Genomic gigantism in plant mitochondria

1. Genomic gigantism in plant mitochondria Andy Alverson

2. Outline • Mitochondrial genome size evolution • Cucurbitaceae • Silene Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella

3. The three plant genomes

4. The disparate trajectories of organelle genomes

5. The disparate trajectories of organelle genomes 1kb = 1000 base pairs

6. The disparate trajectories of organelle genomes 1kb = 1000 base pairs

7. The disparate trajectories of organelle genomes Mutation pressure hypothesis (Lynch et al. 2006. Science) 1kb = 1000 base pairs

8. Estimatedmitochondrial genome sizes in Cucurbitaceae Ward et al. 1981

9. Estimatedmitochondrial genome sizes in Cucurbitaceae Prediction: Larger genomes have lower mutation rates Ward et al. 1981

10. Actualmitochondrial genome sizes in Cucurbitaceae Alverson et al. 2010. Mol. Biol. Evol.

11. 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

12. Do large genomes have lower mutation rates?

13. Do large genomes have lower mutation rates? (dS)

14. Coding sequences in cucurbit mitochondrial genomes 17% 7% 19% 5% 4% Total coding:

15. Large genomes integrate massive amounts of new sequence

16. Traffic patterns of plant DNA

17. Traffic patterns of plant DNA

18. Chloroplast sequences in the mitochondrial genome

19. Chloroplast-derived sequences turn over rapidly

20. Chloroplast-derived sequences turn over rapidly

21. Chloroplast-derived sequences turn over rapidly

22. Traffic patterns of plant DNA

23. Nuclear–mitochondrial sequence exchange Huang et al. 2009

24. The cucumber mitochondrial and nuclear genomes share a lot of DNA 33% of the mitochondrial genome Alverson et al. 2011. Plant Cell.

25. The cucumber mitochondrial and nuclear genomes share a lot of DNA 33% of the mitochondrial genome Alverson et al. 2011. Plant Cell.

26. Outline • Mitochondrial genome size evolution • Cucurbitaceae • Silene Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella

27. Dan Sloan Doug Taylor University of Virginia Mitochondrial genome evolution in Silene

28. Mitochondrial mutation rate variation in Silene

29. Mutation rate and mitochondrial genome size ? ? ? ? 16 kb

30. Mutation rate and mitochondrial genome size ? ? 253 kb 426 kb 16 kb

31. Mutation rate and mitochondrial genome size 253 kb 426 kb 16 kb 6,728 kb 11,318 kb

32. Large multi-chromosomal mitochondrial genomes Silene noctiflora (6.7 Mb) • 59 chromosomes • 66–192 kb in length

33. Genome size summary and conclusions • Unprecedented size and structural variation in plant mitochondrial genomes

34. Genome size summary and conclusions • Unprecedented size and structural variation in plant mitochondrial genomes • Theory: Low mutation rate Larger genome size

35. 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

36. 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.

37. 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

38. Outline • Mitochondrial genome size evolution • Cucurbitaceae • Silene Horizontal gene transfer (HGT) in the mitochondrial genome of Amborella

39. The Amborella mitochondrial genome: another monster! Arabidopsis Amborella total size = 3.9 Mb

40. Features in the Amborella mitochondrial genome Native mito

41. Features in the Amborella mitochondrial genome Native mito chloroplast-derived

42. Features in the Amborella mitochondrial genome Native mito chloroplast-derived Foreign angiosperm mito

43. Features in the Amborella mitochondrial genome Native mito chloroplast-derived Foreign angiosperm mito Foreign moss mito

44. Features in the Amborella mitochondrial genome Native mito chloroplast-derived Foreign angiosperm mito Foreign moss mito Foreign green algal mito

45. Features in the Amborella mitochondrial genome Native mito

46. Features in the Amborella mitochondrial genome Native mito Native chloroplast Foreign angiosperm mito Foreign moss mito Foreign green algal mito

47. cob Amborella other angiosperms mosses green algae N

48. Other genes show the same pattern as cob Amborella other angiosperms mosses N green algae N N N = native

49. What's going on here?

50. Insights into the mechanism of horizontal transfer What the Amborella mitochondrial genome has: What the Amborella mitochondrial genome lacks: