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RXLR evolution

Gaetan J A Thilliez, Miles R Armstrong, Tze-Yin Lim, Katie Baker, Agathe Jouet, Ben Ward, Cock van Oosterhout, Jonathan D G Jones, Edgar Huitema, Paul R J Birch, Ingo Hein
The oomycete pathogens Phytophthora infestans and P. capsici cause significant crop losses world-wide, threatening food security. In each case, pathogenicity factors, called RXLR effectors, contribute to virulence. Some RXLRs are perceived by resistance proteins to trigger host immunity, but our understanding of the demographic processes and adaptive evolution of pathogen virulence remains poor. Here, we describe PenSeq, a highly efficient enrichment sequencing approach for genes encoding pathogenicity determinants which, as shown for the infamous potato blight pathogen Phytophthora infestans, make up < 1% of the entire genome...
October 5, 2018: New Phytologist
Jamie McGowan, David A Fitzpatrick
The oomycetes are a class of microscopic, filamentous eukaryotes within the stramenopiles-alveolate- Rhizaria (SAR) supergroup and include ecologically significant animal and plant pathogens. Oomycetes secrete large arsenals of effector proteins that degrade host cell components, manipulate host immune responses, and induce necrosis, enabling parasitic colonization. This study investigated the expansion and evolution of effectors in 37 oomycete species in 4 oomycete orders, including Albuginales , Peronosporales , Pythiales , and Saprolegniales species...
November 2017: MSphere
Wenwu Ye, Yang Wang, Brett M Tyler, Yuanchao Wang
Comparative genomic analysis is useful for identifying genes affected by evolutionary selection and for studying adaptive variation in gene functions. In Phytophthora sojae, a model oomycete plant pathogen, the related study is lacking. We compared sequence data among four isolates of P. sojae, which represent its four major genotypes. These isolates exhibited >99.688%, >99.864%, and >98.981% sequence identities at genome, gene, and non-gene regions, respectively. One hundred and fifty-three positive selection and 139 negative selection candidate genes were identified...
2016: Frontiers in Microbiology
Hui Liu, Xiao Ma, Haiqin Yu, Dunhuang Fang, Yongping Li, Xiao Wang, Wen Wang, Yang Dong, Bingguang Xiao
BACKGROUND: Black shank is a severe plant disease caused by the soil-borne pathogen Phytophthora nicotianae. Two physiological races of P. nicotianae, races 0 and 1, are predominantly observed in cultivated tobacco fields around the world. Race 0 has been reported to be more aggressive, having a shorter incubation period, and causing worse root rot symptoms, while race 1 causes more severe necrosis. The molecular mechanisms underlying the difference in virulence between race 0 and 1 remain elusive...
2016: GigaScience
María Josefina Iribarren, Cecilia Pascuan, Gabriela Soto, Nicolás Daniel Ayub
Phytophthora capsici is a virulent oomycete pathogen of many vegetable crops. Recently, it has been demonstrated that the recognition of the RXLR effector AVR3a1 of P. capsici (PcAVR3a1) triggers a hypersensitive response and plays a critical role in mediating non-host resistance. Here, we analyzed the occurrence of PcAVR3a1 in 57 isolates of P. capsici derived from globe squash, eggplant, tomato and bell pepper cocultivated in a small geographical area. The occurrence of PcAVR3a1 in environmental strains of P...
November 2015: FEMS Microbiology Letters
Rahul Sharma, Xiaojuan Xia, Liliana M Cano, Edouard Evangelisti, Eric Kemen, Howard Judelson, Stan Oome, Christine Sambles, D Johan van den Hoogen, Miloslav Kitner, Joël Klein, Harold J G Meijer, Otmar Spring, Joe Win, Reinhard Zipper, Helge B Bode, Francine Govers, Sophien Kamoun, Sebastian Schornack, David J Studholme, Guido Van den Ackerveken, Marco Thines
BACKGROUND: Downy mildews are the most speciose group of oomycetes and affect crops of great economic importance. So far, there is only a single deeply-sequenced downy mildew genome available, from Hyaloperonospora arabidopsidis. Further genomic resources for downy mildews are required to study their evolution, including pathogenicity effector proteins, such as RxLR effectors. Plasmopara halstedii is a devastating pathogen of sunflower and a potential pathosystem model to study downy mildews, as several Avr-genes and R-genes have been predicted and unlike Arabidopsis downy mildew, large quantities of almost contamination-free material can be obtained easily...
October 5, 2015: BMC Genomics
Wenwu Ye, Yang Wang, Yuanchao Wang
RxLR effectors represent one of the largest and most diverse effector families in oomycete plant pathogens. These effectors have attracted enormous attention since they can be delivered inside the plant cell and manipulates host immunity. With the exceptions of a signal peptide and the following RxLR-dEER and C-terminal W/Y/L motifs identified from the sequences themselves, nearly no functional domains have been found. Recently, protein structures of several RxLRs were revealed to comprise alpha-helical bundle repeats...
2015: PloS One
Lida Derevnina, Sebastian Chin-Wo-Reyes, Frank Martin, Kelsey Wood, Lutz Froenicke, Otmar Spring, Richard Michelmore
Peronospora tabacina is an obligate biotrophic oomycete that causes blue mold or downy mildew on tobacco (Nicotiana tabacum). It is an economically important disease occurring frequently in tobacco-growing regions worldwide. We sequenced and characterized the genomes of two P. tabacina isolates and mined them for pathogenicity-related proteins and effector-encoding genes. De novo assembly of the genomes using Illumina reads resulted in 4,016 (63.1 Mb, N50 = 79 kb) and 3,245 (55.3 Mb, N50 = 61 kb) scaffolds for isolates 968-J2 and 968-S26, respectively, with an estimated genome size of 68 Mb...
November 2015: Molecular Plant-microbe Interactions: MPMI
Ryan G Anderson, Devdutta Deb, Kevin Fedkenheuer, John M McDowell
Some of the most devastating oomycete pathogens deploy effector proteins, with the signature amino acid motif RXLR, that enter plant cells to promote virulence. Research on the function and evolution of RXLR effectors has been very active over the decade that has transpired since their discovery. Comparative genomics indicate that RXLR genes play a major role in virulence for Phytophthora and downy mildew species. Importantly, gene-for-gene resistance against these oomycete lineages is based on recognition of RXLR proteins...
October 2015: Molecular Plant-microbe Interactions: MPMI
Erica M Goss, Caroline M Press, Niklaus J Grünwald
Phytophthora plant pathogens contain many hundreds of effectors potentially involved in infection of host plants. Comparative genomic analyses have shown that these effectors evolve rapidly and have been subject to recent expansions. We examined the recent sequence evolution of RXLR-class effector gene families in the sudden oak death pathogen, P. ramorum. We found that P. ramorum RXLR effectors have taken multiple evolutionary paths, including loss or gain of repeated domains, recombination or gene conversion among paralogs, and selection on point mutations...
2013: PloS One
Bishwo N Adhikari, John P Hamilton, Marcelo M Zerillo, Ned Tisserat, C André Lévesque, C Robin Buell
The kingdom Stramenopile includes diatoms, brown algae, and oomycetes. Plant pathogenic oomycetes, including Phytophthora, Pythium and downy mildew species, cause devastating diseases on a wide range of host species and have a significant impact on agriculture. Here, we report comparative analyses on the genomes of thirteen straminipilous species, including eleven plant pathogenic oomycetes, to explore common features linked to their pathogenic lifestyle. We report the sequencing, assembly, and annotation of six Pythium genomes and comparison with other stramenopiles including photosynthetic diatoms, and other plant pathogenic oomycetes such as Phytophthora species, Hyaloperonospora arabidopsidis, and Pythium ultimum var...
2013: PloS One
Rays H Y Jiang, Irene de Bruijn, Brian J Haas, Rodrigo Belmonte, Lars Löbach, James Christie, Guido van den Ackerveken, Arnaud Bottin, Vincent Bulone, Sara M Díaz-Moreno, Bernard Dumas, Lin Fan, Elodie Gaulin, Francine Govers, Laura J Grenville-Briggs, Neil R Horner, Joshua Z Levin, Marco Mammella, Harold J G Meijer, Paul Morris, Chad Nusbaum, Stan Oome, Andrew J Phillips, David van Rooyen, Elzbieta Rzeszutek, Marcia Saraiva, Chris J Secombes, Michael F Seidl, Berend Snel, Joost H M Stassen, Sean Sykes, Sucheta Tripathy, Herbert van den Berg, Julio C Vega-Arreguin, Stephan Wawra, Sarah K Young, Qiandong Zeng, Javier Dieguez-Uribeondo, Carsten Russ, Brett M Tyler, Pieter van West
Oomycetes in the class Saprolegniomycetidae of the Eukaryotic kingdom Stramenopila have evolved as severe pathogens of amphibians, crustaceans, fish and insects, resulting in major losses in aquaculture and damage to aquatic ecosystems. We have sequenced the 63 Mb genome of the fresh water fish pathogen, Saprolegnia parasitica. Approximately 1/3 of the assembled genome exhibits loss of heterozygosity, indicating an efficient mechanism for revealing new variation. Comparison of S. parasitica with plant pathogenic oomycetes suggests that during evolution the host cellular environment has driven distinct patterns of gene expansion and loss in the genomes of plant and animal pathogens...
June 2013: PLoS Genetics
Stephen Whisson, Ramesh Vetukuri, Anna Avrova, Christina Dixelius
Transposable elements are ubiquitous residents in eukaryotic genomes. Often considered to be genomic parasites, they can lead to dramatic changes in genome organization, gene expression, and gene evolution. The oomycete plant pathogen Phytophthora infestans has evolved a genome organization where core biology genes are predominantly located in genome regions that have relatively few resident transposons. In contrast, disease effector-encoding genes are most frequently located in rapidly evolving genomic regions that are rich in transposons...
March 1, 2012: Mobile Genetic Elements
Ryan G Anderson, Megan S Casady, Rachel A Fee, Martha M Vaughan, Devdutta Deb, Kevin Fedkenheuer, Alisa Huffaker, Eric A Schmelz, Brett M Tyler, John M McDowell
Diverse pathogens secrete effector proteins into plant cells to manipulate host cellular processes. Oomycete pathogens contain large complements of predicted effector genes defined by an RXLR host cell entry motif. The genome of Hyaloperonospora arabidopsidis (Hpa, downy mildew of Arabidopsis) contains at least 134 candidate RXLR effector genes. Only a small subset of these genes is conserved in related oomycetes from the Phytophthora genus. Here, we describe a comparative functional characterization of the Hpa RXLR effector gene HaRxL96 and a homologous gene, PsAvh163, from the Glycine max (soybean) pathogen Phytophthora sojae...
December 2012: Plant Journal: for Cell and Molecular Biology
Elizabeth A Savory, Cheng Zou, Bishwo N Adhikari, John P Hamilton, C Robin Buell, Shin-Han Shiu, Brad Day
Pseudoperonospora cubensis, an obligate oomycete pathogen, is the causal agent of cucurbit downy mildew, a foliar disease of global economic importance. Similar to other oomycete plant pathogens, Ps. cubensis has a suite of RXLR and RXLR-like effector proteins, which likely function as virulence or avirulence determinants during the course of host infection. Using in silico analyses, we identified 271 candidate effector proteins within the Ps. cubensis genome with variable RXLR motifs. In extending this analysis, we present the functional characterization of one Ps...
2012: PloS One
Matthew G Links, Eric Holub, Rays H Y Jiang, Andrew G Sharpe, Dwayne Hegedus, Elena Beynon, Dean Sillito, Wayne E Clarke, Shihomi Uzuhashi, Mohammad H Borhan
BACKGROUND: Albugo candida is a biotrophic oomycete that parasitizes various species of Brassicaceae, causing a disease (white blister rust) with remarkable convergence in behaviour to unrelated rusts of basidiomycete fungi. RESULTS: A recent genome analysis of the oomycete Hyaloperonospora arabidopsidis suggests that a reduction in the number of genes encoding secreted pathogenicity proteins, enzymes for assimilation of inorganic nitrogen and sulphur represent a genomic signature for the evolution of obligate biotrophy...
2011: BMC Genomics
Laurence S Boutemy, Stuart R F King, Joe Win, Richard K Hughes, Thomas A Clarke, Tharin M A Blumenschein, Sophien Kamoun, Mark J Banfield
Phytopathogens deliver effector proteins inside host plant cells to promote infection. These proteins can also be sensed by the plant immune system, leading to restriction of pathogen growth. Effector genes can display signatures of positive selection and rapid evolution, presumably a consequence of their co-evolutionary arms race with plants. The molecular mechanisms underlying how effectors evolve to gain new virulence functions and/or evade the plant immune system are poorly understood. Here, we report the crystal structures of the effector domains from two oomycete RXLR proteins, Phytophthora capsici AVR3a11 and Phytophthora infestans PexRD2...
October 14, 2011: Journal of Biological Chemistry
Eric Kemen, Anastasia Gardiner, Torsten Schultz-Larsen, Ariane C Kemen, Alexi L Balmuth, Alexandre Robert-Seilaniantz, Kate Bailey, Eric Holub, David J Studholme, Dan Maclean, Jonathan D G Jones
Biotrophic eukaryotic plant pathogens require a living host for their growth and form an intimate haustorial interface with parasitized cells. Evolution to biotrophy occurred independently in fungal rusts and powdery mildews, and in oomycete white rusts and downy mildews. Biotroph evolution and molecular mechanisms of biotrophy are poorly understood. It has been proposed, but not shown, that obligate biotrophy results from (i) reduced selection for maintenance of biosynthetic pathways and (ii) gain of mechanisms to evade host recognition or suppress host defence...
July 2011: PLoS Biology
Vivianne G A A Vleeshouwers, Sylvain Raffaele, Jack H Vossen, Nicolas Champouret, Ricardo Oliva, Maria E Segretin, Hendrik Rietman, Liliana M Cano, Anoma Lokossou, Geert Kessel, Mathieu A Pel, Sophien Kamoun
Potato (Solanum tuberosum) is the world's third-largest food crop. It severely suffers from late blight, a devastating disease caused by Phytophthora infestans. This oomycete pathogen secretes host-translocated RXLR effectors that include avirulence (AVR) proteins, which are targeted by resistance (R) proteins from wild Solanum species. Most Solanum R genes appear to have coevolved with P. infestans at its center of origin in central Mexico. Various R and Avr genes were recently cloned, and here we catalog characterized R-AVR pairs...
2011: Annual Review of Phytopathology
Joe Win, Sophien Kamoun, Alexandra M E Jones
Effectors of plant pathogens play important roles in not only pathogenesis but also plant immunity. Plant pathogens use these effectors to manipulate host cells for colonization, and their activities likely influence the evolution of plant immune responses. Analyses of genome sequences revealed that oomycete pathogens, such as Phytophthora spp., possess hundreds of RXLR effectors that are thought to be delivered into the host cells and hence function inside the cells by interacting with the host protein complexes...
2011: Methods in Molecular Biology
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