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