Plant Resistance Inducers (Pris): Perspectives for Future Disease Management in the Field
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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 Plant 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, plants 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 oomycetes [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 pathogens 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 pathogen 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 oomycete 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 potato fields lead to the same level of ASM, BABA and Cis-jasmonate, barley cultivars 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 tomato 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 Phytophthora infestans 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 Pseudomonas syringae 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 apple 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 gene expression 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–Botrytis cinerea pathosystem, behind IR in a multi-factor environment. In Table 1, we list epilines with reduced sensitivity to salicylic acid (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.