Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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The genome of Peronospora belbahrii reveals high heterozygosity, a low number of canonical effectors and CT-rich promoters
Thines, M. ; Sharma, R. ; Rodenburg, Y.A. ; Gogleva, A. ; Judelson, H.S. ; Xia, X. ; Hoogen, D.J. van den; Kitner, M. ; Klein, J. ; Neilen, M. ; Ridder, D. de; Seidl, M.F. ; Ackerveken, G. van den; Govers, F. ; Schornack, S. ; Studholme, D.J. - \ 2019
Along with Plasmopara destructor, Peronosopora belbahrii has arguably been the economically most important newly emerging downy mildew pathogen of the past two decades. Originating from Africa, it has started devastating basil production throughout the world, most likely due to the distribution of infested seed material. Here we present the genome of this pathogen and results from comparisons of its genomic features to other oomycetes. The assembly of the nuclear genome was ca. 35.4 Mbp in length, with an N50 scaffold length of ca. 248 kbp and an L50 scaffold count of 46. The circular mitochondrial genome consisted of ca. 40.1 kbp. From the repeat-masked genome 9049 protein-coding genes were predicted, out of which 335 were predicted to have extracellular functions, representing the smallest secretome so far found in peronosporalean oomycetes. About 16 % of the genome consists of repetitive sequences, and based on simple sequence repeat regions, we provide a set of microsatellites that could be used for population genetic studies of Pe. belbahrii. Peronospora belbahrii has undergone a high degree of convergent evolution, reflecting its obligate biotrophic lifestyle. Features of its secretome, signalling networks, and promoters are presented, and some patterns are hypothesised to reflect the high degree of host specificity in Peronospora species. In addition, we suggest the presence of additional virulence factors apart from classical effector classes that are promising candidates for future functional studies.
Activity and phylogenetics of the broadly occurring family of microbial nep1-like proteins
Seidl, Michael F. ; Ackerveken, Guido Van Den - \ 2019
Annual Review of Phytopathology 57 (2019). - ISSN 0066-4286 - p. 367 - 386.
Cytolytic activity - GIPC binding - NEP1-like proteins - Pattern-Triggered immunity - Phylogeny - Phytotoxins

Necrosis-and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP) have an extremely broad taxonomic distribution; they occur in bacteria, fungi, and oomycetes. NLPs come in two forms, those that are cytotoxic to eudicot plants and those that are noncytotoxic. Cytotoxic NLPs bind to glycosyl inositol phosphoryl ceramide (GIPC) sphingolipids that are abundant in the outer leaflet of plant plasma membranes. Binding allows the NLP to become cytolytic in eudicots but not monocots. The function of noncytotoxic NLPs remains enigmatic, but the expansion of NLP genes in oomycete genomes suggests they are important. Several plant species have evolved the capacity to recognize NLPs as molecular patterns and trigger plant immunity, e.g., Arabidopsis thaliana detects nlp peptides via the receptor-like protein RLP23. In this review, we provide a historical perspective from discovery to understanding of molecular mechanisms and describe the latest developments in the NLP field to shed light on these fascinating microbial proteins.

Comparative genomics including the basal pathogen Peronospora belbahrii reveal common evolutionary patterns and the monophyly of downy mildews in a paraphyletic Phytophthora
Thines, M. ; Sharma, R. ; Rodenburg, Y.A. ; Gogleva, A. ; Judelson, H.S. ; Xia, X. ; Hoogen, D.J. van den; Kitner, M. ; Klein, J. ; Ridder, D. de; Seidl, M.F. ; Ackerveken, G. van den; Govers, F. ; Schornack, S. ; Studholme, D.J. - \ 2018
PRJEB15119 - ERP016822 - Peronospora belbahrii
The obligate biotrophic downy mildew constitute the most species rich group of oomycetes. So far only handful of genomes of this group of pathogens has been sequenced. Most likely due to low taxon sampling, until now phylogenomic studies with few taxa were in stark contrast to multigene phylogenies with a large number of accessions with respect to the relationships of downy mildews and Phytophthora species. In the current study, we sequenced the whole genome of the economically important basil pathogen Peronospora belbahrii, and performed in-depth comparative genomics and phylogenomics towards clarifying some aspects of downy mildew and Phytophthora evolution.
Effector-mediated discovery of a novel resistance gene against Bremia Lactucae in a nonhost lettuce species
Giesbers, A.K.J. ; Pelgrom, Alexandra ; Visser, R.G.F. ; Niks, R.E. ; Ackerveken, Guido Van Den; Jeuken, M.J.W. - \ 2017
New Phytologist 216 (2017)3. - ISSN 0028-646X - p. 915 - 926.
Candidate effectors from lettuce downy mildew (Bremia lactucae) enable high-throughput germplasm screening for the presence of resistance (R) genes. The nonhost species Lactuca saligna comprises a source of B. lactucae R genes that has hardly been exploited in lettuce breeding. Its cross-compatibility with the host species L. sativa enables the study of inheritance of nonhost resistance (NHR). We performed transient expression of candidate RXLR effector genes from B. lactucae in a diverse Lactuca germplasm set. Responses to two candidate effectors (BLR31 and BLN08) were genetically mapped and tested for co-segregation with disease resistance. BLN08 induced a hypersensitive response (HR) in 55% of the L. saligna accessions, but responsiveness did not co-segregate with resistance to Bl:24. BLR31 triggered an HR in 5% of the L. saligna accessions, and revealed a novel R gene providing complete B. lactucae race Bl:24 resistance. Resistant hybrid plants that were BLR31 nonresponsive indicated other unlinked R genes and/or nonhost QTLs. We have identified a candidate avirulence effector of B. lactucae (BLR31) and its cognate R gene in L. saligna. Concurrently, our results suggest that R genes are not required for NHR of L. saligna.
DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis
Zeilmaker, Tieme ; Ludwig, N.R. ; Elberse, Joyce ; Seidl, M.F. ; Berke, Lidija ; Doorn, Arjen Van; Schuurink, Robert C. ; Snel, Berend ; Ackerveken, Guido Van Den - \ 2015
The Plant Journal 81 (2015)2. - ISSN 0960-7412 - p. 210 - 222.
Arabidopsis thaliana - DMR6-like oxygenase - downy mildew resistant 6 - immunity - negative regulator - suppressor

Arabidopsis downy mildew resistant 6 (dmr6) mutants have lost their susceptibility to the downy mildew Hyaloperonospora arabidopsidis. Here we show that dmr6 is also resistant to the bacterium Pseudomonas syringae and the oomycete Phytophthora capsici. Resistance is accompanied by enhanced defense gene expression and elevated salicylic acid levels. The suppressive effect of the DMR6 oxygenase was confirmed in transgenic Arabidopsis lines overexpressing DMR6 that show enhanced susceptibility to H. arabidopsidis, P. capsici, and P. syringae. Phylogenetic analysis of the superfamily of 2-oxoglutarate Fe(II)-dependent oxygenases revealed a subgroup of DMR6-LIKE OXYGENASEs (DLOs). Within Arabidopsis, DMR6 is most closely related to DLO1 and DLO2. Overexpression of DLO1 and DLO2 in the dmr6 mutant restored the susceptibility to downy mildew indicating that DLOs negatively affect defense, similar to DMR6. DLO1, but not DLO2, is co-expressed with DMR6, showing strong activation during pathogen attack and following salicylic acid treatment. DMR6 and DLO1 differ in their spatial expression pattern in downy mildew-infected Arabidopsis leaves; DMR6 is mostly expressed in cells that are in contact with hyphae and haustoria of H. arabidopsidis, while DLO1 is expressed mainly in the vascular tissues near infection sites. Strikingly, the dmr6-3-dlo1 double mutant, that is completely resistant to H. arabidopsidis, showed a strong growth reduction that was associated with high levels of salicylic acid. We conclude that DMR6 and DLO1 redundantly suppress plant immunity, but also have distinct activities based on their differential localization of expression.

Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora
Sharma, R. ; Xia, X. ; Cano, L.M. ; Evangelisti, E. ; Kemen, E. ; Judelson, H. ; Oome, S. ; Sambles, C. ; Hoogen, D.J. van den; Kitner, M. ; Klein, J. ; Meijer, H.J.G. ; Spring, O. ; Win, J. ; Zipper, R. ; Bode, H.B. ; Govers, F. ; Kamoun, S. ; Schornack, S. ; Studholme, D.J. ; Ackerveken, G. van den; Thines, M. - \ 2015
BMC Genomics 16 (2015). - ISSN 1471-2164 - 23 p.
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. Results Here a high-quality draft genome of Plasmopara halstedii is reported and analysed with respect to various aspects, including genome organisation, secondary metabolism, effector proteins and comparative genomics with other sequenced oomycetes. Interestingly, the present analyses revealed further variation of the RxLR motif, suggesting an important role of the conservation of the dEER-motif. Orthology analyses revealed the conservation of 28 RxLR-like core effectors among Phytophthora species. Only six putative RxLR-like effectors were shared by the two sequenced downy mildews, highlighting the fast and largely independent evolution of two of the three major downy mildew lineages. This is seemingly supported by phylogenomic results, in which downy mildews did not appear to be monophyletic. Conclusions The genome resource will be useful for developing markers for monitoring the pathogen population and might provide the basis for new approaches to fight Phytophthora and downy mildew pathogens by targeting core pathogenicity effectors.
The Top 10 oomycete pathogens in molecular plant pathology
Kamoun, S. ; Furzer, O. ; Jones, J.D.G. ; Judelson, H.S. ; Ali, G.S. ; Dalio, R.J.D. ; Roy, S.G. ; Schena, L. ; Zambounis, A. ; Panabières, F. ; Cahill, D. ; Ruocco, M. ; Figueiredo, A. ; Chen, X.R. ; Hulvey, J. ; Stam, R. ; Lamour, K. ; Gijzen, M. ; Tyler, B.M. ; Grünwald, N.J. ; Mukhtar, M.S. ; Tomé, D.F.A. ; Tör, M. ; Ackerveken, G. van den; McDowell, J. ; Daayf, F. ; Fry, W.E. ; Lindqvist-Kreuze, H. ; Meijer, H.J.G. ; Petre, B. ; Ristaino, J. ; Yoshida, K. ; Birch, P.R.J. ; Govers, F. - \ 2015
Molecular Plant Pathology 16 (2015)4. - ISSN 1464-6722 - p. 413 - 434.
grapevine downy mildew - irish potato famine - sudden oak death - blister rusts albuginaceae - eastern united-states - 3 clonal lineages - nb-lrr gene - phytophthora-infestans - plasmopara-viticola - arabidopsis-thaliana
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.
Genetic investigation of the nonhost resistance of wild lettuce, Lactuca saligna, to lettuce downy mildew, Bremia lactucae
Boer, E. den - \ 2014
Wageningen University. Promotor(en): Richard Visser, co-promotor(en): Marieke Jeuken; Rients Niks. - Wageningen : Wageningen University - ISBN 9789462572072 - 186
lactuca saligna - schimmelziekten - bremia lactucae - ziekteresistentie - terugkruisen - inteeltlijnen - genetische kartering - lactuca sativa - lactuca saligna - fungal diseases - bremia lactucae - disease resistance - backcrossing - inbred lines - genetic mapping - lactuca sativa


Downy mildew (Bremia lactucae) in lettuce (Lactuca sativa) is a devastating foliar disease causing high losses in lettuce cultivation. The wild lettuce and nonhost species, Lactuca saligna, is absolute resistant to downy mildew and cross-fertile with L. sativa, albeit with a low success rate and occasional reduced fertility and/or vitality in later inbred generations. This exceptional availability of hybrid plant offsprings creates a unique opportunity to study nonhost resistance by a genetic approach.

The L. saligna nonhost resistance genes might be more durable than the classical monogenic race-specific R genes that are mainly used in lettuce breeding. The identification of genes conferring nonhost resistance is a crucial step in its understanding and usage in breeding.

In this thesis the quantitative resistances of three backcross introgression lines (BILs), carrying an individual 30 to 50 cM long introgression segment from L. saligna in a L. sativa background, were fine mapped. Disease evaluation of sub-BILs with smaller introgression segments revealed that the resistance of all three BILs was explained by 17 sub-QTLs with a smaller and plant stage dependent effect, some segments reducing, others even promoting downy mildew infection.

Further the potential of stacking quantitative resistances of eight BILs per combinations of two was tested under field conditions. Only three out of ten double-combinations resulted in an increased resistance level compared to their parental individual lines, from which one had additive and two had epistatic interactions between the introgressions.

As the studies on individual QTL effects of BILs did not reveal potential genetic interactions that could explain the complete resistance of L. saligna, a novel approach was set out to search for indications of epistatic interactions. ‘Selective genotyping’ was applied on the phenotypic disease extremes of large F2 offsprings, in which multi-locus interactions between L. saligna alleles are still prevalent. In a kind of bulked segregant analysis approach four major resistance regions were identified. Preliminary results showed epistatic interactions between the regions on Chromosome 6 and 1 and between Chromosome 6 and 7.

During the development of sub-BILs, a digenic hybrid incompatibility was observed: plants carrying a L. saligna segment on Chromosome 6 always required a L. saligna segment on Chromosome 4. Segregation analysis suggested a prezygotic reproductive barrier by non-transmission of one specific hybrid gametophyte (male and female).

In cooperation with the research group of Guido van den Ackerveken of University Utrecht a lettuce germplasm screening was conducted for candidate downy mildew effector proteins, which interact with resistance genes in lettuce and trigger a defence response. One of two responsive effector proteins, ‘BLG01’, triggered a hypersensitive cell death response in most tested L. saligna accessions and its response was mapped on Chromosome 9.

Despite the complex interactions between resistance QTLs, this thesis research has delivered many insights that are important steps forward towards understanding the incompatible interaction between B. lactucae and L. saligna and its future application in resistance breeding.

Fungal endopolygalacturonases are recognized as MAMPs by the Arabidopsis Receptor-Like Protein RBPG1
Zhang, L. ; Kars, I. ; Essenstam, B. ; Liebrand, T.W.H. ; Wagemakers, L. ; Elberse, J. ; Tagkalaki, P. ; Tjoitang, D. ; Ackerveken, G. van den; Kan, J.A.L. van - \ 2014
Plant Physiology 164 (2014)1. - ISSN 0032-0889 - p. 352 - 364.
ethylene-inducing xylanase - agrobacterium-mediated transformation - innate immunity - nicotiana-benthamiana - necrotizing activity - enzymatic-activity - aspergillus-niger - plasma-membrane - plant immunity - active-site
Plants perceive microbial invaders using pattern recognition receptors that recognize microbe-associated molecular patterns. In this study, we identified RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1 (RBPG1), an Arabidopsis (Arabidopsis thaliana) leucine-rich repeat receptor-like protein, AtRLP42, that recognizes fungal endopolygalacturonases (PGs) and acts as a novel microbe-associated molecular pattern receptor. RBPG1 recognizes several PGs from the plant pathogen Botrytis cinerea as well as one from the saprotroph Aspergillus niger. Infiltration of B. cinerea PGs into Arabidopsis accession Columbia induced a necrotic response, whereas accession Brno (Br-0) showed no symptoms. A map-based cloning strategy, combined with comparative and functional genomics, led to the identification of the Columbia RBPG1 gene and showed that this gene is essential for the responsiveness of Arabidopsis to the PGs. Transformation of RBPG1 into accession Br-0 resulted in a gain of PG responsiveness. Transgenic Br-0 plants expressing RBPG1 were equally susceptible as the recipient Br-0 to the necrotroph B. cinerea and to the biotroph Hyaloperonospora arabidopsidis. Pretreating leaves of the transgenic plants with a PG resulted in increased resistance to H. arabidopsidis. Coimmunoprecipitation experiments demonstrated that RBPG1 and PG form a complex in Nicotiana benthamiana, which also involves the Arabidopsis leucine-rich repeat receptor-like protein SOBIR1 (for SUPPRESSOR OF BIR1). sobir1 mutant plants did not induce necrosis in response to PGs and were compromised in PG-induced resistance to H. arabidopsidis.
Exploring evolution and biology of oomycetes; integrative and comparative genomics
Seidl, M.F. - \ 2013
Utrecht University. Promotor(en): P. Hogeweg; Francine Govers, co-promotor(en): B. Snel; A.F.J.M. Ackerveken. - - 174
Powdery Mildew Resistance in Tomato by Impairment of SIPMR4 and SIDMR1
Huibers, R.P. ; Loonen, A.E.H.M. ; Dongli Gao, Dongli ; Ackerveken, G. van den; Visser, R.G.F. ; Bai, Y. - \ 2013
PLoS ONE 8 (2013)6. - ISSN 1932-6203
zinc-finger nucleases - disease resistance - arabidopsis mutants - targeted mutagenesis - gene - plants - pathogenesis - mutation
Genetic dissection of disease susceptibility in Arabidopsis to powdery and downy mildew has identified multiple susceptibility (S) genes whose impairment results in disease resistance. Although several of these S-genes have been cloned and characterized in more detail it is unknown to which degree their function in disease susceptibility is conserved among different plant species. Moreover, it is unclear whether impairment of such genes has potential in disease resistance breeding due to possible fitness costs associated with impaired alleles. Here we show that the Arabidopsis PMR4 and DMR1, genes encoding a callose synthase and homoserine kinase respectively, have functional orthologs in tomato with respect to their S-gene function. Silencing of both genes using RNAi resulted in resistance to the tomato powdery mildew fungus Oidium neolycopersici. Resistance to O. neolycopersici by SlDMR1 silencing was associated with severely reduced plant growth whereas SlPMR4 silencing was not. SlPMR4 is therefore a suitable candidate gene as target for mutagenesis to obtain alleles that can be deployed in disease resistance breeding of tomato.
Specific In Planta Recognition of Two GKLR Proteins of the Downy Mildew Bremia lactucae Revealed in a Large Effector Screen in Lettuce
Stassen, J.H.M. ; Boer, E. den; Vergeer, P.W.J. ; Andel, A. ; Ellendorff, U. ; Pelgrom, K.T.B. ; Pel, M. ; Schut, J. ; Zonneveld, O. ; Jeuken, M.J.W. ; Ackerveken, G. van den - \ 2013
Molecular Plant-Microbe Interactions 26 (2013)11. - ISSN 0894-0282 - p. 1259 - 1270.
backcross inbred lines - genetic-linkage map - disease resistance - phytophthora-infestans - nonhost resistance - avirulence genes - wild lettuce - pathogen - saligna - potato
Breeding lettuce (Lactuca sativa) for resistance to the downy mildew pathogen Bremia lactucae is mainly achieved by introgression of dominant downy mildew resistance (Dm) genes. New Bremia races quickly render Dm genes ineffective, possibly by mutation of recognized host-translocated effectors or by suppression of effector-triggered immunity. We have previously identified 34 potential RXLR(-like) effector proteins of B. lactucae that were here tested for specific recognition within a collection of 129 B. lactucae-resistant Lactuca lines. Two effectors triggered a hypersensitive response: BLG01 in 52 lines, predominantly L. saligna, and BLG03 in two L. sativa lines containing Dm2 resistance. The N-terminal sequences of BLG01 and BLG03, containing the signal peptide and GKLR variant of the RXLR translocation motif, are not required for in planta recognition but function in effector delivery. The locus responsible for BLG01 recognition maps to the bottom of lettuce chromosome 9, whereas recognition of BLG03 maps in the RGC2 cluster on chromosome 2. Lactuca lines that recognize the BLG effectors are not resistant to Bremia isolate Bl:24 that expresses both BLG genes, suggesting that Bl:24 can suppress the triggered immune responses. In contrast, lettuce segregants displaying Dm2-mediated resistance to Bremia isolate Bl:5 are responsive to BLG03, suggesting that BLG03 is a candidate Avr2 protein.
Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica
Jiang, R.H.Y. ; Bruijn, I. de; Haas, B.J. ; Belmonte, R. ; Löbach, L. ; Christie, J. ; Ackerveken, G. van den; Bottin, A. ; Bulone, V. ; Díaz-Moreno, S.M. ; Dumas, B. ; Fan, L. ; Gaulin, E. ; Govers, F. ; Grenville-Briggs, L.J. ; Horner, N.R. ; Levin, J.Z. ; Mammella, M. ; Meijer, H.J.G. ; Morris, P. ; Nusbaum, C. ; Oome, S. ; Phillips, A.J. ; Rooyen, D. van; Rzeszutek, E. ; Saraiva, M. ; Secombes, C.J. ; Seidl, M.F. ; Snel, B. ; Stassen, J.H.M. ; Sykes, S. ; Tripathy, S. ; Berg, H. ; Vega-Arreguin, J.C. ; Wawra, S. ; Young, S.K. ; Zeng, Q. ; Dieguez-Uribeondo, J. ; Russ, C. ; Tyler, B.M. ; West, P. van - \ 2013
Plos Genetics 9 (2013)6. - ISSN 1553-7404 - 20 p.
expressed sequence tags - anthocidaris-crassispina eggs - fully automated process - phytophthora-sojae - aphanomyces-euteiches - plant-pathogens - infestans - cells - evolution - reveals
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. S. parasitica possesses one of the largest repertoires of proteases (270) among eukaryotes that are deployed in waves at different points during infection as determined from RNA-Seq data. In contrast, despite being capable of living saprotrophically, parasitism has led to loss of inorganic nitrogen and sulfur assimilation pathways, strikingly similar to losses in obligate plant pathogenic oomycetes and fungi. The large gene families that are hallmarks of plant pathogenic oomycetes such as Phytophthora appear to be lacking in S. parasitica, including those encoding RXLR effectors, Crinkler's, and Necrosis Inducing-Like Proteins (NLP). S. parasitica also has a very large kinome of 543 kinases, 10% of which is induced upon infection. Moreover, S. parasitica encodes several genes typical of animals or animal-pathogens and lacking from other oomycetes, including disintegrins and galactose-binding lectins, whose expression and evolutionary origins implicate horizontal gene transfer in the evolution of animal pathogenesis in S. parasitica.
Genetical Genomics Reveals Large Scale Genotype-By-Environment Interactions in Arabidopsis thaliana
Snoek, L.B. ; Terpstra, I.R. ; Dekter, R. ; Ackerveken, G. van den; Peeters, A.J. - \ 2013
Frontiers in Genetics Livestock Genomics 3 (2013). - ISSN 1664-8021
One of the major goals of quantitative genetics is to unravel the complex interactions between molecular genetic factors and the environment. The effects of these genotype-by-environment interactions also affect and cause variation in gene expression. The regulatory loci responsible for this variation can be found by genetical genomics that involves the mapping of quantitative trait loci (QTLs) for gene expression traits also called expression-QTL (eQTLs). Most genetical genomics experiments published so far, are performed in a single environment and hence do not allow investigation of the role of genotype-by-environment interactions. Furthermore, most studies have been done in a steady state environment leading to acclimated expression patterns. However a response to the environment or change therein can be highly plastic and possibly lead to more and larger differences between genotypes. Here we present a genetical genomics study on 120 Arabidopsis thaliana, Landsberg erecta × Cape Verde Islands, recombinant inbred lines (RILs) in active response to the environment by treating them with 3 h of shade. The results of this experiment are compared to a previous study on seedlings of the same RILs from a steady state environment. The combination of two highly different conditions but exactly the same RILs with a fixed genetic variation showed the large role of genotype-by-environment interactions on gene expression levels. We found environment-dependent hotspots of transcript regulation. The major hotspot was confirmed by the expression profile of a near isogenic line. Our combined analysis leads us to propose CSN5A, a COP9 signalosome component, as a candidate regulator for the gene expression response to shade.
Bioinformatic Inference of Specific and General Transcription Factor Binding Sites in the Plant Pathogen Phytophthora infestans
Seidl, M.F. ; Wang, R.P. ; Ackerveken, G. van den; Govers, F. ; Snel, B. - \ 2012
PLoS ONE 7 (2012)12. - ISSN 1932-6203 - 12 p.
core promoters - tata box - cryptococcus-neoformans - regulatory elements - genome sequences - oomycete - initiator - identification - activation - expression
Plant infection by oomycete pathogens is a complex process. It requires precise expression of a plethora of genes in the pathogen that contribute to a successful interaction with the host. Whereas much effort has been made to uncover the molecular systems underlying this infection process, mechanisms of transcriptional regulation of the genes involved remain largely unknown. We performed the first systematic de-novo DNA motif discovery analysis in Phytophthora. To this end, we utilized the genome sequence of the late blight pathogen Phytophthora infestans and two related Phytophthora species (P. ramorum and P. sojae), as well as genome-wide in planta gene expression data to systematically predict 19 conserved DNA motifs. This catalog describes common eukaryotic promoter elements whose functionality is supported by the presence of orthologs of known general transcription factors. Together with strong functional enrichment of the common promoter elements towards effector genes involved in pathogenicity, we obtained a new and expanded picture of the promoter structure in P. infestans. More intriguingly, we identified specific DNA motifs that are either highly abundant or whose presence is significantly correlated with gene expression levels during infection. Several of these motifs are observed upstream of genes encoding transporters, RXLR effectors, but also transcriptional regulators. Motifs that are observed upstream of known pathogenicity-related genes are potentially important binding sites for transcription factors. Our analyses add substantial knowledge to the as of yet virtually unexplored question regarding general and specific gene regulation in this important class of pathogens. We propose hypotheses on the effects of cis-regulatory motifs on the gene regulation of pathogenicity-related genes and pinpoint motifs that are prime targets for further experimental validation.
Reconstruction of Oomycete Genome Evolution Identifies Differences in Evolutionary Trajectories Leading to Present-Day Large Gene Families
Seidl, M.F. ; Ackerveken, G. van den; Govers, F. ; Snel, B. - \ 2012
Genome Biology and Evolution 4 (2012)3. - ISSN 1759-6653 - p. 199 - 211.
nonphotosynthetic protists - phytophthora-infestans - pathogen phytophthora - obligate biotrophy - protein families - plant-pathogens - duplication - reveals - cells - mechanisms
The taxonomic class of oomycetes contains numerous pathogens of plants and animals but is related to nonpathogenic diatoms and brown algae. Oomycetes have flexible genomes comprising large gene families that play roles in pathogenicity. The evolutionary processes that shaped the gene content have not yet been studied by applying systematic tree reconciliation of the phylome of these species. We analyzed evolutionary dynamics of ten Stramenopiles. Gene gains, duplications, and losses were inferred by tree reconciliation of 18,459 gene trees constituting the phylome with a highly supported species phylogeny. We reconstructed a strikingly large last common ancestor of the Stramenopiles that contained ~10,000 genes. Throughout evolution, the genomes of pathogenic oomycetes have constantly gained and lost genes, though gene gains through duplications outnumber the losses. The branch leading to the plant pathogenic Phytophthora genus was identified as a major transition point characterized by increased frequency of duplication events that has likely driven the speciation within this genus. Large gene families encoding different classes of enzymes associated with pathogenicity such as glycoside hydrolases are formed by complex and distinct patterns of duplications and losses leading to their expansion in extant oomycetes. This study unveils the large-scale evolutionary dynamics that shaped the genomes of pathogenic oomycetes. By the application of phylogenetic based analyses methods, it provides additional insights that shed light on the complex history of oomycete genome evolution and the emergence of large gene families characteristic for this important class of pathogens
The superfamily of necrosis and ethylene-inducing peptide 1 (Nep1) like proteins (NLPs) harbors cytotoxic and non-cytotoxic, virulence-promoting members
Nuernberger, T. ; Kuefner, I. ; Anderluh, G. ; Oecking, C. ; Whisson, S. ; Thomma, B. ; Ackerveken, G. van den - \ 2011
In: Book of Abstracts 26th Fungal Genetics Conference, Asilomar, Pacific Grove, California, USA, 15-20 March 2011. - - p. 50 - 50.
Members of the superfamily of necrosis and ethylene-inducing peptide 1 (Nep1) like proteins (NLPs) are widely found in bacteria, fungi and oomycetes. A subset of these proteins causes leaf necrosis on dicot, but not on monocot plants. NLP cytotoxicity was shown to be crucial for microbial virulence and a necrotrophic lifestyle of the producing microbe. X-ray crystallography-based analyses of two microbial NLPs revealed substantial fold conservation of these proteins with cytolytic toxins produced by marine organisms (actinoporins). Actinoporins bind to animal host sphingomyelin prior to membrane pore formation and cytolysis. While plants do not produce sphingomyelins, we show that the target site for NLP toxins is of lipid nature and resides in the outer layer of the plasma membrane of dicot plants. Membrane binding and phytotoxicity requires the presence of a coordinately bound calcium cation within an electrophilic cavity on NLPs, suggesting that the plant docking site is negatively charged. In binding assays, NLPs preferentially bind to phosphorylated phosphatidylinositols (PIP), and incubation of NLPs with PIPs inhibits the cytotoxic activities of these proteins. Thus, NLP susceptibility of plant membranes is determined by its interaction with yet unknown PIP-like lipid structures that define a biologically significant difference in the composition of plasma membranes from monocot and dicot plants. Recently, the production by various oomycetes and fungi of non-cytotoxic members of the NLP superfamily was shown. The possible mode of action of these proteins, their biological activity as well as their contribution to microbial virulence will be discussed
A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization
Seidl, M.F. ; Ackerveken, G. van den; Govers, F. ; Snel, B. - \ 2011
Plant Physiology 155 (2011)2. - ISSN 0032-0889 - p. 628 - 644.
berberine bridge enzyme - cell-wall proteins - phytophthora-infestans - gene-expression - saccharomyces-cerevisiae - nucleotide-sequence - evolution - eukaryotes - mechanisms - phylogeny
Oomycetes comprise a diverse group of organisms that morphologically resemble fungi but belong to the stramenopile lineage within the supergroup of chromalveolates. Recent studies have shown that plant pathogenic oomycetes have expanded gene families that are possibly linked to their pathogenic lifestyle. We analyzed the protein domain organization of 67 eukaryotic species including four oomycete and five fungal plant pathogens. We detected 246 expanded domains in fungal and oomycete plant pathogens. The analysis of genes differentially expressed during infection revealed a significant enrichment of genes encoding expanded domains as well as signal peptides linking a substantial part of these genes to pathogenicity. Overrepresentation and clustering of domain abundance profiles revealed domains that might have important roles in host-pathogen interactions but, as yet, have not been linked to pathogenicity. The number of distinct domain combinations (bigrams) in oomycetes was significantly higher than in fungi. We identified 773 oomycete-specific bigrams, with the majority composed of domains common to eukaryotes. The analyses enabled us to link domain content to biological processes such as host-pathogen interaction, nutrient uptake, or suppression and elicitation of plant immune responses. Taken together, this study represents a comprehensive overview of the domain repertoire of fungal and oomycete plant pathogens and points to novel features like domain expansion and species-specific bigram types that could, at least partially, explain why oomycetes are such remarkable plant pathogens
Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome
Baxter, L. ; Tripathy, S. ; Ishaque, N. ; Boot, N. ; Cabral, A. ; Kemen, E. ; Thines, M. ; Ah-Fong, A. ; Anderson, R. ; Badejoko, W. ; Bittner-Eddy, P. ; Boore, J.L. ; Chibucos, M.C. ; Coates, M. ; Dehal, P. ; Delehaunty, K. ; Dong, S. ; Downton, P. ; Dumas, B. ; Fabro, G. ; Fronick, C. ; Fuerstenberg, S.I. ; Fulton, L. ; Gaulin, E. ; Govers, F. ; Hughes, L. ; Humphray, S. ; Jiang, R.H.Y. ; Judelson, H. ; Kamoun, S. ; Kyung, K. ; Meijer, H.J.G. ; Minx, P. ; Morris, P. ; Nelson, J. ; Phuntumart, V. ; Qutob, D. ; Rehmany, A. ; Rougon-Cardoso, A. ; Ryden, P. ; Torto-Alalibo, T. ; Studholme, D. ; Wang, Y. ; Win, J. ; Wood, J. ; Clifton, S.W. ; Rogers, J. ; Ackerveken, G. van den; Jones, J.D.G. ; McDowell, J.M. ; Beynon, J. ; Tyler, B.M. - \ 2010
Science 330 (2010)6010. - ISSN 0036-8075 - p. 1549 - 1551.
sojae-effector avr1b - downy mildew - phytophthora - plant - thaliana - cells - suppression - parasites - proteins - delivery
Many oomycete and fungal plant pathogens are obligate biotrophs, which extract nutrients only from living plant tissue and cannot grow apart from their hosts. Although these pathogens cause substantial crop losses, little is known about the molecular basis or evolution of obligate biotrophy. Here, we report the genome sequence of the oomycete Hyaloperonospora arabidopsidis (Hpa), an obligate biotroph and natural pathogen of Arabidopsis thaliana. In comparison with genomes of related, hemibiotrophic Phytophthora species, the Hpa genome exhibits dramatic reductions in genes encoding (i) RXLR effectors and other secreted pathogenicity proteins, (ii) enzymes for assimilation of inorganic nitrogen and sulfur, and (iii) proteins associated with zoospore formation and motility. These attributes comprise a genomic signature of evolution toward obligate biotrophy
Regulatory Network Identification by Genetical Genomics: Signaling Downstream of the Arabidopsis Receptor-Like Kinase ERECTA
Terpstra, I.R. ; Snoek, L.B. ; Keurentjes, J.J.B. ; Peeters, A.J.M. ; Ackerveken, G. van den - \ 2010
Plant Physiology 154 (2010)3. - ISSN 0032-0889 - p. 1067 - 1078.
wrky transcription factor - defense responses - plant development - mpk4 activation - expression - map - differentiation - resistance - protein - reconstruction
Gene expression differences between individuals within a species can be largely explained by differences in genetic background. The effect of genetic variants (alleles) of genes on expression can be studied in a multifactorial way by application of genetical genomics or expression quantitative trait locus (eQTL) mapping. In this paper we present a strategy to construct regulatory networks by application of genetical genomics in combination with transcript profiling of mutants that are disrupted in single genes. We describe the network identification downstream of the receptor-like kinase ERECTA in Arabidopsis (Arabidopsis thaliana). Extending genetical genomics on the Landsberg erecta/Cape Verde islands (Ler/Cvi) recombinant inbred population with expression profiling of monogenic mutants enabled the identification of regulatory networks in the, so far elusive, ERECTA signal transduction cascade. We provide evidence that ERECTA is the causal gene for the major hotspot for transcript regulation in the Arabidopsis Ler/Cvi recombinant inbred population. We further propose additional genetic variation between Ler and Cvi in loci of the signalling pathway downstream of ERECTA, and suggest candidate genes underlying these loci. Integration of publicly available microarray expression data of other monogenic mutants allowed us to link ERECTA to a downstream MAPK signalling cascade. Our study shows that microarray data of monogenic mutants can be effectively used in combination with genetical genomics data to enhance the identification of genetic regulatory networks.
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