henhaobio
Sign in

Science AdvancesPlant BiologyPeer-reviewed journal article

Alternatives to photorespiration: A systems-level analysis reveals mechanisms of enhanced plant productivity

Edward N. SmithiD, Marvin van AalstiD, Andreas P.M. WeberiD, Oliver EbenhöhiD, Matthias HeinemanniD

PDFDOIPreprintCodeData
In-depth full-text digest available · Jump to digest ↓

Abstract

Photorespiration causes a significant decrease in crop yield due to mitochondrial decarboxylation. Alternative pathways (APs) have been designed to relocate the decarboxylating step or even fix additional carbon. To improve the success of transferring those engineered APs from model species to crops we must understand how they will interact with metabolism and how the plant physiology affects their performance. Here we used multiple mathematical modelling techniques to analyse and compare existing AP designs. We show that carbon-fixing APs are the most promising candidates to replace native photorespiration in major crop species. Our results demonstrate the different metabolic routes that APs employ to increase yield and which plant physiology can profit most from them. We anticipate our results to guide the design of new APs and to help improve existing ones. Codehttps://gitlab.com/gain4crops/2024-paper

In-depth summary

Claude Opus 5.5 · xhigh effort · 8 Nov 2026 · from the full text of version 1 (17 Oct 2024) · CC BY 4.0

Modelling 12 alternative photorespiratory pathways predicts the largest carbon-export gains for carbon-fixing designs (TaCo); complete decarboxylation bypasses help mainly by releasing CO2 in chloroplasts, raising carboxylation and recapturing lost CO2.

Photorespiration costs roughly 26 % of fixed CO2 and up to 36 % of yield in some crops, and engineered bypasses have improved plant growth without a clear mechanism, especially for complete decarboxylation routes. Building on earlier models, the work compares 12 bypasses, including newly designed carbon-neutral and carbon-fixing ones, for their combined carbon, ATP/NADPH and subcellular CO2 effects, and offers a CO2-based explanation for decarboxylation benefits that an earlier kinetic model did not predict.

Key results

  1. SuggestedIn flux-balance analysis, a bypass's net CO2 stoichiometry largely sets its photosynthetic energy efficiency: carbon-fixing designs such as tartronyl-CoA (TaCo) gain most and decarboxylating ones lose most. How much NAD(P)H is captured from 2-phosphoglycolate is the second factor.

    CO2 fixed per photon vs wild type (WT), carboxylase:oxygenase fixed at 3:1, glyceraldehyde-3-phosphate sink of 1 μmol s^−1: ranges from +27 % (TaCo) to -54 % (Shen); carbon-neutral Ara5P and Xylulose rank next after TaCo; partial decarboxylation bypasses range from a small gain to near zero; complete decarboxylation bypasses show large losses. · Carbon-fixing APs are more energy efficient

  2. SuggestedComplete decarboxylation bypasses become more energy efficient than native photorespiration only if releasing CO2 in the chloroplast lifts rubisco's carboxylase:oxygenase ratio well above the 3:1 assumed for the wild type.

    FBA scan of the ratio: break-even at 4.8-6.1:1, a 60-103 % increase over 3:1. At 3:1 the complete decarboxylation pathways are less efficient than WT, while bypasses that release 0.5 CO2, are carbon-neutral or fix CO2 stay more efficient even at lower ratios. · Complete decarboxylation pathways require an…

  3. SuggestedRecapturing CO2 that would otherwise leave the cell is worth at most 20 % more carbon export, and the gain falls as the wild type's own refixation rises. Complete decarboxylation bypasses need some residual native photorespiration to come out ahead.

    FBA with photon and CO2 input fixed at WT values (energy- and CO2-limited), ratio 3:1: carbon-fixing, carbon-neutral and partial decarboxylation bypasses all reach the 20 % maximum. With native flux blocked, complete decarboxylation bypasses fix less CO2 than WT at every refixation potential. At about 25 % WT refixation, every design helps when native photorespiration can also carry flux. · Native CO2 refixation capacity affects AP…

  4. SuggestedIn a kinetic ODE model, carbon-fixing bypasses lower rubisco carboxylation yet export the most carbon, because feeding non-CO2 intermediates into the CBB cycle raises the carbon exported per carboxylation. Complete decarboxylation bypasses show the reverse pattern.

    At 400 ppm CO2 and 700 μmol/m^2s, vs WT: carbon-fixing bypasses have carboxylation below 75 %, carbon export around 120 % and carbon-use efficiency around 190 %. Complete decarboxylation bypasses have carboxylation above 125 %, a carboxylase:oxygenase ratio above 200 %, export slightly above 100 % and carbon-use efficiency around 80 %. · Carbon-fixing pathways are more efficient at…

  5. SuggestedPredicted gains depend on conditions. All bypasses help most under high light and restricted CO2 supply, and carbon-neutral designs match or beat carbon-fixing ones in low light. Complete decarboxylation bypasses do worse in low light or when CO2 supply improves.

    Kinetic-model scans: carbon-fixing bypasses reach 125 % of WT export at high light; carbon-neutral ones lead below 400 μmol illumination; complete decarboxylation falls below WT if CO2 transport rises more than 10 %. At 250 μmol/m^2s carbon-fixing and carbon-neutral export are similar; at 90 % of WT CO2 transport, carbon-fixing is best. · APs are most beneficial at low intracellular CO2; High-light increases AP benefit; Environmental conditions require different AP…

Methods, data and reproducibility

Twelve alternative photorespiratory pathways (APs), grouped by CO2 stoichiometry, were compared using three models: a consumer model of ATP, redox and CO2 per regenerated ribulose-1,5-bisphosphate; flux-balance analysis (FBA) of an Arabidopsis leaf core-metabolism model; and a kinetic ODE model of the Calvin-Benson-Bassham (CBB) cycle and photorespiration with dynamic CO2, scanned over light and CO2 supply.

  • PlantCoreMetabolism_v3 stoichiometric model of core leaf metabolism with photosynthetic electron transport and subcellular compartments, curated from PlantCoreMetabolism_v1_2 · Arabidopsis (leaf model)
  • Arabidopsis phloem exudate composition, used to define phloem output fluxes · Arabidopsis
  • Biomass output fluxes as defined in the AraGEM model
  • Prior kinetic models reused: Pettersson 1988 CBB cycle (Poolman 2000 version), Yokota 1985 photorespiration, Witzel 2010 rubisco kinetics, Matuszyńska 2019, Saadat 2021
  • Published refixation estimates of respired and photorespired CO2 (24-38 %), used to set a fixed 25 % refixation in the kinetic model · wheat and rice
Methods & tools
COBRApy, CPLEX, modelbase, eQuilibrator, Python 3, Jupyter notebooks, SBML, PlantCoreMetabolism_v3, AraGEM
Software & environment
Python 3 with COBRApy and the CPLEX solver for FBA; modelbase for the ODE model. Code is provided as Jupyter notebooks and the stoichiometric model as an SBML file.
Reproducibility gaps
No package versions, dependency files or containers are stated beyond Python 3.
Limitations (6)
  • Predictions are best-case: they assume optimal expression and kinetics of the pathway enzymes, and full recapture of CO2 that bypasses release in the chloroplast (the maximum potential benefit). · stated by the authors
  • Some observations remain unexplained. South AP3 in tobacco raises CO2 assimilation even at very high intracellular CO2, and greenhouse tobacco trials gave larger yield gains for complete-decarboxylating South AP3 than for partial South AP1, the opposite of the model ranking. · stated by the authors
  • All bypasses skip the serine-producing steps and could hurt plants with high serine demand. The WT model withdraws only 6 % of photorespiratory carbon as serine, versus 32 % reported for tobacco leaves. · stated by the authors
  • The electron acceptor of the Chlamydomonas reinhardtii glycolate dehydrogenase used in South AP3 is unknown; the models assume it indirectly yields NADH. · stated by the authors
  • No new experiments: all results are model outputs. The kinetic model was assembled from older CBB-cycle and photorespiration models, with enzyme concentrations and export rates adjusted at several steps to carry the required fluxes rather than calibrated against engineered plants. · noted in this summary
  • The top-ranked TaCo pathway has not yet been tested in a photosynthetic organism, and the headline kinetic results show only the best variant per CO2 group. The text does not report how glycolyl-CoA carboxylase variants with futile ATP use (3.9 and 1.7 ATP per reaction for M5 and L100N) compare. · noted in this summary

Read this if you engineer or model photorespiratory bypasses in C3 plants and want a mechanism-level comparison of carbon, ATP/NADPH and chloroplast CO2 effects across 12 pathway designs.

Citations
23
FWCI
6.05
Field percentile
top 2%

Reproducibility ledger

Nobody has reported trying to reproduce this paper yet. Did you replicate an experiment or run the code? Your report saves the next lab a week.

Sign in to file a reproducibility report.

Related papers

Similarity Map
SelectedSame fieldCross-field
THISWieloch '22Petalcorin '25Hernandez '22Jiang '25Dadras '22Vera‐Vives '25
65% semantic matchPlant Biology
T. Wieloch, T. D. Sharkey·bioRxiv·Jan 28, 2022