First Complete Mitochondrial Genome Sequence from a Box Jellyfish Reveals a Highly Fragmented Linear Architecture and Insights into Telomere Evolution

Smith, David Roy; Kayal, Ehsan; Yanagihara, Angel A.; Collins, Allen G.; Pirro, Stacy; Keeling, Patrick J.

doi:10.1093/gbe/evr127

Cited by 63 publications

(77 citation statements)

References 50 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The shift from a single to a multipartite chromosomal architecture has happened many times in mtDNA evolution but is a surprisingly rare event for ptDNAs (12). No fewer than 12 eukaryotic lineages are known to contain fragmented mitochondrial genomes, and mtDNA splintering has transpired more than once within certain groups, including cnidarians (48), chlamydomonadalean algae (44), and vascular plants (13,49). Sometimes the levels of fragmentation are minor: the mtDNA of the colorless green alga Polytomella piriformis is divided into two small (<15 kb) linear chromosomes (44).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

“…The jakobid Andalucia godoyi has the largest, least-derived mitochondrial gene content (100 genes, ∼66 of which encode proteins) (67), whereas dinoflagellates, apicomplexans, and their close relatives have the most reduced: three or fewer proteins, no tRNAs, and in some instances (e.g., C. velia) even lack complete rRNAs (36,56,57,68). Chlamydomonadalean mtDNAs also have diminished coding contents (10-13 genes) (44), and some land plants (e.g., S. moellendorffii), animals (e.g., the winged box jellyfish), and trypanosomes have lost all or most of their mitochondrial tRNA-coding regions (39,42,48). Plastid genomes are typically more gene-rich than mtDNAs (12), maxing out at ∼250 genes in red algae (69).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

See 1 more Smart Citation

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

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

Self Cite

314

321

View full text Add to dashboard Cite

Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.E ndosymbiosis can dramatically impact cellular and genomic architectures. Mitochondria and plastids exemplify this point. Each of these two types of energy-producing eukaryotic organelle independently arose from the endosymbiosis, retention, and integration of a free-living bacterium into a host cell more than 1.4 billion years ago. Mitochondria came first, evolving from an alphaproteobacterial endosymbiont in an ancestor of all known living eukaryotes, and still exist, in one form or another (1), in all its descendants (2). Plastids came later, via the "primary" endosymbiosis of a cyanobacterium by the eukaryotic ancestor of the Archaeplastida, and then spread laterally to disparate groups through eukaryote-eukaryote endosymbioses (3). Consequently, a significant proportion of the identified eukaryotic diversity has a plastid.With few exceptions (1, 4), mitochondria and plastids contain genomes-chromosomal relics of the bacterial endosymbionts from which they evolved (2, 5). Mitochondrial and plastid DNAs (mtDNAs and ptDNAs) have many traits in common, which is not surprising given their similar evolutionary histories. Both are highly reduced relative to the genomes of extant, free-living alphaproteobacteria and cyanobacteria (2, 5), and both have transferred most of their genes to the host nuclear genome and are therefore reliant on nuclear-encoded, organelle-targeted proteins for the preservation of crucial biochemical pathways and many repair-, replication-, and expression-related functions (6). Both also show a wide and perplexing assortment of genomic architectures (7,8), which has spurred various evolutionary explanations, ranging from ancient inheritance from the RNA world to selection for greater "evolvability" (9, 10).At first glance, genomic complexity w...

show abstract

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

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

Self Cite

314

321

View full text Add to dashboard Cite

show abstract

“…In contrast, mitochondrial genomes in many other eukaryotes have been radically transformed or even lost entirely. One recurring evolutionary pattern is the fragmentation of mitochondrial DNA (mtDNA) into multichromosomal genomes, which has occurred independently in a wide variety of taxa, including kinetoplastids (8), diplonemids (9), dinoflagellates (10), the green alga Polytomella parva (11), ichthyosporean protists (12), chytrid fungi (13), and multiple lineages of both metazoans (14)(15)(16)(17)(18)(19)(20) and angiosperms (21)(22)(23). The fragmentation of genomes into chromosomes is a very general property of eukaryotic nuclear genomes.…”

mentioning

confidence: 99%

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Cuthbert

Taylor

et al. 2015

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

108

View full text Add to dashboard Cite

Across eukaryotes, mitochondria exhibit staggering diversity in genomic architecture, including the repeated evolution of multichromosomal structures. Unlike in the nucleus, where mitosis and meiosis ensure faithful transmission of chromosomes, the mechanisms of inheritance in fragmented mitochondrial genomes remain mysterious. Multichromosomal mitochondrial genomes have recently been found in multiple species of flowering plants, including Silene noctiflora, which harbors an unusually large and complex mitochondrial genome with more than 50 circular-mapping chromosomes totaling ∼7 Mb in size. To determine the extent to which such genomes are stably maintained, we analyzed intraspecific variation in the mitochondrial genome of S. noctiflora. Complete genomes from two populations revealed a high degree of similarity in the sequence, structure, and relative abundance of mitochondrial chromosomes. For example, there are no inversions between the genomes, and there are only nine SNPs in 25 kb of protein-coding sequence. Remarkably, however, these genomes differ in the presence or absence of 19 entire chromosomes, all of which lack any identifiable genes or contain only duplicate gene copies. Thus, these mitochondrial genomes retain a full gene complement but carry a highly variable set of chromosomes that are filled with presumably dispensable sequence. In S. noctiflora, conventional mechanisms of mitochondrial sequence divergence are being outstripped by an apparently nonadaptive process of whole-chromosome gain/loss, highlighting the inherent challenge in maintaining a fragmented genome. We discuss the implications of these findings in relation to the question of why mitochondria, more so than plastids and bacterial endosymbionts, are prone to the repeated evolution of multichromosomal genomes. meiosis | mitochondrial DNA | mitosis | multichromosomal | multipartite

show abstract

“…hydroids and jellyfish) is organized into mono-, bi-, or multi-linear chromosomes. [7][8][9][10][11][12][13]20 Medusozoan mtDNA is very compact with a few small IGRs. 12,15 In hydrozoans, Kayal et al (2015) 15 suggested that both rRNA genes and stemloop-like secondary structures formed by IGRs could be recognized by the nucleolytic processing mechanism, producing mature often multi-cistronic mRNA transcripts.…”

Section: Introductionmentioning

confidence: 99%

“…12,13,20 Mitochondrial chromosomes range from 4 to 6 kbp in length and harbor between one and four genes, flanked by long and conserved telomere-like inverted repeats (IRs) with opposite orientation thought to be involved in the maintenance of the linear mito-chromosomes. 13 In addition to the 13 protein-coding genes common in Metazoa, most medusozoan mtDNA (excluding hydroidolinan hydrozoans) encodes for two extra protein-coding genes (mtpolB and orf314). Mohammadou et al (2004) 21 have found that mt-polB has affinities with polymerases from the B family.…”

Section: Introductionmentioning

confidence: 99%

Insights into the transcriptional and translational mechanisms of linear organellar chromosomes in the box jellyfish Alatina alata (Cnidaria: Medusozoa: Cubozoa)

2016

Self Cite

View full text Add to dashboard Cite

Background: In most animals, the mitochondrial genome is characterized by its small size, organization into a single circular molecule, and a relative conservation of the number of encoded genes. In box jellyfish (Cubozoa, Cnidaria), the mitochondrial genome is organized into 8 linear mito-chromosomes harboring between one and 4 genes each, including 2 extra protein-coding genes: mt-polB and orf314. Such an organization challenges the traditional view of mitochondrial DNA (mtDNA) expression in animals. In this study, we investigate the pattern of mitochondrial gene expression in the box jellyfish Alatina alata, as well as several key nuclear-encoded molecular pathways involved in the processing of mitochondrial gene transcription. Results: Read coverage of DNA-seq data is relatively uniform for all 8 mito-chromosomes, suggesting that each mito-chromosome is present in equimolar proportion in the mitochondrion. Comparison of DNA and RNA-seq based assemblies indicates that mito-chromosomes are transcribed into individual transcripts in which the beginning and ending are highly conserved. Expression levels for mt-polB and orf314 are similar to those of other mitochondrialencoded genes, which provides further evidence for them having functional roles in the mitochondrion. Survey of the transcriptome suggests recognition of the mitochondrial tRNA-Met by the cytoplasmic aminoacyl-tRNA synthetase counterpart and C-to-U editing of the cytoplasmic tRNA-Trp after import into the mitochondrion. Moreover, several mitochondrial ribosomal proteins appear to be lost. Conclusions: This study represents the first survey of mitochondrial gene expression of the linear multi-chromosomal mtDNA in box jellyfish (Cubozoa). Future exploration of small RNAs and the proteome of the mitochondrion will test the hypotheses presented herein.

show abstract

First Complete Mitochondrial Genome Sequence from a Box Jellyfish Reveals a Highly Fragmented Linear Architecture and Insights into Telomere Evolution

Cited by 63 publications

References 50 publications

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

Insights into the transcriptional and translational mechanisms of linear organellar chromosomes in the box jellyfish Alatina alata (Cnidaria: Medusozoa: Cubozoa)

Contact Info

Product

Resources

About