Humboldt ReviewRecognition and defence of plant-infecting fungal pathogens
Introduction
For adapted fungal pathogens, plants represent a source of nutrients and provide a favourable environment for parasitic growth. In the past, plant breeders could only distinguish between crops displaying disease symptoms and those lacking symptoms upon pathogen attack. Today we know that when pathogens attempt host infection, they face the plant immune system. But even before the advent of modern genetics and molecular biology, phytopathologists had described the existence of variable races of fungal phytopathogens with differential infection phenotypes on individual host lines and had observed that radiation can affect disease outcomes by eliciting inheritable changes in host and pathogen genes (Anderson and Hart, 1956; Bridgmon and Wilcoxson, 1959; Caldecott et al., 1959; Flor, 1942, 1960). Because of their economic importance, studies of crops and crop pathogens were of particular interest in the middle of the 20th century. These studies led to the conceptualization and development of the first near-isogenic lines with specific resistance traits and ultimately the onset of cereal crop genetics (Briggle, 1969; Day, 1966; Dyck and Samborski, 1968; Flor, 1956; Moseman and Schaller, 1960).
The ability to genetically manipulate plants and the development of model plants later laid the groundwork for a clearer elucidation of what occurs at the molecular level when a plant becomes infected with fungi. The basic principles of molecular plant-microbe interactions were largely elucidated based on the results of studies from model plant-pathogen systems but are thought to be generally applicable to interactions between Triticeae and fungal pathogens.
It has been known for decades that fungal-derived components must be recognised by plant hosts as specific host responses elicited during infection were associated with reduced fungal proliferation (Esquerretugaye et al., 1979; Hadwiger and Beckman, 1980; Kogel, G. et al., 1988; De Wit and Roseboom, 1980). Some of these components, termed fungal elicitors, were biochemically purified and their actions on host cells further defined (De Wit and Kodde, 1981; Kogel, G. et al., 1991), and many of these molecules were shown to induce a host cell death response (Beardmore et al., 1983; De Wit et al., 1984; Mayama et al., 1986). Currently, microbial elicitors are generally divided into two classes. The first are so-called microbe- or pathogen-associated molecular patterns (M/PAMPs), which are molecules commonly released by a whole class of microbes including non-pathogens. The second class are referred to as effectors, which are specific to certain pathogen species or races and manipulate host components to promote the pathogen’s virulence (Jones and Dangl, 2006).
M/PAMPs are diverse molecules that include peptides and polysaccharide. M/PAMPs are usually recognised in the host apoplast through extracellular-facing transmembrane proteins such as receptor kinases (RLKs) and receptor-like proteins (RLPs) called pattern recognition receptors (PRRs) (Fig. 1) (Couto and Zipfel, 2016; Smakowska-Luzan et al., 2018). The fungal cell wall component chitin is a prominent example for a fungal M/PAMP (Felix et al., 1993; Kombrink et al., 2011; Kuchitsu et al., 1993). The first PRRs that sense chitin were isolated from Arabidopsis thaliana and rice (Kaku et al., 2006; Miya et al., 2007), and later, functional homologs were also identified in Triticeae (see section ‘Triticeae cell surface receptors that mediate Triticeae basal immunity to fungal parasites’ below). Detection of M/PAMPs by PRRs activates signal transduction across the plasma membrane and ultimately induces immune responses collectively called pattern-triggered immunity. One well-described immune response that is effective against fungal invaders involves the production and secretion of plant chitinases to limit fungal proliferation (Schlumbaum et al., 1986). Penetration of host cellular structures by fungal invaders may also be arrested by immune responses such as host cell wall strengthening including lignification and callose deposition (Bishop et al., 2002; Ellinger et al., 2013). Fungal attempts to penetrate host cells can also lead to the release of so-called damage-associated molecular patterns (DAMPs). DAMPs are host components released or produced and secreted upon cell or cell wall damage and are perceived by PRR-like proteins in the extracellular space leading to signalling outputs similar to PTI (Choi and Klessig, 2016). The perception of D/M/PAMPs may greatly contribute to resistance to infection by non-adapted pathogens (Niks and Marcel, 2009; Nürnberger and Lipka, 2005).
The fungal virulence factors now designated effectors are pathogen components that promote fungal proliferation on certain hosts (see section Effectors hijack Triticeae immunity and steer host physiology toward fungal accommodation’ below). Most effectors are proteinaceous or metabolites, and fungal effectors are sometimes described as toxins. The molecular functions of numerous fungal effectors in the host apoplast have been described in detail (He et al., 2020; Lo Presti et al., 2015), and the molecular principles underlying plant-microbe interactions suggest that at least some effectors target the microbial recognition machinery of the host downstream of D/M/PAMP recognition, i.e. they interfere with PTI (Dodds and Rathjen, 2010; Jones and Dangl, 2006). Effectors that activate cell death pathways to promote virulence have also been described, but these are specific to necrotrophic fungi, which benefit from dead host tissue (Tan et al., 2010; Wang et al., 2014a).
The localised host cell death also known as the hypersensitive response (HR) elicited during host infection with obligate biotrophic pathogens or by the infiltration of biotroph elicitors into host tissue is usually the result of effector recognition by host immune receptors encoded by host Resistance (R) genes (Cui et al., 2015; Dodds and Rathjen, 2010; Greenberg and Yao, 2004). The HR is likely heavily implicated in arresting the invasion of biotrophs because these pathogens strictly require living host cells for proliferation, as already speculated by Ward and Marshall in 1902 and Stakman in 1915 (Stakman, 1915; Ward, 1902). The termination of fungal infection by R protein function is known as race-specific resistance and also referred to as effector-triggered immunity (ETI) (Fig. 1). The genetic concept underlying ETI was first described by Harold Flor, who investigated the genetic basis of flax (Linum usitatissimum) resistance to the flax rust fungus Melampsora lini (Flor, 1942). Flor’s investigations led to development of the gene-for-gene theory, which stipulates that resistance to a specific pathogen isolate is determined by an R gene in the plant, and a corresponding Avirulence (Avr) gene in the pathogen (Flor, 1956). It has become clear that Avr genes usually encode effector proteins and that these effectors are secreted (Fig.1) by pathogens to promote pathogen proliferation on susceptible hosts e.g. to overcome basal host immune responses (i.e. PTI).
It is thought that the evolution of secreted effector proteins resembles an evolutionary response to plant basal immunity and further led to the evolution of plant R genes that often encode proteins for effector recognition (receptors). As such, the recognition specificities of R genes towards pathogen effectors and the resulting ETI are often considered an evolutionary countermeasure to adapted plant pathogens.
Because many R genes were found to encode nucleotide-binding leucine-rich repeat receptors (NB-LRRs or NLRs) the terms ‘R protein’ and ‘ETI’ are often used to specifically describe NLRs with recognition specificities towards intracellular effectors encoded at pathogen Avr genes. However, studies on the interaction of fungal pathogens of cereals and other crops have shown that R gene products are variable. For example, they can also encode receptors for the detection of apoplastic effectors (Fig.1) or have enzymatic activity that disables the virulence function of fungal effectors (e.g. detoxification of fungal toxins; see sections ‘Triticeae Resistance (R) gene products as sensors of fungal invasion’ and ‘Non-conventional Resistance genes, Susceptibility genes and major QTL’ below).
Here, we provide an overview of mechanisms underlying fungal defence in Triticeae. We highlight molecular principles of pathogen recognition and discuss advances in understanding fungal effector-mediated infection strategies. Finally, we summarize findings that give insight into how a Triticeae host terminates fungal infection. We apologize to those colleagues, who contributed to the field but whose publications have not been discussed here, because we aimed to condense available data to a digestible volume.
Section snippets
Triticeae cell surface receptors that mediate basal immunity to fungal parasites
Plants sense fungal pathogens at the cell surface/plasma membrane via PRRs (Fig. 1). Indeed, an immunogenic elicitor from Puccinia graminis f. sp. tritici was isolated already in the late 1980ies and found to specifically bind to the plasma membrane of wheat and barley cells (Kogel et al., 1988, 1991). In spite of this early demonstration, we still know relatively little about Triticeae cell surface PRRs. Some candidate PRRs have been identified in Triticeae. For instance, a candidate barley
Triticeae Resistance (R) gene products as sensors of fungal invasion
Specific lines of a certain host plant that completely lack or display only low susceptibility to an adapted pathogen are known as resistant. Already decades ago, breeding for resistant traits and the generation of near-isogenic cereal lines, also known as inbred or backcross lines, demonstrated that resistance traits can be dominantly or recessively inherited (Jorgensen, 1994; Keller et al., 2018). Mapping and cloning of dominantly inherited R genes and the molecular characterisation of their
Non-conventional resistance genes, susceptibility genes and major QTL
Although the modes of action of the majority of molecularly characterised R genes involve receptor-mediated recognition of a pathogen’s effector, genetic dissection of resistance traits has shown that a number of non-receptor-like coding R genes exist in nature (Table 3). Some of these confer gene-for-gene resistance, while others mediated broad-spectrum disease resistance. In addition, it has become clear that recessively inherited resistance traits are often associated with the disruption of
Effectors hijack Triticeae immunity and steer host physiology toward fungal accommodation
Fungal pathogens utilize so-called effector molecules to manipulate host functions for their own benefit (Fig. 1). The largest class of characterised effectors are probably effector proteins, but small RNAs and metabolites are also secreted during host infection and these molecules have been shown to act as virulence factors too.
Susceptibility factors, Achilles heels of triticeae crops
Our understanding of disease susceptibility has advanced greatly in the last 20 years and with that susceptibility became a target of breeding and targeted mutagenesis approaches (Büschges et al., 1997; Dangl et al., 2013; Engelhardt et al., 2018; Faris et al., 2010; Hückelhoven, 2005; Lapin and Van den Ackerveken, 2013; van Schie and Takken, 2014). Initially, this field of research was driven by forward genetic approaches that identified the genes underlying recessively inherited resistance
Cell autonomous and non-cell autonomous defence in Triticeae
Strikingly, we still only poorly understand what actually stops a fungus from growing on resistant plants. However, we know that tissue-wide resistance is achieved by a number of preformed metabolic antimicrobial compounds collectively called phytoanticipins (VanEtten et al., 1994). E.g. Benzoxazinoids (BXs) are phytoanticipins mostly found in grasses and their biosynthesis from indole has been thoroughly studied (Elnaghy and Shaw, 1966; Elnaghy and Linko, 1962; Niculaes et al., 2018). Biocidal
Future research
Our understanding of Triticeae pathology has advanced greatly in the last 30 years, progress, which has been largely facilitated by better genomic resources and the development of tools for functional genetics in small grain cereals (Alqudah et al., 2020; Feuillet et al., 2012; Hensel, 2020; Lin et al., 2020; Monat et al., 2019). Despite this, our mechanistic understanding of the factors that promote or hinder pathogen proliferation on a particular host genotype is still fragmented. We now have
Concluding remarks
More than hundred years of research on the interaction of fungal pathogens with Triticeae hosts revealed a treasure of fascinating mechanisms of host resistance to diseases caused by those fungi. We learned about host resistance genes, mechanisms of pathogen recognition, cellular and chemical defence. We have seen a major investment of society in supporting this research because the food supply threatened by pathogens and the biological principles underlying diseases are of socioeconomic and
CRediT authorship contribution statement
Isabel M.L. Saur: Conceptualization, Writing - original draft, Writing - review & editing. Ralph Hückelhoven: Conceptualization, Visualization, Writing - original draft, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
I.M.L.S. is supported by the Daimler and Benz Foundation. Projects in the R.H. lab have been recently supported by the German Research Foundation (SFB924, HU886/8, HU886/11), by the Bavarian State Ministry of the Environment and Consumer Protection (TGC01GCUFuE69781), by the BASF Plant Science GmbH and by German Ministry of Economics and Energy (AIF 17221 N).
References (240)
- et al.
GWAS: fast-forwarding gene identification and characterization in temperate cereals: lessons from barley - A review
J. Adv. Res.
(2020) - et al.
Cellular lignification as a factor in the hypersensitive resistance of wheat to stem rust
Physiol Plant Pathol.
(1983) - et al.
Changes in carbohydrate coordinated partitioning and cell wall remodeling with stress-induced pathogenesis in wheat sheaths
Physiol. Mol. Biol. Plants
(2002) - et al.
The barley Mlo gene: a novel control element of plant pathogen resistance
Cell
(1997) - et al.
Gene expression in Fusarium graminearum grown on plant cell wall
Fungal Genet. Biol.
(2008) - et al.
Structure and biosynthesis of benzoxazinoids: plant defence metabolites with potential as antimicrobial scaffolds
Phytochemistry
(2018) - et al.
Further characterization and cultivar-specificity of glycoprotein elicitors from culture filtrates and cell-walls of Cladosporium fulvum
Physiol. Plant Pathol.
(1981) - et al.
Isolation, partial characterization and specificity of glycoprotein elicitors from culture filtrates, mycelium and cell walls of Cladosporium fulvum
Phys. Plant Pathol.
(1980) - et al.
Plant genes hijacked by necrotrophic fungal pathogens
Curr. Opin. Plant Biol.
(2020) The complementary genic systems in flax and flax rust
Adv. Genet.
(1956)
All Roads Lead to Susceptibility: the many modes of action of fungal and oomycete intracellular effectors
Plant Communications
Genetic transformation of Triticeae cereals - summary of almost three-decade’s development
Biotechnol. Adv.
Powdery mildew susceptibility and biotrophic infection strategies
FEMS Microbiol. Lett.
Cell biology of the plant-powdery mildew interaction
Curr. Opin. Plant Biol.
Mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach
Plant Biotechnol. J.
The plasma membrane-an integrating compartment for mechano-signaling
Plants
Benzoxazinoid metabolites regulate mnnate mmmunity against aphids and fungi in maize
Plant Physiol.
Papillae and related wound plugs of plant cells
Ann. Rev. Phytopathol.
Multivesicular bodies participate in a cell wall-associated defence response in barley leaves attacked by the pathogenic powdery mildew fungus
. Cellular Microbiol
Effects of ionizing radiations on the host-parasite relationship of stem rust of wheat
Phytopathol.
Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions
Genome Biol.
Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways
Mol. Plant Pathol.
Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus
Proc. Natl. Acad. Sci. U. S. A.
Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project
BMC Plant Biol.
The multivesicular body-localized GTPase ARFA1b/1c is important for callose deposition and ror2 syntaxin-dependent preinvasive basal defense in barley
Plant Cell
The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species
Mol. Microbiol.
Dissection of cell death induction by wheat stem rust resistance protein Sr35 and its matching effector AvrSr35
Mol. Plant Microbe Interact.
Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew
Plant Cell
Avirulence genes in cereal powdery mildews: the gene-for-gene hypothesis 2.0
Front. Plant Sci.
The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat
Nat. Commun.
The effects of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe-graminis f. Sp. Hordei and host responses
Plant J.
A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen
Phytopathology
Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins
Plant J.
New races from mixtures of urediospores of varieties of Puccinia graminis
Phytopathology
Near‐isogenic Lines of wheat with genes for resistance to Erysiphe graminis f. Sp. Tritici
Crop Sci.
Coevolution and life cycle specialization of plant cell wall degrading enzymes in a hemibiotrophic pathogen
Mol. Biol. Evol.
QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review
Plant Breed.
Stem rust resistant variants in irradiated populations - mutations or field hybrids?
Agron. J.
The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding
Plant Cell
Two members of TaRLK family confer powdery mildew resistance in common wheat
BMC Plant Biol.
Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat
Science
DAMPs, MAMPs, and NAMPs in plant innate immunity
BMC Plant Biol.
Fungal plant cell wall-degrading enzyme database: a platform for comparative and evolutionary genomics in fungi and oomycetes
BMC Genomics
Differential accumulation of callose, arabinoxylan and cellulose in nonpenetrated versus penetrated papillae on leaves of barley infected with Blumeria graminis f. Sp. Hordei
New Phytol.
Down-regulation of the glucan synthase-like 6 gene (HvGsl6) in barley leads to decreased callose accumulation and increased cell wall penetration byBlumeria graminis f. sp. hordei
New Phytol.
The germinlike protein GLP4 exhibits superoxide dismutase activity and is an important component of quantitative resistance in wheat and barley
Mol. Plant Microbe Interact.
SNARE-protein-mediated disease resistance at the plant cell wall
Nature
Resistance to cereal rusts at the plant cell wall—what can we learn from other host-pathogen systems?
Australian J. Agricul. Research
Broad-spectrum acquired resistance in barley induced by the pseudomonas pathosystem shares transcriptional components with Arabidopsis systemic acquired resistance
Mol. Plant Microbe Interact.
Systemic acquired resistance
Plant Signal. Behav.
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