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Split photosystem protein, linear-mapping topology, and growth of structural complexity in the plastid genome of Chromera velia

Split photosystem protein, linear-mapping topology, and growth of structural complexity in the plastid genome of Chromera velia
Split photosystem protein, linear-mapping topology, and growth of structural complexity in the plastid genome of Chromera velia
The canonical photosynthetic plastid genomes consist of a single circular-mapping chromosome that encodes a highly conserved protein core, involved in photosynthesis and ATP generation. Here, we demonstrate that the plastid genome of the photosynthetic relative of apicomplexans, Chromera velia, departs from this view in several unique ways. Core photosynthesis proteins PsaA and AtpB have been broken into two fragments, which we show are independently transcribed, oligoU-tailed, translated, and assembled into functional photosystem I and ATP synthase complexes. Genome-wide transcription profiles support expression of many other highly modified proteins, including several that contain extensions amounting to hundreds of amino acids in length. Canonical gene clusters and operons have been fragmented and reshuffled into novel putative transcriptional units. Massive genomic coverage by paired-end reads, coupled with pulsed-field gel electrophoresis and polymerase chain reaction, consistently indicate that the C. velia plastid genome is linear-mapping, a unique state among all plastids. Abundant intragenomic duplication probably mediated by recombination can explain protein splits, extensions, and genome linearization and is perhaps the key driving force behind the many features that defy the conventional ways of plastid genome architecture and function.
1537-1719
2447–2462
Janouskovec, J
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Sobotka, R
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Lai, De-Hua
da8ca99a-82a8-4be1-945f-47142be1af58
Flegontov, Pavel
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Koník, Peter
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Komenda, Josef
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Ali, Shahjahan
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Prasil, Ondrej
df604afc-c0f3-4a27-806a-129d67355176
Pain, Arnab
2ba45805-5611-4347-a49b-22e6392d13d8
Obornik, Miroslav
ead34df5-cb1e-465a-871c-5069abed979e
Lukes, Julius
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Keeling, Patrick J.
fd51c2ef-1daa-442d-b186-71001aa7ca7d
Janouskovec, J
fbaa4a5d-872e-465b-b2c3-bb35df455cc6
Sobotka, R
5587e889-8c14-47e7-bdf4-19191a9a5e12
Lai, De-Hua
da8ca99a-82a8-4be1-945f-47142be1af58
Flegontov, Pavel
5d93825a-a2ec-4545-ac52-3099bf68836e
Koník, Peter
b4354352-e230-4f85-80c8-e7aca0f25978
Komenda, Josef
e6a1557c-3606-485e-9e0f-5c788b92ab14
Ali, Shahjahan
cbb0fd4f-eb3d-4843-8c82-96a4552a911f
Prasil, Ondrej
df604afc-c0f3-4a27-806a-129d67355176
Pain, Arnab
2ba45805-5611-4347-a49b-22e6392d13d8
Obornik, Miroslav
ead34df5-cb1e-465a-871c-5069abed979e
Lukes, Julius
255eee10-9411-4fdc-ad90-7b7df733bad3
Keeling, Patrick J.
fd51c2ef-1daa-442d-b186-71001aa7ca7d

Janouskovec, J, Sobotka, R, Lai, De-Hua, Flegontov, Pavel, Koník, Peter, Komenda, Josef, Ali, Shahjahan, Prasil, Ondrej, Pain, Arnab, Obornik, Miroslav, Lukes, Julius and Keeling, Patrick J. (2013) Split photosystem protein, linear-mapping topology, and growth of structural complexity in the plastid genome of Chromera velia. Molecular Biology and Evolution, 30 (11), 2447–2462. (doi:10.1093/molbev/mst144).

Record type: Article

Abstract

The canonical photosynthetic plastid genomes consist of a single circular-mapping chromosome that encodes a highly conserved protein core, involved in photosynthesis and ATP generation. Here, we demonstrate that the plastid genome of the photosynthetic relative of apicomplexans, Chromera velia, departs from this view in several unique ways. Core photosynthesis proteins PsaA and AtpB have been broken into two fragments, which we show are independently transcribed, oligoU-tailed, translated, and assembled into functional photosystem I and ATP synthase complexes. Genome-wide transcription profiles support expression of many other highly modified proteins, including several that contain extensions amounting to hundreds of amino acids in length. Canonical gene clusters and operons have been fragmented and reshuffled into novel putative transcriptional units. Massive genomic coverage by paired-end reads, coupled with pulsed-field gel electrophoresis and polymerase chain reaction, consistently indicate that the C. velia plastid genome is linear-mapping, a unique state among all plastids. Abundant intragenomic duplication probably mediated by recombination can explain protein splits, extensions, and genome linearization and is perhaps the key driving force behind the many features that defy the conventional ways of plastid genome architecture and function.

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More information

e-pub ahead of print date: 22 August 2013
Published date: 1 November 2013
Additional Information: The Author 2013.

Identifiers

Local EPrints ID: 467625
URI: http://eprints.soton.ac.uk/id/eprint/467625
ISSN: 1537-1719
PURE UUID: c18e114b-0f84-468a-a010-317ece1ad74c
ORCID for J Janouskovec: ORCID iD orcid.org/0000-0001-6547-749X

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Date deposited: 15 Jul 2022 19:21
Last modified: 19 Jul 2022 02:13

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Contributors

Author: J Janouskovec ORCID iD
Author: R Sobotka
Author: De-Hua Lai
Author: Pavel Flegontov
Author: Peter Koník
Author: Josef Komenda
Author: Shahjahan Ali
Author: Ondrej Prasil
Author: Arnab Pain
Author: Miroslav Obornik
Author: Julius Lukes
Author: Patrick J. Keeling

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