Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum

Barbrook, Adrian C.; Howe, Christopher J.

doi:10.1007/s004380050042

Cited by 95 publications

(103 citation statements)

References 17 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…If the model of recombination among cores is correct (Zhang et al, 1999(Zhang et al, , 2002Barbrook & Howe, 2000) then the hypervariable sequences of the Symbiodinium V regions would indicate that these do not homogenize or recombine nearly as often as the cores. It is possible that the V regions act as buffer zones lowering the probability that recombination will extend into the protein-coding regions of minicircles.…”

Section: Discussionmentioning

confidence: 99%

“…Likewise, core regions are identifiable across all the minicircles from Amphidinium operculatum, again implying intra-circle recombination (Barbrook & Howe, 2000;Howe et al, 2003), but the sequence of these cores is not alignable with those from Heterocapsa triquetra. A hypothesis of species-specific conserved cores has been tested on two minicircles, psbA and 23S rDNA, from three further species of Heterocapsa and from the distantly related A. carterae, and was supported in each case (Zhang et al, 2002).…”

Section: Introductionmentioning

confidence: 95%

“…Unigenic DNA minicircles of 2-3 kbp that encode plastid gene functions have been found in a number of different peridinin-containing dinoflagellates, including species of Heterocapsa (Zhang et al, 1999(Zhang et al, , 2002, Amphidinium operculatum (Barbrook & Howe, 2000;Barbrook et al, 2001), Amphidinium carterae (Hiller, 2001) and Protoceratium reticulatum (Zhang et al, 2002). The non-coding regions of the minicircles are highly divergent across dinoflagellate genera, except that short stretches of a single nucleotide are frequent.…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

Moore

2003

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

View full text Add to dashboard Cite

The chloroplast genes of dinoflagellates are distributed among small, circular dsDNA molecules termed minicircles. In this paper, we describe the structure of the non-coding region of the psbA minicircle from Symbiodinium. DNA sequence was obtained from five Symbiodinium strains obtained from four different coral host species (Goniopora tenuidens, Heliofungia actiniformis, Leptastrea purpurea and Pocillopora damicornis), which had previously been determined to be closely related using LSU rDNA region D1/D2 sequence analysis. Eight distinct sequence blocks, consisting of four conserved cores interspersed with two metastable regions and flanked by two variable regions, occurred at similar positions in all strains. Inverted repeats (IRs) occurred in tandem or 'twin' formation within two of the four cores. The metastable regions also consisted of twin IRs and had modular behaviour, being either fully present or completely absent in the different strains. These twin IRs are similar in sequence to double-hairpin elements (DHEs) found in the mitochondrial genomes of some fungi, and may be mobile elements or may serve a functional role in recombination or replication. Within the central unit (consisting of the cores plus the metastable regions), all IRs contained perfect sequence inverses, implying they are highly evolved. IRs were also present outside the central unit but these were imperfect and possessed by individual strains only. A central adenine-rich sequence most closely resembled one in the centre of the non-coding part of Amphidinium operculatum minicircles, and is a potential origin of replication. Sequence polymorphism was extremely high in the variable regions, suggesting that these regions may be useful for distinguishing strains that cannot be differentiated using molecular markers currently available for Symbiodinium. INTRODUCTIONUnigenic DNA minicircles of 2-3 kbp that encode plastid gene functions have been found in a number of different peridinin-containing dinoflagellates, including species of Heterocapsa (Zhang et al., 1999(Zhang et al., , 2002, Amphidinium operculatum (Barbrook & Howe, 2000;Barbrook et al., 2001), Amphidinium carterae (Hiller, 2001) and Protoceratium reticulatum (Zhang et al., 2002). The non-coding regions of the minicircles are highly divergent across dinoflagellate genera, except that short stretches of a single nucleotide are frequent. A common format across dinoflagellate genera and species is that the non-coding regions contain conserved core regions, usually of between two and four in number, separated by variable regions (Zhang et al., 2002;Howe et al., 2003). In a given species, two or more cores are often identical to each other, seemingly duplicated or triplicated within the same minicircle, such as the two 9G regions of Heterocapsa triquetra (Zhang et al., 1999(Zhang et al., , 2002, and the three 5G regions of Heterocapsa pygmeae (Zhang et al., 2002).It has been shown that conserved core regions are shared between all the minicircles present in one culture of Abbreviat...

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 95%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

Moore

2003

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

View full text Add to dashboard Cite

show abstract

“…Some time after the haptophyte replacement of the plastid, the dinoflagellates diverged into two groups. One group retained the ancestral haptophyte characteristics in its plastid (fucoxanthin, chlorophyll c 1 ϩ c 2 ), whereas the second group underwent several major changes including the evolution of peridinin (replacing fucoxanthin), loss of chlorophyll c 1 , the remarkable reduction of its plastid genome to single gene circles (7,39), the development of cellulose armor, and the origin of a divergent nuclear encoded ''Form II'' rbcL gene (40,41). It is possible that peridinin could have evolved from a modification of the ancestral fucoxanthin biosynthesis pathway because these are structurally related xanthophylls (for details, see refs.…”

Section: Evolution Of Dinoflagellate Plastidsmentioning

confidence: 99%

A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis

Yoon

Hackett

Bhattacharya

2002

Proc. Natl. Acad. Sci. U.S.A.

369

251

View full text Add to dashboard Cite

The most widely distributed dinoflagellate plastid contains chlorophyll c 2 and peridinin as the major carotenoid. A second plastid type, found in taxa such as Karlodinium micrum and Karenia spp., contains chlorophylls c 1 ؉ c2 and 19 -hexanoyloxy-fucoxanthin and͞or 19 -butanoyloxy-fucoxanthin but lacks peridinin. Because the presence of chlorophylls c 1 ؉ c2 and fucoxanthin is typical of haptophyte algae, the second plastid type is believed to have originated from a haptophyte tertiary endosymbiosis in an ancestral peridinin-containing dinoflagellate. This hypothesis has, however, never been thoroughly tested in plastid trees that contain genes from both peridinin-and fucoxanthin-containing dinoflagellates. To address this issue, we sequenced the plastid-encoded psaA (photosystem I P700 chlorophyll a apoprotein A1), psbA (photosystem II reaction center protein D1), and ''Form I'' rbcL (ribulose-1,5-bisphosphate carboxylase͞oxygenase) genes from various red and dinoflagellate algae. The combined psaA ؉ psbA tree shows significant support for the monophyly of peridinin-and fucoxanthin-containing dinoflagellates as sister to the haptophytes. The monophyly with haptophytes is robustly recovered in the psbA phylogeny in which we increased the sampling of dinoflagellates to 14 species. As expected from previous analyses, the fucoxanthin-containing dinoflagellates formed a wellsupported sister group with haptophytes in the rbcL tree. Based on these analyses, we postulate that the plastid of peridinin-and fucoxanthin-containing dinoflagellates originated from a haptophyte tertiary endosymbiosis that occurred before the split of these lineages. Our findings imply that the presence of chlorophylls c 1 ؉ c2 and fucoxanthin, and the Form I rbcL gene are in fact the primitive (not derived, as widely believed) condition in dinoflagellates.

show abstract

“…Uchida (1988) showed that peridinin dinoflagellates have a divergent ferredoxin and later found that dinoflagellate psbA sequences are also extremely divergent from other algae (Takishita and Uchida 1999). Using density gradient centrifugation Zhang (1999) and later Barbrook and Howe (2000) as well as Hiller (2001), and Bachvaroff (unpublished) have separated circular, or plasmid-like DNAs from peridinin dinoflagellates. These minicircles encode one or sometimes two genes, although partial or incomplete genes have also been found (Hiller 2001).…”

Section: Bmentioning

confidence: 99%

5  The origin of the dinoflagellate plastid

Bachvaroff

Concepcion

Rogers

et al. 2003

Journal of Phycology

View full text Add to dashboard Cite

The peridinin pigmented dinoflagellate chloroplasts are the result of a secondary endosymbiotic event between a photosynthetic eukaryote and a dinoflagellate.Dinoflagellate chloroplast and nuclear evolution were independent before this endosymbiotic event. To reconstruct the evolution of the dinoflagellate chloroplast, phylogenies were constructed with a chloroplast gene psbB. The gene phylogeny should reflect the evolution of the chloroplast and indicate the plastid donor lineage. Gene sequences derived from the dinoflagellate chloroplast were extremely divergent but suggested that the plastid donor could have been a haptophyte. In an attempt to find better genes for analysis and to further understand gene transfer about 4900 randomly selected expressed genes were sequenced from two dinoflagellates, Lingulodinium polyedra and Amphidinium carterae. From these genes, thirty typically plastid-encoded genes were found, including eight otherwise known only from plastid genomes. Based on poly-A tails, gene families, and leader sequences these genes appear to be nuclearencoded in dinoflagellates. This result suggests that dinoflagellate chloroplasts may have the smallest protein-coding potential yet known. These genes and the partially sequenced chloroplast genome of a haptophyte were used in a phylogenetic analysis. There is strong conflict between genes encoded in the chloroplast and those in the nucleus. The chloroplast genes suggest relationship between haptophyte and dinoflagellate plastids, while the nuclear-encoded genes suggest a relationship with heterokonts. Chromophyte plastid monophyly is supported by these data but the single origin of the chromophyte plastid from red algae does not mean that the host lineages are monophyletic. These results are consistent with at least two different scenarios: either dinoflagellates and haptophytes independently acquired a plastid from the heterokonts, or dinoflagellates acquired their plastids from haptophtyes, who in turn acquired their plastids from heterokonts. The evolutionary rate of the remaining plastid-encoded genes was compared with formerly plastid-encoded genes. These relative rate tests revealed strong incongruence between minicircle genes, formerly plastid-encoded genes and genes that were likely to have been acquired from the nucleus of the plastid donor lineage.

show abstract

Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum

Cited by 95 publications

References 17 publications

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis

5  The origin of the dinoflagellate plastid

Contact Info

Product

Resources

About

Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum

Cited by 95 publications

References 17 publications

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

Highly organized structure in the non-coding region of the psbA minicircle from clade C Symbiodinium

A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis

5 The origin of the dinoflagellate plastid

Contact Info

Product

Resources

About

5  The origin of the dinoflagellate plastid