Systems Modeling of C4 and CAM Photosynthesis

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1 Systems Modeling of C4 and CAM Photosynthesis Xinguang Zhu Plant Systems Biology Group CAS-MPG Partner Institute for Computational Biology C4-CAM Meeting, Aug 9 th 2013, Urbana IL

2 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 blueprint for 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?

3 Total solar energy Conversion efficiency W h = S i c Harvested yield Partitioning efficiency 60% Interception efficiency 90% Monteith (1977) Philosophical Transactions of the Royal Society of London,

4 4.6% 6% Zhu et al (2008) Current Opinion in Biotechnology

5 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

7 How to engineer a higher efficiency? A systems approach!

8 Ru5P Ri5P Xu5P DHAP GAP Pi Pi DHAP Ru5P 10 S7P 9 SBP Pi 8 DHAP E4P 21 F6P Pi 6 FBP 5 GAP DHAP GAP 4 7 Ru5P 12 Xu5P Pi ATP ADPG GAP ADP Starch 23 G1P 22 G6P NADP+Pi PPi ATP 3 25 Pi NADPH +H CO 2 Sink RUBP 1 PGA + PGA 2 DPGA ATP ADP Pi GAP FBP 52 F6P 53 G6P 54 G1P UDPGlu OP F26BP ATP ADP 60 UDP UTP OPOP F6P OP Pi Pi SUCP UDP Model of carbon metabolism PGA OP 57 SUC 62 Sink O PGA ATP GCEA NADH NAD ADP + GLY GCEA HPR GOA SER CO 2 + NADH Stroma 131 Pi O 2 H 2 O 2 GLU KG PGCA GCA GCA GOA 124 GLY 101 GLY + NAD + Cytosol, mitochondria, and peroxisome 101 Drawn based on Zhu et al (2007) Plant Physiology 145:

9 Evolutionary algorithm Zhu et al (2007) Plant Physiol.

10 Raines (2003) Photosynthesis Research 75:1-10

11 Evolution selects for fecundity, not productivity High yield Defense (e.g. insects) Preparation for rare disaster Wild plants Desired crops

12 Global Climatic Change Elevated [CO 2 ] Increased temperature Increased O 3 Altered precipitation pattern

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

13 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 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 primary metabolism b) Modeling the partitioning of photosynthate for building metabolic 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 CO 2, humidity and temperature distributions inside a canopy with realistic 3d architecture d) Modeling reaction diffusion and related physical processes inside a leaf 4. Canopy microenvironments a) Ray tracing algorithm inside a canopy b) Modeling CO 2, humidity and temperature distributions inside a canopy with realistic 3d architecture 5. Photosynthate partitioning The eplant Project

14 Mechanistic model of mesophyll conductance Tholen et al (2012) Plant Physiology; Tholen et al (2012) Plant Cell and Environment

15 Potential Targets to Improve Water Use Efficiency Decrease cell wall thickness Increase stromal CA concentration Increase the permeability of chloroplast envelop to CO 2 Decrease the permeability of chloroplast envelop to HCO 3 -

16 Light inside a canopy is highly heterogeneous both temporarily and spatially

17 See poster P12

Overall C4 systems modeling and design Questions to address: Define key anatomical and biochemical features required for high efficiencies of C4 photosynthesis Identify viable and

18 Overall C4 systems modeling and design Questions to address: Define key anatomical and biochemical features required for high efficiencies of C4 photosynthesis Identify viable and optimal steps to engineer a C4 rice Models to develop Kinetic systems model of C4 photosynthesis Reaction diffusion models for C4 photosynthesis Dynamic systems model of C4 canopy photosynthesis

19 A dynamic systems model of C4 photosynthesis

20 Novel features of the C4 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 photorespiratory metabolism in a cell specific manner, but also incorporates detailed diffusion of metabolites between these two cell types; The metabolite transport between BSCs and MCs was described as a diffusional process through plasmodesmata, and metabolite transport across chloroplast envelope was assumed to follow Michaelis-Menten kinetics; Starch synthesis and breakdown occur at the same time; The electron transfer rate, directly linked to ATP and NADPH synthesis were explicitly modeled.

21 A dynamic systems model of C4 photosynthesis predicts Ac i and AQ curves.

22 Responses of metabolite levels under different Ci

23 Responses of metabolite levels under PPFD levels

24 Key enzymes controlling A-C i responses of C4 photosynthesis

25 Control coefficients for parameters related to C4 photosynthesis Flux Control Coefficient Enzyme V EC Number max Abbreviation (μmol m -2 s -1 High Low ) Low CO light 2 light CA PEPC NADP-ME Rubisco_CO PGAK &GAPDH & SBPase PRK PGAK_M &GAPDH_M M & M Rubisco_O J max I 2000 or Flux Control Coefficient Diffusion parameter Value Low High light Low CO 2 light g m 0.7mol m -2 s -1 bar P mal 42.14μm/s P co μm/s φ L pd 400 nm

26 Necessity of using C4 isoforms in C4 engineering Enzymes Comparison (C3/C4) PEPC NADP-MDH PPDK NADP-ME Rubisco C i =50 mbar CO 2 uptake ratio C i =200 mbar Nitrogen cost ratio

28 Maize leaf gradient (Pick et al. 2011) Cleome gynandra displays age-dependent plasticity of C4 decarboxylation biochemistry (Sommer et al. 2012)

29 Having the mixed pathway does not increase CO 2 uptake rate

30 Having mixed pathway decrease malate levels in BSC and MC

31 The decreased photosynthetic efficiency in a mixture pathway is related to the increased leakage in the system

32 Different combinations of transported four carbon compounds and decarboxylation mechanisms

33 A compromise between efficiency and capacity Assuming only cyclic electron transport occurs in BSC.

34 Leakiness increases by additional C4 pathways Assuming only cyclic electron transport occurs in BSC.

35 Photorespiration rate decreases by additional C4 pathways

36 Can PCK pathway exist alone?

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

38 Increase linear electron transport in BSC increases CO 2 assimilation rate u=v=0 Assuming only cyclic electron transport occurs in BSC u=v=1 Assuming only linear electron transport occurs in BSC

39 The limited access to light by BSC limit the photosynthetic efficiency of the PCK pathway PPFD = 2000 μmol m -2 s -1 PPFD = 300 μmol m -2 s -1 Assuming linear electron transport occurring in BSC X: proportion of light partitioned into mesophyll cells

40 Physiological significance of co-existing decarboxylases A mixture of PEPCK and NADP-ME decrease the quantum yield but increase the capacity of CO 2 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 light accessible by BSC. See poster P31

41 Developing a Reaction Diffusion Model of C4 Leaf Photosynthesis to Explore Anatomical Requirement for C4 Photosynthesis Predicted CO 2 distribution in cells affiliated with a Kranz Structure Red: Reactions implemented in the model

42 A ( mol m -2 s -1 ) Rice chloroplast number needs to be decreased for C4 engineering 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] Ci ( bar)

43 A (umol/(m^2*s)) Increase of carbonic anhydrase concentration can enhance CO 2 assimilation rate in C CA concentration=0.5[mol/m^3] CA concentration=0.27[mol/m^3] CA concentration=0.16[mol/m^3] Ci (ubar)

44 What is the critical step for C4 emergence? Sage and Zhu (2011) Journal of Experimental Botany; Zhu et al (2010) Journal of Integrative Biology

45 Zhu et al (2008) Current Opinion in Biotechnology Christin et al (2008) Current Biology

46 Single Cell C4 system is more efficient than C3 system only under low CO 2 levels

47 Single-cell C4 photosynthesis is a survival strategy under low CO 2 Salvucci and Bowes Plant Physiol. 67, (1981)

48 The Critical Step for Kranz Type C4 photosynthesis ME? ME MC BSC MC BSC

49 Predictions if cellular compartmentation of ME is a critical step during C4 emergence C4 type NADP-ME should appear much later than C4 type PEPC in evolution; After establishment of the C4 cycle, there should be dramatic changes in the redox property and correspondingly the expression of genes related to light reactions; The emergence of C4 species needs anatomical preconditioning to decrease the leakiness to CO 2.

50 PEPC V MDH V ME/PEPCK V PPDK V SSU

51 PEPC V MDH V ME/PEPCK V PPDK V SSU

52 The ds values of the C4 shuttle genes SSU PPDK PEPCK ME ds MDH PEPC

53 rpm rpm rpm rpm rpm rpm rpm rpm rpm rpm rpm rpm rpm Optimization of the light reaction occurred at a late stage of C4 evolution A TC G 00590(b6f com ple x) A T1G 70760(N A D H ) A T1G 74880(N A D H O ) A T2G 39470(P N S L1) A T1G 14150(P N S L2) A T3G 01440(P N S L3) A TC G 00700(P S II) A T4G 37230(P S II) A T1G 60950(Ferredo xin1) A T1G 45474(LH C P S I) A T5G 64040(P S I) A T2G 46820(P S I) A T3G 62410(C P 12) Red: C3 Yellow: C3-C4 Orange: C4-like Blue: C4

55 Conclusions A systems model of C4 photosynthesis with detailed description of the involved biochemical and biophysical processes is developed and there is much space to increase C4 photosynthetic energy conversion efficiency through manipulation of C4 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 malate concentration in the system. PCK pathway can exists alone if there is linear electron transfer in the bundle sheath cells. Proper cellular positioning of decarboxylases might be a critical step during emergence of C4 photosynthesis.

Acknowledgements Yu Wang Danny Tholen Qingfeng Song Yimin Tao Mingzhu Lv Collaborators: C4 Rice Consortium, 3to4 consortium, Global Wheat Yield Consortium,

56 Acknowledgements Yu Wang Danny Tholen Qingfeng Song Yimin Tao Mingzhu Lv 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 Funding: MOST, NSFC, CAS, MPG, Pujiang Plan, SIBS

NOTES: CH 10, part 3 Calvin Cycle (10.3) & Alternative Mechanisms of C-Fixation (10.4)

NOTES: CH 10, part 3 Calvin Cycle (10.3) & Alternative Mechanisms of C-Fixation (10.4) 10.3 - The Calvin cycle uses ATP and NADPH to convert CO 2 to sugar The Calvin cycle, like the citric acid cycle,