Evolutionary history and stress responsiveness of plant receptor like kinases
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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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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

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


Evolutionary history and stress responsiveness of plant receptor like kinases

  • 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


Duplication mechanisms

+

Duplication mechanisms

  • Whole genome duplication (polyploidization)

  • Tandem duplication

  • Segmental duplication

  • Replicative transposition


Why is knowing duplication mechanism important

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tandem repeats are enriched with genes that are involved in stress response (Rizzon et al., 2006; Hanada and Shiu, unpublished results)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

Why are genes retained after duplication?

A.

B.

C., D.


What can we learn from studying the evolutionary histories of gene families

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


Protein kinase gene families unique

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.


The rlk pelle family has experienced dramatic differential expansion

Arabidopsis

Rice

The RLK/Pelle family has experienced dramatic differential expansion

Shiu et al., 2004


Evolutionary history and stress responsiveness of plant receptor like kinases

RLK/Pelle members have diverse

kinase configurations


Rlks function in signal transduction pathways

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


Identify kinases from sequenced plant genomes

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


Kinase classification

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


When was the receptor kinase configuration established

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?


How many receptor kinase configurations are present in moss

How many receptor kinase configurations are present in moss?


What innovation in receptor configuration has occurred

LysM

GDPD

Thaumatin

CHASE

DUF26

LRR

GH18

LRR

LRR

DUF26

GH18

DUF26

Thaumatin

Thaumatin

What innovation in receptor configuration has occurred?


Calculating lineage specific gene gains

Which RLK subfamilies have undergone lineage-specific expansion?

B1

Duplication in

species A

Gene loss

in species B

Species divergence

GainsLossesNet 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


Which rlk subfamilies have undergone lineage specific expansion

Which RLK subfamilies have undergone lineage-specific expansion?

Subfamilies not found in moss: DUF26, LRK10L-2, SD1, WAK


Is there a correlation between expansion rate and location in tandem repeats

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


Evolutionary history of the rlk pelle family

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

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.


Genes differentially up 1 or down 1 regulated under each condition

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


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

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 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

Is subfamily responsiveness to stress correlated with the proportion found in tandem repeats?

ColdDrought Heat … flg22 Responsiveness

C-LEC

CR4L

CrRLK1L-1

00 0 … 0 0.0

00 0 … 0.125 0.93

0.20 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


Stress responsiveness and tandem rlks

Stress responsiveness and tandem RLKs

X10

(subfamilies with ≥ 10 genes)


Relationship between rlks stress and tandem duplication

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.


The rlk swarm model

The “RLK swarm” model


Acknowledgements

Acknowledgements

  • Funding:

  • Shiu lab

    • Shinhan Shiu

    • Kousuke Hanada

    • Cheng Zou

    • Jessica Oswald

    • Amanda Tabbert

    • Gaurav Moghe


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