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Lessons from my favorite symbionts , Questions from my favorite inscape

Lessons from my favorite symbionts , Questions from my favorite inscape . Christopher L. Schardl. SAMSI Workshop on Algebraic Methods in Systems Biology and Statistics Research Triangle Park, North Carolina 14-17 September 2008. Epichloë/Neotyphodium in a grass plant. Symbioses are:

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Lessons from my favorite symbionts , Questions from my favorite inscape

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  1. Lessons from my favorite symbionts,Questions from my favorite inscape Christopher L. Schardl SAMSI Workshop on Algebraic Methods in Systems Biology and Statistics Research Triangle Park, North Carolina 14-17 September 2008

  2. Epichloë/Neotyphodium in a grass plant • Symbioses are: • Systemic • Constitutive • Often heritable • Symbiotic continuum: • Mutualistic • Pleiotropic • Antagonistic

  3. Vertical transmissibility Lolium pratense shoot and meristem with Epichloë festucae (w/GFP) Confocal micrograph by Dr. Koya Sugawara • Lolium perenne embryo with • Epichloë festucae (w/GFP) • Christensen et al. 2008

  4. Endophytes protect against insects, nematodes, etc. E– E+

  5. Currencies of grass-endophyte mutualisms anti-insect anti-vertebrate anti-nematode drought tolerance etc. nutrition shelter dispersal

  6. Sexual vs. asexual,Mutualistic vs. antagonistic

  7. Biological questions • Can we elucidate patterns of host and symbiont/parasite codivergence? • What happens (phylogenetically) during invasion of new niches? • How do sex and asex affect evolution? • Do neofunctionalized genes have unusual evolution ?

  8. Hypothesis: • Pooideae and epichloae have codiverged. Schardl CL, Craven KD, Speakman S, Stromberg A, Lindstrom A, Yoshida R. 2008. Systematic Biology 57: 483-498.

  9. E. amarillans (IV) Aveneae Agrostis spp., Sphenopholis spp. E. baconii (V) Aveneae Agrostis spp., Calamagrostis spp. Epichloë sp. Aveneae Holcus mollis E. brachyelytri (IX) Brachyelytreae Brachyelytrum erectum Epichloë sp. Stipeae Achnatherum sibiricum E. bromicola (VI) Bromeae Bromus spp. Triticeae Epichloë yangzii (VI) Roegneria kamoji E. elymi (III) Triticeae Elymus spp. E. festucae (II) Poeae,Aveneae Festucaspp., Loliumspp.,Koeleria sp. E. glyceriae (VIII) Meliceae Glyceria striata Poeae E. clarkii (I) Holcus lanatus Brachypodieae E. sylvatica (VII) Brachypodium sylvaticum Aveneae Brachypodieae Poeae Phleum pratense, Anthoxanthum odoratum Brachypodiumspp. Poa nemoralis, Poa trivialis, Dactylis glomerata, Puccinellia distans, Lolium perenne E. typhina (I) Hosts of Epichloë spp. Epichloë sp. (MP) Host tribe Hosts

  10. Epichloë gene trees

  11. Lineage sorting effects and the species cloud

  12. Host and epichloë phylogenies Host cpDNA Fungus tubB + tefA

  13. g t = 3 f e a b c d phylogenetic tree Problem with pairwise distance approach

  14. (G,g) G g (F,f) f (E,e) E F e pw distance (Endophyte) A B C D a b c d Host tree Endophyte tree MRCA pair Pairs of H and E taxon pairs pw distance (Host) (E,e) ((A,B),(a,b)) (F,f) ((C,D),(c,d)) (G,g) ((A,C),(a,c)), ((A,D),(a,d)), ((B,C),(b,c)), ((B,D),(b,d)) Pairwise distancesto compare divergence times

  15. G g (G,g) f E F e Node age (Endophyte) (F,f) A B C D a b c d (E,e) Host tree Endophyte tree MRCA pair Pairs of H and E taxon pairs Node age (Host) (E,e) ((A,B),(a,b)) (F,f) ((C,D),(c,d)) (G,g) ((A,C),(a,c)), ((A,D),(a,d)), ((B,C),(b,c)), ((B,D),(b,d)) MRCALink: Sample each pair of nodes once if ‘valid,’ otherwise not.

  16. (F,g) (G,g) Node age (Endo) (G,f) G g (E,e) f E F e Node age (Host) A B C D a b c d MRCA pair Pairs of H and E taxon pairs Host tree Endophyte tree (E,e) ((A,B),(a,b)) (G,f) ((A,C),(a,c)), ((B,C),(b,c)) (G,g) ((A,D),(a,d)), ((B,D),(b,d)) (F,g) ((C,D),(c,d)) MRCALink on incongruent trees

  17. Apply MRCALinkto Pooideae-epichloae

  18. Full p= 0.123 p< 0.001 Bivariate plots: Full and trimmed

  19. Codivergence of epichloae and Pooideae. • Suggests ancestral symbiosis 30–40 Mya.

  20. Working on identifying likely host jumps

  21. Test for differentiation of populations based on hosts. Hosts sampled: Dactylis glomerata Poa trivialis Poa nemoralis Brachypodium pinnatum Sites sampled in and near Switzerland Hypothesis: E. typhina is a complex of cryptic, host-based species.

  22. HOSTS: Poa trivialis D. glomerata H. lanatus D. glomerata Poa nemoralis Bp. pinnatum tubB haplotypes • Support for cryptic species hypothesis. • No haplotypes shared between host-associated populations. • but some popns were not monophyletic

  23. HOSTS: Poa trivialis D. glomerata H. lanatus D. glomerata Poa nemoralis Bp. pinnatum Cautionary tale for phylogenetics • Compatibility analysis with Carbonne’s SNAP workbench • Intron 1 shows evidence of extensive recombination

  24. 1 H2 Dg 1 1 H5 Dg 2 1 H6 Dg 1 1 H7 Dg 4 2 H9 Dg 52 1 H12 Dg 1 1 1 ex D. glomerata H14 Dg 2 1 H15 Dg 3 4 1 H11 Dg 4 3 H3 Dg 3 1 H8 Dg 10 2 1 H13 Dg 1 H17 Dg 23 H18 Pn 18 ex Poa nemoralis 1 H16 Pn 8 1 H1 Bp 12 ex Bp. pinnatum 1 H4 Bp 17 6 H10 Bp 9 Remove incompatible region • Looks a bit better.

  25. Hypothesis: Recombination is associated with new colonization events. HOSTS: Poa trivialis D. glomerata OREGON D. glomerata H. lanatus D. glomerata Poa nemoralis D. glomerata OREGON Bp. pinnatum

  26. Sex vs. Asex • Hypothesis: asexual lineages have shortened life spans.

  27. Sexual and clonal taxa on the gene trees • Work of Jan Schmid & Barbara Howlett, Massey University. tefA tubB S C C C C C S S C S S S S S S S S S S S S C C S S C S S S S S S S C C C S S C C S S C C S S C C S S S S C S S C C S C S C C C S clonal sexual C S

  28. Sexual and clonal taxa Hybrids excluded tefA tubB S C C C C C S S C S S S S S S S S S S S S C C S S C S S S S S S S C C C S S C C S S C C S S C C S S S S C S S C C S C S C C C S clonal sexual C S

  29. Neotyphodium sp. LpTG-2 Neotyphodium coenophialum Epichloë festucae Epichloë typhina 55 57 29 29 Manyasexual epichloae have multiple gene copies • Southern blot of -tubulin genes Genome sizes (Mb) Kuldau et al. 1999

  30. Hybrid origins of most asexual epichloae Moon et al. 2004

  31. Phylogenetic tracking and hybridization E. bromicola • Hypothesis: parasexual recombination extends life of asexual lineages. N. occultans L. multiflorum N. coenophialum L. arundinaceum E. typhina , E. festucae E. festucae Neotyphodium sp. FaTG-2 Lolium sp. Lolium sp. Neotyphodium sp.FaTG-3 E. typhina

  32. O CH N CH3 O N Hypothesis: Genes for conditionally dispensable functions have unusual evolutionary patterns. • Loline alkaloids

  33. Loline biosynthesis pathway • Novel -substitution rxn • Unusual ether bridge Blankenship et al. 2005 Faulkner et al. 2006

  34. Relationships and proposed role of LolC • Neofunctionalization

  35. cysD and lolC relationships • Why? • Paralogs with many losses? • Long-branch attraction? • Horizontal transfer?

  36. lolC vs. tub2 phylogeny

  37. Collaborators: Jerzy W. Jaromczyk (UK) Robert B. Grossman (UK) Daniel G. Panaccione (West Virginia Univ.) Bruce Roe (Univ. Oklahoma) Barry Scott (Massey Univ., New Zealand) Jan Schmid (Massey Univ., New Zealand) RurikoYoshida (UK) Carolyn Young (Noble Foundation) UK-AGTC: AbbeKesterson Jennifer Webb & al. Acknowledgments • NSF • USDA-NRI • USDA-ARS

  38. Lab: KalinaAndreeva Jimmy D. Blankenship Alfred D. Byrd Jerome R. Faulkner SimonaFlorea Love Gill UljanaHesse Walter Hollin Eun Jung Lee Jinge Liu Caroline Machado Lab: Lesley J. Mann Christina D. Moon PadmajaNagabhyru Kathryn Schweri Martin J. Spiering Huei-Fung Tsai Jinghong Wang Ella V. Wilson Dong-Xiu Zhang many undergraduate scholars Acknowledgments • NSF • USDA-NRI • USDA-ARS

  39. E. typhina from D. glomerata, 2Nem 2.03 3.12 SH ZH 39.6 26.4 0.90 21.2 VD 50 km

  40. Q = 2Neµ 0.011 SH 0.012 ZH VD 0.001 50 km

  41. Bruce Roe (UO, Norman) Jerzy W. Jaromczyk (UK) Wayne Beech (UK) Mark L. Farman (UK) Arny Stromberg (UK) Uljana Hesse Kalina Andreeva Dongxiu Zhang Ellie Arnaoudova Paul Maynard Na Ren Venu-Gopal Puram Jennifer L. Wiseman Jennifer Webb Abbe Kesterson Love Gill S. Macmil G. Wiley • Funding: • NSF • USDA-NRI • USDA-ARS Acknowledgments

  42. Loline biosynthesis pathway • Novel -substitution rxn • Probably catalyzed by LolC • Unusual ether bridge Blankenship et al. 2005 Faulkner et al. 2006

  43. tubB tefA Epichloë phylogeny ETC ETC

  44. c a b live 60 dead 40 367– 4871 67– 576 Number of Aphids 20 0 E– Nun Lol+ Lol– E. festucae Lolines protect against insects • Plants with lolines are resistant to bird-cherry oat aphid (Rhopalosiphum padi) Wilkinson et al. 2000

  45. cysD and lolC relationships • Why?

  46. Polymorphisms for alkaloid expression

  47. Genetic identification of LOL locus • 1:1 Segregation • Implies single gene locus • (These fungi are haploids) Wilkinson et al. 2000

  48. lolF lolC lolD lolO lolA lolU lolP lolT lolE Myb DNA binding HxD...H Facial triad HxD...H Facial triad Heme binding FAD binding PLP binding PLP binding PLP binding 0 5 10 15 20 25 kb Loline biosynthesis gene cluster • The LOL1 gene cluster from Neotyphodium uncinatum Spiering et al. 2005

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