1. Evolutionary History and Stress Responsiveness of the Plant Receptor-Like Kinase Family
Shin-Han Shiu and Melissa D. Lehti-Shiu
Department of Plant Biology
Michigan State University

2. Intro 1: Duplicate genes in the genome
Protein kinase:
~1000
*: Clusters of Markov clustering using all-against-all BLAST E values as distance measures
Hanada & Shiu, in prep.

3. Intro 2: Plant vs. animal Gain rate relative to within genome average
Higher
Lower
Category
Arabidopsis
Human
Defense response
Proteolysis
Transport
Ion channel activity
Metabolism
Development
Protein kinase activity
Transcription factor activity
Shiu et al., 2006

4. Intro 3: The RLK/Pelle family
Gene count differences among families indicate differential expansion
Animal homolog:
Drsophila: Pelle
Mammalian: IRAKs
Shiu et al., 2004

5. Intro 4: Diversity of RLK/Pelles
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase
Shiu & Bleecker 2001

6. Intro 5: RLK function and expansion
Shiu et al., 2004

7. AtGenExpress microarray dataset
Major questions
Diversity
When were the receptor configuration established?
Expansion history
What are the patterns of expansion of RLK subfamilies over land plant evolution?
Stress responsiveness
What are the properties of stress responsive RLKs?
3 major questions:
Establishment of RLK diversity
Expansion history of RLKs
Stress responsiveness of RLKs
AtGenExpress microarray dataset
22 stress conditions

8. The kinase superfamily in land plants
RLK/Pelle members vs. other kinases
~400

9. Establishment of receptor kinase subfamily
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase

10. Innovation LysM GDPD Thaumatin CHASE DUF26 LRR GH18
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase
LRR
GH18

11. Family size over land plant evolution
Substantial differences in # of gene gains among lineages
N1-N7: 0.14 genes / 106 yr
N1-N2: 0.52
N2-N4: 0.91
N2-N5: 6.71
N2-N6: 5.5 1 2 4 3 7 6 5
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase

12. Differences in subfamily turnover patterns
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase

13. 4 distinct patterns of turnover
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase

14. Differences in recent expansion among lineages

15. Stress responsiveness of RLKs
Low
expansion rates
High
expansion rates
Non-tandem
Tandem
Shiu et al., 2004

16. Likelihood ratio test Hypothesis:
Gene in class A is significantly more responsive to a stress condition than random expectation.
Cumulative chi square distribution function
Res-ponsive
Non res-ponsive
% Res-ponsive
Class A 15 5
75%
Class B
100
900
10%

17. Stress responsiveness of RLKs
Hypothesis 1: RLKs are more responsive to stress than genome average
Significantly responsive in essentially all stress conditions
Particularly for biotic stress
Particularly for up-regulation

18. Stress responsiveness of RLKs
Hypothesis 2: Tandem RLKs are more responsive to stress than non-tandem RLKs
Over-representation in abiotic stress categories are mostly influenced by both tandem and non-tandem RLKs
But responsiveness in biotic stress is mainly due to tandemly duplicated RLKs

19. Comparison against AP2 transcription factors
Large number of AP2 family members are stress responsive
Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants

20. Properties of RLK subfamilies
Should do a clustering based on stress responsiveness (may be based on the intensity data)
Then check the properties (e.g. expansion rate, tandemness) of each cluster.

21. Stress responsiveness and tandem RLKs
Responsiveness (R) of an RLK subfamily
For subfamilies with ≥ 10 genes
i: subfamily
j: condition
UP: # of up-regulated genes
DN: # of down-regulated
Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants

22. Why tandem RLKs Stress responsiveness
Tandem genes > non-tandem genes.
RLK > genome average
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.
Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants

23. The “RLK swarm” model Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants

24. Summary Innovation in the RLK/Pelle family
Most RK configuration established > 700 million ago.
Plenty evidence of domain shuffling, but the rate is not high.
Shuffled domains suggest involvement in biotic stress perception.
History of expansion
4 major turnover patterns
Substantially more recent gains in poplar and rice
Mostly involved subfamilies with lots of tandem repeats
Stress responsiveness
RLK > genome average
Tandem > non-tandem
Biotic > abiotic
The RLK swarm model

25. Acknowledgement Lab members Past member Funding: Melissa Lehti-Shiu
Cheng Zou
Kousuke Hanada

26. The kinase superfamily in land plants
Many of the RK configurations are established long ago
Relatively few new configuration has arisen
Potential evidence for lost of certain configuration, eg. chitinase

27. AtGenExpress: stress array data
Do certain RLKs induced under specific subset of stress conditions?
Are tandemly duplicated RLKs tend to be induced under stress conditions?
22 conditions
w/ time series
Raw
intensity
GCRMA
Normalized
intensity
LIMMA
Genes with
Diff. expr.

28. Duplication mechanisms
Whole genome duplication
Tandem duplication
Segmental duplication
Replicative transposition +

29. Breadth of stress responsiveness
# of up-regulaton conditions per gene per subfamily
Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants

30. Sizes of different types of RLKs
Most successful RLK: LRR type
But Arabidopsis may not be representative of land plants