Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants

Zhenzhen Yang, Eric K. Wafula, Gunjune Kim, Saima Shahid, Joel R. McNeal, Paula E. Ralph, Prakash R. Timilsena, Wen bin Yu, Elizabeth A. Kelly, Huiting Zhang, Thomas Nate Person, Naomi S. Altman, Michael J. Axtell, James H. Westwood, Claude W. dePamphilis

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Horizontal gene transfer (HGT), the movement and genomic integration of DNA across species boundaries, is commonly associated with bacteria and other microorganisms, but functional HGT (fHGT) is increasingly being recognized in heterotrophic parasitic plants that obtain their nutrients and water from their host plants through direct haustorial feeding. Here, in the holoparasitic stem parasite Cuscuta, we identify 108 transcribed and probably functional HGT events in Cuscuta campestris and related species, plus 42 additional regions with host-derived transposon, pseudogene and non-coding sequences. Surprisingly, 18 Cuscuta fHGTs were acquired from the same gene families by independent HGT events in Orobanchaceae parasites, and the majority are highly expressed in the haustorial feeding structures in both lineages. Convergent retention and expression of HGT sequences suggests an adaptive role for specific additional genes in parasite biology. Between 16 and 20 of the transcribed HGT events are inferred as ancestral in Cuscuta based on transcriptome sequences from species across the phylogenetic range of the genus, implicating fHGT in the successful radiation of Cuscuta parasites. Genome sequencing of C. campestris supports transfer of genomic DNA—rather than retroprocessed RNA—as the mechanism of fHGT. Many of the C. campestris genes horizontally acquired are also frequent sources of 24-nucleotide small RNAs that are typically associated with RNA-directed DNA methylation. One HGT encoding a leucine-rich repeat protein kinase overlaps with a microRNA that has been shown to regulate host gene expression, suggesting that HGT-derived parasite small RNAs may function in the parasite–host interaction. This study enriches our understanding of HGT by describing a parasite–host system with unprecedented gene exchange that points to convergent evolution of HGT events and the functional importance of horizontally transferred coding and non-coding sequences.

Original languageEnglish (US)
Pages (from-to)991-1001
Number of pages11
JournalNature Plants
Volume5
Issue number9
DOIs
StatePublished - Sep 1 2019

Fingerprint

parasitic plants
nucleic acids
Cuscuta
Cuscuta campestris
parasites
RNA
genes
horizontal gene transfer
Orobanchaceae
genomics
convergent evolution
pseudogenes
DNA methylation
microRNA
transcriptome
transposons
protein kinases
leucine
host plants
nucleotides

All Science Journal Classification (ASJC) codes

  • Plant Science

Cite this

Yang, Zhenzhen ; Wafula, Eric K. ; Kim, Gunjune ; Shahid, Saima ; McNeal, Joel R. ; Ralph, Paula E. ; Timilsena, Prakash R. ; Yu, Wen bin ; Kelly, Elizabeth A. ; Zhang, Huiting ; Person, Thomas Nate ; Altman, Naomi S. ; Axtell, Michael J. ; Westwood, James H. ; dePamphilis, Claude W. / Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants. In: Nature Plants. 2019 ; Vol. 5, No. 9. pp. 991-1001.
@article{24d0b1d3f6264b088768da0c5af88548,
title = "Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants",
abstract = "Horizontal gene transfer (HGT), the movement and genomic integration of DNA across species boundaries, is commonly associated with bacteria and other microorganisms, but functional HGT (fHGT) is increasingly being recognized in heterotrophic parasitic plants that obtain their nutrients and water from their host plants through direct haustorial feeding. Here, in the holoparasitic stem parasite Cuscuta, we identify 108 transcribed and probably functional HGT events in Cuscuta campestris and related species, plus 42 additional regions with host-derived transposon, pseudogene and non-coding sequences. Surprisingly, 18 Cuscuta fHGTs were acquired from the same gene families by independent HGT events in Orobanchaceae parasites, and the majority are highly expressed in the haustorial feeding structures in both lineages. Convergent retention and expression of HGT sequences suggests an adaptive role for specific additional genes in parasite biology. Between 16 and 20 of the transcribed HGT events are inferred as ancestral in Cuscuta based on transcriptome sequences from species across the phylogenetic range of the genus, implicating fHGT in the successful radiation of Cuscuta parasites. Genome sequencing of C. campestris supports transfer of genomic DNA—rather than retroprocessed RNA—as the mechanism of fHGT. Many of the C. campestris genes horizontally acquired are also frequent sources of 24-nucleotide small RNAs that are typically associated with RNA-directed DNA methylation. One HGT encoding a leucine-rich repeat protein kinase overlaps with a microRNA that has been shown to regulate host gene expression, suggesting that HGT-derived parasite small RNAs may function in the parasite–host interaction. This study enriches our understanding of HGT by describing a parasite–host system with unprecedented gene exchange that points to convergent evolution of HGT events and the functional importance of horizontally transferred coding and non-coding sequences.",
author = "Zhenzhen Yang and Wafula, {Eric K.} and Gunjune Kim and Saima Shahid and McNeal, {Joel R.} and Ralph, {Paula E.} and Timilsena, {Prakash R.} and Yu, {Wen bin} and Kelly, {Elizabeth A.} and Huiting Zhang and Person, {Thomas Nate} and Altman, {Naomi S.} and Axtell, {Michael J.} and Westwood, {James H.} and dePamphilis, {Claude W.}",
year = "2019",
month = "9",
day = "1",
doi = "10.1038/s41477-019-0458-0",
language = "English (US)",
volume = "5",
pages = "991--1001",
journal = "Nature Plants",
issn = "2055-026X",
publisher = "Palgrave Macmillan Ltd.",
number = "9",

}

Yang, Z, Wafula, EK, Kim, G, Shahid, S, McNeal, JR, Ralph, PE, Timilsena, PR, Yu, WB, Kelly, EA, Zhang, H, Person, TN, Altman, NS, Axtell, MJ, Westwood, JH & dePamphilis, CW 2019, 'Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants', Nature Plants, vol. 5, no. 9, pp. 991-1001. https://doi.org/10.1038/s41477-019-0458-0

Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants. / Yang, Zhenzhen; Wafula, Eric K.; Kim, Gunjune; Shahid, Saima; McNeal, Joel R.; Ralph, Paula E.; Timilsena, Prakash R.; Yu, Wen bin; Kelly, Elizabeth A.; Zhang, Huiting; Person, Thomas Nate; Altman, Naomi S.; Axtell, Michael J.; Westwood, James H.; dePamphilis, Claude W.

In: Nature Plants, Vol. 5, No. 9, 01.09.2019, p. 991-1001.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Convergent horizontal gene transfer and cross-talk of mobile nucleic acids in parasitic plants

AU - Yang, Zhenzhen

AU - Wafula, Eric K.

AU - Kim, Gunjune

AU - Shahid, Saima

AU - McNeal, Joel R.

AU - Ralph, Paula E.

AU - Timilsena, Prakash R.

AU - Yu, Wen bin

AU - Kelly, Elizabeth A.

AU - Zhang, Huiting

AU - Person, Thomas Nate

AU - Altman, Naomi S.

AU - Axtell, Michael J.

AU - Westwood, James H.

AU - dePamphilis, Claude W.

PY - 2019/9/1

Y1 - 2019/9/1

N2 - Horizontal gene transfer (HGT), the movement and genomic integration of DNA across species boundaries, is commonly associated with bacteria and other microorganisms, but functional HGT (fHGT) is increasingly being recognized in heterotrophic parasitic plants that obtain their nutrients and water from their host plants through direct haustorial feeding. Here, in the holoparasitic stem parasite Cuscuta, we identify 108 transcribed and probably functional HGT events in Cuscuta campestris and related species, plus 42 additional regions with host-derived transposon, pseudogene and non-coding sequences. Surprisingly, 18 Cuscuta fHGTs were acquired from the same gene families by independent HGT events in Orobanchaceae parasites, and the majority are highly expressed in the haustorial feeding structures in both lineages. Convergent retention and expression of HGT sequences suggests an adaptive role for specific additional genes in parasite biology. Between 16 and 20 of the transcribed HGT events are inferred as ancestral in Cuscuta based on transcriptome sequences from species across the phylogenetic range of the genus, implicating fHGT in the successful radiation of Cuscuta parasites. Genome sequencing of C. campestris supports transfer of genomic DNA—rather than retroprocessed RNA—as the mechanism of fHGT. Many of the C. campestris genes horizontally acquired are also frequent sources of 24-nucleotide small RNAs that are typically associated with RNA-directed DNA methylation. One HGT encoding a leucine-rich repeat protein kinase overlaps with a microRNA that has been shown to regulate host gene expression, suggesting that HGT-derived parasite small RNAs may function in the parasite–host interaction. This study enriches our understanding of HGT by describing a parasite–host system with unprecedented gene exchange that points to convergent evolution of HGT events and the functional importance of horizontally transferred coding and non-coding sequences.

AB - Horizontal gene transfer (HGT), the movement and genomic integration of DNA across species boundaries, is commonly associated with bacteria and other microorganisms, but functional HGT (fHGT) is increasingly being recognized in heterotrophic parasitic plants that obtain their nutrients and water from their host plants through direct haustorial feeding. Here, in the holoparasitic stem parasite Cuscuta, we identify 108 transcribed and probably functional HGT events in Cuscuta campestris and related species, plus 42 additional regions with host-derived transposon, pseudogene and non-coding sequences. Surprisingly, 18 Cuscuta fHGTs were acquired from the same gene families by independent HGT events in Orobanchaceae parasites, and the majority are highly expressed in the haustorial feeding structures in both lineages. Convergent retention and expression of HGT sequences suggests an adaptive role for specific additional genes in parasite biology. Between 16 and 20 of the transcribed HGT events are inferred as ancestral in Cuscuta based on transcriptome sequences from species across the phylogenetic range of the genus, implicating fHGT in the successful radiation of Cuscuta parasites. Genome sequencing of C. campestris supports transfer of genomic DNA—rather than retroprocessed RNA—as the mechanism of fHGT. Many of the C. campestris genes horizontally acquired are also frequent sources of 24-nucleotide small RNAs that are typically associated with RNA-directed DNA methylation. One HGT encoding a leucine-rich repeat protein kinase overlaps with a microRNA that has been shown to regulate host gene expression, suggesting that HGT-derived parasite small RNAs may function in the parasite–host interaction. This study enriches our understanding of HGT by describing a parasite–host system with unprecedented gene exchange that points to convergent evolution of HGT events and the functional importance of horizontally transferred coding and non-coding sequences.

UR - http://www.scopus.com/inward/record.url?scp=85070264313&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85070264313&partnerID=8YFLogxK

U2 - 10.1038/s41477-019-0458-0

DO - 10.1038/s41477-019-0458-0

M3 - Article

C2 - 31332314

AN - SCOPUS:85070264313

VL - 5

SP - 991

EP - 1001

JO - Nature Plants

JF - Nature Plants

SN - 2055-026X

IS - 9

ER -