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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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Presentation Transcript
slide2

Outline

  • Mitochondrial genome size evolution
      • Cucurbitaceae
      • Silene

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

slide7

The disparate trajectories of organelle genomes

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

1kb = 1000 base pairs

slide9

Estimatedmitochondrial genome sizes in Cucurbitaceae

Prediction: Larger genomes have lower mutation rates

Ward et al. 1981

slide10

Actualmitochondrial genome sizes in Cucurbitaceae

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

slide11

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
slide24

The cucumber mitochondrial and nuclear genomes

share a lot of DNA

33% of the mitochondrial genome

Alverson et al. 2011. Plant Cell.

slide25

The cucumber mitochondrial and nuclear genomes

share a lot of DNA

33% of the mitochondrial genome

Alverson et al. 2011. Plant Cell.

slide26

Outline

  • Mitochondrial genome size evolution
      • Cucurbitaceae
      • Silene

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

slide27

Dan Sloan

Doug Taylor

University of Virginia

Mitochondrial genome evolution in Silene

slide31

Mutation rate and mitochondrial genome size

253 kb

426 kb

16 kb

6,728 kb

11,318 kb

slide32

Large multi-chromosomal mitochondrial genomes

Silene noctiflora (6.7 Mb)

  • 59 chromosomes
  • 66–192 kb in length
slide33

Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes
slide34

Genome size summary and conclusions

  • Unprecedented size and structural variation in plant mitochondrial genomes
  • Theory: Low mutation rate

Larger genome size

slide35

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
slide36

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.
slide37

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
slide38

Outline

  • Mitochondrial genome size evolution
      • Cucurbitaceae
      • Silene

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

slide39

The Amborella mitochondrial genome: another monster!

Arabidopsis

Amborella

total size = 3.9 Mb

slide42

Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito

slide43

Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito

Foreign moss mito

slide44

Features in the Amborella mitochondrial genome

Native mito

chloroplast-derived

Foreign angiosperm mito

Foreign moss mito

Foreign green algal mito

slide46

Features in the Amborella mitochondrial genome

Native mito

Native chloroplast

Foreign angiosperm mito

Foreign moss mito

Foreign green algal mito

slide47

cob

Amborella

other angiosperms

mosses

green algae

N

slide48

Other genes show the same pattern as cob

Amborella

other angiosperms

mosses

N

green algae

N

N

N = native

slide50

Insights into the mechanism of horizontal transfer

What the Amborella mitochondrial genome has:

What the Amborella mitochondrial genome lacks:

slide51

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:

slide52

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:

slide54

Mitochondrial fission/fusion arose twice during eukaryotic evolution

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

slide59

How does Amborella acquire foreign mitochondria?

  • direct, plant-to-plant contact?
    • parasitic angiosperms
    • epiphytic plants & algae
slide60

How does Amborella acquire foreign mitochondria?

  • direct, plant-to-plant contact?
    • parasitic angiosperms
    • epiphytic plants & algae
slide61

cob

Donors are probably lichen-forming

green algae

slide62

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
slide63

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
slide64

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
slide65

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
slide66

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.
slide67

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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