Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae)

Jeanmaire Molina, Khaled M. Hazzouri, Daniel Nickrent, Matthew Geisler, Rachel S. Meyer, Melissa M. Pentony, Jonathan Flowers, Pieter Pelser, Julie Barcelona, Samuel Alan Inovejas, Iris Uy, Wei Yuan, Olivia Wilkins, Claire Iphanise Michel, Selina Locklear, Gisela P. Concepcion, Michael Purugganan

Research output: Contribution to journalArticle

Abstract

Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ∼350× sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2×) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp, ndh, pet, psa, psb, rbcL), ribosomal RNA genes (rrn16, rrn23), ribosomal protein genes (rps7, rps11, rps16), transfer RNA genes, as well as matK, accD, ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ∼33% of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50% bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches - despite success in identifying and developing a draft assembly of the much larger mitochondrial genome - suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if present is found in cryptic form at very low levels.

Original languageEnglish (US)
Pages (from-to)793-803
Number of pages11
JournalMolecular Biology and Evolution
Volume31
Issue number4
DOIs
StatePublished - Apr 2014

Fingerprint

Rafflesia
Rafflesiaceae
Chloroplast Genome
chloroplast
angiosperm
plastid
Angiospermae
Plastids
genome
plastids
gene
Plastid Genomes
Genes
application coverage
Mitochondrial Genome
genes
Photosynthesis
Tetrastigma
RNA
photosynthesis

Keywords

  • Gene loss
  • Holoparasite
  • Horizontal gene transfer
  • NUPTs
  • Plastid
  • Tetrastigma

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). / Molina, Jeanmaire; Hazzouri, Khaled M.; Nickrent, Daniel; Geisler, Matthew; Meyer, Rachel S.; Pentony, Melissa M.; Flowers, Jonathan; Pelser, Pieter; Barcelona, Julie; Inovejas, Samuel Alan; Uy, Iris; Yuan, Wei; Wilkins, Olivia; Michel, Claire Iphanise; Locklear, Selina; Concepcion, Gisela P.; Purugganan, Michael.

In: Molecular Biology and Evolution, Vol. 31, No. 4, 04.2014, p. 793-803.

Research output: Contribution to journalArticle

Molina, J, Hazzouri, KM, Nickrent, D, Geisler, M, Meyer, RS, Pentony, MM, Flowers, J, Pelser, P, Barcelona, J, Inovejas, SA, Uy, I, Yuan, W, Wilkins, O, Michel, CI, Locklear, S, Concepcion, GP & Purugganan, M 2014, 'Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae)', Molecular Biology and Evolution, vol. 31, no. 4, pp. 793-803. https://doi.org/10.1093/molbev/msu051
Molina, Jeanmaire ; Hazzouri, Khaled M. ; Nickrent, Daniel ; Geisler, Matthew ; Meyer, Rachel S. ; Pentony, Melissa M. ; Flowers, Jonathan ; Pelser, Pieter ; Barcelona, Julie ; Inovejas, Samuel Alan ; Uy, Iris ; Yuan, Wei ; Wilkins, Olivia ; Michel, Claire Iphanise ; Locklear, Selina ; Concepcion, Gisela P. ; Purugganan, Michael. / Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae). In: Molecular Biology and Evolution. 2014 ; Vol. 31, No. 4. pp. 793-803.
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abstract = "Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ∼350× sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2×) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp, ndh, pet, psa, psb, rbcL), ribosomal RNA genes (rrn16, rrn23), ribosomal protein genes (rps7, rps11, rps16), transfer RNA genes, as well as matK, accD, ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ∼33{\%} of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50{\%} bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches - despite success in identifying and developing a draft assembly of the much larger mitochondrial genome - suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if present is found in cryptic form at very low levels.",
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AU - Meyer, Rachel S.

AU - Pentony, Melissa M.

AU - Flowers, Jonathan

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AU - Barcelona, Julie

AU - Inovejas, Samuel Alan

AU - Uy, Iris

AU - Yuan, Wei

AU - Wilkins, Olivia

AU - Michel, Claire Iphanise

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