Evolutionary History and Stress Evolutionary History and Stress Responsiveness of the Plant Receptor-Like Responsiveness of the Plant Receptor-Like Kinase FamilyKinase Family
Shin-Han Shiu and Melissa D. Lehti-ShiuShin-Han Shiu and Melissa D. Lehti-Shiu
Department of Plant Biology Department of Plant Biology Michigan State UniversityMichigan State University
Intro 1: Duplicate genes in the genomeIntro 1: Duplicate genes in the genome
*: Clusters of Markov clustering using all-against-all BLAST E values as distance measures
Protein kinase:~1000
Hanada & Shiu, in prep.
Intro 2: Plant vs. animalIntro 2: Plant vs. animal
Category Arabidopsis Human
Defense response
Proteolysis
Transport
Ion channel activity
Metabolism
Development
Protein kinase activity
Transcription factor activity
Gain rate relativeto within genome average
Higher
Lower
Shiu et al., 2006
Intro 3: The RLK/Pelle familyIntro 3: The RLK/Pelle family
Gene count differences among families indicate Gene count differences among families indicate differential expansiondifferential expansion
Animal homolog:Animal homolog: Drsophila: PelleDrsophila: Pelle Mammalian: IRAKsMammalian: IRAKs
Shiu et al., 2004
Intro 4: Diversity of RLK/PellesIntro 4: Diversity of RLK/Pelles
Shiu & Bleecker 2001
Intro 5: RLK function and expansionIntro 5: RLK function and expansion
Shiu et al., 2004
Major questionsMajor 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?
AtGenExpress microarray dataset22 stress conditions
The kinase superfamily in land plantsThe kinase superfamily in land plants
~400
RLK/Pelle members vs. other kinasesRLK/Pelle members vs. other kinases
Establishment of receptor kinase subfamilyEstablishment of receptor kinase subfamily
InnovationInnovation
LysM
GDPD
CHASE
LRR
LRR
LRR
Thaumatin
ThaumatinThaumatin
GH18
GH18
DUF26
DUF26DUF26
1
2
43
7
6
5
Family size over land plant evolutionFamily 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
Differences in subfamily turnover patternsDifferences in subfamily turnover patterns
12logN
NC ii
4 distinct patterns of turnover4 distinct patterns of turnover
Differences in recent expansion among Differences in recent expansion among lineageslineages
Stress responsiveness of RLKsStress responsiveness of RLKs
Shiu et al., 2004
Highexpansion
rates
Lowexpansion
rates
TandemNon-tandem
Likelihood ratio testLikelihood ratio test
Res-Res-ponsiveponsive
Non res-Non res-ponsiveponsive
% Res-% Res-ponsivponsiv
ee
Class Class AA
1515 55 75%75%
Class Class BB
100100 900900 10%10%
Hypothesis: Gene in class A is significantly more responsive to a stress
condition than random expectation.
Cumulative chi square distribution function
1.0
75.0ln2ln2
2
12 L
L
Stress responsiveness of RLKs Stress responsiveness of RLKs
Hypothesis 1: RLKs are more responsive to stress than genome average
Stress responsiveness of RLKs Stress responsiveness of RLKs
Hypothesis 2: Tandem RLKs are more responsive to stress than non-tandem RLKs
Comparison against AP2 transcription Comparison against AP2 transcription factors factors
Large number of AP2 family members are stress responsive
Properties of RLK subfamiliesProperties of RLK subfamilies
Stress responsiveness and tandem RLKsStress responsiveness and tandem RLKs
Responsiveness (R) of an RLK subfamilyResponsiveness (R) of an RLK subfamily For subfamilies with ≥ 10 genesFor subfamilies with ≥ 10 genes i: subfamilyi: subfamily j: conditionj: condition UP: # of up-regulated genesUP: # of up-regulated genes DN: # of down-regulatedDN: # of down-regulated
j i
ji
j i
ji N
DNR
N
UPR or
Why tandem RLKsWhy tandem RLKs
Stress responsivenessStress responsiveness Tandem genes Tandem genes >> non-tandem genes. non-tandem genes. RLK RLK >> genome average genome average Biotic Biotic >> abiotic abiotic
Duplication rate (event per unit time):Duplication rate (event per unit time): Whole genome duplication: 1 event / ~50 million yearsWhole genome duplication: 1 event / ~50 million years Tandem duplication: multiple events / generationTandem duplication: multiple events / generation
Rate of recombinationRate of recombination Recombination rate: Pathogen attack > controlRecombination rate: Pathogen attack > control
Lucht et al., 2002. Nature.Lucht et al., 2002. Nature. Recombination rate: Tandem Recombination rate: Tandem > > non-tandemnon-tandem
Zhang & Gaut, 2003. Genome Res.Zhang & Gaut, 2003. Genome Res.
The “RLK swarm” modelThe “RLK swarm” model
SummarySummary
Innovation in the RLK/Pelle familyInnovation in the RLK/Pelle family Most RK configuration established > 700 million ago.Most RK configuration established > 700 million ago. Plenty evidence of domain shuffling, but the rate is not high.Plenty evidence of domain shuffling, but the rate is not high. Shuffled domains suggest involvement in biotic stress Shuffled domains suggest involvement in biotic stress
perception. perception.
History of expansionHistory of expansion 4 major turnover patterns4 major turnover patterns Substantially more recent gains in poplar and riceSubstantially more recent gains in poplar and rice Mostly involved subfamilies with lots of tandem repeatsMostly involved subfamilies with lots of tandem repeats
Stress responsivenessStress responsiveness RLK > genome averageRLK > genome average Tandem > non-tandemTandem > non-tandem Biotic > abioticBiotic > abiotic The RLK swarm modelThe RLK swarm model
AcknowledgementAcknowledgement
Lab membersLab members
Past memberPast member
Melissa Lehti-Shiu
Cheng Zou
Kousuke Hanada
Funding:Funding:
The kinase superfamily in land plantsThe kinase superfamily in land plants
AtGenExpress: stress array dataAtGenExpress: stress array data
Raw intensity
Normalizedintensity
22 conditionsw/ time series
GCRMA
Genes withDiff. expr.
LIMMA
Do certain RLKs induced under specific subset of stress conditions?
Are tandemly duplicated RLKs tend to be induced under stress conditions?
Duplication mechanismsDuplication mechanisms
+
Whole genome duplicationWhole genome duplication
Tandem duplicationTandem duplication
Segmental duplicationSegmental duplication
Replicative transpositionReplicative transposition
Breadth of stress responsivenessBreadth of stress responsiveness
# of up-regulaton conditions per gene per subfamily# of up-regulaton conditions per gene per subfamily
Sizes of different types of RLKs Sizes of different types of RLKs