Literature DB >> 22736827

Evidence for horizontally transferred genes involved in the biosynthesis of vitamin B(1), B(5), and B(7) in Heterodera glycines.

James P Craig1, Sadia Bekal, Terry Niblack, Leslie Domier, Kris N Lambert.   

Abstract

Heterodera glycines is a nematode that is highly adapted to manipulate and parasitize plant hosts. The molecular players involved in these interactions have only recently begun to be identified. Here, the sequencing of the second stage juvenile transcriptome, followed by a bioinformatic screen for novel genes, identified seven new genes involved in biosynthesis and salvage of vitamins B₁, B₅, and B₇. With no confirmed reports in the literature, each of these biosynthesis pathways is believed to have been lost in multicellular animals. However, eukaryotic-like introns in the genomic sequences of the genes confirmed eukaryotic origin and nematode-specific splice leaders found on five of the cDNAs confirmed their nematode origin. Two of the genes were found to be flanked by known nematode sequences and quantitative polymerase chain reactions on individual nematodes showed similar and consistent amplification between the vitamin B biosynthesis genes and other known H. glycines genes. This further confirmed their presence in the nematode genome. Similarity to bacterial sequences at the amino acid level suggested a prokaryotic ancestry and phylogenetic analysis of the genes supported a likely horizontal gene transfer event, suggesting H. glycines re-appropriated the genes from the prokaryotic kingdom. This finding complements the previous discovery of a vitamin B₆ biosynthesis pathway within the nematode. However, unlike the complete vitamin B₆ pathway, many of these vitamin B pathways appear to be missing the initial enzymes required for full de novo biosynthesis, suggesting that initial substrates in the pathways are obtained exogenously. These partial vitamin B biosynthesis enzymes have recently been identified in other single-celled eukaryotic parasites and on rhizobia symbiosis plasmids, indicating that they may play an important role in host-parasite interactions and survival within the plant environment.

Entities:  

Keywords:  Heterodera glycines; biosynthetic pathways; biotin; horizontal gene transfer; pantothenate; thiamin; vitamin B1; vitamin B5; vitamin B7

Year:  2009        PMID: 22736827      PMCID: PMC3381462     

Source DB:  PubMed          Journal:  J Nematol        ISSN: 0022-300X            Impact factor:   1.402


  53 in total

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Journal:  Methods       Date:  2001-12       Impact factor: 3.608

2.  Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica.

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Journal:  Mol Plant Microbe Interact       Date:  1999-04       Impact factor: 4.171

3.  Mutagenesis studies on TenA: a thiamin salvage enzyme from Bacillus subtilis.

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Journal:  Bioorg Chem       Date:  2007-12-03       Impact factor: 5.275

4.  Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes.

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Journal:  Proc Natl Acad Sci U S A       Date:  1998-04-28       Impact factor: 11.205

5.  Distribution, Density, and Diversity of Heterodera glycines in Missouri.

Authors:  T L Niblack; R D Heinz; G S Smith; P A Donald
Journal:  J Nematol       Date:  1993-12       Impact factor: 1.402

6.  Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines.

Authors:  James P Craig; Sadia Bekal; Matthew Hudson; Leslie Domier; Terry Niblack; Kris N Lambert
Journal:  Mol Biol Evol       Date:  2008-06-26       Impact factor: 16.240

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Authors:  Axel A Elling; Eric L Davis; Richard S Hussey; Thomas J Baum
Journal:  Int J Parasitol       Date:  2007-04-13       Impact factor: 3.981

Review 8.  Plant parasitic nematode proteins and the host parasite interaction.

Authors:  Rosane H C Curtis
Journal:  Brief Funct Genomic Proteomic       Date:  2007-05-24

9.  A review of the biochemistry, metabolism and clinical benefits of thiamin(e) and its derivatives.

Authors:  Derrick Lonsdale
Journal:  Evid Based Complement Alternat Med       Date:  2006-03       Impact factor: 2.629

10.  Horizontally transferred genes in plant-parasitic nematodes: a high-throughput genomic approach.

Authors:  Elizabeth H Scholl; Jeffrey L Thorne; James P McCarter; David Mck Bird
Journal:  Genome Biol       Date:  2003-05-19       Impact factor: 13.583

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  14 in total

Review 1.  Horizontal gene transfer in the acquisition of novel traits by metazoans.

Authors:  Luis Boto
Journal:  Proc Biol Sci       Date:  2014-01-08       Impact factor: 5.349

Review 2.  Functional horizontal gene transfer from bacteria to eukaryotes.

Authors:  Filip Husnik; John P McCutcheon
Journal:  Nat Rev Microbiol       Date:  2017-11-27       Impact factor: 60.633

3.  The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5.

Authors:  Zoran S Radakovic; Clarissa Hiltl; Clement Pellegrin; Shahid Siddique; Thomas J Baum; Helen Beasley; Andrew F Bent; Oliver Chitambo; Divykriti Chopra; Etienne G J Danchin; Eric Grenier; Samer S Habash; M Shamim Hasan; Johannes Helder; Tarek Hewezi; Julia Holbein; Martijn Holterman; Sławomir Janakowski; Georgios D Koutsovoulos; Olaf P Kranse; Jose L Lozano-Torres; Tom R Maier; Rick E Masonbrink; Badou Mendy; Esther Riemer; Mirosław Sobczak; Unnati Sonawala; Mark G Sterken; Peter Thorpe; Joris J M van Steenbrugge; Nageena Zahid; Florian Grundler; Sebastian Eves-van den Akker
Journal:  Nat Commun       Date:  2022-10-19       Impact factor: 17.694

4.  Genome streamlining in a minute herbivore that manipulates its host plant.

Authors:  Robert Greenhalgh; Wannes Dermauw; Joris J Glas; Stephane Rombauts; Nicky Wybouw; Jainy Thomas; Juan M Alba; Ellen J Pritham; Saioa Legarrea; René Feyereisen; Yves Van de Peer; Thomas Van Leeuwen; Richard M Clark; Merijn R Kant
Journal:  Elife       Date:  2020-10-23       Impact factor: 8.140

5.  A SNARE-Like Protein and Biotin Are Implicated in Soybean Cyst Nematode Virulence.

Authors:  Sadia Bekal; Leslie L Domier; Biruk Gonfa; Naoufal Lakhssassi; Khalid Meksem; Kris N Lambert
Journal:  PLoS One       Date:  2015-12-29       Impact factor: 3.240

6.  The Transcriptomes of Xiphinema index and Longidorus elongatus Suggest Independent Acquisition of Some Plant Parasitism Genes by Horizontal Gene Transfer in Early-Branching Nematodes.

Authors:  Etienne G J Danchin; Laetitia Perfus-Barbeoch; Corinne Rancurel; Peter Thorpe; Martine Da Rocha; Simon Bajew; Roy Neilson; Elena Sokolova Guzeeva; Corinne Da Silva; Julie Guy; Karine Labadie; Daniel Esmenjaud; Johannes Helder; John T Jones; Sebastian Eves-van den Akker
Journal:  Genes (Basel)       Date:  2017-10-23       Impact factor: 4.096

7.  The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode.

Authors:  James A Cotton; Catherine J Lilley; Laura M Jones; Taisei Kikuchi; Adam J Reid; Peter Thorpe; Isheng J Tsai; Helen Beasley; Vivian Blok; Peter J A Cock; Sebastian Eves-van den Akker; Nancy Holroyd; Martin Hunt; Sophie Mantelin; Hardeep Naghra; Arnab Pain; Juan E Palomares-Rius; Magdalena Zarowiecki; Matthew Berriman; John T Jones; Peter E Urwin
Journal:  Genome Biol       Date:  2014-03-03       Impact factor: 13.583

8.  Horizontal gene transfer of acetyltransferases, invertases and chorismate mutases from different bacteria to diverse recipients.

Authors:  Jason B Noon; Thomas J Baum
Journal:  BMC Evol Biol       Date:  2016-04-12       Impact factor: 3.260

9.  The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence.

Authors:  Sebastian Eves-van den Akker; Dominik R Laetsch; Peter Thorpe; Catherine J Lilley; Etienne G J Danchin; Martine Da Rocha; Corinne Rancurel; Nancy E Holroyd; James A Cotton; Amir Szitenberg; Eric Grenier; Josselin Montarry; Benjamin Mimee; Marc-Olivier Duceppe; Ian Boyes; Jessica M C Marvin; Laura M Jones; Hazijah B Yusup; Joël Lafond-Lapalme; Magali Esquibet; Michael Sabeh; Michael Rott; Hein Overmars; Anna Finkers-Tomczak; Geert Smant; Georgios Koutsovoulos; Vivian Blok; Sophie Mantelin; Peter J A Cock; Wendy Phillips; Bernard Henrissat; Peter E Urwin; Mark Blaxter; John T Jones
Journal:  Genome Biol       Date:  2016-06-10       Impact factor: 13.583

10.  Alienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life.

Authors:  Corinne Rancurel; Ludovic Legrand; Etienne G J Danchin
Journal:  Genes (Basel)       Date:  2017-09-29       Impact factor: 4.096

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