A Mass and Charge Balanced Metabolic Model of Setaria Viridis Revealed Mechanisms of Proton Balancing in C4 Plants

Overview

Journal BMC Bioinformatics

Publisher Biomed Central

Specialty Biology

Date 2019 Jun 29

PMID 31248364

Citations 12

Authors

Rahul Shaw

C Y Maurice Cheung

Affiliations

Soon will be listed here.

Abstract

Background: C4 photosynthesis is a key domain of plant research with outcomes ranging from crop quality improvement, biofuel production and efficient use of water and nutrients. A metabolic network model of C4 "lab organism" Setaria viridis with extensive gene-reaction associations can accelerate target identification for desired metabolic manipulations and thereafter in vivo validation. Moreover, metabolic reconstructions have also been shown to be a significant tool to investigate fundamental metabolic traits.

Results: A mass and charge balance genome-scale metabolic model of Setaria viridis was constructed, which was tested to be able to produce all major biomass components in phototrophic and heterotrophic conditions. Our model predicted an important role of the utilization of NH[Formula: see text] and NO[Formula: see text] ratio in balancing charges in plants. A multi-tissue extension of the model representing C4 photosynthesis was able to utilize NADP-ME subtype of C4 carbon fixation for the production of lignocellulosic biomass in stem, providing a tool for identifying gene associations for cellulose, hemi-cellulose and lignin biosynthesis that could be potential target for improved lignocellulosic biomass production. Besides metabolic engineering, our modeling results uncovered a previously unrecognized role of the 3-PGA/triosephosphate shuttle in proton balancing.

Conclusions: A mass and charge balance model of Setaria viridis, a model C4 plant, provides the possibility of system-level investigation to identify metabolic characteristics based on stoichiometric constraints. This study demonstrated the use of metabolic modeling in identifying genes associated with the synthesis of particular biomass components, and elucidating new role of previously known metabolic processes.

Citing Articles

A diel multi-tissue genome-scale metabolic model of Vitis vinifera.

Sampaio M, Rocha M, Dias O PLoS Comput Biol. 2024; 20(10):e1012506.

PMID: 39388487 PMC: 11495577. DOI: 10.1371/journal.pcbi.1012506.

A multi-organ maize metabolic model connects temperature stress with energy production and reducing power generation.

Chowdhury N, Simons-Senftle M, Decouard B, Quillere I, Rigault M, Sajeevan K iScience. 2023; 26(12):108400.

PMID: 38077131 PMC: 10709110. DOI: 10.1016/j.isci.2023.108400.

The first multi-tissue genome-scale metabolic model of a woody plant highlights suberin biosynthesis pathways in Quercus suber.

Cunha E, Silva M, Chaves I, Demirci H, Lagoa D, Lima D PLoS Comput Biol. 2023; 19(9):e1011499.

PMID: 37729340 PMC: 10545120. DOI: 10.1371/journal.pcbi.1011499.

Toward mechanistic modeling and rational engineering of plant respiration.

Wendering P, Nikoloski Z Plant Physiol. 2023; 191(4):2150-2166.

PMID: 36721968 PMC: 10069892. DOI: 10.1093/plphys/kiad054.

Multi-omics intervention in to dissect climate-resilient traits: Progress and prospects.

Aggarwal P, Pramitha L, Choudhary P, Singh R, Shukla P, Prasad M Front Plant Sci. 2022; 13:892736.

PMID: 36119586 PMC: 9470963. DOI: 10.3389/fpls.2022.892736.

References

Josse E, Simkin A, Gaffe J, Laboure A, Kuntz M, Carol P . A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 2000; 123(4):1427-36. PMC: 59099. DOI: 10.1104/pp.123.4.1427. View

Keegstra K, Raikhel N . Plant glycosyltransferases. Curr Opin Plant Biol. 2001; 4(3):219-24. DOI: 10.1016/s1369-5266(00)00164-3. View

Perez J, Munoz-Dorado J, de la Rubia T, Martinez J . Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol. 2002; 5(2):53-63. DOI: 10.1007/s10123-002-0062-3. View

Boerjan W, Ralph J, Baucher M . Lignin biosynthesis. Annu Rev Plant Biol. 2003; 54:519-46. DOI: 10.1146/annurev.arplant.54.031902.134938. View

Csermely P, Agoston V, Pongor S . The efficiency of multi-target drugs: the network approach might help drug design. Trends Pharmacol Sci. 2005; 26(4):178-82. DOI: 10.1016/j.tips.2005.02.007. View

Avenson T, Cruz J, Kanazawa A, Kramer D . Regulating the proton budget of higher plant photosynthesis. Proc Natl Acad Sci U S A. 2005; 102(27):9709-13. PMC: 1172270. DOI: 10.1073/pnas.0503952102. View

Kirkby E, Knight A . Influence of the level of nitrate nutrition on ion uptake and assimilation, organic Acid accumulation, and cation-anion balance in whole tomato plants. Plant Physiol. 1977; 60(3):349-53. PMC: 542614. DOI: 10.1104/pp.60.3.349. View

Gaxiola R, Palmgren M, Schumacher K . Plant proton pumps. FEBS Lett. 2007; 581(12):2204-14. DOI: 10.1016/j.febslet.2007.03.050. View

Gevorgyan A, Poolman M, Fell D . Detection of stoichiometric inconsistencies in biomolecular models. Bioinformatics. 2008; 24(19):2245-51. DOI: 10.1093/bioinformatics/btn425. View

10.

Doust A, Kellogg E, Devos K, Bennetzen J . Foxtail millet: a sequence-driven grass model system. Plant Physiol. 2009; 149(1):137-41. PMC: 2613750. DOI: 10.1104/pp.108.129627. View

11.

Poolman M, Miguet L, Sweetlove L, Fell D . A genome-scale metabolic model of Arabidopsis and some of its properties. Plant Physiol. 2009; 151(3):1570-81. PMC: 2773075. DOI: 10.1104/pp.109.141267. View

12.

Gomes de Oliveira DalMolin C, Quek L, Palfreyman R, Brumbley S, Nielsen L . AraGEM, a genome-scale reconstruction of the primary metabolic network in Arabidopsis. Plant Physiol. 2010; 152(2):579-89. PMC: 2815881. DOI: 10.1104/pp.109.148817. View

13.

Zhu X, Long S, Ort D . Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol. 2010; 61:235-61. DOI: 10.1146/annurev-arplant-042809-112206. View

14.

Orth J, Thiele I, Palsson B . What is flux balance analysis?. Nat Biotechnol. 2010; 28(3):245-8. PMC: 3108565. DOI: 10.1038/nbt.1614. View

15.

Zhu X, Shan L, Wang Y, Quick W . C4 rice - an ideal arena for systems biology research. J Integr Plant Biol. 2010; 52(8):762-70. DOI: 10.1111/j.1744-7909.2010.00983.x. View

16.

Brutnell T, Wang L, Swartwood K, Goldschmidt A, Jackson D, Zhu X . Setaria viridis: a model for C4 photosynthesis. Plant Cell. 2010; 22(8):2537-44. PMC: 2947182. DOI: 10.1105/tpc.110.075309. View

17.

Gomes de Oliveira DalMolin C, Quek L, Palfreyman R, Brumbley S, Nielsen L . C4GEM, a genome-scale metabolic model to study C4 plant metabolism. Plant Physiol. 2010; 154(4):1871-85. PMC: 2996019. DOI: 10.1104/pp.110.166488. View

18.

Byrt C, Grof C, Furbank R . C4 plants as biofuel feedstocks: optimising biomass production and feedstock quality from a lignocellulosic perspective. J Integr Plant Biol. 2011; 53(2):120-35. DOI: 10.1111/j.1744-7909.2010.01023.x. View

19.

Yamamoto H, Peng L, Fukao Y, Shikanai T . An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell. 2011; 23(4):1480-93. PMC: 3101538. DOI: 10.1105/tpc.110.080291. View

20.

Furbank R . Evolution of the C(4) photosynthetic mechanism: are there really three C(4) acid decarboxylation types?. J Exp Bot. 2011; 62(9):3103-8. DOI: 10.1093/jxb/err080. View