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Comparative Plastid Genomics of Cryptomonas Species Reveals Fine-Scale Genomic Responses to Loss of Photosynthesis

橋本, 哲男 稲垣, 祐司 Archibald, John M Kashiyama, Yuichiro Onodera, Naoko T Mills, Tyler Moore, Christa E Kamikawa, Ryoma Tanifuji, Goro 筑波大学 DOI:31922581

2020.09.16

概要

Loss of photosynthesis is a recurring theme in eukaryotic evolution. In organisms that have lost the ability to photosynthesize, nonphotosynthetic plastids are retained because they play essential roles in processes other than photosynthesis. The unicellular algal genus Cryptomonas contains both photosynthetic and nonphotosynthetic members, the latter having lost the ability to photosynthesize on at least three separate occasions. To elucidate the evolutionary processes underlying the loss of photosynthesis, we sequenced the plastid genomes of two nonphotosynthetic strains, Cryptomonas sp. CCAC1634B and SAG977-2f, as well as the genome of the phototroph Cryptomonas curvata CCAP979/52. These three genome sequences were compared with the previously sequenced plastid genome of the nonphotosynthetic species Cryptomonas paramecium CCAP977/2a as well as photosynthetic members of the Cryptomonadales, including C. curvata FBCC300012D. Intraspecies comparison between the two C. curvata strains showed that although their genome structures are stable, the substitution rates of their genes are relatively high. Although most photosynthesis-related genes, such as the psa and psb gene families, were found to have disappeared from the nonphotosynthetic strains, at least ten pseudogenes are retained in SAG977-2f. Although gene order is roughly shared among the plastid genomes of photosynthetic Cryptomonadales, genome rearrangements are seen more frequently in the smaller genomes of the nonphotosynthetic strains. Intriguingly, the light-independent protochlorophyllide reductase comprising chlB, L, and N is retained in nonphotosynthetic SAG977-2f and CCAC1634B. On the other hand, whereas CCAP977/2a retains ribulose-1,5-bisphosphate carboxylase/oxygenase-related genes, including rbcL, rbcS, and cbbX, the plastid genomes of the other two nonphotosynthetic strains have lost the ribulose-1,5-bisphosphate carboxylase/oxygenase protein-coding genes.

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参考文献

Adl SM, et al. 2019. Revisions to the classification, nomenclature, and

diversity of eukaryotes. J Eukaryot Microbiol. 66(1):4–119.

Archibald JM. 2015. Endosymbiosis and eukaryotic cell evolution. Curr

Biol. 25(19):R911–R921.

Arisue N, et al. 2012. The Plasmodium apicoplast genome: conserved

structure and close relationship of P. ovale to rodent Malaria parasites.

Mol Biol Evol. 29(9):2095–2099.

Bankevich A, et al. 2012. SPAdes: a new genome assembly algorithm and

its applications to single-cell sequencing. J Comput Biol.

19(5):455–477.

Blanc-Mathieu R, Sanchez-Ferandin S, Eyre-Walker A, Piganeau G. 2013.

Organellar inheritance in the green lineage: insights from

Ostreococcus tauri. Genome Biol Evol. 5(8):1503–1511.

Cenci U, et al. 2018. Nuclear genome sequence of the plastid-lacking

cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids. BMC Biol. 16(1):137.

Curtis BA, et al. 2012. Algal genomes reveal evolutionary mosaicism and

the fate of nucleomorphs. Nature 492(7427):59–65.

Darling ACE, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome

Res. 14(7):1394–1403.

Donaher N, et al. 2009. The complete plastid genome sequence of the

secondarily nonphotosynthetic alga Cryptomonas paramecium:

Genome Biol. Evol. 12(2):3926–3937 doi:10.1093/gbe/evaa001 Advance Access publication January 10, 2020

3935

Downloaded from https://academic.oup.com/gbe/article/12/2/3926/5699913 by University of Tsukuba user on 16 September 2020

(Suzuki and Bauer 1995; Hunsperger et al. 2015). In eukaryotes, the genes encoding POR have been transferred to the

nuclear genome. In contrast, the genes encoding LIPOR remain in some plastid genomes but have been lost outright in

many others (i.e., not transferred to the nuclear genome).

Additionally, gene duplication and horizontal transfer of

POR gave rise to various distribution patterns of coding POR

in eukaryotes (Hunsperger et al. 2015; Matsuo and Inagaki

2018). In photosynthetic Cryptomonadales, LIPOR was found

to be intact in C. curvata and Storeatula sp. CCMP 1868 (Kim

et al. 2017). In contrast, G. theta and Teleaulax amphioxeia

completely lost LIPOR from their plastid genomes (Douglas

and Penny 1999; Kim et al. 2015), and Rhodomonas salina,

Chroomonas placoidea, and Chroomonas mesostigmatica appear to have LIPOR only as pseudogenes (Khan et al. 2007;

Kim et al. 2017). These distribution patterns of LIPOR suggest

that nuclear POR is the main POR in Cryptomonadales,

whereas plastid LIPOR is dispensable. On the other hand, it

is still unclear whether nonphotosynthetic Cryptomonas species are currently undergoing gene loss because, despite the

complete loss or degradation of all other photosynthesisrelated proteins, they have retained intact chlorophyll biosynthesis enzymes. Furthermore, because chlorophyll precursors

are photo-toxins generating reactive oxygen species (ROS), it

is likely that those proteins potentially causing ROS generation

disappear at an early stage of the loss of photosynthesis. This

implies that they might have biological significance, such as in

diverting chlorophyll precursors required for still unknown

plastid functions in nonphotosynthetic Cryptomonas species.

Future study of their functions is necessary.

GBE

Tanifuji et al.

3936

Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT version 5: improvement

in accuracy of multiple sequence alignment. Nucleic Acids Res.

33(2):511–518.

Keeling PJ, et al. 2014. The marine microbial eukaryote transcriptome

sequencing project (MMETSP): illuminating the functional diversity of

eukaryotic life in the oceans through transcriptome sequencing. PLoS

Biol. 12 (6):e1001889.

Khan H, Archibald JM. 2008. Lateral transfer of introns in the cryptophyte

plastid genome. Nucleic Acids Res. 36(9):3043–3053.

Khan H, et al. 2007. Plastid genome sequence of the cryptophyte alga

Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol

Evol. 24(8):1832–1842.

Kim JI, Yoon HS, Yi G, Shin W, Archibald JM. 2018. Comparative mitochondrial genomics of cryptophyte algae: gene shuffling and dynamic

mobile genetic elements. BMC Genomics. 19(1):275.

Kim JI, et al. 2015. The plastid genome of the cryptomonad Teleaulax

amphioxeia. PLoS One 10(6):e0129284.

Kim JI, et al. 2017. Evolutionary dynamics of cryptophyte plastid genomes.

Genome Biol Evol. 9(7):1859–1872.

Kolpakov R, Bana G, Kucherov G. 2003. mreps: efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res.

31(13):3672–3678.

Krause K. 2008. From chloroplasts to “cryptic” plastids: evolution of plastid genomes in parasitic plants. Curr Genet. 54(3):111–121.

Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection

of transfer RNA genes in genomic sequence. Nucleic Acids Res.

25(5):955–964.

Matsuo E, Inagaki Y. 2018. Patterns in evolutionary origins of heme, chlorophyll a and isopentenyl diphosphate biosynthetic pathways suggest

non-photosynthetic periods prior to plastid replacements in dinoflagellates. PeerJ 6:e5345.

McFadden GI, Melkonian M. 1986. Use of HEPES buffer for microalgal

culture media and fixation for electron microscopy. Phycologia

25(4):551–557.

Moore CE, Archibald JM. 2009. Nucleomorph genomes. Annu Rev Genet.

43(1):251–264.

Moore CE, Curtis B, Mills T, Tanifuji G, Archibald JM. 2012. Nucleomorph

genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol Evol. 4(11):1162–1175.

Muraki N, et al. 2010. X-ray crystal structure of the light-independent

protochlorophyllide reductase. Nature 465(7294):110–114.

Nowack ECM, Weber APM. 2018. Genomics-Informed insights into endosymbiotic organelle evolution in photosynthetic eukaryotes. Annu

Rev Plant Biol. 69(1):51–84.

Palmer JD, Thompson WF. 1982. Chloroplast DNA rearrangements are

more frequent when a large inverted repeat sequence is lost. Cell

29(2):537–550.

Rutherford K, et al. 2000. Artemis: sequence visualization and annotation.

Bioinformatics 16(10):944–945.

Sabir JSM, et al. 2014. Conserved gene order and expanded inverted

repeats characterize plastid genomes of Thalassiosirales. PLoS One

9(9):e107854.

Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF. 2007. Plastid

genes in a non-photosynthetic dinoflagellate. Protist 158(1):

105–117.

Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y. 2004. Rubisco

without the Calvin cycle improves the carbon efficiency of developing

green seeds. Nature 432(7018):779–782.

Sekiguchi H, Moriya M, Nakayama T, Inouye I. 2002. Vestigial chloroplasts

in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys

infusionum (Dictyochophyceae). Protist 153(2):157–167.

Genome Biol. Evol. 12(2):3926–3937 doi:10.1093/gbe/evaa001 Advance Access publication January 10, 2020

Downloaded from https://academic.oup.com/gbe/article/12/2/3926/5699913 by University of Tsukuba user on 16 September 2020

reduction, compaction, and accelerated evolutionary rate. Genome

Biol Evol. 1:439–448.

Dorrell RG, et al. 2019. Principles of plastid reductive evolution illuminated

by nonphotosynthetic chrysophytes. Proc Natl Acad Sci U S A.

116(14):6914–6923.

Douglas SE, Penny SL. 1999. The plastid genome of the cryptophyte alga,

Guillardia theta: complete sequence and conserved synteny groups

confirm its common ancestry with red algae. J Mol Evol.

48(2):236–244.

Fujita Y, Bauer C. 2003. The light-dependent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening

in the dark. In: Kadish K, Smith K, Guilard R, editors. The porphyrin

handbook. San Diego (CA): Elsevier Science. p 109–156.

Gockel G, Hachtel W. 2000. Complete gene map of the plastid genome of

the nonphotosynthetic euglenoid flagellate Astasia longa. Protist

151(4):347–351.

Gould SB, Maier UG, Martin WF. 2015. Protein import and the origin of

red complex plastids. Curr Biol. 25(12):R515–R521.

Grisdale CJ, Smith DR, Archibald JM. 2019. Relative mutation rates in

nucleomorph-bearing algae. Genome Biol Evol. 11(4):1045–1053.

Guillard RL, Lorenzen CJ. 1972. Yellow-green algae with chlorophyllide C.

J Phycol. 8:10–14.

Hadariova L, Vesteg M, Hampl V, Krajcovic J. 2018. Reductive evolution of

chloroplasts in non-photosynthetic plants, algae and protists. Curr

Genet. 64(2):365–387.

Hempel F, Bolte K, Klingl A, Zauner S, Maier UG. 2014. Protein transport

into plastids of secondarily evolved organisms. In: Theg SM, Wollman

F-A, editors. Plastid Biology. New York: Springer. p. 291–303.

Hoef-Emden K. 2005. Multiple independent losses of photosynthesis and

differing evolutionary rates in the genus Cryptomonas (Cryptophyceae):

combined phylogenetic analyses of DNA sequences of the nuclear and

the nucleomorph ribosomal operons. J Mol Evol. 60(2):183–195.

Hoef-Emden K. 2007. Revision of the genus Cryptomonas

(Cryptophyceae) II: incongruences between the classical morphospecies concept and molecular phylogeny in smaller pyrenoid-less cells.

Phycologia 46(4):402–428.

Hoef-Emden K, Archibald JM. 2016. Phylum Cryptophyta (cryptomonads).

In: Archibald JM, Simpson AGB, Slamovits C, editors. Handbook of the

protists. Berlin: Springer-Verlag. p.851–891.

Hoef-Emden K, Tran HD, Melkonian M. 2005. Lineage-specific variations

of congruent evolution among DNA sequences from three genomes,

and relaxed selective constraints on rbcL in Cryptomonas

(Cryptophyceae). BMC Evol Biol. 5(1):56.

Hunsperger HM, Randhawa T, Cattolico RA. 2015. Extensive horizontal

gene transfer, duplication, and loss of chlorophyll synthesis genes in

the algae. BMC Evol Biol. 15(1):16.

Janouskovec J, et al. 2013. Evolution of red algal plastid genomes: ancient

architectures, introns, horizontal gene transfer, and taxonomic utility

of plastid markers. PLoS One 8(3):e59001.

Johnson LK, Alexander H, Brown CT. 2018. Re-assembly, quality evaluation, and annotation of 678 microbial eukaryotic reference transcriptomes. Gigascience 8(4):giy158.

Kamikawa R, Azuma T, Ishii K-I, Matsuno Y, Miyashita H. 2018. Diversity

of organellar genomes in non-photosynthetic diatoms. Protist

169(3):351–361.

Kamikawa R, Tanifuji G, et al. 2015. Proposal of a twin arginine translocator system-mediated constraint against loss of ATP synthase genes

from nonphotosynthetic plastid genomes. Mol Biol Evol.

32(10):2598–2604.

Kamikawa R, Yubuki N, et al. 2015. Multiple losses of photosynthesis in

Nitzschia (Bacillariophyceae). Phycol Res. 63(1):19–28.

Kamikawa R, et al. 2017. A non-photosynthetic diatom reveals early steps

of reductive evolution in plastids. Mol Biol Evol. 34(9):2355–2366.

GBE

Comparative Plastid Genomics of Cryptomonas

Vieira Ldo N, et al. 2014. The complete chloroplast genome sequence of

Podocarpus lambertii: genome structure, evolutionary aspects, gene

content and SSR detection. PLoS One 9(3):e90618.

Wei L, et al. 2013. Nannochloropsis plastid and mitochondrial

phylogenomes reveal organelle diversification mechanism and

intragenus phylotyping strategy in microalgae. BMC Genomics.

14(1):534.

Wicke S, et al. 2013. Mechanisms of functional and physical genome

reduction in photosynthetic and nonphotosynthetic parasitic plants

of the broomrape family. Plant Cell 25(10):3711–3725.

Wickett NJ, et al. 2008. Functional gene losses occur with minimal size

reduction in the plastid genome of the parasitic liverwort Aneura mirabilis. Mol Biol Evol. 25(2):393–401.

Wilson RJ, et al. 1996. Complete gene map of the plastid-like DNA of

the malaria parasite Plasmodium falciparum. J Mol Evol.

261(2):155–172.

Wolfe AD, dePamphilis CW. 1997. Alternate paths of evolution for the

photosynthetic gene rbcL in four nonphotosynthetic species of

Orobanche. Plant Mol Biol. 33(6):965–977.

Wolfe KH, Morden CW, Palmer JD. 1992. Function and evolution of a

minimal plastid genome from a nonphotosynthetic parasitic plant.

Proc Natl Acad Sci U S A. 89(22):10648–10652.

Yabuki A, et al. 2014. Palpitomonas bilix represents a basal cryptist

lineage: insight into the character evolution in Cryptista. Sci Rep.

4(1):4641.

Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol

Biol Evol. 24(8):1586–1591.

Z

ahonov

a K, Fu¨ssy Z, Obornık M, Eli

as M, Yurchenko V. 2016. RuBisCO in

non-photosynthetic alga Euglena longa: divergent features, transcriptomic analysis and regulation of complex formation. PLoS One

11(7):e0158790.

Zimorski V, Ku C, Martin WF, Gould SB. 2014. Endosymbiotic theory for

organelle origins. Curr Opin Microbiol. 22:38–48.

Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization

prediction. Nucleic Acids Res. 31(13):3406–3415.

Associate editor: Gwenael Piganeau

Genome Biol. Evol. 12(2):3926–3937 doi:10.1093/gbe/evaa001 Advance Access publication January 10, 2020

3937

Downloaded from https://academic.oup.com/gbe/article/12/2/3926/5699913 by University of Tsukuba user on 16 September 2020

Smith DR, Lee RW. 2014. A plastid without a genome: evidence from the

nonphotosynthetic green algal genus Polytomella. Plant Physiol.

164(4):1812–1819.

Strauss SH, Palmer JD, Howe GT, Doerksen AH. 1988. Chloroplast

genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proc Natl Acad Sci U S A. 85(11):3898–3902.

Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of

protein sequence alignments into the corresponding codon alignments. Nucleic Acid Res. 34(Web Server):W609–W612.

Suzuki JY, Bauer CE. 1995. A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants. Proc Natl Acad Sci U S A.

92(9):3749–3753.

Suzuki S, Endoh R, Manabe R-I, Ohkuma M, Hirakawa Y. 2018. Multiple

losses of photosynthesis and convergent reductive genome evolution

in the colourless green algae Prototheca. Sci Rep. 8(1):940.

Tanifuji G, Archibald JM. 2014. Nucleomorph comparative genomics. In:

Lo¨ffelhardt W, editor. Endosymbiosis. Vienna (Austria): Springer. p.

197–213.

Tanifuji G, Archibald JM, Hashimoto T. 2016. Comparative genomics of

mitochondria in chlorarachniophyte algae: endosymbiotic gene transfer and organellar genome dynamics. Sci Rep. 6(1):21016.

Tanifuji G, Onodera NT. 2017. Chapter eight—cryptomonads: a model

organism sheds light on the evolutionary history of genome reorganization in secondary endosymbioses. In: Hirakawa Y, editor. Advances

in botanical research. Cambridge: Academic Press. p. 263–320.

Tanifuji G, et al. 2011. Complete nucleomorph genome sequence of the

nonphotosynthetic alga Cryptomonas paramecium reveals a core

nucleomorph gene set. Genome Biol Evol. 3:44– 54.

Tanifuji G, et al. 2014. Nucleomorph and plastid genome sequences of the

chlorarachniophyte Lotharella oceanica: convergent reductive evolution and frequent recombination in nucleomorph-bearing algae. BMC

Genomics. 15(1):374.

Turmel M, Lopes Dos Santos A, Otis C, Sergerie R, Lemieux C. 2019.

Tracing the evolution of the plastome and mitogenome in the

Chloropicophyceae uncovered convergent tRNA gene losses and a

variant plastid genetic code. Genome Biol Evol. 11(4):1275–1292.

Turmel M, Otis C, Lemieux C. 2017. Divergent copies of the large inverted

repeat in the chloroplast genomes of ulvophycean green algae. Sci

Rep. 7(1):994.

...

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