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Open Access Highly Accessed Research article

Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species

Yeting Zhang12, Monica Fernandez-Aparicio34, Eric K Wafula5, Malay Das3, Yuannian Jiao5, Norman J Wickett56, Loren A Honaas5, Paula E Ralph5, Martin F Wojciechowski7, Michael P Timko8, John I Yoder9, James H Westwood3 and Claude W dePamphilis125*

Author Affiliations

1 Intercollege Graduate Program in Genetics, Institute of Molecular Evolutionary Genetics, Penn State University, University Park, PA 16802, USA

2 Huck Institutes of the Life Science, Penn State University, University Park, PA 16802, USA

3 Department of Plant Pathology, Physiology and Weed Science, Virginia Tech, Blacksburg, VA, 24061, USA

4 Department of Plant Breeding, Institute for Sustainable Agriculture, IAS-CSIC, Córdoba, 14080, Spain

5 Department of Biology and Institute of Molecular Evolutionary Genetics, Penn State University, University Park, 16802, PAU.S.A

6 Chicago Botanic Garden, Glencoe, IL, 60022, U.S.A

7 School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA

8 Department of Biology, University of Virginia, Charlottesville, VA 22904, U.S.A

9 Department of Plant Sciences, University of California, Davis, CA 95616, U.S.A

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BMC Evolutionary Biology 2013, 13:48  doi:10.1186/1471-2148-13-48

Published: 20 February 2013

Abstract

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.

Keywords:
Parasitic plants; Horizontal gene transfer; Phelipanche; Orobanche; Legume; KNOTTIN; Albumin 1; Evolution