TY - JOUR
T1 - Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species
AU - Zhang, Yeting
AU - Fernandez-Aparicio, Monica
AU - Wafula, Eric K.
AU - Das, Malay
AU - Jiao, Yuannian
AU - Wickett, Norman J.
AU - Honaas, Loren A.
AU - Ralph, Paula E.
AU - Wojciechowski, Martin F.
AU - Timko, Michael P.
AU - Yoder, John I.
AU - Westwood, James H.
AU - Depamphilis, Claude W.
N1 - Funding Information:
We thank Yongdae Bao (University of Virginia), Loren A. Honaas, Paula E. Ralph, Lena Landherr, Lynn P. Tomsho and Stephan C. Schuster (Penn State University), Pradeepa Gunathilake and Bio Wu (University of California-Davis) and Marta Matvienko (UC Davis Genome Center) for generation of the PPGP transcriptome data, and Gunjun Kim and Megan LeBlanc (Virginia Tech), and the 1KP transcriptome project (Gane Ka-Shu Wong, University of Alberta) for generation of the Cuscuta and Pilostyles transcriptome data from samples provided by J.H.W. and C.W.D, respectively. We also thank Arthur Lesk, Joshua P. Der, Paula E. Ralph, and Zhenzhen Yang for discussion and suggestions, and the KNOTTIN database for access to their 3D modeling software. Thoughtful comments by two anonymous reviewers also helped to improve the paper. This work was supported by NSF Plant Genome award DBI-0701748 (“The Parasitic Plant Genome Project”) to J.H.W., C.W.D., M.P.T., and J.Y. Graduate fellowship support for Y. Zhang was provided by the Intercollege Graduate Program in Genetics and the Department of Biology (Penn State University), and M. Fernández-Aparicio was supported by an International Outgoing European Marie Curie postdoctoral fellowship (PIOF-GA-2009-252538). Additional support was provided from the U.S. Department of Agriculture (Hatch project no. 135798) and NSF IOS-0843372 to J.H.W. and by NSF award DEB-0542958 to M.F.W. Data reported in this paper are archived at Parasitic Plant Genome Project and in the short read archive of N.C.B.I. GenBank (SRP001053) with additional materials and methods and results tabulated in the Supporting Online Material.
PY - 2013
Y1 - 2013
N2 - Background: Parasitic plants, represented by several thousand species of angiosperms, use modified structures known as haustoria to tap into photosynthetic host plants and extract nutrients and water. As a result of their direct plant-plant connections with their host plant, parasitic plants have special opportunities for horizontal gene transfer, the nonsexual transmission of genetic material across species boundaries. There is increasing evidence that parasitic plants have served as recipients and donors of horizontal gene transfer (HGT), but the long-term impacts of eukaryotic HGT in parasitic plants are largely unknown. Results: Here we show that a gene encoding albumin 1 KNOTTIN-like protein, closely related to the albumin 1 genes only known from papilionoid legumes, where they serve dual roles as food storage and insect toxin, was found in Phelipanche aegyptiaca and related parasitic species of family Orobanchaceae, and was likely acquired by a Phelipanche ancestor via HGT from a legume host based on phylogenetic analyses. The KNOTTINs are well known for their unique "disulfide through disulfide knot" structure and have been extensively studied in various contexts, including drug design. Genomic sequences from nine related parasite species were obtained, and 3D protein structure simulation tests and evolutionary constraint analyses were performed. The parasite gene we identified here retains the intron structure, six highly conserved cysteine residues necessary to form a KNOTTIN protein, and displays levels of purifying selection like those seen in legumes. The albumin 1 xenogene has evolved through >150 speciation events over ca. 16 million years, forming a small family of differentially expressed genes that may confer novel functions in the parasites. Moreover, further data show that a distantly related parasitic plant, Cuscuta, obtained two copies of albumin 1 KNOTTIN-like genes from legumes through a separate HGT event, suggesting that legume KNOTTIN structures have been repeatedly co-opted by parasitic plants. Conclusions: The HGT-derived albumins in Phelipanche represent a novel example of how plants can acquire genes from other plants via HGT that then go on to duplicate, evolve, and retain the specialized features required to perform a unique host-derived function.
AB - Background: Parasitic plants, represented by several thousand species of angiosperms, use modified structures known as haustoria to tap into photosynthetic host plants and extract nutrients and water. As a result of their direct plant-plant connections with their host plant, parasitic plants have special opportunities for horizontal gene transfer, the nonsexual transmission of genetic material across species boundaries. There is increasing evidence that parasitic plants have served as recipients and donors of horizontal gene transfer (HGT), but the long-term impacts of eukaryotic HGT in parasitic plants are largely unknown. Results: Here we show that a gene encoding albumin 1 KNOTTIN-like protein, closely related to the albumin 1 genes only known from papilionoid legumes, where they serve dual roles as food storage and insect toxin, was found in Phelipanche aegyptiaca and related parasitic species of family Orobanchaceae, and was likely acquired by a Phelipanche ancestor via HGT from a legume host based on phylogenetic analyses. The KNOTTINs are well known for their unique "disulfide through disulfide knot" structure and have been extensively studied in various contexts, including drug design. Genomic sequences from nine related parasite species were obtained, and 3D protein structure simulation tests and evolutionary constraint analyses were performed. The parasite gene we identified here retains the intron structure, six highly conserved cysteine residues necessary to form a KNOTTIN protein, and displays levels of purifying selection like those seen in legumes. The albumin 1 xenogene has evolved through >150 speciation events over ca. 16 million years, forming a small family of differentially expressed genes that may confer novel functions in the parasites. Moreover, further data show that a distantly related parasitic plant, Cuscuta, obtained two copies of albumin 1 KNOTTIN-like genes from legumes through a separate HGT event, suggesting that legume KNOTTIN structures have been repeatedly co-opted by parasitic plants. Conclusions: The HGT-derived albumins in Phelipanche represent a novel example of how plants can acquire genes from other plants via HGT that then go on to duplicate, evolve, and retain the specialized features required to perform a unique host-derived function.
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U2 - 10.1186/1471-2148-13-48
DO - 10.1186/1471-2148-13-48
M3 - Article
C2 - 23425243
AN - SCOPUS:84873961817
SN - 1471-2148
VL - 13
JO - BMC Evolutionary Biology
JF - BMC Evolutionary Biology
IS - 1
M1 - 48
ER -