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Evolutionary History and Stress Responsiveness of Plant Receptor-Like Kinases

Evolutionary History and Stress Responsiveness of Plant Receptor-Like Kinases. Melissa Lehti-Shiu Shiu lab. The evolution of duplicate genes. Phylogenetic tree of the Arabidopsis RLK/Pelle gene family. When and how did gene duplication occur? How do gene duplicates diverge in function?

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Evolutionary History and Stress Responsiveness of Plant Receptor-Like Kinases

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  1. Evolutionary History and Stress Responsiveness of Plant Receptor-Like Kinases Melissa Lehti-Shiu Shiu lab

  2. The evolution of duplicate genes Phylogenetic tree of the Arabidopsis RLK/Pelle gene family • When and how did gene duplication occur? • How do gene duplicates diverge in function? • Why are some duplicates more likely to be retained than others? Shiu, S.-H., et al. Plant Physiol. 2003;132:530-543

  3. Background • Duplication mechanisms • Models for duplicate retention • What evolutionary histories can tell us • The RLK/Pelle gene family • The Evolutionary history of the Receptor-Like Kinase (RLK)/Pelle gene family • RLKs and stress response

  4. + Duplication mechanisms • Whole genome duplication (polyploidization) • Tandem duplication • Segmental duplication • Replicative transposition

  5. Why is knowing duplication mechanism important? • Gene duplicates are formed at different rates depending on mechanism • Tandem >> whole genome duplication • How genes are duplicated affects duplicate retention • e.g. tandem repeats are enriched with genes that are involved in stress response (Rizzon et al., 2006; Hanada and Shiu, unpublished results)

  6. A. Subfunctionalization: Ancestral functions are divided between both genes B. Neofunctionalization: One or both copies gain a new function C. Dosage: Additional copies of the gene may be advantageous D. Neutral processes: Both genes kept just because they are not selected against Why are genes retained after duplication? A. B. C., D.

  7. http://www.sheppardsoftware.com/ Europeweb/factfile/Unique-facts-Europe33.htm What can we learn from studying the evolutionary histories of gene families? Grape 1 Grape 2 Grape 3 Grape 4 Poplar 1 Ancestral Gene Arabidopsis 1 Rice 1 Rice 2

  8. Protein kinase: ~1000 Protein kinase gene families unique *: Clusters of Markov clustering using all-against-all BLAST E values as distance measures Hanada & Shiu, in prep.

  9. Arabidopsis Rice The RLK/Pelle family has experienced dramatic differential expansion Shiu et al., 2004

  10. RLK/Pelle members have diverse kinase configurations

  11. RLKs function in signal transduction pathways PAMP recognition Development CLV3 Flagellin CLV1 (LRR-XI) CLV2 FLS2 (LRR-XII) LRR LRR LRR Kinase Kinase Flagellin defense related gene expression Meristem proliferation

  12. Identify kinases from sequenced plant genomes Arabidopsis thaliana http://www.pg.ipw.biol.ethz.ch/Title.html Populus trichocarpa http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html Oryza sativa http://www.genomics.zju.edu.cn/ricetdna.html Physcomitrella patens http://www.jgi.doe.gov/sequencing/why /CSP2005/physcomitrella.html Chlamydomonas reinhardtii http://genome.jgi-psf.org/Chlre3/Chlre3.home.html Ostreococcus tauri http://genome.jgi-psf.org/Ostta4/Ostta4.home.html

  13. Kinase classification • Align kinase domains from all species and construct a phylogenetic tree • Assign kinases to families based on grouping with known Arabidosis kinases • Assign RLK/Pelle kinases to subfamilies based on the classification from Shiu et al., 2004 Shiu, S.-H., et al. Plant Cell 2004;16:1220-1234

  14. Kinase ECD Arabidopsis thaliana (A) 148 RLK Kinase 388 RLCK 462 187 Other Kinases Populus trichocarpa (P) 453 1003 Oryza sativa (O) 159 376 911 Physcomitrella patens (M) 73 356 256 Chlamydomonas reinhardtii 2 424 Ostreococcus tauri 93 When was the receptor kinase configuration established?

  15. How many receptor kinase configurations are present in moss?

  16. LysM GDPD Thaumatin CHASE DUF26 LRR GH18 LRR LRR DUF26 GH18 DUF26 Thaumatin Thaumatin What innovation in receptor configuration has occurred?

  17. Which RLK subfamilies have undergone lineage-specific expansion? B1 Duplication in species A Gene loss in species B Species divergence Gains Losses Net Gain 1 0 1 Species A Species B 0 1 -1 (2 genes) Calculating lineage-specific gene gains A1 A2-1 A2-2 B2 AB common ancestor

  18. Which RLK subfamilies have undergone lineage-specific expansion? Subfamilies not found in moss: DUF26, LRK10L-2, SD1, WAK

  19. Is there a correlation between expansion rate and location in tandem repeats? r2 =0.66 p<0.001 r2 =0.62 p<0.001 r2 =0.37 p=0.01

  20. Evolutionary History of the RLK/Pelle family • The receptor kinase configuration was established early in the evolution of land plants • Differential of expansion of the RLK/Pelle family has occurred • New kinase configurations were formed through domain shuffling in all lineages • Dramatic increase in RLK/Pelle genes in rice and poplar can be explained by expansion of a relatively few subfamilies • See a significant correlation between recent expansion and tandem duplication

  21. AtGenExpress: stress array data http://www.weigelworld.org/resources/microarray/AtGenExpress/ Biotic avrRpm1 DC3000 Flg22 HrcC- HrpZ LPS Psph P. infestans 16 conditions w/ time series Abiotic Cold Heat Drought Salt Osmotic Genotoxic Wounding UV-B Raw intensity GCRMA Normalized intensity LIMMA Genes with Diff. expr.

  22. Genes differentially up (1) or down (-1) regulated under each condition P. infestans Wounding Genotoxic avrRpm1 Drought Osmotic DC3000 Flg22 HrcC- Psph UV-B HrpZ Heat Cold LPS Salt At1g1 At1g2 At1g3 At1g4 At1g5 At1g6

  23. Is the number of RLKs up or down regulated by stress different from the genome average?

  24. Is the number of tandem RLKs regulated by stress different from non-tandem RLKs?

  25. Is subfamily responsiveness to stress correlated with the proportion found in tandem repeats? Cold Drought Heat … flg22 Responsiveness C-LEC CR4L CrRLK1L-1 0 0 0 … 0 0.0 0 0 0 … 0.125 0.93 0.2 0 0.14 … 1.0 2.875 Fraction of subfamily members up (or down) regulated by cold Treatment (e.g. 5 out of 10=0.5) Sum of fractions for all 16 conditions

  26. Stress responsiveness and tandem RLKs X10 (subfamilies with ≥ 10 genes)

  27. Relationship between RLKs, stress and tandem duplication • Stress responsiveness • RLK > genome average • Tandem genes > non-tandem genes. • Biotic > abiotic • Duplication rate (event per unit time): • Whole genome duplication: 1 event / ~50 million years • Tandem duplication: multiple events / generation • Rate of recombination • Recombination rate: Pathogen attack > control • Lucht et al., 2002. Nature. • Recombination rate: Tandem > non-tandem • Zhang & Gaut, 2003. Genome Res.

  28. The “RLK swarm” model

  29. Acknowledgements • Funding: • Shiu lab • Shinhan Shiu • Kousuke Hanada • Cheng Zou • Jessica Oswald • Amanda Tabbert • Gaurav Moghe

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