The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes
Abstract
Background: Heterodera glycines, commonly referred to as the soybean cyst nematode (SCN), is an obligatory and sedentary plant parasite that causes over a billion-dollar yield loss to soybean production annually. Although there are genetic determinants that render soybean plants resistant to certain nematode genotypes, resistant soybean cultivars are increasingly ineffective because their multi-year usage has selected for virulent H. glycines populations. The parasitic success of H. glycines relies on the comprehensive re-engineering of an infection site into a syncytium, as well as the long-term suppression of host defense to ensure syncytial viability. At the forefront of these complex molecular interactions are effectors, the proteins secreted by H. glycines into host root tissues. The mechanisms of effector acquisition, diversification, and selection need to be understood before effective control strategies can be developed, but the lack of an annotated genome has been a major roadblock. Results: Here, we use PacBio long-read technology to assemble a H. glycines genome of 738 contigs into 123 Mb with annotations for 29,769 genes. The genome contains significant numbers of repeats (34%), tandem duplicates (18.7 Mb), and horizontal gene transfer events (151 genes). A large number of putative effectors (431 genes) were identified in the genome, manymore »
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1618564
- Alternate Identifier(s):
- OSTI ID: 1616080
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- BMC Genomics
- Additional Journal Information:
- Journal Name: BMC Genomics Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1471-2164
- Publisher:
- Springer
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Heterodera glycines; SCN; Soybean cyst nematode; Genome; Tandem duplication; Effector; Evolution
Citation Formats
Masonbrink, Rick, Maier, Tom R., Muppirala, Usha, Seetharam, Arun S., Lord, Etienne, Juvale, Parijat S., Schmutz, Jeremy, Johnson, Nathan T., Korkin, Dmitry, Mitchum, Melissa G., Mimee, Benjamin, den Akker, Sebastian Eves-van, Hudson, Matthew, Severin, Andrew J., and Baum, Thomas J. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. United Kingdom: N. p., 2019.
Web. doi:10.1186/s12864-019-5485-8.
Masonbrink, Rick, Maier, Tom R., Muppirala, Usha, Seetharam, Arun S., Lord, Etienne, Juvale, Parijat S., Schmutz, Jeremy, Johnson, Nathan T., Korkin, Dmitry, Mitchum, Melissa G., Mimee, Benjamin, den Akker, Sebastian Eves-van, Hudson, Matthew, Severin, Andrew J., & Baum, Thomas J. The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. United Kingdom. https://doi.org/10.1186/s12864-019-5485-8
Masonbrink, Rick, Maier, Tom R., Muppirala, Usha, Seetharam, Arun S., Lord, Etienne, Juvale, Parijat S., Schmutz, Jeremy, Johnson, Nathan T., Korkin, Dmitry, Mitchum, Melissa G., Mimee, Benjamin, den Akker, Sebastian Eves-van, Hudson, Matthew, Severin, Andrew J., and Baum, Thomas J. Thu .
"The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes". United Kingdom. https://doi.org/10.1186/s12864-019-5485-8.
@article{osti_1618564,
title = {The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes},
author = {Masonbrink, Rick and Maier, Tom R. and Muppirala, Usha and Seetharam, Arun S. and Lord, Etienne and Juvale, Parijat S. and Schmutz, Jeremy and Johnson, Nathan T. and Korkin, Dmitry and Mitchum, Melissa G. and Mimee, Benjamin and den Akker, Sebastian Eves-van and Hudson, Matthew and Severin, Andrew J. and Baum, Thomas J.},
abstractNote = {Background: Heterodera glycines, commonly referred to as the soybean cyst nematode (SCN), is an obligatory and sedentary plant parasite that causes over a billion-dollar yield loss to soybean production annually. Although there are genetic determinants that render soybean plants resistant to certain nematode genotypes, resistant soybean cultivars are increasingly ineffective because their multi-year usage has selected for virulent H. glycines populations. The parasitic success of H. glycines relies on the comprehensive re-engineering of an infection site into a syncytium, as well as the long-term suppression of host defense to ensure syncytial viability. At the forefront of these complex molecular interactions are effectors, the proteins secreted by H. glycines into host root tissues. The mechanisms of effector acquisition, diversification, and selection need to be understood before effective control strategies can be developed, but the lack of an annotated genome has been a major roadblock. Results: Here, we use PacBio long-read technology to assemble a H. glycines genome of 738 contigs into 123 Mb with annotations for 29,769 genes. The genome contains significant numbers of repeats (34%), tandem duplicates (18.7 Mb), and horizontal gene transfer events (151 genes). A large number of putative effectors (431 genes) were identified in the genome, many of which were found in transposons. Conclusions:This advance provides a glimpse into the host and parasite interplay by revealing a diversity of mechanisms that give rise to virulence genes in the soybean cyst nematode, including: tandem duplications containing over a fifth of the total gene count, virulence genes hitchhiking in transposons, and 107 horizontal gene transfers not reported in other plant parasitic nematodes thus far. Through extensive characterization of the H. glycines genome, we provide new insights into H. glycines biology and shed light onto the mystery underlying complex host-parasite interactions. This genome sequence is an important prerequisite to enable work towards generating new resistance or control measures against H. glycines.},
doi = {10.1186/s12864-019-5485-8},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United Kingdom},
year = {Thu Feb 07 00:00:00 EST 2019},
month = {Thu Feb 07 00:00:00 EST 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1186/s12864-019-5485-8
https://doi.org/10.1186/s12864-019-5485-8
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 44 works
Citation information provided by
Web of Science
Web of Science
Figures / Tables:
Fig. 1: Phylogenetic relationships of species related to H. glycines. Phylogenetic tree of BUSCO genes with synteny representing the relatedness of each species. Synteny is inversely correlated with phylogenetic distance, as syntenic multiplicons decrease from hundreds in Globodera species, to zero in B. xylophilus, Green contigs denote H. glycines, whilemore »
All figures and tables
(5 total)
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
BRAKER1: Unsupervised RNA-Seq-Based Genome Annotation with GeneMark-ET and AUGUSTUS: Table 1.
journal, November 2015
- Hoff, Katharina J.; Lange, Simone; Lomsadze, Alexandre
- Bioinformatics, Vol. 32, Issue 5
Bandage: interactive visualization of de novo genome assemblies: Fig. 1.
journal, June 2015
- Wick, Ryan R.; Schultz, Mark B.; Zobel, Justin
- Bioinformatics, Vol. 31, Issue 20
FIMO: scanning for occurrences of a given motif
journal, February 2011
- Grant, Charles E.; Bailey, Timothy L.; Noble, William Stafford
- Bioinformatics, Vol. 27, Issue 7
UniProt: the universal protein knowledgebase
journal, November 2016
- :(unav),
- Nucleic Acids Research, Vol. 45, Issue D1, p. D158-D169
Detecting long tandem duplications in genomic sequences
journal, May 2012
- Audemard, Eric; Schiex, Thomas; Faraut, Thomas
- BMC Bioinformatics, Vol. 13, Issue 1
Disparate gain and loss of parasitic abilities among nematode lineages
journal, September 2017
- Holterman, Martijn; Karegar, Akbar; Mooijman, Paul
- PLOS ONE, Vol. 12, Issue 9
Analysis of a Horizontally Transferred Pathway Involved in Vitamin B6 Biosynthesis from the Soybean Cyst Nematode Heterodera glycines
journal, July 2008
- Craig, J. P.; Bekal, S.; Hudson, M.
- Molecular Biology and Evolution, Vol. 25, Issue 10
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
UniRef: comprehensive and non-redundant UniProt reference clusters
journal, March 2007
- Suzek, B. E.; Huang, H.; McGarvey, P.
- Bioinformatics, Vol. 23, Issue 10
HelitronScanner uncovers a large overlooked cache of Helitron transposons in many plant genomes
journal, June 2014
- Xiong, W.; He, L.; Lai, J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 28
Suppression of Soybean Yield Potential in the Continental United States by Plant Diseases from 2006 to 2009
journal, January 2010
- Koenning, Stephen R.; Wrather, J. Allen
- Plant Health Progress, Vol. 11, Issue 1
Fast and SNP-tolerant detection of complex variants and splicing in short reads
journal, February 2010
- Wu, T. D.; Nacu, S.
- Bioinformatics, Vol. 26, Issue 7, p. 873-881
Circos: An information aesthetic for comparative genomics
journal, June 2009
- Krzywinski, M.; Schein, J.; Birol, I.
- Genome Research, Vol. 19, Issue 9
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
journal, January 2013
- Kim, Daehwan; Pertea, Geo; Trapnell, Cole
- Genome Biology, Vol. 14, Issue 4
De novo assembly and phasing of a Korean human genome
journal, October 2016
- Seo, Jeong-Sun; Rhie, Arang; Kim, Junsoo
- Nature, Vol. 538, Issue 7624
Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes
journal, September 2010
- Danchin, Etienne G. J.; Rosso, Marie-Noëlle; Vieira, Paulo
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
Plant Parasitic Nematodes: Habitats, Hormones, and Horizontally-Acquired Genes
journal, June 2000
- Bird, David McKenzie; Koltai, Hinanit
- Journal of Plant Growth Regulation, Vol. 19, Issue 2
ASTRAL: genome-scale coalescent-based species tree estimation
journal, August 2014
- Mirarab, S.; Reaz, R.; Bayzid, Md. S.
- Bioinformatics, Vol. 30, Issue 17
BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015
- Simão, Felipe A.; Waterhouse, Robert M.; Ioannidis, Panagiotis
- Bioinformatics, Vol. 31, Issue 19
Horizontal Gene Transfer from Bacteria Has Enabled the Plant-Parasitic Nematode Globodera pallida to Feed on Host-Derived Sucrose
journal, February 2016
- Danchin, Etienne G. J.; Guzeeva, Elena A.; Mantelin, Sophie
- Molecular Biology and Evolution, Vol. 33, Issue 6
Inosine−Uridine Nucleoside Hydrolase from Crithidia fasciculata . Genetic Characterization, Crystallization, and Identification of Histidine 241 as a Catalytic Site Residue † , ‡
journal, January 1996
- Gopaul, Deshmukh N.; Meyer, Sheryl L.; Degano, Massimo
- Biochemistry, Vol. 35, Issue 19
XSEDE: Accelerating Scientific Discovery
journal, September 2014
- Towns, John; Cockerill, Timothy; Dahan, Maytal
- Computing in Science & Engineering, Vol. 16, Issue 5
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks
journal, March 2012
- Trapnell, Cole; Roberts, Adam; Goff, Loyal
- Nature Protocols, Vol. 7, Issue 3
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005
- Conesa, A.; Gotz, S.; Garcia-Gomez, J. M.
- Bioinformatics, Vol. 21, Issue 18
Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita
journal, July 2008
- Abad, Pierre; Gouzy, Jérôme; Aury, Jean-Marc
- Nature Biotechnology, Vol. 26, Issue 8
Sequence and genetic map of Meloidogyne hapla: A compact nematode genome for plant parasitism
journal, September 2008
- Opperman, C. H.; Bird, D. M.; Williamson, V. M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 39
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features
journal, November 2013
- Liao, Y.; Smyth, G. K.; Shi, W.
- Bioinformatics, Vol. 30, Issue 7
CAP3: A DNA Sequence Assembly Program
journal, September 1999
- Huang, X.
- Genome Research, Vol. 9, Issue 9
The MEME Suite
journal, May 2015
- Bailey, Timothy L.; Johnson, James; Grant, Charles E.
- Nucleic Acids Research, Vol. 43, Issue W1
RXLR effectors of plant pathogenic oomycetes
journal, August 2007
- Morgan, William; Kamoun, Sophien
- Current Opinion in Microbiology, Vol. 10, Issue 4
Gene duplication as a mechanism of genomic adaptation to a changing environment
journal, October 2012
- Kondrashov, Fyodor A.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1749
Detailed analysis of 15q11-q14 sequence corrects errors and gaps in the public access sequence to fully reveal large segmental duplications at breakpoints for Prader-Willi, Angelman, and inv dup(15) syndromes
journal, January 2007
- Makoff, Andrew J.; Flomen, Rachel H.
- Genome Biology, Vol. 8, Issue 6
Endogenous cellulases in animals: Isolation of -1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes
journal, April 1998
- Smant, G.; Stokkermans, J. P. W. G.; Yan, Y.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 9
Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins
journal, March 2009
- Vanholme, Bartel; Kast, Peter; Haegeman, Annelies
- Molecular Plant Pathology, Vol. 10, Issue 2
Horizontal gene transfer between bacteria and animals
journal, April 2011
- Dunning Hotopp, Julie C.
- Trends in Genetics, Vol. 27, Issue 4
InterPro in 2017—beyond protein family and domain annotations
journal, November 2016
- Finn, Robert D.; Attwood, Teresa K.; Babbitt, Patricia C.
- Nucleic Acids Research, Vol. 45, Issue D1
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
InterProScan 5: genome-scale protein function classification
journal, January 2014
- Jones, P.; Binns, D.; Chang, H. -Y.
- Bioinformatics, Vol. 30, Issue 9
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Bridges: a uniquely flexible HPC resource for new communities and data analytics
conference, January 2015
- Nystrom, Nicholas A.; Levine, Michael J.; Roskies, Ralph Z.
- Proceedings of the 2015 XSEDE Conference on Scientific Advancements Enabled by Enhanced Cyberinfrastructure - XSEDE '15
Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory
journal, September 2012
- Chaisson, Mark J.; Tesler, Glenn
- BMC Bioinformatics, Vol. 13, Issue 1
SynChro: A Fast and Easy Tool to Reconstruct and Visualize Synteny Blocks along Eukaryotic Chromosomes
journal, March 2014
- Drillon, Guénola; Carbone, Alessandra; Fischer, Gilles
- PLoS ONE, Vol. 9, Issue 3
The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode
journal, January 2014
- Cotton, James A.; Lilley, Catherine J.; Jones, Laura M.
- Genome Biology, Vol. 15, Issue 3
i-ADHoRe 3.0—fast and sensitive detection of genomic homology in extremely large data sets
journal, November 2011
- Proost, Sebastian; Fostier, Jan; De Witte, Dieter
- Nucleic Acids Research, Vol. 40, Issue 2
The Draft Genome of Globodera ellingtonae
journal, January 2017
- S. Phillips, Wendy; K. Howe, Dana; M. V. Brown, Amanda
- Journal of Nematology, Vol. 49, Issue 2
A high-performance computing toolset for relatedness and principal component analysis of SNP data
journal, October 2012
- Zheng, X.; Levine, D.; Shen, J.
- Bioinformatics, Vol. 28, Issue 24
The Parasitome of the Phytonematode Heterodera glycines
journal, August 2003
- Gao, Bingli; Allen, R.; Maier, Tom
- Molecular Plant-Microbe Interactions, Vol. 16, Issue 8
The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence
journal, June 2016
- Eves-van den Akker, Sebastian; Laetsch, Dominik R.; Thorpe, Peter
- Genome Biology, Vol. 17, Issue 1
Horizontal gene transfer from bacteria and fungi as a driving force in the evolution of plant parasitism in nematodes
journal, January 2005
- Kikuchi, Taisei; Furlanetto, Cleber; Jones, John
- Nematology, Vol. 7, Issue 5
Genotype Imputation with Millions of Reference Samples
journal, January 2016
- Browning, Brian L.; Browning, Sharon R.
- The American Journal of Human Genetics, Vol. 98, Issue 1
Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene
journal, April 2018
- Lilley, Catherine J.; Maqbool, Abbas; Wu, Duqing
- PLOS Genetics, Vol. 14, Issue 4
Basic local alignment search tool
journal, October 1990
- Altschul, Stephen F.; Gish, Warren; Miller, Webb
- Journal of Molecular Biology, Vol. 215, Issue 3, p. 403-410
The C. elegans genome sequencing project: a beginning
journal, March 1992
- Sulston, J.; Du, Z.; Thomas, K.
- Nature, Vol. 356, Issue 6364
Novel global effector mining from the transcriptome of early life stages of the soybean cyst nematode Heterodera glycines
journal, February 2018
- Gardner, Michael; Dhroso, Andi; Johnson, Nathan
- Scientific Reports, Vol. 8, Issue 1
Organization and evolution of transposable elements along the bread wheat chromosome 3B
journal, December 2014
- Daron, Josquin; Glover, Natasha; Pingault, Lise
- Genome Biology, Vol. 15, Issue 12
Disease-Inducing Secretions of Plant-Parasitic Nematodes
journal, September 1989
- Hussey, R. S.
- Annual Review of Phytopathology, Vol. 27, Issue 1
Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies By Use of Localized Haplotype Clustering
journal, November 2007
- Browning, Sharon R.; Browning, Brian L.
- The American Journal of Human Genetics, Vol. 81, Issue 5
Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients
journal, April 2016
- Noon, Jason B.; Baum, Thomas J.
- BMC Evolutionary Biology, Vol. 16, Issue 1
A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern
journal, May 2001
- Prior, Alison; Jones, John T.; Blok, Vivian C.
- Biochemical Journal, Vol. 356, Issue 2
Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots
journal, January 2013
- Kumar, Sujai; Jones, Martin; Koutsovoulos, Georgios
- Frontiers in Genetics, Vol. 4
Gene amplification and insecticide resistance
journal, May 2011
- Bass, Chris; Field, Linda M.
- Pest Management Science, Vol. 67, Issue 8
WormBase 2016: expanding to enable helminth genomic research
journal, November 2015
- Howe, Kevin L.; Bolt, Bruce J.; Cain, Scott
- Nucleic Acids Research, Vol. 44, Issue D1
Nematode effector proteins: an emerging paradigm of parasitism
journal, May 2013
- Mitchum, Melissa G.; Hussey, Richard S.; Baum, Thomas J.
- New Phytologist, Vol. 199, Issue 4
“Cyst-ained” research into Heterodera parasitism
journal, February 2018
- Juvale, Parijat S.; Baum, Thomas J.
- PLOS Pathogens, Vol. 14, Issue 2
The Transcriptomes of Xiphinema index and Longidorus elongatus Suggest Independent Acquisition of Some Plant Parasitism Genes by Horizontal Gene Transfer in Early-Branching Nematodes
journal, October 2017
- Danchin, Etienne; Perfus-Barbeoch, Laetitia; Rancurel, Corinne
- Genes, Vol. 8, Issue 10
A Model Plant Pathogen from the Kingdom Animalia: Heterodera glycines , the Soybean Cyst Nematode
journal, September 2006
- Niblack, T. L.; Lambert, K. N.; Tylka, G. L.
- Annual Review of Phytopathology, Vol. 44, Issue 1
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities
journal, May 2010
- Heinz, Sven; Benner, Christopher; Spann, Nathanael
- Molecular Cell, Vol. 38, Issue 4
Only a small subset of the SPRY domain gene family in Globodera pallida is likely to encode effectors, two of which suppress host defences induced by the potato resistance gene Gpa2
journal, January 2015
- Mei, Yuanyuan; Thorpe, Peter; Guzha, Athanas
- Nematology, Vol. 17, Issue 4
Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium
journal, October 2006
- Hawkins, J. S.; Kim, H.; Nason, J. D.
- Genome Research, Vol. 16, Issue 10
Cellular Signaling Pathways and Posttranslational Modifications Mediated by Nematode Effector Proteins
journal, August 2015
- Hewezi, Tarek
- Plant Physiology, Vol. 169, Issue 2
HISAT: a fast spliced aligner with low memory requirements
journal, March 2015
- Kim, Daehwan; Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 12, Issue 4
Reconstruction of a composite comparative map composed of ten legume genomes
journal, October 2016
- Lee, Chaeyoung; Yu, Dongwoon; Choi, Hong-Kyu
- Genes & Genomics, Vol. 39, Issue 1
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
journal, December 2014
- Love, Michael I.; Huber, Wolfgang; Anders, Simon
- Genome Biology, Vol. 15, Issue 12
Massive Horizontal Gene Transfer in Bdelloid Rotifers
journal, May 2008
- Gladyshev, E. A.; Meselson, M.; Arkhipova, I. R.
- Science, Vol. 320, Issue 5880
Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes
journal, January 2006
- Castagnone-Sereno, P.
- Heredity, Vol. 96, Issue 4
Figures / Tables found in this record:
Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.