Phytopathogenic bacteria of the Xanthomonas genus cause severe diseases on hundreds host plants, including economically important crops, such as rice, wheat, cassava, banana, mango, tomato, citrus, cabbage, pepper, bean and cotton. Diseases occurring in nature comprise black rot, leaf/fruit spot, canker, wilt, leaf blight and streak. These bacteria are present worldwide where some phytopathogenic strains are emergent or re-emergent and, consequently, dramatically impact agriculture, economy and food safety.
Xanthomonas bacteria provide excellent models for genomic studies and hundreds of Xanthomonas genome sequences have been obtained since 2002 and many other are underway (www.xanthomonas.org/genomes.html). Comparative genomics between and/or within bacterial species and/or pathovars will be of a great help to decipher commonalities and particularities that underly host range definition.
Most of the Xanthomonas possesses a type III secretion system (T3SS) that is required for injection of various effectors inside plant cells, thus contributing to pathogenicity. Transcription Activator-Like (tal) genes, encode bacterial transcription factors which are injected through the T3SS by many Xanthomonas to promote pathogenicity. Some Ralstonia, Bulkholderia and marine bacteria also express TAL-like proteins which function and mode of action is starting to be deciphered. TALs are addressed to the plant nucleus where they activate plant gene expression by direct binding to the corresponding promoter sequences. Targeted genes essentially act as susceptibility genes. A few years after the cracking of the code allowing the TAL/Host promoter sequence recognition, combined to the ever-growing availability of plant genomes, many efforts have been done to identify TAL targets. These data collected for many Xanthomonas/host pathosystems will assuredly help breeders to breed resistance resistant in important crops.
In this Research Topic we aim to collect manuscripts covering the current knowledge of Xanthomonas genomics and effectomics, with a special focus on TAL effector biology. Specifically, we encourage the submission of manuscripts (Original Research, Hypothesis & Theory, Methods, Reviews, Mini Reviews, Perspective and Opinion) covering the following topics: 1. Manuscripts reporting genome sequencing of Xanthomonas strains. 2. Manuscripts describing functional and comparative genomics in Xanthomonas species/pathovars. 3. Manuscripts describing functional studies on Xanthomonas type III effectors. 3. Manuscripts describing discovery, evolution, bio-informatics and functional genomics of TAL effectors and their targets in plant genomes, as well as for TAL-like in non-Xanthomonas bacteria. 4. Manuscripts describing applications of TAL effector research for resistance breeding in crops.
We anticipate that this Research Topic will be of importance for plant pathologists and breeders.
Banana is a major staple crop in East Africa produced mostly by smallholder subsistence farmers. More bananas are produced and consumed in East Africa than in any region of the world. Uganda is the world’s second foremost grower with a total annual production of about 10.5 million tons. The average daily per capita consumption in Uganda ranges from 0.61 to over 1.6 kg, one of the highest in the world. In this Correspondence, we report preliminary results from a confined field trial in Uganda of transgenic bananas resistant to the deadly banana Xanthomonas wilt disease.
Leena Tripathi, Jaindra Nath Tripathi, Andrew Kiggundu, Sam Korie, Frank Shotkoski & Wilberforce Kateera Tushemereirwe
The Pseudomonas syringae complex is composed of numerous genetic lineages of strains from both agricultural and environmental habitats including habitats closely linked to the water cycle. The new insights from the discovery of this bacterial species in habitats outside of agricultural contexts per se have led to the revelation of a wide diversity of strains in this complex beyond what was known from agricultural contexts. Here, through Multi Locus Sequence Typing (MLST) of 216 strains, we identified 23 clades within 13 phylogroups among which the seven previously described P. syringae phylogroups were included. The phylogeny of the core genome of 29 strains representing nine phylogroups was similar to the phylogeny obtained with MLST thereby confirming the robustness of MLST-phylogroups. We show that phenotypic traits rarely provide a satisfactory means for classification of strains even if some combinations are highly probable in some phylogroups. We demonstrate that the citrate synthase (cts) housekeeping gene can accurately predict the phylogenetic affiliation for more than 97% of strains tested. We propose a list of cts sequences to be used as a simple tool for quickly and precisely classifying new strains. Finally, our analysis leads to predictions about the diversity of P. syringae that is yet to be discovered. We present here an expandable framework mainly based on cts genetic analysis into which more diversity can be integrated.
Odile Berge, Caroline L. Monteil, Claudia Bartoli, Charlotte Chandeysson, Caroline Guilbaud
Breeding agricultural crops for resistance against pathogens is essential to secure global food production. Despite efforts to control crop diseases, pathogens are estimated to account for losses of 15% of global food production. It is suggested that losses would be almost twice as much without disease control measures, such as crop resistance breeding . There are now opportunities to improve the effectiveness of breeding crops for resistance against damaging pathogens by exploiting new molecular and genetic insights to improve understanding of the defence system of crop plants against pathogens. In this opinion, we focus on the resistance of crops against foliar fungal pathogens that exploit the host apoplast for retrieval of nutrients. Some of these pathogens are globally widespread and of considerable economic importance. They include pathogens that penetrate the host leaf cuticle and then exploit a niche underneath it (e.g., Pyrenopeziza brassicae, oilseed rape light leaf spot; Venturia inaequalis, apple scab; and Rhynchosporium commune, barley leaf blotch, global losses of approximately US$3.5 billion per year). Others enter leaves through stomata, then grow between host mesophyll cells (e.g., Cladosporium fulvum, tomato leaf mould; Leptosphaeria maculans, oilseed rape phoma stem canker, global losses of approximately US$1 billion per year; and Zymoseptoria tritici, wheat septoria leaf blotch, with a global loss of approximately US$5 billion per year) (Table 1, Figure 1). These apoplastic pathogens are all ascomycetes and many of them are dothideomycetes .
We report here the draft genome sequence of Xanthomonas axonopodis pv. allii strain CFBP 6369, the causal agent of bacterial blight of onion. The draft genome has a size of 5,425,942 bp and a G+C content of 64.4%.
L. Gagnevin, S. Bolot, J. L. Gordon, O. Pruvost, C. Vernière, I. Robène, M. Arlat, L. D. Noël, S. Carrère, M.-A. Jacques, R. Koebnik
The gene-for-gene concept has historically been applied to describe a specific resistance interaction wherein single genes from the host and the pathogen dictate the outcome. These interactions have been observed across the plant kingdom and all known plant microbial pathogens. In recent years, this concept has been extended to susceptibility phenotypes in the context of transcription activator like (TAL) effectors that target SWEET sugar transporters. However, as this interaction has only been observed in rice, it was not clear whether the gene-for-gene susceptibility was unique to that system. Here we show, through a combined systematic analysis of the TAL effector-complement of Xanthomonas axonopodis pv. manihotis (Xam), and RNA-Sequencing to identify targets in cassava, that TAL20Xam668 specifically induces the sugar transporter MeSWEET10a to promote virulence. Designer TAL effectors (dTALEs) complement TAL20Xam668 mutant phenotypes, demonstrating that MeSWEET10a is a susceptibility gene in cassava. Sucrose uptake-deficient Xam do not lose virulence, indicating that sucrose may be cleaved extracellularly and taken up as hexoses into Xam. Together, our data suggest that pathogen hijacking of plant nutrients is not unique to rice blight but also plays a role in bacterial blight of the dicot cassava.
Plants protect themselves from the harmful effects of pathogens by resistance and tolerance. Disease resistance, which eliminates pathogens, can be modulated by bacterial type III effectors. Little is known about whether disease tolerance, which sustains host fitness with a given pathogen burden, is regulated by effectors. Here, we examined the effects of the Xanthomonas effector protein XopDXcc8004 on plant disease defenses by constructing knockout and complemented Xanthomonas strains, and performing inoculation studies in radish (Raphanus sativus L. var. radiculus XiaoJinZhong) and Arabidopsis plants. XopDXcc8004 suppresses disease symptoms without changing bacterial titers in infected leaves. In Arabidopsis, XopDXcc8004 delays the hormone gibberellin (GA)-mediated degradation of RGA (repressor of ga1-3), one of five DELLA proteins that repress GA signaling and promote plant tolerance under biotic and abiotic stresses. The ERF-associated amphiphilic repression (EAR) motif-containing region of XopDXcc8004 interacts with the DELLA domain of RGA and might interfere with the GA-induced binding of GID1, a GA receptor, to RGA. The EAR motif was found to be present in a number of plant transcriptional regulators. Thus, our data suggest that bacterial pathogens might have evolved effectors, which probably mimic host components, to initiate disease tolerance and enhance their survival.
Leitao Tan, Wei Rong, Hongli Luo, Yinhua Chen, and Chaozu He
Recent advances in DNA targeting allow unprecedented control over gene function and expression. Targeting based on TAL effectors is arguably the most promising for systems biology and metabolic engineering. Multiple, orthogonal TAL-effector reagents of different types can be used in the same cell. Furthermore, variation in base preferences of the individual structural repeats that make up the TAL effector DNA recognition domain makes targeting stringency tunable. Realized applications range from genome editing to epigenome modification to targeted gene regulation to chromatin labeling and capture. The principles that govern TAL effector DNA recognition make TAL effectors well suited for applications relevant to plant physiology and metabolism. TAL effector targeting has merits that are distinct from those of the RNA-based DNA targeting CRISPR/Cas9 system.
In this paper, we show how a single web resource can engage a wide student audience with plant science. Developed by the University of Leeds, UK, the Plant Science TREE (Tool for Research Engaged Education (www.tree.leeds.ac.uk)) is an online teaching tool giving access to online research lectures, downloadable lecture slides, practicals, movies and other material on topical plant science to support lecturers in their teaching. The Plant Science TREE complements the annual Gatsby Plant Science Summer School, which has already succeeded in engaging undergraduates with plant science (Levesley et al., 2012). Both initiatives were instigated to address the decline in student numbers in plant science (Sundberg, 2004; Stagg et al., 2009; Jones, 2010; Drea, 2011) at a time when there is concern that future demand for plant scientists will not be met (The Royal Society, 2009). The causes of this decline are unproven but may be the result of a combination of factors including, greater preference by students for animal and medically-based degrees, disengagement from plant science at school, and narrowing of plant-based undergraduate curricula. Where the summer school aims, by face-to-face contact, to inspire relatively small numbers of high-achieving students to consider plant science as a career option, the Plant Science TREE aims to reach a much larger, more diverse global audience through the use of web technologies.
Aurora Levesley, Steve Paxton, Richard Collins, Alison Baker and Celia Knight
Scott Jackson, Jeremy Schmutz, Phillip McClean and colleagues report the genome sequence of the common bean (Phaseolus vulgaris) and resequenced wild individuals and landraces from Mesoamerican and Andean gene pools, showing that common bean underwent two independent domestications.
Next generation sequencing (NGS) technologies have impressively accelerated research in biological science during the last years by enabling the production of large volumes of sequence data to a drastically lower price per base, compared to traditional sequencing methods. The recent and ongoing developments in the field allow addressing research questions in plant-microbe biology that were not conceivable just a few years ago. The present review provides an overview of NGS technologies and their usefulness for the analysis of microorganisms that live in association with plants. Possible limitations of the different sequencing systems, in particular sources of errors and bias, are critically discussed and methods are disclosed that help to overcome these shortcomings. A focus will be on the application of NGS methods in metagenomic studies, including the analysis of microbial communities by amplicon sequencing, which can be considered as a targeted metagenomic approach. Different applications of NGS technologies are exemplified by selected research articles that address the biology of the plant associated microbiota to demonstrate the worth of the new methods.
While conceptual principles governing plant immunity are becoming clear, its systems-level organization and the evolutionary dynamic of the host-pathogen interface are still obscure. We generated a systematic protein-protein interaction network of virulence effectors from the ascomycete pathogen Golovinomyces orontii and Arabidopsis thaliana host proteins. We combined this data set with corresponding data for the eubacterial pathogen Pseudomonas syringae and the oomycete pathogen Hyaloperonospora arabidopsidis. The resulting network identifies host proteins onto which intraspecies and interspecies pathogen effectors converge. Phenotyping of 124 Arabidopsis effector-interactor mutants revealed a correlation between intraspecies and interspecies convergence and several altered immune response phenotypes. Several effectors and the most heavily targeted host protein colocalized in subnuclear foci. Products of adaptively selected Arabidopsis genes are enriched for interactions with effector targets. Our data suggest the existence of a molecular host-pathogen interface that is conserved across Arabidopsis accessions, while evolutionary adaptation occurs in the immediate network neighborhood of effector targets.
Ralf Weßling, Petra Epple, Stefan Altmann,Yijian He, Li Yang, Stefan R. Henz, Nathan McDonald, Kristin Wiley, Kai Christian Bader, Christine Glaßer, M. Shahid Mukhtar, Sabine Haigis, Lila Ghamsari, Amber E. Stephens, Joseph R. Ecker, Marc Vidal, Jonathan D.G. Jones,Klaus F.X. Mayer, Emiel Ver Loren van Themaat, Detlef Weigel, Paul Schulze-Lefert, Jeffery L. Dangl, Ralph Panstruga, and Pascal Braun
The type III secretion system (T3SS) is a membrane-embedded nanomachine found in several Gram-negative bacteria. Upon contact between bacteria and host cells, the syringe-like T3SS transfers proteins termed effectors from the bacterial cytosol to the cytoplasm or the plasma membrane of a single target cell. This is a major difference from secretion systems that merely release molecules into the extracellular milieu, where they act on potentially distant target cells expressing the relevant surface receptors. The syringe architecture is conserved at the structural and functional level and supports injection into a great variety of hosts and tissues. However, the pool of effectors is species specific and determines the outcome of the interaction, via modulation of target-cell function.
Transcription activator-like effectors (TALEs) from plant pathogenic Xanthomonas spp. and the related RipTALs from Ralstonia solanacearum are DNA-binding proteins with a modular DNA-binding domain. This domain is both predictable and programmable, which simplifies elucidation of TALE function in planta and facilitates generation of DNA-binding modules with desired specificity for biotechnological approaches. Recently identified TALE host target genes that either promote or stop bacterial disease provide new insights into how expression of TALE genes affects the plant–pathogen interaction. Since its elucidation the TALE code has been continuously refined and now provides a mature tool that, in combination with transcriptome profiling, allows rapid isolation of novel TALE target genes. The TALE code is also the basis for synthetic promoter-traps that mediate recognition of TALE or RipTAL proteins in engineered plants. In this review, we will summarize recent findings in plant-focused TALE research. In addition, we will provide an outline of the newly established gene isolation approach for TALE or RipTAL host target genes with an emphasis on potential pitfalls.
The YopJ-family of type III effector (T3E) proteins is one of the largest and widely distributed families of effector proteins whose members are highly diversified in virulence functions. In the present study, HopZ4, a member of the YopJ-family of T3Es from the cucumber pathogen Pseudomonas syringae pv. lachrymans is described. HopZ4 shares high sequence similarity with the Xanthomonas T3E XopJ and a functional analysis suggests a conserved virulence function between these two T3Es. As has previously shown for XopJ, HopZ4 interacts with the proteasomal subunit RPT6 in yeast and in planta to inhibit proteasome activity during infection. The inhibitory effect on the proteasome is dependent on localization of HopZ4 to the plasma membrane as well as on an intact catalytic triad of the effector protein. Furthermore, HopZ4 is able to complement loss of XopJ in Xanthomonas as it prevents precocious host cell death during a compatible interaction of Xanthomonas with pepper. The data presented here suggest that different bacterial species employ inhibition of the proteasome as a virulence strategy by making use of conserved T3Es from the YopJ-family of bacterial effector proteins.
Terrestrial plants rely on stomata, small pores in the leaf surface, for photosynthetic gas exchange and transpiration of water. The stomata, formed by a pair of guard cells, dynamically increase and decrease their volume to control the pore size in response to environmental cues. Stresses can trigger similar or opposing movements: for example, drought induces closure of stomata, whereas many pathogens exploit stomata and cause them to open to facilitate entry into plant tissues. The latter is an active process as stomatal closure is part of the plant's immune response. Stomatal research has contributed much to clarify the signalling pathways of abiotic stress, but guard cell signalling in response to microbes is a relatively new area of research. In this article, we discuss present knowledge of stomatal regulation in response to microbes and highlight common points of convergence, and differences, compared to stomatal regulation by abiotic stresses. We also expand on the mechanisms by which pathogens manipulate these processes to promote disease, for example by delivering effectors to inhibit closure or trigger opening of stomata. The study of pathogen effectors in stomatal manipulation will aid our understanding of guard cell signalling.
Deirdre H. McLachlan, Michaela Kopischke and Silke Robatzek
Les chercheurs du Laboratoire des Interactions Plantes-Microorganismes (LIPM) du centre INRA de Toulouse ont déterminé comment le xylane, un composé majeur de la paroi cellulaire végétale, était décomposé par la bactérie phytopathogène Xanthomonas campestris pv campestris (Xcc). Leurs résultats ont mis en évidence que cette dégradation dépendait d’un système spécifique composé de transporteurs et d’enzymes. Plus intéressant encore, ce même système de dégradation est utilisé par les bactéries symbiotiques de l’intestin humain ! Cette découverte a fait l’objet d’une publication dans la revue scientifique New Phytologist. (Déjean et al. 2013, 198(3):899-915).
Plants sense invasion of potential microbial pathogens using various receptors and launch cascades of innate immune responses that are critical for survival and fecundity. Recognition of pathogens occurs through detection of pathogen-associated patterns (PAMPs) or pathogen effectors, setting off a cascade of signaling events that triggers early cellular and molecular responses. Plant innate immunity is constituted by an elaborate, multilayered system involving two intertwined lines of defense: a first level of immunity termed PAMP–triggered immunity (PTI) or basal resistance, and a second layer of plant defense, mediated by resistance (R) proteins, leading to a complete resistance response often accompanied by the hypersensitive cell death (HR), and called effector-triggered immunity (ETI; Jones & Dangl, 2006). Another form of resistance, that confers partial resistance to pathogens and usually referred as quantitative disease resistance (QDR), has been extensively observed in crops and natural plant populations (Kover & Cheverud, 2007; Poland et al., 2009; Roux et al., 2014). However, there is still very limited information about the molecular mechanisms underlying this form of immunity. More generally, protein kinases play critical roles during immunity in signaling through phosphorylation of target proteins and as modulators of cell metabolism and gene expression (Romeis, 2001; Meng & Zhang, 2013). Pseudokinases are topologically related to protein kinases but lack catalytic residue(s) classically required for phosphotransfer. Interestingly, recent reports identified two Arabidopsis pseudokinases, RKS1 and ZED1, that belong to a gene cluster within the receptor-like cytoplasmic kinase (RLCK)-XII-2 subfamily and confer different forms of immunity....
Fabrice Roux, Laurent Noël, Susana Rivas and Dominique Roby