Genomic gigantism in plant mitochondria
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Genomic gigantism in plant mitochondria. Andy Alverson. Outline. Mitochondrial genome size evolution Cucurbitaceae Silene. Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella. The three plant genomes. The disparate trajectories of organelle genomes.

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Genomic gigantism in plant mitochondria

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Genomic gigantism in plant mitochondria

Andy Alverson


Outline

  • Mitochondrial genome size evolution

    • Cucurbitaceae

    • Silene

Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella


The three plant genomes


The disparate trajectories of organelle genomes


The disparate trajectories of organelle genomes

1kb = 1000 base pairs


The disparate trajectories of organelle genomes

1kb = 1000 base pairs


The disparate trajectories of organelle genomes

Mutation pressure hypothesis (Lynch et al. 2006. Science)

1kb = 1000 base pairs


Estimatedmitochondrial genome sizes in Cucurbitaceae

Ward et al. 1981


Estimatedmitochondrial genome sizes in Cucurbitaceae

Prediction: Larger genomes have lower mutation rates

Ward et al. 1981


Actualmitochondrial genome sizes in Cucurbitaceae

Alverson et al. 2010. Mol. Biol. Evol.


CUA

CUC

CUG

CUU

CCA

CCC

CCG

CCU

GGA

GGC

GGG

GGU

Leu

Pro

Gly

Estimating the mutation rate of a genome

  • Multiple codons for the same amino acid

  • Synonymous mutations

    • do not change the amino acid

    • invisible to natural selection ≈ neutral

    • rate of neutral change ≈ mutation rate


Do large genomes have lower mutation rates?


Do large genomes have lower mutation rates?

(dS)


Coding sequences in cucurbit mitochondrial genomes

17%

7%

19%

5%

4%

Total coding:


Large genomes integrate massive amounts of new sequence


Traffic patterns of plant DNA


Traffic patterns of plant DNA


Chloroplast sequences in the mitochondrial genome


Chloroplast-derived sequences turn over rapidly


Chloroplast-derived sequences turn over rapidly


Chloroplast-derived sequences turn over rapidly


Traffic patterns of plant DNA


Nuclear–mitochondrial sequence exchange

Huang et al. 2009


The cucumber mitochondrial and nuclear genomes

share a lot of DNA

33% of the mitochondrial genome

Alverson et al. 2011. Plant Cell.


The cucumber mitochondrial and nuclear genomes

share a lot of DNA

33% of the mitochondrial genome

Alverson et al. 2011. Plant Cell.


Outline

  • Mitochondrial genome size evolution

    • Cucurbitaceae

    • Silene

Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella


Dan Sloan

Doug Taylor

University of Virginia

Mitochondrial genome evolution in Silene


Mitochondrial mutation rate variation in Silene


Mutation rate and mitochondrial genome size

?

?

?

?

16 kb


Mutation rate and mitochondrial genome size

?

?

253 kb

426 kb

16 kb


Mutation rate and mitochondrial genome size

253 kb

426 kb

16 kb

6,728 kb

11,318 kb


Large multi-chromosomal mitochondrial genomes

Silene noctiflora (6.7 Mb)

  • 59 chromosomes

  • 66–192 kb in length


Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes


Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes

  • Theory: Low mutation rate

Larger genome size


Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes

  • Theory: Low mutation rate

Larger genome size

  • Cucurbitaceae and Silene show the opposite pattern


Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes

  • Theory: Low mutation rate

Larger genome size

  • Cucurbitaceae and Silene show the opposite pattern

  • What drives genome size evolution in plant mitochondria?

    • mutation rate? Not likely.

    • intramolecular recombination? Maybe.


Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes

  • Theory: Low mutation rate

Larger genome size

  • Cucurbitaceae and Silene show the opposite pattern

  • What drives genome size evolution in plant mitochondria?

    • mutation rate? Not likely.

    • intramolecular recombination? Maybe.

  • Much of the "extra" intergenic DNA may derive from the chloroplast and the nuclear genomes


Outline

  • Mitochondrial genome size evolution

    • Cucurbitaceae

    • Silene

Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella


The Amborella mitochondrial genome: another monster!

Arabidopsis

Amborella

total size = 3.9 Mb


Features in the Amborella mitochondrial genome

Native mito


Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived


Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito


Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito

Foreign moss mito


Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito

Foreign moss mito

Foreign green algal mito


Features in the Amborella mitochondrial genome

Native mito


Features in the Amborella mitochondrial genome

Native mito

Native chloroplast

Foreign angiosperm mito

Foreign moss mito

Foreign green algal mito


cob

Amborella

other angiosperms

mosses

green algae

N


Other genes show the same pattern as cob

Amborella

other angiosperms

mosses

N

green algae

N

N

N = native


What's going on here?


Insights into the mechanism of horizontal transfer

What the Amborella mitochondrial genome has:

What the Amborella mitochondrial genome lacks:


Insights into the mechanism of horizontal transfer

What the Amborella mitochondrial genome has:

  • entire foreign mitochondrial genomes

  • donors are all "green plants"

What the Amborella mitochondrial genome lacks:


Insights into the mechanism of horizontal transfer

What the Amborella mitochondrial genome has:

  • foreign nuclear DNA

  • bacterial DNA

  • fungal DNA

  • mitochondrial DNA from non-"green plants"

  • entire foreign mitochondrial genomes

  • donors are all "green plants"

What the Amborella mitochondrial genome lacks:


Mitochondrial fission/fusion arose twice during eukaryotic evolution

The machines that divide and fuse mitochondria. 2007. Ann. Rev. Biochem. 76:751-780.


How do foreign mitochondria get into Amborella?


Amborella is endemic to New Caledonia


How does Amborella acquire foreign mitochondria?

  • direct, plant-to-plant contact?

    • parasitic angiosperms

    • epiphytic plants & algae


How does Amborella acquire foreign mitochondria?

  • direct, plant-to-plant contact?

    • parasitic angiosperms

    • epiphytic plants & algae


cob

Donors are probably lichen-forming

green algae


How does Amborella acquire foreign mitochondria?

  • direct, plant-to-plant contact

    • parasitic angiosperms

    • epiphytes plants & algae

  • biological vectoring agents

    • viruses

    • bacteria

    • fungi (pathogenic or mycorrhizal)

    • insects


Amborella summary and conclusions

  • Growth of the Amborella genome reflects large-scale acquisitions of foreign DNA from other "green" plants

    • angiosperms, mosses, and green algae

    • mitochondrial DNA


Amborella summary and conclusions

  • Growth of the Amborella genome reflects large-scale acquisitions of foreign DNA from other "green" plants

    • angiosperms, mosses, and green algae

    • mitochondrial DNA

  • acquisitions include entire mitochondrial genomes


Amborella summary and conclusions

  • Growth of the Amborella genome reflects large-scale acquisitions of foreign DNA from other "green" plants

    • angiosperms, mosses, and green algae

    • mitochondrial DNA

  • acquisitions include entire mitochondrial genomes

  • the mechanism of HGT

    • introduction of foreign (but "green") mitochondria

    • fusion between native and foreign mitochondria


Amborella summary and conclusions

  • Growth of the Amborella genome reflects large-scale acquisitions of foreign DNA from other "green" plants

    • angiosperms, mosses, and green algae

    • mitochondrial DNA

  • acquisitions include entire mitochondrial genomes

  • the mechanism of HGT

    • introduction of foreign (but "green") mitochondria

    • fusion between native and foreign mitochondria

  • Are there more Amborella's out there? Almost certainly.


Dan Sloan

(Virginia/Yale)

Doug Taylor

(Virginia)

Jeff Palmer

(Indiana)

Danny Rice

(Indiana)

Acknowledgements

  • Funding

  • NIH Ruth L. Kirschstein postdoctoral fellowship (Alverson)

  • NIH Research grant (Palmer)


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