christin presentation
TRANSCRIPT
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Evolutionary facilitators and the recurrent assembly of C4 photosynthesis in grasses
Pascal-Antoine Christin
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C4 origins clustered in some groups
20 origins
Poaceae
Caryophylalles
>66 C4 origins in flowering plants
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C4 grasses
~60% of C4 species are grasses
Includes major crops and most highly productive weeds
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Woodward et al. 2004; Woodward and Lomas 2004
C4 grasses
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Grass phylogeny
PA
CM
AD
BE
P
Grass Phylogeny Working Group II 2012, New Phytol
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Grass phylogeny
PA
CM
AD
BE
P
28
5423
5706
Grass Phylogeny Working Group II 2012, New Phytol
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Grass phylogeny
PA
CM
AD
BE
P
28
5423
5706
0
0
4657
Grass Phylogeny Working Group II 2012, New Phytol
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Grass phylogeny
>24 C4 groups
Grass Phylogeny Working Group II 2012, New Phytol
>22-24 C4 origins
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Grass phylogeny
Why so many C4 origins?
Why all in the PACMAD?
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Rubisco land plants
flowering plants
30004000 2000 1000 Ma
Earth
0.1 O2
leve
l (ba
r)
0
0.2
0.31
CO
2 le
vel (
bar)
0.1
0.01
0.001
C4 recurrent origins
Christin and Osborne 2013, Photosynth Res
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Environmental drivers
C4 is advantageous in many conditions
The CO2-pump advantage is exacerbated under low CO
2
CO2 levels decreased
around 30 Ma
Beerling and Royer 2011, Nature Geoscience
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Environmental drivers
Molecular dating places all C4 origins during the last ~ 30 million years
Estimated C4 origins:
monocots
eudicots
Christin et al. 2008, Curr Biol; 2011, J Exp Bot
0 Ma102030Time
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Environmental drivers
Modelling suggests C4 evolvability strongly increased after ~30 Ma
Christin et al. 2008, Curr Biol; 2011, J Exp Bot
Model with different transition rates after a given time
eudicots
grasses
Rate of C3 to C4 transition:
Before 28 Ma
After 28 Ma
0
6.6
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Environmental drivers
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Environmental drivers
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C4 clustering
Model in Marazzi et al. 2012, Evolution
Modelling of C4 photosynthesis model with a precursor model
-
a
a
-
C3
C4
C3 C4
-
a
a
-
C3
P
C3 P
-
b
C4
- bC4 -
Null model: Precursor model:
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C4 clustering
Christin et al. 2013, PNAS
Precursor model significantly better
Evolution of an unidentified “precursor” at the base of the PACMAD clade
C3 P: 0.003
P C4: 0.016
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C4 components
Compartment 1 Compartment 2
1 4Atmospheric CO2 2 3
Multiple anatomical and biochemical components
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C3 plants
CO2
CO2
CO2 fixation in chloroplasts
Mesophyll important
Bundle sheath, few
Leaf cross-section
Christin et al. 2011, Evolution
C3 vs C4 photosynthesis
Viburnum punctatum (courtesy D. Chatelet)
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C4 plants
CO2 fixation in chloroplasts
Mesophyll reduced
Bundle sheath increased
C4 transport of CO2
CO2
CO2
Christin et al. 2011, Evolution
C4 photosynthesis requires a low mesophyll:bundle sheath ratio
C3 vs C4 photosynthesis
Pennisetum villosum (grass genera of the world)
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C4 plants
CO2
CO2
Christin et al. 2011, Evolution
C3 vs C4 photosynthesis
C3 plants
CO2
CO2
More BS per M
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Leaf anatomy in grasses
Christin et al. 2013, PNAS
Sartidia sp.
C3
C4
Centropodia glauca
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Measurements
BSDOS width
mesophyll
outer bundle sheathinner bundle sheathvein
Christin et al. 2013, PNAS
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Grass anatomy%OS
0.1
0.3
0.5o
utg
roup
s
C3 B
EP
C3
PA
CM
AD
C4-O
S
C4 species have larger %OS
C3 PACMAD have more C4-like values
Christin et al. 2013, PNAS
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Grass anatomy
Modeling of C4 evolvability as a function of anatomy
When anatomical trait below threshold (variable)→ no transition possible
Comparison with null model through LRT
Christin et al. 2013, PNAS
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Grass anatomy
Modeling of C4 evolvability as a function of anatomy
When anatomical trait below threshold (variable)→ no transition possible
Comparison with null model through LRT
%OS above 0.15 significantly increase C4 evolvability
P-value < 0.001
Christin et al. 2013, PNAS
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Grass anatomy
C3 species only
%OS > 0.15
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Grass anatomy
C3 species only
%OS > 0.15
Large %OS appeared at the base of the PACMAD
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Grass anatomy
C3 species only
%OS > 0.15
Large %OS appeared at the base of the PACMAD
Several C3 PACMAD have “C4” value
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Grass anatomy%OS
0.1
0.3
0.5
OS area per vein
2000
10000
out
grou
ps
C3 B
EP
C3
PA
CM
AD
C4-O
S
out
gro
ups
C3 B
EP
C3
PA
CM
AD
C4-O
S
Christin et al. 2013, PNAS
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Grass anatomy%OS
0.1
0.3
0.5
OS area per vein
2000
10000
OS width
0
20
40
out
gro
ups
C3 B
EP
C3
PA
CM
AD
C4-O
S
outg
roup
s
C3 B
EP
C3
PA
CM
AD
C4-O
S
outg
roup
s
C3 B
EP
C3
PA
CM
AD
C4-O
S
OS cells above 15.7 significantly increase C4 evolvability
P-value = 0.021
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Grass anatomy
C3 species only
%OS > 0.15
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Grass anatomy
C3 species only
%OS > 0.15
OS cells decreased in BEP
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Grass anatomy%OS
0.1
0.3
0.5
OS area per vein
M area per vein
2000
10000
50000
10000
OS width
0
20
40
outg
roup
s
C3 B
EP
C3 P
AC
MA
D
C4-
OS
out
gro
ups
C3 B
EP
C3
PA
CM
AD
C4-O
S
Christin et al. 2013, PNAS
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Grass anatomy%OS
0.1
0.3
0.5
OS area per vein
M area per vein
2000
10000
50000
10000
OS width
BSD
100
200
300
0
20
40
outg
roup
s
C3 B
EP
C3 P
AC
MA
D
C4-
OS
outg
rou
ps
C3 B
EP
C3 P
AC
MA
D
C4-
OS
Christin et al. 2013, PNAS
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Grass anatomy%OS
0.1
0.3
0.5
OS area per vein
M area per vein
2000
10000
50000
10000
OS width
BSD
100
200
300
0
20
40
outg
roup
s
C3 B
EP
C3 P
AC
MA
D
C4-
OS
outg
rou
ps
C3 B
EP
C3 P
AC
MA
D
C4-
OS
BSD below 196 significantly increase C4 evolvability
P-value = 0.012
Christin et al. 2013, PNAS
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Grass anatomy
C3 species only
%OS > 0.15
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Grass anatomy
C3 species only
%OS > 0.15BSD decreased at the base of the BEP-PACMAD clade
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Grass anatomy
%OS > 0.15BSD decreased at the base of the BEP-PACMAD clade
OS cells decreased in BEP
Large %OS characterize the PACMAD
Explains clustering of C4 origins in PACMAD
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C4 recurrent origins
Christin and Osborne 2013, Photosynth Res
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Genetic facilitators
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Sage et al. 2012 Annu Rev Plant Biol
C3 fixation of CO2
Biochemical adaptation
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Sage et al. 2012 Annu Rev Plant Biol
Co-option of enzymes present in C3 ancestors→ adaptation of expression and catalytic properties
C4 cycle
Biochemical adaptation
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Comparison of three independently evolved C4 transcriptomes
Evolution of C4 enzymes
Most C4 enzymes are encoded by multigene families
Are all copies equally suitable for the C4 pathway?
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Comparison of three independently evolved C4 transcriptomes
Evolution of C4 enzymes
0 Ma81624
ZeaC4 Alloteropsis
Setaria
C3C4
mixed
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Evolution of C4 enzymes
Model species
NAD(P)-MDH multigene family
1
POPTR 0904s00200.1 POPTR 0010s08180.1 POPTR 0008s16670.1 Glyma10g00920.1 Glyma02g00810.1 AT1G04410.1
AT5G43330.1 Bradi3g28820.1 Os10g33800.1
GRMZM2G415359 T01 Sb01g019280.1 Si036876m
Si036550m POPTR 0002s14270.1
Glyma13g16440.1 AT5G56720.1
POPTR 0014s05660.1 POPTR 0002s14290.1
Os04g46560.1 Bradi5g17700.1
Si010442m Sb06g024610.1 GRMZM2G101290 T01
GRMZM5G811212 T01 GRMZM2G035767 T01
Glyma20g33380.1 Glyma10g34150.1
POPTR 0008s03160.1 AT5G58330.1 Si029817m
Os08g44810.1 Bradi3g12460.1
Si013711m Si013632m Sb07g023920.1 GRMZM2G129513 T01
Sb07g023910.1
42
1005
14
100
10098
66
100
100
100100
82
100
79
48
37
100100100
10055
100
60100
100
100
91
100
97
100
84
6199
0.2
2
3
4
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Evolution of C4 enzymes
eudicots
grasses 4
eudicots
grasses 3
eudicots
grasses 2
grasses 1
14
100
79
48
37
100
100
97
100
84
0.2
Model species
NAD(P)-MDH multigene family
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NADP-MDH
eudicots
grasses 4
eudicots
grasses 3
eudicots
grasses 2
grasses 1
14
100
79
48
37
100
100
97
100
84
0.2
Allo Allo
C3 C4
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NADP-MDH
eudicots
grasses 4
eudicots
grasses 3
eudicots
grasses 2
grasses 1
14
100
79
48
37
100
100
97
100
84
0.2
Allo Allo SetariaAB CD
C3 C4
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NADP-MDH
eudicots
grasses 4
eudicots
grasses 3
eudicots
grasses 2
grasses 1
14
100
79
48
37
100
100
97
100
84
0.2
Allo Allo Setaria ZeaAB CD AB CD
C3 C4
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Evolution of C4 enzymes
Same gene lineages used by independently evolved C4: 6/10
Probability of occurring by chance:< 0.0005
Some genes are more suitable for the C4 function
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C4 recurrent origins
Some genes are more suitable for the C4 function
Can the taxonomic distribution of C4-suitable genes affect C4 evolvability?
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Acknowledgments
Marie Curie IOF 252568 fellowship
Erika J. Edwards, Brown University, RI, USAColin P. Osborne, University of Sheffield, UKGuillaume Besnard, Universite de Toulouse, France
Rowan F. Sage, University of Toronto, CanadaNicolas Salamin, Universite de Lausanne, SwitzerlandMartha Ludwig, University of Western Australia, AustraliaDavid S. Chatelet, Brown University, RI, USAMonica Arakaki, Brown University, RI, USAJ. Travis Columbus, Rancho Santa Ana, CA, USATrevor R. Hodkinson, Trinity College Dublin, Ireland