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Journal: Molecular plant pathology

29

BACKGROUND: Xanthomonas campestris pv. campestris (Xcc) (Pammel) Dowson is a Gram-negative bacterium that causes black rot, the most important disease of vegetable brassica crops worldwide. Intensive molecular investigation of Xcc is gaining momentum and several whole genome sequences are available. TAXONOMY: Bacteria; Phylum Proteobacteria; Class Gammaproteobacteria; Order Xanthomonadales; Family Xanthomonadacea; Genus Xanthomonas; Species X. campestris. HOST RANGE AND SYMPTOMS: Xcc can cause disease in a large number of species of Brassicaceae (ex-Cruciferae), including economically important vegetable Brassica crops and a number of other cruciferous crops, ornamentals and weeds, including the model plant Arabidopsis thaliana. Black rot is a systemic vascular disease. Typical disease symptoms include V-shaped yellow lesions starting from the leaf margins and blackening of the veins. RACE STRUCTURE, PATHOGENESIS AND EPIDEMIOLOGY: Collections of Xcc isolates have been differentiated into physiological races based on the response of several brassica species lines. Black rot is a seed-borne disease. The disease is favoured by warm, humid conditions and can spread rapidly from rain dispersal and irrigation water. DISEASE CONTROL: The control of black rot is difficult and relies on the use of pathogen-free planting material and the elimination of other potential inoculum sources (infected crop debris and cruciferous weeds). Major gene resistance is very rare in B. oleracea (brassica C genome). Resistance is more readily available in other species, including potentially useful sources of broad-spectrum resistance in B. rapa and B. carinata (A and BC genomes, respectively) and in the wild relative A. thaliana. GENOME: The reference genomes of three isolates have been released. The genome consists of a single chromosome of approximately 5 100 000 bp, with a GC content of approximately 65% and an average predicted number of coding DNA sequences (CDS) of 4308. IMPORTANT GENES IDENTIFIED: Three different secretion systems have been identified and studied in Xcc. The gene clusters xps and xcs encode a type II secretion system and xps genes have been linked to pathogenicity. The role of the type IV secretion system in pathogenicity is still uncertain. The hrp gene cluster encodes a type III secretion system that is associated with pathogenicity. An inventory of candidate effector genes has been assembled based on homology with known effectors. A range of other genes have been associated with virulence and pathogenicity, including the rpf, gum and wxc genes involved in the regulation of the synthesis of extracellular degrading enzymes, xanthan gum and lipopolysaccharides. USEFUL WEBSITE: http://www.xanthomonas.org/

Concepts: Gene, Xanthomonas campestris, Genetics, Arabidopsis thaliana, Brassicaceae, Secretion, Genome, DNA

28

Plant-parasitic nematodes secrete so-called effectors into their host plant which are able to suppress the plant’s defence responses, alter plant signalling pathways and, in the case of root knot nematodes, induce the formation of giant cells. Putative effectors have been successfully identified by genomics, transcriptomics and proteomics approaches. In this study, we investigated the transcriptome of the rice root knot nematode Meloidogyne graminicola by 454 sequencing of second-stage juveniles as well as mRNA-seq of rice infected tissue. Over 350 000 reads derived from M. graminicola preparasitic juveniles were assembled, annotated and checked for homologues in different databases. From infected rice tissue, 1.4% of all reads generated were identified as being derived from the nematode. Using multiple strategies, several putative effector genes were identified, both pioneer genes and genes corresponding to already known effectors. To check whether these genes could be involved in the interaction with the plant, in situ hybridization was performed on a selection of genes to localize their expression in the nematode. Most were expressed in the gland cells or amphids of the nematode, confirming possible secretion of the proteins and hence a role in infection. Other putative effectors showed a different expression pattern, potentially linked with the excretory/secretory system. This transcriptome study is a good starting point to functionally investigate novel effectors derived from M. graminicola. This will lead to better insights into the interaction between these nematodes and the model plant rice. Moreover, the transcriptome can be used to identify possible target genes for RNA interference (RNAi)-based control strategies. Four genes proved to be interesting targets by showing up to 40% higher mortality relative to the control treatment when soaked in gene-specific small interfering RNAs (siRNAs).

Concepts: Protein, Gene, Secretion, Bacteria, Model organism, Gene expression, RNA, Root-knot nematode

28

Plant roots react to pathogen attack by the activation of general and systemic resistance, including the lignification of cell walls and increased release of phenolic compounds in root exudate. Some fungi have the capacity to degrade lignin using ligninolytic extracellular peroxidases and laccases. Aromatic lignin breakdown products are further catabolized via the β-ketoadipate pathway. In this study, we investigated the role of 3-carboxy-cis,cis-muconate lactonizing enzyme (CMLE), an enzyme of the β-ketoadipate pathway, in the pathogenicity of Fusarium oxysporum f. sp. lycopersici towards its host, tomato. As expected, the cmle deletion mutant cannot catabolize phenolic compounds known to be degraded via the β-ketoadipate pathway. In addition, the mutant is impaired in root invasion and is nonpathogenic, even though it shows normal superficial root colonization. We hypothesize that the β-ketoadipate pathway in plant-pathogenic, soil-borne fungi is necessary to degrade phenolic compounds in root exudate and/or inside roots in order to establish disease.

Concepts: Fusarium oxysporum, Enzyme, Vanillin, Root, Lignin, Cell wall, Plant, Bacteria

28

Grapevine leafroll disease (GLRD) is one of the most economically important virus diseases of grapevine (Vitis spp.) worldwide. In this study, we used high-throughput sequencing of cDNA libraries made from small RNAs (sRNAs) to compare profiles of sRNA populations recovered from own-rooted Merlot grapevines with and without GLRD symptoms. The data revealed the presence of sRNAs specific to Grapevine leafroll-associated virus 3, Hop stunt viroid (HpSVd), Grapevine yellow speckle viroid 1 (GYSVd-1) and Grapevine yellow speckle viroid 2 (GYSVd-2) in symptomatic grapevines and sRNAs specific only to HpSVd, GYSVd-1 and GYSVd-2 in nonsymptomatic grapevines. In addition to 135 previously identified conserved microRNAs in grapevine (Vvi-miRs), we identified 10 novel and several candidate Vvi-miRs in both symptomatic and nonsymptomatic grapevine leaves based on the cloning of miRNA star sequences. Quantitative real-time reverse transcriptase-polymerase chain reaction (RT-PCR) of selected conserved Vvi-miRs indicated that individual members of an miRNA family are differentially expressed in symptomatic and nonsymptomatic leaves. The high-resolution mapping of sRNAs specific to an ampelovirus and three viroids in mixed infections, the identification of novel Vvi-miRs and the modulation of certain conserved Vvi-miRs offers resources for the further elucidation of compatible host-pathogen interactions and for the provision of ecologically relevant information to better understand host-pathogen-environment interactions in a perennial fruit crop.

Concepts: Viticulture, DNA, Phylloxera, Vitaceae, Grape, Vitis vinifera, Vitis, RNA

26

Citrus tristeza virus (CTV) is phloem-restricted in natural citrus hosts. The 23 kDa protein (p23) encoded by the virus is an RNA silencing suppressor and a pathogenicity determinant. Expression of p23, or its N-terminal 157 amino acid fragment comprising the zinc-finger and flanking basic motifs, driven by the constitutive 35S promoter of cauliflower mosaic virus incites CTV-like symptoms and other aberrations in transgenic citrus. To better define the role of p23 in CTV pathogenesis, we compared the phenotypes of Mexican limes transformed with p23-derived transgenes from the severe T36 or the mild T317 CTV isolates under the control of the phloem-specific promoter from commelina yellow mottle virus (CoYMV) or the 35S promoter. Expression of the constructs restricted to the phloem incited a phenotype resembling CTV-specific symptoms (vein clearing and necrosis, and stem pitting), but not the non-specific aberrations (like mature leaf epinasty and yellow pinpoints, growth cease and apical necrosis) observed when p23 was ectopically expressed. Furthermore, vein necrosis and stem pitting in Mexican lime appeared specifically associated with p23 from T36. Phloem-specific accumulation of the p23Δ158-209(T36) fragment was sufficient to incite the same anomalies, indicating that the region comprising the N-terminal 157 amino acids of p23 is responsible (at least in part) for the vein clearing, stem pitting and possibly vein corking in this host.

Concepts: Persian lime, Rutaceae, Bacteria, Amino acid, Acid, Citrus, Protein, Gene

25

While quantitative disease resistance (QDR) is a durable and broad spectrum form of resistance in plants, identifying genes underlying QDR is still in its infancy. RKS1 (Resistance related KinaSe1) was recently reported to confer QDR in Arabidopsis thaliana to most but not all races of the bacterial pathogen Xanthomonas campestris pv. campestris (Huard-Chauveau et al., 2013). We therefore explored the genetic bases of QDR in A. thaliana to diverse races of Xc. A nested Genome Wide Association mapping approach was used to finely map genomic regions associated with QDR to Xcc12824 (race 2) and XccCFBP6943 (race 6), respectively. To identify the gene(s) implicated in QDR, insertional mutants (T-DNA) were selected for the candidate genes and phenotyped in response to Xc. Either for Xcc12824 or XccCFBP6943, we identified a major QTL conferring resistance. Whereas QDR to Xcc12824 is conferred by the At5g22540 encoding for a protein of unknown function, QDR to XccCFBP6943 involves the well-known immune receptor pair RRS1/RPS4. In addition to RKS1, this study reveals that three genes are involved in resistance to Xc with strikingly different ranges of specificity, suggesting that QDR to Xc involves a complex network integrating multiple response pathways triggered by distinct pathogen molecular determinants.

Concepts: Chromosome, Arabidopsis, Xanthomonas campestris, Immune system, Gene, Arabidopsis thaliana, Genome, Genetics

25

Several plant lipid transfer proteins (LTP) act positively in plant disease resistance. Here, we show that LTP3 (At5g59320), a pathogen and ABA-induced gene, negatively regulates plant immunity in Arabidopsis. Overexpression of LTP3 (LTP3-OX) led indeed to an enhanced susceptibility to virulent bacteria and compromised resistance to avirulent bacteria. Upon infection of LTP3-OX plants with Pseudomonas syringae pv. tomato, genes involved in abscisic acid (ABA) biosynthesis, NCED3 and AAO3 were highly induced whereas salicylic acid (SA) related genes, ICS1 and PR1 were down-regulated. Accordingly, in LTP3-OX plants we observed an increased ABA levels and lower SA levels compared to the wild type. We also showed that the LTP3-overexpression-mediated enhanced susceptibility was partially dependent of AAO3. Interestingly, loss of function of LTP3 (ltp3-1) did not affect ABA pathways, but resulted in PR1 gene induction and elevated SA levels, suggesting that LTP3 can negatively regulate SA in an ABA-independent manner. However, double mutant consisting of ltp3-1 and silent LTP4 (ltp3/ltp4) showed reduced susceptibility to Pseudomonas and down-regulation of ABA biosynthesis genes, suggesting that LTP3 acts in a redundant way with its closest homologue LTP4 by modulating ABA pathway. Taken together, our data show that LTP3 is a novel negative regulator of plant immunity that is acting through the manipulation of the ABA-SA balance.

Concepts: Cell wall, DNA, Amino acid, Protein, Bacteria, Plant pathogens and diseases, Gene, Pseudomonas syringae

23

Xanthomonas arboricola pv. pruni (Xap) causes bacterial spot of stone fruits and almond, an important disease that may reduce the yield and vigor of the trees, as well as the marketability of affected fruits. Xap, is within the Xanthomonas genus which has been intensively studied due its strain specialization and the host range complexity. Here, we have summarized the recent advances in our understanding of the complexities of Xap, including the studies of molecular features that resulted after comparative phenotypic and genomic analyses, in order to obtain a clearer overview of the bacterial behavior and their infection mechanisms in the context of the X. arboricola species. Taxonomic status: Bacteria; Phylum Proteobacteria; Class Gammaproteobacteria; Order Xanthomonadales; Family Xanthomonadaceae; Genus Xanthomonas; Species X. arboricola; Pathovar pruni. Host range and symptoms: Xap infects most Prunus species including apricot, peach, nectarine, plum and almond, and occasionally cherry. Symptoms are found on leaves, fruits, twigs and branches or trunks. In severe infections defoliation and fruit dropping may occur. Distribution: Bacterial spot of stone fruits and almond is worldwide in distribution with Xap being isolated in Africa, North and South America, Asia, Europe and Oceania continents. It is a common disease in geographic areas where stone fruits and almond are grown. Xap is listed as a quarantine organism in several areas of the world. Genome: Genomes of six isolates from Xap have been publicly released. The genome consists of a single chromosome around 5,000,000 bp with a 65 mol% GC content and extrachromosomal plasmid element of around 41,000 bp with a 62 mol% GC content. Genomic comparative studies in X. arboricola allowed identification of putative virulence components associated with the infection process of bacterial spot of stone fruits and almond. Disease control: Management of bacterial spot of stone fruits and almond is based on an integrated approach that comprises essentially measures to avoid Xap introduction in a producing zone, as well as the use of tolerant or resistant plant material and chemical treatments, mainly based in copper compounds. Management programs include also the use of proper cultivation practices when the disease is already stablished. Finally, for effective control of the disease, proper detection and characterization methods are needed to be used in symptomatic or asymptomatic samples as a first approach for pathogen exclusion. This article is protected by copyright. All rights reserved.

Concepts: Drupe, Proteobacteria, Infection, Prunus, Bacteria, DNA, Gene, Genome

13

Oomycetes form a deep lineage of eukaryotic organisms that includes a large number of plant pathogens that threaten natural and managed ecosystems. We undertook a survey to query the community for their ranking of plant pathogenic oomycete species based on scientific and economic importance. In total, we received 263 votes from 62 scientists in 15 countries for a total of 33 species. The Top 10 species and their ranking are: (1) Phytophthora infestans; (2, tied) Hyaloperonospora arabidopsidis; (2, tied) Phytophthora ramorum; (4) Phytophthora sojae; (5) Phytophthora capsici; (6) Plasmopara viticola; (7) Phytophthora cinnamomi; (8, tied) Phytophthora parasitica; (8, tied) Pythium ultimum; and (10) Albugo candida. The article provides an introduction to these 10 taxa and a snapshot of current research. We hope that the list will serve as a benchmark for future trends in oomycete research.

Concepts: Heterokont, Eukaryote, Sudden oak death, Phytophthora infestans, Oomycete, Phytophthora, Plant pathogens and diseases, Water moulds

12

Fusarium oxysoporum f. sp. radicis-cucumerinum (Forc) is able to cause disease in cucumber, melon, and watermelon, while F. oxysporum f. sp. melonis (Fom) can only infect melon plants. Earlier research showed that mobile chromosomes in Forc and Fom determine the difference in host range between Forc and Fom. By closely comparing these pathogenicity chromosomes combined with RNA-sequencing data, we selected 11 candidate genes that we tested for involvement in the difference in host range between Forc and Fom. One of these candidates is a putative effector gene on the Fom pathogenicity chromosome that has nonidentical homologs on the Forc pathogenicity chromosome. Four independent Forc transformants with this gene from Fom showed strongly reduced or no pathogenicity towards cucumber, while retaining pathogenicity towards melon and watermelon. This suggests that the protein encoded by this gene is recognized by an immune receptor in cucumber plants. This is the first time that a single gene has been demonstrated to determine a difference in host specificity between formae speciales of F. oxysporum.