Organization and expression of organellar genomes

Barbrook, Adrian C.; Howe, Christopher J.; Kurniawan, Davy Putra; Tarr, Sarah J.

doi:10.1098/rstb.2009.0250

Cited by 64 publications

(62 citation statements)

References 101 publications

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“…We therefore anticipated modest changes in the levels of organelle-encoded transcripts. Mitochondrial genomes encode proteins that function in mitochondrial processes, particularly translation and oxidative phosphorylation (41). Examination of transcripts from ise1 and ise2 mutants revealed that numerous mitochondria-encoded genes are induced (Table 3); strikingly, different genes are affected in each mutant.…”

Section: Ise2 Is Found In Chloroplastsmentioning

confidence: 99%

Organelle–nucleus cross-talk regulates plant intercellular communication via plasmodesmata

Burch‐Smith¹,

Brunkard²,

Choi

et al. 2011

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

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We use Arabidopsis thaliana embryogenesis as a model system for studying intercellular transport via plasmodesmata (PD). A forward genetic screen for altered PD transport identified increased size exclusion limit (ise) 1 and ise2 mutants with increased intercellular transport of fluorescent 10-kDa tracers. Both ise1 and ise2 exhibit increased formation of twinned and branched PD. ISE1 encodes a mitochondrial DEAD-box RNA helicase, whereas ISE2 encodes a DEVH-type RNA helicase. Here, we show that ISE2 foci are localized to the chloroplast stroma. Surprisingly, plastid development is defective in both ise1 and ise2 mutant embryos. In an effort to understand how RNA helicases that localize to different organelles have similar impacts on plastid and PD development/function, we performed whole-genome expression analyses. The most significantly affected class of transcripts in both mutants encode products that target to and enable plastid function. These results reinforce the importance of plastid-mitochondria-nucleus cross-talk, add PD as a critical player in the plant cell communication network, and thereby illuminate a previously undescribed signaling pathway dubbed organelle-nucleus-plasmodesmata signaling. Several genes with roles in cell wall synthesis and modification are also differentially expressed in both mutants, providing new targets for investigating PD development and function.

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Section: Ise2 Is Found In Chloroplastsmentioning

confidence: 99%

Organelle–nucleus cross-talk regulates plant intercellular communication via plasmodesmata

Burch‐Smith¹,

Brunkard²,

Choi

et al. 2011

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

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“…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).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

“…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). Plants and algae that have lost photosynthetic capabilities have reduced plastid gene contents (<75) (63,64,70), but the absolute lowest are in the photosynthetic, peridinin plastids of dinoflagellates, which encode <20 genes (62).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

“…As with size and structure, mtDNAs show greater variation in gene number and organization than ptDNAs (12). 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).…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

“…Indeed, both organelle genomes have, in many instances, taken parallel evolutionary roads, independently adopting almost identical architectures (12), as well as similar mutational patterns (13), replication and gene expression strategies (14,15), and modes of inheritance (16). There are, however, some major differences between mitochondrial and plastid genomes, including structures and/or embellishments present in one but not the other.…”

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

Smith

Keeling

2015

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

321

344

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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...

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Chloroplast Genome

Howe¹

2012

Encyclopedia of Life Sciences

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Chloroplasts contain a genome that is a relic of the endosymbiont that gave rise to the organelle. These genomes typically contain 100–200 genes and encode proteins important for photosynthesis and other chloroplast functions, although dinoflagellate algae have a greatly reduced and fragmented chloroplast genome. Many nonphotosynthetic taxa retain a remnant chloroplast genome. In some organisms the chloroplast genome may be retained to allow redox‐mediated control of gene expression, whereas in others it may continue to exist because transfer of essential genes to the nucleus is no longer possible. Multiple ribonucleic acid (RNA) polymerases are involved in chloroplast transcription in land plants, and post‐transcriptional processing involving nuclear‐encoded RNA‐binding proteins also plays an important part in the expression of the chloroplast genome. Gene expression may be regulated at a number of levels, and redox poise in the organelle may be particularly important for this. Key Concepts: Chloroplasts originated in the ancestor of plants and red and green algae by endosymbiotic acquisition of a cyanobacterium, and then spread to many other eukaryotic lineages. There are other examples of stable acquisition of a cyanobacterium by a nonphotosynthetic host. Chloroplast genomes are typically 100–200 kbp in size, and include a set of genes for proteins essential to photosynthesis. Other genes present in the ancestral symbiont have been lost or relocated to the nucleus. Many nonphotosynthetic organisms retain remnant chloroplasts, with genomes, reflecting the fact that photosynthesis is not the only biochemical process that takes place in the chloroplast. In many organisms, gene transfer from chloroplast to nucleus can still take place, at an unexpectedly high frequency. Establishment of the chloroplast has resulted in the development of nuclear‐encoded RNA‐binding protein families and, in land plants, additional RNA polymerases that play a central role in chloroplast gene expression. Post‐transcriptional RNA processing plays an important role in chloroplast gene expression. In photosynthetic organisms, chloroplast gene expression is closely linked to the organelle's redox poise. The chloroplast can also influence the expression of nuclear genes.

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Organization and expression of organellar genomes

Cited by 64 publications

References 101 publications

Organelle–nucleus cross-talk regulates plant intercellular communication via plasmodesmata

Organelle–nucleus cross-talk regulates plant intercellular communication via plasmodesmata

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

Chloroplast Genome

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