TY - JOUR
T1 - Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty
AU - Yang, Zhenzhen
AU - Wafula, Eric K.
AU - Honaas, Loren A.
AU - Zhang, Huiting
AU - Das, Malay
AU - Fernandez-Aparicio, Monica
AU - Huang, Kan
AU - Bandaranayake, Pradeepa C.G.
AU - Wu, Biao
AU - Der, Joshua P.
AU - Clarke, Christopher R.
AU - Ralph, Paula E.
AU - Landherr, Lena
AU - Altman, Naomi S.
AU - Timko, Michael P.
AU - Yoder, John I.
AU - Westwood, James H.
AU - DePamphilis, Claude W.
N1 - Funding Information:
Sequence data are archived at National Center for Biotechnology Information BioProject ID SRP001053, and at http://ppgp.huck.psu.edu. This research was supported by awards DBI-0701748 and IOS-1238057 to J.H.W, C.W.D., M.P.T, and J.H.Y. from the NSF’s Plant Genome Research Program, with the additional support for Y.Z., L.A.H, and H.Z. from the Plant Biology and Biology Department graduate programs at Penn State, the National Institute of Food and Agriculture Project No. 131997 to J.H.W., and from NSF IOS-1213059 for M.P.T. and K.H. M.F.-A. was supported by an International Outgoing European Marie Curie postdoctoral fellowship (PIOF-GA-2009-252538). The authors thank Yongde Bao for Illumina sequencing at the University of Virginia, Lynn Tomsho and Stephan Schuster for 454 and Illumina sequencing at Penn State University, and UC Davis Genome Center for generating normalized whole plant libraries and Illumina sequence data. They also thank Verlyn Stromberg for technical assistance, Yu Zhang for providing constructive ideas in candidate gene identif ication, Ningtao Wang and Iman Farasat for developing the initial R code for the cluster analyses, and Lenwood Heath and Yeting Zhang for helpful suggestions on the manuscript. Authors’ contribution is as follows: Conceived of project: J.H.W., C.W.D., J.I.Y., and M.P.T.; cultivated plants and generated staged tissue samples: M.D., M.F.A., P.C.G.B., K.H., L.A.H., and P.E.R.; RNAs and libraries: M.D., M.F.A., P.C.G.B., K.H., L.A.H., L.L., P.E.R., and B.W.; RT-PCR: Z.Y., H.Z., and C.R.C.; conceived of paper: C.W.D. and Z.Y.; designed and performed data analyses and results visualization: Z.Y. (primary), E.K.W. (primary), J.P.D., H.Z., N.S.A., and C.W.D. (primary); wrote the paper: Z.Y. (primary), C.W.D. (primary), and E.K.W.; additional text, editing, and comments: J.H.W., J.I.Y., M.P.T., N.S.A., C.R.C., P.E.R., L.A.H., M.F.A., K.H., and P.C.G.B.; Read and approved the text: all authors.
Publisher Copyright:
© The Author 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
PY - 2015/3/1
Y1 - 2015/3/1
N2 - 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.
AB - 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.
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U2 - 10.1093/molbev/msu343
DO - 10.1093/molbev/msu343
M3 - Article
C2 - 25534030
AN - SCOPUS:84982161457
SN - 0737-4038
VL - 32
SP - 767
EP - 790
JO - Molecular Biology and Evolution
JF - Molecular Biology and Evolution
IS - 3
ER -