Christin Presentation

Evolutionary facilitators and the recurrent assembly of C4 photosynthesis in grasses

Pascal-Antoine Christin

C4 origins clustered in some groups

20 origins

Poaceae

Caryophylalles

>66 C4 origins in flowering plants

C4 grasses

~60% of C4 species are grasses

Includes major crops and most highly productive weeds

Woodward et al. 2004; Woodward and Lomas 2004

C4 grasses

Grass phylogeny

PA

CM

AD

BE

P

Grass Phylogeny Working Group II 2012, New Phytol

Grass phylogeny

PA

CM

AD

BE

P

28

5423

5706


Grass phylogeny

PA

CM

AD

BE

P

28

5423

5706

0

0

4657


Grass phylogeny

>24 C4 groups


>22-24 C4 origins

Grass phylogeny

Why so many C4 origins?

Why all in the PACMAD?

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

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


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


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

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:

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

C4 components

Compartment 1 Compartment 2

1 4Atmospheric CO2 2 3

Multiple anatomical and biochemical components

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)

C4 plants

CO2 fixation in chloroplasts

Mesophyll reduced

Bundle sheath increased

C4 transport of CO2

CO2

CO2


C4 photosynthesis requires a low mesophyll:bundle sheath ratio


Pennisetum villosum (grass genera of the world)

C4 plants

CO2

CO2



C3 plants

CO2

CO2

More BS per M

Leaf anatomy in grasses


Sartidia sp.

C3

C4

Centropodia glauca

Measurements

BSDOS width

mesophyll

outer bundle sheathinner bundle sheathvein


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


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


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


Grass anatomy

C3 species only

%OS > 0.15

Grass anatomy

C3 species only

%OS > 0.15

Large %OS appeared at the base of the PACMAD

Grass anatomy

C3 species only

%OS > 0.15

Large %OS appeared at the base of the PACMAD

Several C3 PACMAD have “C4” value

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


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

Grass anatomy

C3 species only

%OS > 0.15

Grass anatomy

C3 species only

%OS > 0.15

OS cells decreased in BEP

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


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


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


Grass anatomy

C3 species only

%OS > 0.15

Grass anatomy

C3 species only

%OS > 0.15BSD decreased at the base of the BEP-PACMAD clade

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


Christin and Osborne 2013, Photosynth Res

Genetic facilitators

Sage et al. 2012 Annu Rev Plant Biol

C3 fixation of CO2

Biochemical adaptation

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

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?

Comparison of three independently evolved C4 transcriptomes


0 Ma81624

ZeaC4 Alloteropsis

Setaria

C3C4

mixed


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


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

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

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

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


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


Some genes are more suitable for the C4 function

Can the taxonomic distribution of C4-suitable genes affect C4 evolvability?

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

Christin Presentation

Documents

Transcript of Christin Presentation