Plastid and mitochondrial genomes of Coccophora langsdorfii (Fucales, Phaeophyceae) and the utility of molecular markers

Graf, Louis; Kim, Yae Jin; Cho, Ga Youn; Miller, Kathy Ann; Yoon, Hwan Su

doi:10.1371/journal.pone.0187104

Cited by 12 publications

(12 citation statements)

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“…Although there were long intergenic sequences in the Pylaiella littoralis mtDNA, an analysis of synteny with other available brown algal mtDNAs indicated strong conservation of genome structures across all taxa, regardless of the type of fertilization (isogamous Ectocarpales and oogamous Fucales, Laminariales, Dictyotales, and Desmarestiales; Fig. S4), which is consistent with previous reports 27,34,35 .…”

Section: Alignments Of Brown Algal Mtdnassupporting

confidence: 90%

Organelle inheritance and genome architecture variation in isogamous brown algae

Choi

Graf

Peters

et al. 2020

Sci Rep

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Among the brown algal lineages, ectocarpales species have isogamous fertilization in which male and female gametes are morphologically similar. in contrast, female gametes are much larger than male gametes in the oogamous species found in many other brown algal lineages. it has been reported that the plastids of isogamous species are biparentally inherited whereas the plastids of oogamous species are maternally inherited. in contrast, in both isogamous and oogamous species, the mitochondria are usually inherited maternally. to investigate whether there is any relationship between the modes of inheritance and organellar genome architecture, we sequenced six plastid genomes (ptDnA) and two mitochondrial genomes (mtDnA) of isogamous species from the ectocarpales and compared them with previously sequenced organellar genomes. We found that the biparentally inherited ptDnAs of isogamous species presented distinctive structural rearrangements whereas maternally inherited ptDnAs of oogamous species showed no rearrangements. our analysis permits the hypothesis that structural rearrangements in ptDnAs may be a consequence of the mode of inheritance. The brown algae (Phaeophyceae) are a group of photosynthetic heterokonts (=stramenopiles), a secondary endosymbiotic lineage containing red algal-derived plastids 1. The four brown algal orders analyzed in this study, Ectocarpales, Fucales, Laminariales, and Dictyotales, have macroscopic thalli and are distributed worldwide in low-to-mid latitudes where they play important roles in marine ecosystems. Also, they have great potential for commercial uses such as food or in other seaweed industries. From a taxonomic point of view, the orders Ectocarpales, Fucales and Laminariales are grouped into the subclass Fucophycidae, which is defined as a lineage derived from the brown algal crown radiation (BACR), whereas Dictyotales is classified into the Dictyotophycidae 2 (Fig. S1). The life cycles of most brown algae, including species of the Laminariales and Ectocarpales, are characterized by an alternation between a diploid sporophyte and a haploid gametophyte (i.e., a diploid-haploid life cycle). In contrast, in the Fucales meiosis occurs in the parental diploid plants and they directly produce gametes (i.e., a diplontic life cycle) 3,4. Three fertilization types can be defined based on the morphologies and flagella of gametes, independent of whether they are produced via a gametophyte stage or not: the isogamous type in which flagellated gametes are morphologically similar; the anisogamous type where one flagellated gamete is larger than the other; and the oogamous type in which one gamete is a non-motile cell called the egg cell (or oocyte) and the other is a smaller, flagellated sperm cell 5. Most brown algae, including the Laminariales and most species of the Fucales, are oogamous. Anisogamy is only observed in a few lineages such as the Onslowiales, Asterocladales, Nemodermatales, and in some Fucales, Sphacelariales and Ectocarpales species. With the exception of the orders Ecto...

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Section: Alignments Of Brown Algal Mtdnassupporting

confidence: 90%

Organelle inheritance and genome architecture variation in isogamous brown algae

Choi

Graf

Peters

et al. 2020

Sci Rep

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“…Newly sequenced plastomes varied from 128,910 to 131,355 bp and were all AT rich, ranging from 68.53 to 69.72% AT content. Our results indicate that the plastomes of brown algae consist of a core set of 173 unique genes: 141 protein-coding sequences, three unique rRNA genes (that are each duplicated in the inverted repeat region), typically 28 (but up to 31) tRNA genes, along with a widely conserved ORF occurring between rps 4 and ycf 65, adding slightly to the gene totals of previous studies ( Graf et al 2017 ). The inverted repeat regions are typically ∼5,500 bp in length, capturing mostly rRNA genes but occasionally capturing flanking genes ycf 37 and rpl 21.…”

Section: Resultssupporting

confidence: 50%

“…Plastids and mitochondria are eukaryotic organelles that have evolved after ancient endosymbioses ( Margulis 1970 ; Keeling 2004 ; Smith and Keeling 2015 ) and typically retain their own genomes. Organellar genes and genomes have been used as essential phylogenetic markers, both to distinguish species (e.g., Ratnasingham and Hebert 2007 ; Graf et al 2017 ; Hind et al 2019 ) and to reconstruct recent and deep evolutionary relationships (e.g., Rai et al 2003 ; Janouškovec et al 2013 ). Organellar genomes have variable sequence evolution rates across taxa, across organelles (i.e., plastid vs. mitochondrion), and across genes within a single genome ( Smith and Keeling 2015 ).…”

Section: Introductionmentioning

confidence: 99%

“…This limits our ability to recognize and interpret patterns of organellar genome evolution across the group. Moreover, studies on the rates of sequence evolution, patterns of structural evolution, and the prevalence of introns across brown algal organelles have been mostly uniorganellar (e.g., Liu et al 2015 , 2019 ; Zhang et al 2015 ; Yang et al 2016 ; but see Graf et al 2017 ). Thus, patterns of evolution across plastids and mitochondria have yet to be thoroughly compared in parallel across different brown algal taxa, further limiting our understanding of organellar genome evolution across this globally significant group.…”

Section: Introductionmentioning

confidence: 99%

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Genomic Rearrangements and Sequence Evolution across Brown Algal Organelles

Starko

Bringloe

Gomez

et al. 2021

Genome Biology and Evolution

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Organellar genomes serve as useful models for genome evolution and contain some of the most widely used phylogenetic markers, but they are poorly characterized in many lineages. Here we report 20 novel mitochondrial genomes and 16 novel plastid genomes from the brown algae. We focused our efforts on the orders Chordales and Laminariales, but also provide the first plastid genomes (plastomes) from Desmarestiales and Sphacelariales, the first mitochondrial genome (mitome) from Ralfsiales and a nearly complete mitome from Sphacelariales. We then compared gene content, sequence evolution rates, shifts in genome structural arrangements, and intron distributions across lineages. We confirm that gene content is largely conserved in both organellar genomes across the brown algal tree of life, with few cases of gene gain or loss. We further show that substitution rates are generally lower in plastid than mitochondrial genes, but plastomes are more variable in gene arrangement, as mitomes tend to be colinear even among distantly related lineages (with exceptions). Patterns of intron distribution across organellar genomes are complex. In particular, the mitomes of several laminarialean species possess group II introns that have T7-like ORFs, found previously only in mitochondrial genomes of Pylaiella spp. (Ectocarpales). The distribution of these mitochondrial introns is inconsistent with vertical transmission, and likely reflects invasion by horizontal gene transfer between lineages. In the most extreme case, the mitome of Hedophyllum nigripes is ∼40% larger than the mitomes of close relatives because of these introns. Our results provide substantial insight into organellar evolution across the brown algae.

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“…The use of complete sequences provides a more robust and comprehensive perspective of the molecular events occurred at genomic level (e.g. rearrangements by recombination, gene losses and gains), which can be used also as markers of biological diversification events at different evolutionary scales (Choi et al 2020;Fu et al 2019;Graf et al 2017;Kim et al 2019;Kleffmann et al 2004;Lee et al 2018;Lemieux et al 2016; Sev c ıkov a et al 2016).…”

Section: Organelle Comparative Genomics and Species Diversitymentioning

confidence: 99%

High Sequence Divergence but Limited Architectural Rearrangements in Organelle Genomes of Cyanophora (Glaucophyta) Species

Russell

Jackson

Reyes‐Prieto

2020

J Eukaryotic Microbiology

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Cyanophora is the glaucophyte model taxon. Following the sequencing of the nuclear genome of C. paradoxa, studies based on single organelle and nuclear molecular markers revealed previously unrecognized species diversity within this glaucophyte genus. Here, we present the complete plastid (ptDNA) and mitochondrial (mtDNA) genomes of C. kugrensii, C. sudae, and C. biloba. The respective sizes and coding capacities of both ptDNAs and mtDNAs are conserved among Cyanophora species with only minor differences due to specific gene duplications. Organelle phylogenomic analyses consistently recover the species C. kugrensii and C. paradoxa as a clade and C. sudae and C. biloba as a separate group. The phylogenetic affiliations of the four Cyanophora species are consistent with architectural similarities shared at the organelle genomic level. Genetic distance estimations from both organelle sequences are also consistent with phylogenetic and architecture evidence. Comparative analyses confirm that the Cyanophora mitochondrial genes accumulate substitutions at 3-fold higher rates than plastid counterparts, suggesting that mtDNA markers are more appropriate to investigate glaucophyte diversity and evolutionary events that occur at a population level. The study of complete organelle genomes is becoming the standard for species delimitation and is particularly relevant to study cryptic diversity in microbial groups. THE Glaucophyta is one of three major lineages bearing primary plastids united in the contentious Archaeplastida supergroup (Adl et al. 2012; Burki et al. 2020). The rareness and scarcity of glaucophytes partially explain why this algal group has been marginally studied. The vast majority of investigations of glaucophytes are focused on the biflagellate genus Cyanophora, which can be easily maintained in relatively dense cultures and has become the "model" glaucophyte taxon. In recent years, investigations of other glaucophyte genera have provided insights into diverse aspects of the general biology of these rare algae (

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Plastid and mitochondrial genomes of Coccophora langsdorfii (Fucales, Phaeophyceae) and the utility of molecular markers

Cited by 12 publications

References 77 publications

Organelle inheritance and genome architecture variation in isogamous brown algae

Organelle inheritance and genome architecture variation in isogamous brown algae

Genomic Rearrangements and Sequence Evolution across Brown Algal Organelles

High Sequence Divergence but Limited Architectural Rearrangements in Organelle Genomes of Cyanophora (Glaucophyta) Species

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