title: Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty.
abstract: The origin of novel traits is recognized as an important process underlying many major evolutionary radiations. We studied the genetic basis for the evolution of haustoria, the novel feeding organs of parasitic flowering plants, using comparative transcriptome sequencing in three species of Orobanchaceae. Around 180 genes are upregulated during haustorial development following host attachment in at least two species, and these are enriched in proteases, cell wall modifying enzymes, and extracellular secretion proteins. Additionally, about 100 shared genes are upregulated in response to haustorium inducing factors prior to host attachment. Collectively, we refer to these newly identified genes as putative "parasitism genes." Most of these parasitism genes are derived from gene duplications in a common ancestor of Orobanchaceae and Mimulus guttatus, a related nonparasitic plant. Additionally, the signature of relaxed purifying selection and/or adaptive evolution at specific sites was detected in many haustorial genes, and may play an important role in parasite evolution. Comparative analysis of gene expression patterns in parasitic and nonparasitic angiosperms suggests that parasitism genes are derived primarily from root and floral tissues, but with some genes co-opted from other tissues. Gene duplication, often taking place in a nonparasitic ancestor of Orobanchaceae, followed by regulatory neofunctionalization, was an important process in the origin of parasitic haustoria.
authors.affiliation: Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University Department of Biology, The Pennsylvania State University Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University.
authors.forename: Zhenzhen
authors.initials: Z
authors.lastname: Yang
authors.affiliation: Department of Biology, The Pennsylvania State University Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University.
authors.forename: Eric K
authors.initials: EK
authors.lastname: Wafula
authors.affiliation: Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University Department of Biology, The Pennsylvania State University Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University.
authors.forename: Loren A
authors.initials: LA
authors.lastname: Honaas
authors.affiliation: Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University Department of Biology, The Pennsylvania State University.
authors.forename: Huiting
authors.initials: H
authors.lastname: Zhang
authors.affiliation: Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University.
authors.forename: Malay
authors.initials: M
authors.lastname: Das
authors.affiliation: Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University Department of Biology, University of Virginia.
authors.forename: Monica
authors.initials: M
authors.lastname: Fernandez-Aparicio
authors.affiliation: Department of Biology, University of Virginia.
authors.forename: Kan
authors.initials: K
authors.lastname: Huang
authors.affiliation: Department of Plant Sciences, University of California, Davis.
authors.forename: Pradeepa C G
authors.initials: PC
authors.lastname: Bandaranayake
authors.affiliation: Department of Plant Sciences, University of California, Davis.
authors.forename: Biao
authors.initials: B
authors.lastname: Wu
authors.affiliation: Department of Biology, The Pennsylvania State University Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University.
authors.forename: Joshua P
authors.initials: JP
authors.lastname: Der
authors.affiliation: Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University.
authors.forename: Christopher R
authors.initials: CR
authors.lastname: Clarke
authors.affiliation: Department of Biology, The Pennsylvania State University.
authors.forename: Paula E
authors.initials: PE
authors.lastname: Ralph
authors.affiliation: Department of Biology, The Pennsylvania State University.
authors.forename: Lena
authors.initials: L
authors.lastname: Landherr
authors.affiliation: Department of Statistics and Huck Institutes of the Life Sciences, The Pennsylvania State University.
authors.forename: Naomi S
authors.initials: NS
authors.lastname: Altman
authors.affiliation: Department of Biology, University of Virginia.
authors.forename: Michael P
authors.initials: MP
authors.lastname: Timko
authors.affiliation: Department of Plant Sciences, University of California, Davis.
authors.forename: John I
authors.initials: JI
authors.lastname: Yoder
authors.affiliation: Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University.
authors.forename: James H
authors.initials: JH
authors.lastname: Westwood
authors.affiliation: Intercollege Graduate Program in Plant Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University Department of Biology, The Pennsylvania State University Institute of Molecular Evolutionary Genetics, Huck Institutes of the Life Sciences, The Pennsylvania State University cwd3@psu.edu.
authors.forename: Claude W
authors.initials: CW
authors.lastname: dePamphilis
mesh_terms: D016000:Cluster Analysis; D019143:Evolution, Molecular; D020440:Gene Duplication / Q000235:genetics*; D020869:Gene Expression Profiling; D017343:Genes, Plant / Q000235:genetics; D032241:Mimulus / Q000235:genetics / Q000502:physiology; D031670:Orobanchaceae / Q000235:genetics* / Q000502:physiology; D059467:Transcriptome / Q000235:genetics*
keywords: Orobanchaceae; gene duplication; novel traits; parasitism; protease; transcriptome