Systems Modeling of C4 and CAM Photosynthesis

8/17/2019 Systems Modeling of C4 and CAM Photosynthesis

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Systems Modeling of C4 andCAM Photosynthesis

Xinguang Zhu

Plant Systems Biology Group

CAS-MPG Partner Institute for Computational Biology

C4-CAM Meeting, Aug 9th 2013, Urbana IL



Roadmap

• Rationale of dynamic systems modeling and new options to

improve light and water use efficiency

• Systems model of NADP-ME type C4 photosynthesis and blueprintfor engineering an NADP-ME type C4 photosynthesis into a C3 crop

• Physiological significance of co-existing decarboxylases?

• What is the critical step for C4 evolution?



Wh =

Harvested

yield

S

Total solar

energy

i

Interception

efficiency

c

Conversion

efficiency

Partitioning

efficiency

Monteith (1977) Philosophical Transactions of the Royal Society of London, 281 277-294

90%

60%



Zhu et al (2008) Current Opinion in Biotechnology4.6% 6%



What c is achieved in the field?

• The highest c over a whole growing

season:

–

C3: 2.4% – C4: 3.7%

• Common c over a whole growing season:

–< 0.5%

Reviewed in: Zhu et al (2008) Current Opinion in Biotechnology



How to engineer a higher efficiency?

A systems approach!



Evolutionary algorithm

Zhu et al (2007) Plant Physiol.



Raines (2003) Photosynthesis Research 75:1-10



Evolution selects for fecundity, not

productivity

High yield Defense (e.g.

insects)

Preparation for

rare disaster

Wild plants

Desired crops



• Elevated [CO2 ]

• Increased temperature

• Increased O3

• Altered precipitation pattern

Global Climatic Change



1. Photosynthetic processes

a) Photosynthetic light reactions

b) Photosynthetic carbon metabolism

c) Whole photosynthetic process

2. Leaf primary metabolism

a) The dynamic systems model of plant primarymetabolism

b) Modeling the partitioning of photosynthate for buildingmetabolic machinery, cellular compounds and export etc

3. Reaction diffusion models of leaf photosynthesis

a) Reconstruction of 3D leaf anatomy

b) Ray tracing algorithm inside a leaf

c) Modeling CO2 , humidity and temperature distributions

inside a canopy with realistic 3d architectured) Modeling reaction diffusion and related physical

processes inside a leaf

4. Canopy microenvironments

a) Ray tracing algorithm inside a canopy

b) Modeling CO2 , humidity and temperature distributionsinside a canopy with realistic 3d architecture

5. Photosynthate partitioningThe ePlant Project

The Mission and Major Activities of the ePlant Project

Mission• To quantitatively study photosynthesis and plant

primary metabolism and its regulation• To systematically identify new targets and

strategies to optimize photosynthesis



Mechanistic model of mesophyll conductance

Tholen et al (2012) Plant Physiology; Tholen et al (2012) Plant Cell and Environment



Potential Targets to Improve Water Use Efficiency

• Decrease cell wall thickness

• Increase stromal CA concentration

• Increase the permeability of chloroplast envelop to CO2

• Decrease the permeability of chloroplast envelop to

HCO3-



Light inside a canopy is highly heterogeneous both temporarily

and spatially


http://slidepdf.com/reader/full/systems-modeling-of-c4-and-cam-photosynthesis 17/56See poster P12



Overall C systems modeling and design

• Questions to address: – Define key anatomical

and biochemicalfeatures required forhigh efficiencies of C4photosynthesis

– Identify viable andoptimal steps toengineer a C4 rice

• Models to develop – Kinetic systems model

of C4 photosynthesis

– Reaction diffusionmodels for C4photosynthesis

– Dynamic systemsmodel of C4 canopyphotosynthesis



A dynamic systems model of C photosynthesis



Novel features of the C systems model

• Detailed and updated description of the BSC and MC metabolism,i.e. incorporation of the Calvin-Benson cycle, starch, sucrose,mitochondria respiratory and complete photorespiratorymetabolism in a cell specific manner, but also incorporatesdetailed diffusion of metabolites between these two cell types;

• The metabolite transport between BSCs and MCs was described

as a diffusional process through plasmodesmata, and metabolitetransport across chloroplast envelope was assumed to followMichaelis-Menten kinetics;

• Starch synthesis and breakdown occur at the same time;

• The electron transfer rate, directly linked to ATP and NADPHsynthesis were explicitly modeled.



A dynamicsystems model

of C4photosynthesispredicts Aci and

AQ curves.



Responses of metabolite levels under different Ci



Responses of metabolite levels under PPFD levels



Ke

y enzymes controlling A-C i responses of C4 photosynthesis



Enzyme

Abbreviation EC Number

Vmax

(μmol m-2 s-1)

Flux Control Coefficient

High

light Low CO2

Low

light

CA 4.2.1.1 200000 0.001 0.203 0.000PEPC 4.1.1.31 170 0.011 0.431 0.000

NADP-ME 1.1.1.40 90 0.008 0.037 0.000

Rubisco_CO2 4.1.1.39 65 0.349 0.119 0.041

PGAK &GAPDH 2.7.2.3 &1.2.1.13 225 0.034 0.002 0.024

SBPase 3.1.3.37 29.18 0.052 0.020 0.050

PRK 2.7.1.19 1170 0.043 0.019 0.061

PGAK_M &GAPDH_M 2.7.2.3M &1.2.1.13M 300 0.018 -0.150 0.020

Rubisco_O2 4.1.1.39 7.15 -0.017 0.032 -0.036

Jmax 500 0.637 -0.017 0.082

I 2000 or 200 0.148 -0.007 1.091

Diffusion parameter Value

Flux Control Coefficient

High light Low CO2 Low

light

gm 0.7mol m-2 s-1bar-1 0.003 0.533 0.000

Pmal

42.14μm/s 0.001 0.047 0.000

Pco2 113.92μm/s -0.044 -0.058 -0.023

φ 0.03 -0.037 -0.032 -0.018

Lpd 400 nm 0.041 0.035 0.018

Control coefficients for parameters related to C4 photosynthesi



Enzymes Comparison (C3/C4) PEPC NADP-MDH PPDK NADP-ME Rubisco

CO2 uptake ratio

Ci=50

mbar

0.34 1.00 1.00 1.00 1.03

Ci=200

mbar 0.59 1.00 1.00 1.00 1.03

Nitrogen cost ratio 1.10 5.14 1.20 1.39 1.24

Necessity of using C4 isoforms in C4 engineering



• Cleome gynandra displays age-dependentplasticity of C4 decarboxylation biochemistry(Sommer et al. 2012)

• Maize leaf gradient (Pick et al. 2011)



Having the mixed pathway does not increase CO2 uptake rate



Having mixed pathway decrease malate levels in BSC and MC



The decreased photosynthetic efficiency in a mixturepathway is related to the increased leakage in the system



Different combinations of transported four carboncompounds and decarboxylation mechanisms



A compromise between efficiency and capacity

Assuming only cyclic electron transport occurs in BSC.



Leakiness increases by additional C4 pathways

Assuming only cyclic electron transport occurs in BSC.



Photorespiration rate decreases by additional C4 pathways



Can PCK pathway exist alone?



If there is only cyclic ETR in BSC, PCK can not exists alone



Increase linear electron transport in BSC increases CO2 assimilation rate

u=v=0

Assuming only cyclic electron

transport occurs in BSC

u=v=1

Assuming only linear electron

transport occurs in BSC



The limited access to light by BSC limit the photosyntheticefficiency of the PCK pathway

PPFD = 2000 μmol m-2 s-1PPFD = 300 μmol m-2 s-1

Assuming linear electron transport occurring in BSC

X: proportion of light partitioned into mesophyll cells



Physiological significance of

co-existing decarboxylases

• A mixture of PEPCK and NADP-ME decrease the

quantum yield but increase the capacity of CO2

uptake.

• Having additional 4-C shuttle and decarxylases

decreases the cellular malate concentrations and

avoid potential osmotic toxicity.

• The PCK pathway is limited by the amount of lightaccessible by BSC.

See poster P31



Developing a Reaction Diffusion Model of C4 LeafPhotosynthesis to Explore Anatomical Requirement for C4Photosynthesis

Predicted CO2 distribution in cellsaffiliated with a Kranz Structure

Red: Reactions implemented in the model



0 200 400 600 800 1000 1200 1400

24

30

36

42

48

A ( m o l m

- 2 s

- 1 )

Ci (bar)

coverage=80%,mesophyll chloroplast thickness=1.5[m] coverage=95%,mesophyll chloroplast thickness=1.5[m]

coverage=80%,mesophyll chloroplast thickness=0.75[m]

coverage=95%,mesophyll chloroplast thickness=0.75[m]

Rice chloroplast number needs to be decreased for C4engineering

Increase of carbonic anhydrase concentration can enhance



0 500 1000 1500

35

42

49

A ( u m o l / ( m ^ 2 * s

) )

Ci (ubar)

CA concentration=0.5[mol/m^3]



Increase of carbonic anhydrase concentration can enhanceCO2 assimilation rate in C4



What is the critical step for C4 emergence?

Sage and Zhu (2011) Journal of Experimental Botany; Zhu et al (2010) Journal of Integrative Biology



Christin et al (2008)Current Biology

Zhu et al (2008) Current

Opinion in Biotechnology

i l C ll C4 i ffi i h C3



Single Cell C4 system is more efficient than C3 systemonly under low CO2 levels

Si l ll C4 h t th i i i l t t d l CO



Salvucci and Bowes Plant Physiol . 67, 335-340 (1981)

Single-cell C4 photosynthesis is a survival strategy under low CO2

Th C iti l St f K T C4 h t th i

http://www48.tok2.com/home/mizubasyou/



The Critical Step for Kranz Type C4 photosynthesis

MC MCBSC BSC

ME

ME

P di ti if ll l t t ti f ME i iti l t



Predictions if cellular compartmentation of ME is a critical stepduring C4 emergence

• C4 type NADP-ME should appear much later than C4type PEPC in evolution;

• After establishment of the C4 cycle, there should bedramatic changes in the redox property andcorrespondingly the expression of genes related tolight reactions;

• The emergence of C4 species needs anatomicalpreconditioning to decrease the leakiness to CO2.



PEPC

VMDH

V

ME/PEPCKV

PPDK

V

SSU



PEPC

V

MDH

V

ME/PEPCKV

PPDKV

SSU

Th dS l f th C4 h ttl



The dS values of the C4 shuttle genes

0 0.2 0.4 0.6 0.8 1

PEPC

MDH

ME

PEPCK

PPDK

SSU

dS

Optimization of the light reaction occurred at a late stage of C4 evolution



Optimization of the light reaction occurred at a late stage of C4 evolution

Red: C3

Yellow: C3-C4

Orange: C4-like

Blue: C4

ATC G 00590 b6f−com ple

x

0

5

1 0

1 5

2 0

2 5

3 0

3 5

AT1G 70760 NA DH

0

1 0 0

2 0 0

3 0 0

4 0 0

5 0 0

AT1G74880 NA DH −O

0

5 0

1 0 0

1 5 0

2 0 0

2 5 0

3 0 0

3 5 0

AT2G 39470 PN SL1

0

2 0 0

4 0 0

6 0 0

8 0 0

AT1G14150 PN SL2

0

5 0

1 0 0

1 5 0

2 0 0

2 5 0

3 0 0

AT3G01440 PN SL3

0

2 0

4 0

6 0

8 0

AT C G 00700 PS II

0

2 0

4 0

6 0

8 0

AT 4G 37230 P S II

0

2 0

4 0

6 0

8 0

1 0 0

1 4 0

AT 1G 60950 F erredo xin1

0

5 0 0

1 0 0 0

1 5 0 0

AT1G 45474 LH C −P S I

0

2 0 0

4 0 0

6 0 0

8 0

0

AT5G 64040 PS I

0

2 0 0 0

4 0 0 0

6 0 0 0

AT2G 46820 PS I

0

5 0 0

1 0 0 0

1 5 0 0

2 0 0 0

AT3G 62410 C P

− 2

0

1 0 0

2 0 0

3 0 0

4 0 0

5 0 0



l i



Conclusions

• A systems model of C4 photosynthesis with detailed description of the involvedbiochemical and biophysical processes is developed and there is much space toincrease C4 photosynthetic energy conversion efficiency through manipulation ofC4 related parameters.

• Having mixtures of C4 subtypes can increase the photosynthetic capacity but

decrease the light use efficiency.

• Incorporation of aspartate as a C4-shuttle compound can decrease the malateconcentration in the system.

•

PCK pathway can exists alone if there is linear electron transfer in the bundle sheathcells.

• Proper cellular positioning of decarboxylases might be a critical step duringemergence of C4 photosynthesis.

A k l d t



Funding: MOST NSFC CAS MPG Pujiang Plan SIBS

Collaborators:C4 Rice Consortium, 3to4 consortium, Global Wheat Yield Consortium, Grassmargin consortium,

RIPE consortium.

Stephen Long, Donald Ort, Andreas Weber, Peter Westhoff, Mark Stitt, Yan Li, Hui Zhang

Acknowledgements

Yu Wang

Danny Tholen

Qingfeng Song

Yimin Tao

Mingzhu Lv

Systems Modeling of C4 and CAM Photosynthesis

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