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

Yeting Zhang, Monica Fernandez-Aparicio, Eric K. Wafula, Malay Das, Yuannian Jiao, Norman J. Wickett, Loren A. Honaas, Paula E. Ralph, Martin Wojciechowski, Michael P. Timko, John I. Yoder, James H. Westwood, Claude W. Depamphilis

Research output: Contribution to journalArticle

33 Citations (Scopus)

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.

Original languageEnglish (US)
Article number48
JournalBMC Evolutionary Biology
Volume13
Issue number1
DOIs
StatePublished - 2013

Fingerprint

parasitic plant
parasitic plants
gene transfer
albumins
legumes
gene
genes
parasite
sulfides
parasites
host plant
protein
host plants
food storage
Orobanchaceae
Cuscuta
knots
protein structure
horizontal gene transfer
angiosperm

Keywords

  • Albumin 1
  • Evolution
  • Horizontal gene transfer
  • KNOTTIN
  • Legume
  • Orobanche
  • Parasitic plants
  • Phelipanche

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics

Cite this

Zhang, Y., Fernandez-Aparicio, M., Wafula, E. K., Das, M., Jiao, Y., Wickett, N. J., ... Depamphilis, C. W. (2013). Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species. BMC Evolutionary Biology, 13(1), [48]. https://doi.org/10.1186/1471-2148-13-48

Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species. / Zhang, Yeting; Fernandez-Aparicio, Monica; Wafula, Eric K.; Das, Malay; Jiao, Yuannian; Wickett, Norman J.; Honaas, Loren A.; Ralph, Paula E.; Wojciechowski, Martin; Timko, Michael P.; Yoder, John I.; Westwood, James H.; Depamphilis, Claude W.

In: BMC Evolutionary Biology, Vol. 13, No. 1, 48, 2013.

Research output: Contribution to journalArticle

Zhang, Y, Fernandez-Aparicio, M, Wafula, EK, Das, M, Jiao, Y, Wickett, NJ, Honaas, LA, Ralph, PE, Wojciechowski, M, Timko, MP, Yoder, JI, Westwood, JH & Depamphilis, CW 2013, 'Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species', BMC Evolutionary Biology, vol. 13, no. 1, 48. https://doi.org/10.1186/1471-2148-13-48
Zhang, Yeting ; Fernandez-Aparicio, Monica ; Wafula, Eric K. ; Das, Malay ; Jiao, Yuannian ; Wickett, Norman J. ; Honaas, Loren A. ; Ralph, Paula E. ; Wojciechowski, Martin ; Timko, Michael P. ; Yoder, John I. ; Westwood, James H. ; Depamphilis, Claude W. / Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species. In: BMC Evolutionary Biology. 2013 ; Vol. 13, No. 1.
@article{871b051f2c1f41fd8670ac8a696447fe,
title = "Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species",
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 = "Albumin 1, Evolution, Horizontal gene transfer, KNOTTIN, Legume, Orobanche, Parasitic plants, Phelipanche",
author = "Yeting Zhang and Monica Fernandez-Aparicio and Wafula, {Eric K.} and Malay Das and Yuannian Jiao and Wickett, {Norman J.} and Honaas, {Loren A.} and Ralph, {Paula E.} and Martin Wojciechowski and Timko, {Michael P.} and Yoder, {John I.} and Westwood, {James H.} and Depamphilis, {Claude W.}",
year = "2013",
doi = "10.1186/1471-2148-13-48",
language = "English (US)",
volume = "13",
journal = "BMC Evolutionary Biology",
issn = "1471-2148",
publisher = "BioMed Central",
number = "1",

}

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

AU - Timko, Michael P.

AU - Yoder, John I.

AU - Westwood, James H.

AU - Depamphilis, Claude W.

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.

KW - Albumin 1

KW - Evolution

KW - Horizontal gene transfer

KW - KNOTTIN

KW - Legume

KW - Orobanche

KW - Parasitic plants

KW - Phelipanche

UR - http://www.scopus.com/inward/record.url?scp=84873961817&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84873961817&partnerID=8YFLogxK

U2 - 10.1186/1471-2148-13-48

DO - 10.1186/1471-2148-13-48

M3 - Article

C2 - 23425243

AN - SCOPUS:84873961817

VL - 13

JO - BMC Evolutionary Biology

JF - BMC Evolutionary Biology

SN - 1471-2148

IS - 1

M1 - 48

ER -