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Evolutionary History and Stress Responsiveness of Plant Receptor-
Like Kinases
Melissa Lehti-Shiu
Shiu lab
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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;132:530-543
Phylogenetic tree of the Arabidopsis RLK/Pelle gene family
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• 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
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• Whole genome duplication (polyploidization)
• Tandem duplication
• Segmental duplication
• Replicative transposition
Duplication mechanisms
+
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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are involved in stress response (Rizzon et al., 2006; Hanada and Shiu, unpublished results)
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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.
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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
AncestralGene
Arabidopsis 1
http://www.sheppardsoftware.com/Europeweb/factfile/Unique-facts-Europe33.htm
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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.
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The RLK/Pelle family has experienced dramatic differential expansion
Shiu et al., 2004
Arabidopsis
Rice
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RLK/Pelle members have diverse kinase configurations
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RLKs function in signal transduction pathways
Flagellin
FLS2(LRR-XII)
Flagellin defense relatedgene expression
CLV1(LRR-XI)
LRR
LRR
LRR
CLV2
CLV3
Meristem proliferation
PAMP recognition Development
Kin
ase
Kin
ase
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Identify kinases from sequenced plant genomes
http://genome.jgi-psf.org/Ostta4/Ostta4.home.html
http://genome.jgi-psf.org/Chlre3/Chlre3.home.html
http://www.jgi.doe.gov/sequencing/why/CSP2005/physcomitrella.html
http://www.genomics.zju.edu.cn/ricetdna.html
Chlamydomonasreinhardtii
Ostreococcustauri
Physcomitrellapatens
Oryza sativa
Arabidopsisthaliana
Populustrichocarpa
http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html
http://www.pg.ipw.biol.ethz.ch/Title.html
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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
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Chlamydomonasreinhardtii
Ostreococcustauri
Physcomitrellapatens (M)
Oryza sativa (O)
Arabidopsisthaliana (A)
Populustrichocarpa (P)
356
73
256
388148
462
376
159
911
453
187
1003
When was the receptor kinase configuration established?
424
2
93
RLKRLCKOther Kinases
ECD Kinase
Kinase
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How many receptor kinase configurations are present in moss?
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What innovation in receptor configuration has occurred?
LysM
GDPD
CHASE
LRR
LRR
LRR
Thaumatin
ThaumatinThaumatin
GH18
GH18
DUF26
DUF26DUF26
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Calculating lineage-specific gene gains
AB common ancestor
A1 A2-1 A2-2 B2
Species divergence
Duplication inspecies A
Gains Losses Net Gain
Species A
Species B
1 0 1
0 1 -1
B1
Gene lossin species B
(2 genes)
Which RLK subfamilies have undergone lineage-specific expansion?
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-15-10-505
101520253035404550556065707580859095
100
C-LECCR4L
CrRLK1L-1Extensin
L-LECLRR_XVI
LRR-ILRR-IILRR-IIILRR-IVLRR-VLRR-VI-1LRR-VI-2
LRR-VIILRR-VIII-1LRR-VIII-2
LRR-IXLRR-XaLRR-XbLRR-XILRR-XIILRR-XIIIaLRR-XIIIbLRR-XIVLRR-XV
LysM-ILysM-IIPERKRKF3SD-2bURK-1
WAK_LRK
Gains since the APOM common ancestor
ArabidopsisPoplarRiceMoss
Subfamilies not found in moss: DUF26, LRK10L-2, SD1, WAK
Which RLK subfamilies have undergone lineage-specific expansion?
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-0.4
-0.3
-0.2
-0.1
0
0.1
0.2
0.3
0.4
0.5
0.6
0 10 20 30 40 50 60 70 80 90 100
% of subfamily members in tandem repeats
Expansion rate (number of gains since
APO ancestor normalized by
subfamily size)
Rice
Arabidopsis
Poplar
Linear (Poplar)
Linear (Rice)
Linear (Arabidopsis)
Is there a correlation between expansion rate and location in tandem repeats?
r2 =0.66p<0.001
r2 =0.62p<0.001
r2 =0.37p=0.01
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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
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AtGenExpress: stress array data
Raw intensity
Normalizedintensity
16 conditionsw/ time series
GCRMA
Genes withDiff. expr.
LIMMA
http://www.weigelworld.org/resources/microarray/AtGenExpress/
BioticavrRpm1DC3000
Flg22HrcC-HrpZLPSPsph
P. infestans
AbioticColdHeat
DroughtSalt
OsmoticGenotoxicWounding
UV-B
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Genes differentially up (1) or down (-1) regulated under each condition
0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
1 0 1 0 0 0 0 0 0 0 0 0 -1 0 -1 -1
-1 0 1 1 0 0 -11/-1
0 0 0 0 0 0 1 0
1 1 1 1 1 1 1 1 0 0 0 0 0 0 0 0
0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
0 0 0 0 0 0 0 0 1 0 0 1 1 0 0 0
At1g1
At1g2
At1g3
At1g4
At1g5
At1g6
avrR
pm
1
DC
3000
Flg
22
Hrc
C-
Hrp
Z
LP
S
P.
infe
stan
s
Psp
h
Co
ld
Dro
ug
ht
Gen
oto
xic
Hea
t
Osm
oti
c
Sal
t
UV
-B
Wo
un
din
g
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Is the number of RLKs up or down regulated by stress different from the genome average?
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Is the number of tandem RLKs regulated by stress different from non-tandem RLKs?
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Is subfamily responsiveness to stress correlated with the proportion found in tandem repeats?
C-LEC
CR4L
CrRLK1L-1
Cold Drought Heat … flg22 Responsiveness
0 0 0 … 0 0.0
0 0 0 … 0.125 0.93
0.2 0 0.14 … 1.0 2.875
Fraction of subfamily membersup (or down) regulated by coldTreatment (e.g. 5 out of 10=0.5)
Sum of fractions for all16 conditions
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Stress responsiveness and tandem RLKs
(subfamilies with ≥ 10 genes)
X1
0
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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.
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The “RLK swarm” model
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Acknowledgements
• Shiu lab – Shinhan Shiu– Kousuke Hanada– Cheng Zou– Jessica Oswald– Amanda Tabbert– Gaurav Moghe
• Funding:
–
–