviews pathways is not only promising for the development of pathogen-specific resistant plants but also for designing lines with higher responsiveness to PRIs. [77] [37] [78] [76] [71] References [75] [37] Selecting for IR is promising, as it might be less likely for pathogens to overcome IR in comparison to resistance expressed constitutively by the plant based on single genes. Even though, the prospect of pathogens developing pv. resistance against IR needs further study. Recently, differ- ences in sensitivity of P. infestans strains towards the PRI Phi were reported in two independent studies [36, 37]. This resistance is related to the direct toxicity of Phi rather than its IR effect. Still, resistance development could, in X. axonopodis in two locations. Improved the specific case of phosphite, become a non-desired side-effect. Bringing resistance inducibility towards the focus of breeders will continue to be a challenge as more infor- mation is needed on the trade-offs of inducing resistance and how to overcome inconsistencies of PRIs efficacy [38].

in all three years of the study, with ASM being Furthermore, the stability of epigenetic inheritance of the resistance phenotype needs to be considered, although tritici both in tuber and foliage in the two years of the in the three years of the experiment. Combination of in the three years of the experiment. Combination of transgenerational stability was observed with vegetative and suppression of lesions on foliage and fruits.

f. sp. propagation and, to some extent, self-fertilization [35]. Finally, more mechanistic studies are needed on epigenetic infestans

tomato changes affecting disease resistance as the alteration of . P P. infestans P. infestans

pv. specific signalling pathways may result in undesirable cross- talks and increase the crop susceptibility to non-targeted pathogens. The advance of molecular network modelling of

Blumeria graminis crops and model plants can help elucidate the complexity of plant–pathogen interactions and propose specific hypo- theses of signalling mechanisms that can be implemented in breeding strategies [39]. Pseudomonas syringae IR in Future Climates

The effect of climate change on plant protection strategies has recently received considerable interest [40]. Higher temperatures, altered water availability leading to changed Increased efficiency in diseaseASM, control copper, with and pre-treatment mancozeb of ASM compared to in only nurseries prior field to applications. field co-applications of half-dose of phosphite withfungicide. half-dose of fungicide was not significantly different than recommended dose of the most efficient. plant height, increased numberphenylalanine of ammonia pods lyase per (PAL) plant, activity, increased and seed increased yield, phenolic increased content. POD, PPO, and vesicatoria compared to individual applications. experiment, and increased tuber yield. half-dose of phosphite withfungicide. half-dose of fungicide was not significantly different than recommended dose of All PRIs decreased the infection of Combined treatment had exhibited induced resistance, but no additive effect against humidity as well as increased levels of CO2 will affect both the geographical distribution of pests and pathogens and how plants and pathogens interact since these environ- mental factors will influence the plants’ physiology including the innate . For example, it has been shown

INR7) that growing plants in increased CO2 levels lead to less infection by some strains of the oomycetes Peronospora machurica and P. infestans in and potato, respect- ively [41, 42]. Since PRIs work by activating the plants’ own defence system and often impose a mild stress reaction, e.g. as Bacillus pumilus supposed upon Phi treatment [43], it is likely that the effectiveness of PRIs is altered due to the change in stress Phosphite Reduced the severity of late blight caused by Salicylic acid Plant extracts PGPR ( Phosphite Suppression of late blight severity caused by Phosphite Reduced the severity of late blight caused by reactions due to climate change. A deeper understanding of the in planta mechanisms triggered by PRIs and how they

(Continued) lead to resistance in expected future climates will be rele- vant to further develop and apply PRIs in agriculture. So far, few studies have explored the effects of changing Acibenzolar-S-methyl TobaccoTomato Acibenzolar-S-methyl Acibenzolar-S-methyl Effective control of Table 1 Crop PRI Effects/results Soybean Acibenzolar-S-methyl Reduced incidence of damping-off and wilt severity caused by climate conditions on the plant innate immunity, and

http://www.cabi.org/cabreviews M. Sandroni, E. Liljeroth, T. Mulugeta, E. Alexandersson 5

Figure 1 Challenges, knowledge gaps, advantages and future applications of plant resistance inducers (PRIs) in the field.

Figure 2 Future research perspectives for integrating plant resistance inducers (PRIs) in IPM and breeding strategies for enhancing plant defence mechanisms. whether an altered climate condition is reflected in the expression in Arabidopsis and tomato even if there was expression of defence genes in the plant is varying between a change in host resistance [44, 45]. However, other reports. For example, after elevated CO2, there was no common marker transcripts for stress signalling changed marked difference in pathogenesis-related protein 1 (PR1) [44]. There are a few studies on the effect of PRI treatments

http://www.cabi.org/cabreviews 6 CAB Reviews and combinatorial abiotic and biotic stresses. In tomato, with suitable regulatory frameworks, integrated pest BABA was still very effective when plants were subjected to management (IPM) and the development of precision a mild salt stress before B. cinerea infection [46]. In agriculture based on technical advances such as advanced grapevine, the effects of heat and drought on ISR triggered remote sensing. Aligning these areas is a long-term effort, by Trichoderma harzianum T39 revealed an attenuated effect and there are significant challenges. on the expression of defence genes, which was in line with a We will not discuss the regulatory framework in this decreased level of Trichoderma-protection against downy review, but note that PRIs can be registered as several mildew [47]. different types of agents. Since PRIs work through an Even if there is an absence of studies on PRIs’ effec- indirect mode of action, many should fall into the category tiveness in future climate scenarios, several studies show an of low-risk plant protection products [55]. impact of altered environmental factors on both PTI and Phenotyping of plants is an emerging field for both ETI. There are several reports that humidity influences breeding and precision agriculture [56]. It is likely to play the effectiveness of PTI [40]. Humidity levels in the host an essential role in the future both for efficient screening are even manipulated by effectors secreted by the bacteria of inducibility of resistance in plant breeding and provide Pseudomonas to establish an aqueous apoplast as part of valuable information for precision agriculture. For the the bacteria’s infection strategy [48]. Furthermore, whereas latter, early detection of disease is critical, and the prospect increased temperature can have a positive effect on PTI of also including other tools such as weather-based pre- signalling, it might have a negative effect on ETI [49]. One dictions of disease as part of a more comprehensive reason possibly explaining the negative effect on ETI is decision support system (DSS) could be a way to establish the change of subcellular locations of R-gene products the use of PRIs. In order to refine the timing of inducing upon increased temperatures [50]. Elevated CO2 has been resistance by PRIs, automated disease detection is essential. shown to have a varying effect on PTI and decrease ETI. In Efficient monitoring is also of great importance for Medicago truncatula, the altered efficiency of PTI and ETI IPM where consideration on the effect of the application of resistance against pea aphids due to increased CO2 was PRIs on natural enemies, beneficial microbiota and other suggested to be mediated through the changed expression living biocontrol agents needs to be taken into account of a heat shock protein 90 [51]. [57, 58]. To date, there is a lack of studies of the effects Studies on the possible effects of elevated CO2 on the of PRIs and the defence status of the plant on the micro- efficiency of PRIs are lacking. These can fairly easily be con- biome, and here clearly more basic research is needed to ducted in controlled greenhouse conditions, but for observ- understand the effects of IR and host resistance in an ations more relevant for agricultural applications, they agro-ecological context. We have previously shown that should be carried out by free-air concentration enrichment the application of Phi did not affect the presence of a (FACE) experiments in order to be able to elevate the beneficial insect biocontrol of potato tuber in field CO2 levels in the field with natural multi-stress and light conditions [59]. conditions. There have been efforts in modelling the effects of IR by expanding epidemiological models to account for the transient nature of IR, and the fact that plants will revert Could PRIs Become an Affordable Alternative for to be susceptible again a certain time after the application Small-Scale Farmers in Low-Income Countries? of PRIs [52]. Future modelling efforts could also take scenarios with climate change into account. The overall market of biostimulants, where many PRIs fall, One challenge which needs more attention is whether is increasing in the developed world and was estimated to we can expect rapid adaptations of pathogens to future be €800 million in Europe in 2018 [60]. This is in stark climates. For example, isolates of P. infestans from different contrast to the market in the Middle East and Africa climate zones show local adaptation to temperature [53]. estimated to be only $70 million in 2016 [61]. Thus, In wheat, there are indications that Fusarium graminearum currently, chemical are used as a major tool for and Zymoseptoria tritici acclimatized to elevated CO2 better pest and disease control for farming in developing countries than resistant wheat lines, which led to more severe disease when affordable. [54]. Thus, we need to assess the effects in both host and For farming in Africa, studies have shown promising pathogen and use this combined knowledge to design results of PRIs even though the number of studies is limited protection strategies. [58]. Recently, we showed that late blight infestation in potato and tomato plants under field conditions in Ethiopia was reduced by Phi as much as by the conventional fungi- Incorporating PRIs in Precision Agriculture cide RidomilGold™. Even more importantly as of afford- and IPM ability for resource-poor farmers, a yield-to-cost analysis part of this study found Phi to be cheaper than the con- The incorporation of PRIs as a common practice in plant ventional fungicide. Still, PRIs are often expensive and even protection is complex and will need to go hand-in-hand if in some cases cheaper than conventional pesticides, they

http://www.cabi.org/cabreviews M. Sandroni, E. Liljeroth, T. Mulugeta, E. Alexandersson 7 are still unaffordable to smallholder farmers in low-income the points to tackle for bringing PRIs closer to practice as countries [37]. they can form an important part for reducing pesticide There are additional issues to be considered before usage and prevent crop losses to insect pests and resource-poor farmers could benefit from PRIs. To start phytopathogens. with, farmers’ acceptance of new protection strategies is one of the reasons for limited utilization [62]. Secondly, PRI and extensive knowledge of timing and technique for application are needed to make them a viable option [12]. References Thirdly, distribution chains, storage capacity and appro- 1. Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, priate conditions to maintain efficiency and be able to reach Nelson A. 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