Plant plasma membrane-bound receptors with extracellular lysin motif (LysM) domains participate in interactions with microorganisms. In Medicago truncatula, the LysM receptor-like kinase gene nodulation (Nod) factor perception (NFP) is a key gene that controls the perception of rhizobial lipochitooligosaccharide (LCO) Nod factors for the establishment of the Rhizobium–legume symbiosis. In this article, we review recent data that have refined our understanding of this function and that have revealed a role for NFP in the perception of arbuscular mycorrhizal (AM) symbiotic signals and plant pathogenic microorganisms. The dual role of NFP in symbiosis and immunity suggests that this receptor protein controls the perception of different signals and the activation of different downstream signalling pathways. These advances provide new insights into the evolution and functioning of this versatile plant protein.
The cellulose binding elicitor lectin (CBEL) of the genus Phytophthora induces necrosis and immune responses in several plant species, including Arabidopsis thaliana. However, the role of CBEL-induced responses in the outcome of the interaction is still unclear. This study shows that some of CBEL-induced defence responses, but not necrosis, required the receptor-like kinase BAK1, a general regulator of basal immunity in Arabidopsis, and the production of a reactive oxygen burst mediated by respiratory burst oxidases homologues (RBOH). Screening of a core collection of 48 Arabidopsis ecotypes using CBEL uncovered a large variability in CBEL-induced necrotic responses. Analysis of non-responsive CBEL lines Ws-4, Oy-0, and Bla-1 revealed that Ws-4 and Oy-0 were also impaired in the production of the oxidative burst and expression of defence genes, whereas Bla-1 was partially affected in these responses. Infection tests using two Phytophthora parasitica strains, Pp310 and Ppn0, virulent and avirulent, respectively, on the Col-0 line showed that BAK1 and RBOH mutants were susceptible to Ppn0, suggesting that some immune responses controlled by these genes, but not CBEL-induced cell death, are required for Phytophthora parasitica resistance. However, Ws-4, Oy-0, and Bla-1 lines were not affected in Ppn0 resistance, showing that natural variability in CBEL responsiveness is not correlated to Phytophthora susceptibility. Overall, the results uncover a BAK1- and RBOH-dependent CBEL-triggered immunity essential for Phytophthora resistance and suggest that natural quantitative variation of basal immunity triggered by conserved general elicitors such as CBEL does not correlate to Phytophthora susceptibility.
Mathieu Larroque, Elodie Belmas, Thomas Martinez, Sophie Vergnes, Nathalie Ladouce, Claude Lafitte, Elodie Gaulin, and Bernard Dumas
The pleiotropic drug resistance (PDR) proteins belong to the super-family of ATP-binding cassette (ABC) transporters. AtPDR8, also called PEN3, is required for penetration resistance of Arabidopsis to nonadapted powdery mildew fungi. During fungal infection, plasma-membrane-localized PEN3 is concentrated at fungal entry sites, as part of the plant's focal immune response. Here, we show that the pen3mutant is compromised in resistance to the bacterial pathogenPseudomonas syringae pv. tomato DC3000. P. syringae pv. tomatoDC3000 infection or treatment with a flagellin-derived peptide, flg22, induced strong focal accumulation of PEN3-green fluorescent protein. Interestingly, after an initial induction of PEN3 accumulation, P. syringae pv. tomato DC3000 but not the type-III-secretion-deficient mutant hrcC could suppress PEN3 accumulation. Moreover, transgenic overexpression of the P. syringae pv. tomato DC3000 effector AvrPto was sufficient to suppress PEN3 focal accumulation in response to flg22. Analyses of P. syringae pv. tomato DC3000 effector deletion mutants showed that individual effectors, including AvrPto, appear to be insufficient to suppress PEN3 accumulation when delivered by bacteria, suggesting a requirement for a combined action of multiple effectors. Collectively, our results indicate that PEN3 plays a positive role in plant resistance to a bacterial pathogen and show that focal accumulation of PEN3 protein may be a useful cellular response marker for theArabidopsis–P. syringae interaction.
Toll/interleukin receptor (TIR) domain-containing proteins encoded in the Arabidopsis (Arabidopsis thaliana) genome include the TIR-nucleotide binding site (TN) and TIR-unknown site/domain (TX) families. We investigated the function of these proteins. Transient overexpression of five TX and TN genes in tobacco (Nicotiana benthamiana) induced chlorosis. This induced chlorosis was dependent on ENHANCED DISEASE RESISTANCE1, a dependency conserved in both tobacco and Arabidopsis. Stable overexpression transgenic lines of TX and TN genes in Arabidopsis produced a variety of phenotypes associated with basal innate immune responses; these were correlated with elevated levels of salicylic acid. The TN protein AtTN10 interacted with the chloroplastic protein phosphoglycerate dehydrogenase in a yeast (Saccharomyces cerevisiae) two-hybrid screen; other TX and TN proteins interacted with nucleotide binding-leucine-rich repeat proteins and effector proteins, suggesting that TN proteins might act in guard complexes monitoring pathogen effectors.
Raja Sekhar Nandety, Jeffery L. Caplan, Keri Cavanaugh, Bertrand Perroud, Tadeusz Wroblewski, Richard W. Michelmore, and Blake C. Meyers
Stripe rust caused by the fungus Puccinia striiformis f.sp. tritici (Pst) is a major constraint to wheat production worldwide. The molecular events that underlie Pst pathogenicity are largely unknown. Like all rusts, Pst creates a specialized cellular structure within host cells called the haustorium to obtain nutrients from wheat, and to secrete pathogenicity factors called effector proteins. We purified Pst haustoria and used next-generation sequencing platforms to assemble the haustorial transcriptome as well as the transcriptome of germinated spores. 12,282 transcripts were assembled from 454-pyrosequencing data and used as reference for digital gene expression analysis to compare the germinated uredinospores and haustoria transcriptomes based on Illumina RNAseq data. More than 400 genes encoding secreted proteins which constitute candidate effectors were identified from the haustorial transcriptome, with two thirds of these up-regulated in this tissue compared to germinated spores. RT-PCR analysis confirmed the expression patterns of 94 effector candidates. The analysis also revealed that spores rely mainly on stored energy reserves for growth and development, while haustoria take up host nutrients for massive energy production for biosynthetic pathways and the ultimate production of spores. Together, these studies substantially increase our knowledge of potential Pst effectors and provide new insights into the pathogenic strategies of this important organism.
Genome Sequences of Pseudomonas spp. Isolated from Cereal CropsDonald M. Gardiner, Jiri Stiller, Lorenzo Covarelli, Magdalen Lindeberg, Roger G. Shivas, and John M. MannersGenome Announc. May/June 2013 1:e00209-13; doi:10.1128/genomeA.00209-13http://genomea.asm.org/content/1/3/e00209-13.abstract.html
Complete Genome Sequence of Xanthomonas citri subsp. citri Strain Aw12879, a Restricted-Host-Range Citrus Canker-Causing Bacterium
The phytopathogenic bacterium Xanthomonas campestris pv. vesicatoria (Xcv) requires type III effector proteins (T3Es) for virulence. After translocation into the host cell, T3Es are thought to interact with components of host immunity to suppress defence responses. XopJ is a T3E protein from Xcv that interferes with plant immune responses; however, its host cellular target is unknown. Here we show that XopJ interacts with the proteasomal subunit RPT6 in yeast andin planta to inhibit proteasome activity. A C235A mutation within the catalytic triad of XopJ as well as a G2A exchange within the N-terminal myristoylation motif abolishes the ability of XopJ to inhibit the proteasome. Xcv ΔxopJ mutants are impaired in growth and display accelerated symptom development including tissue necrosis on susceptible pepper leaves. Application of the proteasome inhibitor MG132 restored the ability of the Xcv ΔxopJ to attenuate the development of leaf necrosis. The XopJ dependent delay of tissue degeneration correlates with reduced levels of salicylic acid (SA) and changes in defence- and senescence-associated gene expression. Necrosis upon infection with Xcv ΔxopJ was greatly reduced in pepper plants with reduced expression of NPR1, a central regulator of SA responses, demonstrating the involvement of SA-signalling in the development of XopJ dependent phenotypes. Our results suggest that XopJ-mediated inhibition of the proteasome interferes with SA-dependent defence response to attenuate onset of necrosis and to alter host transcription. A central role of the proteasome in plant defence is discussed.
The bacterium Xanthomonas campestris is an economically important pathogen of many crop species and a model for the study of bacterial phytopathogenesis. In X. campestris, a regulatory system mediated by the signal molecule DSF controls virulence to plants. The synthesis and recognition of the DSF signal depends upon different Rpf proteins. DSF signal generation requires RpfF whereas signal perception and transduction depends upon a system comprising the sensor RpfC and regulator RpfG. Here we have addressed the action and role of Rpf/DSF signalling in phytopathogenesis by high-resolution transcriptional analysis coupled to functional genomics. We detected transcripts for many genes that were unidentified by previous computational analysis of the genome sequence. Novel transcribed regions included intergenic transcripts predicted as coding or non-coding as well as those that were antisense to coding sequences. In total, mutation of rpfF, rpfG and rpfC led to alteration in transcript levels (more than fourfold) of approximately 480 genes. The regulatory influence of RpfF and RpfC demonstrated considerable overlap. Contrary to expectation, the regulatory influence of RpfC and RpfG had limited overlap, indicating complexities of the Rpf signalling system. Importantly, functional analysis revealed over 160 new virulence factors within the group of Rpf-regulated genes.
Shi-Qi An, Melanie Febrer, Yvonne McCarthy, Dong-Jie Tang, Leah Clissold, Gemy Kaithakottil, David Swarbreck, Ji-Liang Tang, Jane Rogers, J. Maxwell Dow, Robert P. Ryan
Ralstonia solanacearum is a soil-borne bacterium causing the widespread disease known as bacterial wilt. Ralstonia solanacearum is also the causal agent of Moko disease of banana and brown rot of potato. Since the last R. solanacearum pathogen profile was published 10 years ago, studies concerning this plant pathogen have taken a genomic and post-genomic direction. This was pioneered by the first sequenced and annotated genome for a major plant bacterial pathogen and followed by many more genomes in subsequent years. All molecular features studied now have a genomic flavour. In the future, this will help in connecting the classical field of pathology and diversity studies with the gene content of specific strains. In this review, we summarize the recent research on this bacterial pathogen, including strain classification, host range, pathogenicity determinants, regulation of virulence genes, type III effector repertoire, effector-triggered immunity, plant signalling in response to R. solanacearum, as well as a review of different new pathosystems.
Bacteria; Proteobacteria; β subdivision; Ralstonia group; genus Ralstonia.
Ralstonia solanacearum is the agent of bacterial wilt of plants, characterized by a sudden wilt of the whole plant. Typically, stem cross-sections will ooze a slimy bacterial exudate. In the case of Moko disease of banana and brown rot of potato, there is also visible bacterial colonization of banana fruit and potato tuber.
As a soil-borne pathogen, infected fields can rarely be reused, even after rotation with nonhost plants. The disease is controlled by the use of resistant and tolerant plant cultivars. The prevention of spread of the disease has been achieved, in some instances, by the application of strict prophylactic sanitation practices.
Schornack et al. (2013) [in advance version, changes will occur]
Transcription activator-like (TAL) effectors are encoded by plantpathogenic bacteria and induce expression of plant host genes. TAL effectors bind DNA on the basis of a unique code that specifies binding of amino acid residues in repeat units to particular DNA bases in a one-to-one correspondence. This code can be used to predict binding sites of natural TAL effectors and to design novel synthetic DNA-binding domains for targeted genome manipulation. Natural mechanisms of resistance in plants against TAL effector–containing pathogens have given insights into new strategies for disease control.
Plants are sessile organisms that are under constant attack from microbes. They rely on both preformed defenses, and their innate immune system to ward of the microbial pathogens. Preformed defences include for example the cell wall and cuticle, which act as physical barriers to microbial colonization. The plant immune system is composed of surveillance systems that perceive several general microbe elicitors, which allow plants to switch from growth and development into a defense mode, rejecting most potentially harmful microbes. The elicitors are essential structures for pathogen survival and are conserved among pathogens. The conserved microbe-specific molecules, referred to as microbe- or pathogen-associated molecular patterns (MAMPs or PAMPs), are recognized by the plant innate immune systems pattern recognition receptors (PRRs). General elicitors like flagellin (Flg), elongation factor Tu (EF-Tu), peptidoglycan (PGN), lipopolysaccharides (LPS), Ax21 (Activator of XA21-mediated immunity in rice), fungal chitin, and β-glucans from oomycetes are recognized by plant surface localized PRRs. Several of the MAMPs and their corresponding PRRs have, in recent years, been identified. This review focuses on the current knowledge regarding important MAMPs from bacteria, fungi, and oomycetes, their structure, the plant PRRs that recognizes them, and how they induce MAMP-triggered immunity (MTI) in plants.
Mari-Anne Newman, Thomas Sundelin, Jon T. Nielsen and Gitte Erbs
Only a few plant target genes of TAL effectors have been identified, so far. Three plant SWEET genes encoding putative sugar transporters are known to be induced by TAL effectors from rice-pathogenic Xanthomonas oryzae pv. oryzae (Xoo). We predict and validate that expression of OsSWEET14 is induced by a novel TAL effector, Tal5, from an African Xoo strain. Artificial TAL effectors (ArtTALs) were constructed to individually target 20 SWEET orthologs in rice. They were used as designer virulence factors to study which rice SWEET genes can support Xoo virulence. The Tal5 target box differs from those of the already known TAL effectors TalC, AvrXa7 and PthXo3, which also induce expression of OsSWEET14, suggesting evolutionary convergence on key targets. ArtTALs efficiently complemented an Xoo talC mutant, demonstrating that specific induction of OsSWEET14 is the key target of TalC. ArtTALs that specifically target individual members of the rice SWEET family revealed three known and two novel SWEET genes to support bacterial virulence. Our results demonstrate that five phylogenetically close SWEET proteins, which presumably act as sucrose transporters, can support Xoo virulence.
Xanthomonas campestris pv. campestris is the causal agent of black rot on Brassicaceae. The draft genome sequences of three strains (CN14, CN15, and CN16) that are highly aggressive on Arabidopsis have been determined. These genome sequences present an unexpected genomic diversity in X. campestris pv. campestris, which will be valuable for comparative analyses.
In plants, efficient immune responses against microbial infection depend on the ability to rapidly couple pathogen recognition to downstream signaling responses. In this context, plant immunity requires highly dynamic responses that involve multiple organelles during the recognition and signaling events associated to defense. Nuclear dynamics plays a critical role in plant immunity based to the growing number of reports revealing that nuclear localization of pathogen effectors, plant disease resistance proteins, and key plant components, including transcription factors and regulators, are essential for immunity.
Following their delivery into plant cells, a significant number of effector proteins from different pathogenic microorganisms, including viruses, oomycetes, fungi, nematodes, and bacteria, are targeted to the nucleus by co-opting the host nuclear import machinery. This suggests that effectors may manipulate host transcription or directly target essential host nuclear components for the benefit of the pathogen. Indeed, pathogen-induced transcriptional regulation in host cells plays a crucial role in the establishment of plant defense and associated plant cell death responses. Along these lines, it has been estimated that about 25% of Arabidopsis genes are transcriptionally regulated in response to pathogen infection and a significant number of transcription factors are involved in the defense gene regulation. Moreover, spatial restriction of defense regulators by the nuclear envelope as well as their stimulus-induced nuclear translocation provide an important mechanism for defense regulation, as their level of nuclear accumulation determines the magnitude of the defense response. In addition, nuclear translocation of effectors may also affect subcellular localization of their cognate resistance proteins in a process that is essential for plant immunity. Finally, mutations in plant cellular factors involved in the transport of macromolecules through the nuclear envelope compromise plant resistance signaling, underlining the importance of nucleocytoplasmic trafficking during plant innate immunity. Together, these findings situate the nucleus at the forefront of the mutual recognition between plants and pathogens.
In this Research Topic, we aim to provide an open-access update on the current knowledge about the importance of nuclear components – both from the “microbial side” and from the “plant side”- and nuclear dynamics during the establishment of plant immune responses. We will collect Original Research and Review papers on the topic, but also other article types, such as Methods, Commentaries and Opinions are welcome.
The Arabidopsis PENETRATION RESISTANCE 3 (PEN3) ATP binding cassette transporter participates in nonhost resistance to fungal and oomycete pathogens and is required for full penetration resistance to the barley powdery mildew Blumeria graminis f. sp. hordei. PEN3 resides in the plasma membrane and is recruited to sites of attempted penetration by invading fungal appressoria, where the transporter shows strong focal accumulation. We report that recruitment of PEN3 to sites of pathogen detection is triggered by perception of pathogen-associated molecular patterns, such as flagellin and chitin. PEN3 recruitment requires the corresponding pattern recognition receptors but does not require the BAK1 coreceptor. Pathogen- and pathogen-associated molecular pattern-induced focal accumulation of PEN3 and the PENETRATION RESISTANCE 1 (PEN1) syntaxin show differential sensitivity to specific pharmacological inhibitors, indicating distinct mechanisms for recruitment of these defense-associated proteins to the host–pathogen interface. Focal accumulation of PEN3 requires actin but is not affected by inhibitors of microtubule polymerization, secretory trafficking, or protein synthesis, and plasmolysis experiments indicate that accumulation of PEN3 occurs outside of the plasma membrane within papillae. Our results implicate pattern recognition receptors in the recruitment of defense-related proteins to sites of pathogen detection. Additionally, the process through which PEN3 is recruited to the host–pathogen interface is independent of new protein synthesis and BFA-sensitive secretory trafficking events, suggesting that existing PEN3 is redirected through an unknown trafficking pathway to sites of pathogen detection for export into papillae.
Plant nucleotide-binding leucine-rich repeat (NB-LRR) proteins serve as intracellular sensors to detect pathogen effectors and trigger immune responses. Transcription of the NB-LRR-encoding Resistance (R) genes needs to be tightly controlled to avoid inappropriate defense activation. How the expression of the NB-LRR R genes is regulated is poorly understood. The Arabidopsis snc1 mutant carries a gain-of-function mutation in a TIR-NB-LRR-encoding gene, resulting in the constitutive activation of plant defence responses. A snc1 suppressor screen identified modifier of snc1, 9 (mos9), which partially suppresses the autoimmune phenotypes of snc1. Positional cloning revealed that MOS9 encodes a plant-specific protein of unknown function. Expression analysis showed that MOS9 is required for the full expression of TIR-NB-LRR protein-encoding RPP4 and SNC1, both of which reside in the RPP4 cluster. Co-immunoprecipitation and mass spectrometry analyses revealed that MOS9 associates with the Set1 class H3K4 methyl transferase ATXR7. Like MOS9, ATXR7 is also required for the full expression of SNC1 and the autoimmune phenotypes in the snc1 mutant. In atxr7 mutant plants, the expression of RPP4 is similarly reduced and resistance against Hyaloperonospora arabidopsidis Emwa1 is compromised. Consistent with the attenuated expression of SNC1 and RPP4, H3K4me3 marks are reduced around the promoters of SNC1 and RPP4 in mos9 plants. Our data suggest that MOS9 functions together with ATXR7 to regulate the expression of SNC1 and RPP4 through H3K4 methylation, which plays an important role in fine-tuning their transcription levels and functions in plant defence.
As part of their immune system, plants have pattern recognition receptors (PRRs) that can detect a broad range of microbe-associated molecular patterns (MAMPs). Here, we identified a PRR of Arabidopsis thaliana with specificity for the bacterialMAMP eMax from xanthomonads. Response to eMax seems to be restricted to theBrassicaceae family and also varied among different accessions of Arabidopsis. In crosses between sensitive accessions and the insensitive accession Shakhdara, eMax perception mapped to RECEPTOR-LIKE PROTEIN1 (RLP1). Functional complementation of rlp1 mutants required gene constructs that code for a longer version of RLP1 that we termed ReMAX (for receptor of eMax). ReMAX/RLP1 is a typical RLP with structural similarity to the tomato (Solanum lycopersicum) RLP Eix2, which detects fungal xylanase as a MAMP. Attempts to demonstrate receptor function by interfamily transfer of ReMAX to Nicotiana benthamiana were successful after using hybrid receptors with the C-terminal part of ReMAX replaced by that of Eix2. These results show that ReMAX determines specificity for eMax. They also demonstrate hybrid receptor technology as a promising tool to overcome problems that impede interfamily transfer of PRRs to enhance pathogen detection in crop plants.
Understanding commonalities and differences of how symbiotic and parasitic microbes interact with plants will improve advantageous interactions and allow pathogen control strategies in crops. Recently established systems enable studies of root pathogenic and symbiotic interactions in the same plant species.
Scooped from: Annual Review of Phytopathology, 2013 Authors: Xiu-Fang Xin and Sheng Yang He
Summary: Since the early 1980s, various strains of the gram-negative bacterial pathogen Pseudomonas syringae have been used as models for understanding plant-bacterial interactions. In 1991, a P. syringae pathovar tomato (Pst) strain, DC3000, was reported to infect not only its natural host tomato but also Arabidopsis in the laboratory, a finding that spurred intensive efforts in the subsequent two decades to characterize the molecular mechanisms by which this strain causes disease in plants. Genomic analysis shows that Pst DC3000 carries a large repertoire of potential virulence factors, including proteinaceous effectors that are secreted through the type III secretion system and a polyketide phytotoxin called coronatine, which structurally mimics the plant hormone jasmonate ( JA). Study of Pst DC3000 pathogenesis has not only provided several conceptual advances in understanding how a bacterial pathogen employs type III effectors to suppress plant immune responses and promote disease susceptibility but has also facilitated the discovery of the immune function of stomata and key components of JA signaling in plants. The concepts derived from the study of Pst DC3000 pathogenesis may prove useful in understanding pathogenesis mechanisms of other plant pathogens.
RNA-Seq is opening new doors for the functional understanding of microorganisms. Advances in RNA-Seq technology are allowing investigators to focus their studies on specific functional questions. An interesting example is presented by An et al. (2013) in this issue of Molecular Microbiology. New genes were identified for proteins and ncRNAs when the authors concentrated on the role of the rpf genes, which code for key components of a signal transduction hub in the plant pathogen Xanthomonas campestris pv. campestris. Although rpf gene products were already known to be involved in controlling transcription of many genes, including those encoding several important virulence factors, novel and unexpected properties of this signal transduction system emerged from the RNA-Seq analysis. In addition to identifying new target genes influenced by the rpf genes, the study found that the regulons of RpfC and RpfG, the sensor and response regulator of the master two-component regulatory system, only partially overlapped, indicating that the Rpf signalling system is even more complex than previously appreciated.
The pathogenic bacterium Xanthomonas campestris pv. campestris, the causal agent of black rot of Brassicaceae, manipulates the physiology and the innate immunity of its hosts. Association genetic and reverse-genetic analyses of a world panel of 45 X. campestris pv. campestris strains were used to gain understanding of the genetic basis of the bacterium’s pathogenicity to Arabidopsis thaliana. We found that the compositions of the minimal predicted type III secretome varied extensively, with 18 to 28 proteins per strain. There were clear differences in aggressiveness of those X. campestris pv. campestris strains on two Arabidopsis natural accessions. We identified 3 effector genes (xopAC, xopJ5, and xopAL2) and 67 amplified fragment length polymorphism (AFLP) markers that were associated with variations in disease symptoms. The nature and distribution of the AFLP markers remain to be determined, but we observed a low linkage disequilibrium level between predicted effectors and other significant markers, suggesting that additional genetic factors make a meaningful contribution to pathogenicity. Mutagenesis of type III effectors in X. campestris pv. campestris confirmed that xopAC functions as both a virulence and an avirulence gene in Arabidopsis and that xopAM functions as a second avirulence gene on plants of the Col-0 ecotype. However, we did not detect the effect of any other effector in the X. campestris pv. campestris 8004 strain, likely due to other genetic background effects. These results highlight the complex genetic basis of pathogenicity at the pathovar level and encourage us to challenge the agronomical relevance of some virulence determinants identified solely in model strains.
IMPORTANCE The identification and understanding of the genetic determinants of bacterial virulence are essential to be able to design efficient protection strategies for infected plants. The recent availability of genomic resources for a limited number of pathogen isolates and host genotypes has strongly biased our research toward genotype-specific approaches. Indeed, these do not consider the natural variation in both pathogens and hosts, so their applied relevance should be challenged. In our study, we exploited the genetic diversity of Xanthomonas campestris pv. campestris, the causal agent of black rot on Brassicaceae (e.g., cabbage), to mine for pathogenicity determinants. This work evidenced the contribution of known and unknown loci to pathogenicity relevant at the pathovar level and identified these virulence determinants as prime targets for breeding resistance to X. campestris pv. campestris in Brassicaceae.
Endrick Guy, Anne Genissel, Ahmed Hajric, Matthieu Chabannes, Perrine David, Sébastien Carrere, Martine Lautier, Brice Roux, Tristan Boureau, Matthieu Arlat, Stéphane Poussierf, Laurent D. Noël
(Via T. Lahaye & T. Schreiber) De Lange et al 2013 Ralstonia solanacearum is a devastating bacterial phytopathogen with a broad host range. Ralstonia solanacearum injected effector proteins (Rips) are key to the successful invasion of host plants. We have characterized Brg11(hrpB-regulated 11), the first identified member of a class of Rips with high sequence similarity to the transcription activator-like (TAL) effectors of Xanthomonas spp., collectively termed RipTALs. Fluorescence microscopy of in planta expressed RipTALs showed nuclear localization. Domain swaps between Brg11 and Xanthomonas TAL effector (TALE) AvrBs3 (avirulence protein triggering Bs3 resistance) showed the functional interchangeability of DNA-binding and transcriptional activation domains. PCR was used to determine the sequence of brg11 homologs from strains infecting phylogenetically diverse host plants. Brg11 localizes to the nucleus and activates promoters containing a matching effector-binding element (EBE). Brg11 and homologs preferentially activate promoters containing EBEs with a 5′ terminal guanine, contrasting with the TALE preference for a 5′ thymine. Brg11 and other RipTALs probably promote disease through the transcriptional activation of host genes. Brg11 and the majority of homologs identified in this study were shown to activate similar or identical target sequences, in contrast to TALEs, which generally show highly diverse target preferences. This information provides new options for the engineering of plants resistant to R. solanacearum.
Resistance (R) proteins recognize pathogen avirulence (Avr) proteins by direct or indirect binding and are multidomain proteins generally carrying a nucleotide binding (NB) and a leucine-rich repeat (LRR) domain. Two NB-LRR protein-coding genes from rice (Oryza sativa), RGA4 and RGA5, were found to be required for the recognition of the Magnaporthe oryzae effector AVR1-CO39. RGA4 and RGA5 also mediate recognition of the unrelated M. oryzae effector AVR-Pia, indicating that the corresponding R proteins possess dual recognition specificity. For RGA5, two alternative transcripts, RGA5-A and RGA5-B, were identified. Genetic analysis showed that only RGA5-A confers resistance, while RGA5-B is inactive. Yeast two-hybrid, coimmunoprecipitation, and fluorescence resonance energy transfer–fluorescence lifetime imaging experiments revealed direct binding of AVR-Pia and AVR1-CO39 to RGA5-A, providing evidence for the recognition of multiple Avr proteins by direct binding to a single R protein. Direct binding seems to be required for resistance as an inactive AVR-Pia allele did not bind RGA5-A. A small Avr interaction domain with homology to the Avr recognition domain in the rice R protein Pik-1 was identified in the C terminus of RGA5-A. This reveals a mode of Avr protein recognition through direct binding to a novel, non-LRR interaction domain.
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