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

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

The evolution of duplicate genes 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: Phylogenetic tree of the Arabidopsis RLK/Pelle gene family

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

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

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tandem repeats are enriched with genes that are involved in stress response (Rizzon et al., 2006; Hanada and Shiu, unpublished results)

Why are genes retained after duplication? 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 A. B. C., D.

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

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

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

RLK/Pelle members have diverse kinase configurations

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

Identify kinases from sequenced plant genomes /CSP2005/physcomitrella.html Chlamydomonas reinhardtii Ostreococcus tauri Physcomitrella patens Oryza sativa Arabidopsis thaliana Populus trichocarpa

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:

Chlamydomonas reinhardtii Ostreococcus tauri Physcomitrella patens (M) Oryza sativa (O) Arabidopsis thaliana (A) Populus trichocarpa (P) When was the receptor kinase configuration established? RLK RLCK Other Kinases ECD Kinase

How many receptor kinase configurations are present in moss?

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

Calculating lineage-specific gene gains AB common ancestor A1A2-1A2-2B2 Species divergence Duplication in species A GainsLossesNet Gain Species A Species B B1 Gene loss in species B (2 genes) Which RLK subfamilies have undergone lineage- specific expansion?

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

Is there a correlation between expansion rate and location in tandem repeats? r 2 =0.66 p<0.001 r 2 =0.62 p<0.001 r 2 =0.37 p=0.01

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

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

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

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

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

Is subfamily responsiveness to stress correlated with the proportion found in tandem repeats? C-LEC CR4L CrRLK1L-1 ColdDrought Heat … flg22 Responsiveness 00 0 … … … 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

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

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., Nature. –Recombination rate: Tandem > non-tandem Zhang & Gaut, Genome Res.

The “RLK swarm” model

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