Metabolomic response to high light from pgrl1 and pgr5 mutants of Chlamydomonas reinhardtii.
Chlamydomonas reinhardtii
Correlation analysis
Gene expression
High-light stress
Metabolomics
Network analysis
RT-PCR
Journal
Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology
ISSN: 1474-9092
Titre abrégé: Photochem Photobiol Sci
Pays: England
ID NLM: 101124451
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
01
05
2023
accepted:
31
08
2023
medline:
8
11
2023
pubmed:
26
9
2023
entrez:
26
9
2023
Statut:
ppublish
Résumé
Chlamydomonas (C.) reinhardtii metabolomic changes in cyclic electron flow-dependent mutants are still unknown. Here, we used mass spectrometric analysis to monitor the changes in metabolite levels in wild-type, cyclic electron-deficient mutants pgrl1 and pgr5 grown under high-light stress. A total of 55 metabolites were detected using GC-MS analysis. High-light stress-induced selective anaplerotic amino acids in pgr5. In addition, pgr5 showed enhancement in carbohydrate, polyamine, and polyol metabolism by 2.5-fold under high light. In response to high light, pgr5 triggers an increase in several metabolites involved in regulating osmotic pressure. Among these metabolites are glycerol pathway compounds such as glycerol-3-phosphate and glyceryl-glycoside, which increase significantly by 1.55 and 3.07 times, respectively. In addition, pgr5 also enhanced proline and putrescine levels by 2.6- and 1.36-fold under high light. On the other hand, pgrl1-induced metabolites, such as alanine and serine, are crucial for photorespiration when subjected to high-light stress. We also observed a significant increase in levels of polyols and glycerol by 1.37- and 2.97-fold in pgrl1 under high-light stress. Both correlation network studies and KEGG pathway enrichment analysis revealed that metabolites related to several biological pathways, such as amino acid, carbohydrate, TCA cycle, and fatty acid metabolism, were positively correlated in pgrl1 and pgr5 under high-light stress conditions. The relative mRNA expression levels of genes related to the TCA cycle, including PDC3, ACH1, OGD2, OGD3, IDH3, and MDH4, were significantly upregulated in pgrl1 and pgr5 under HL. In pgr5, the MDH1 level was significantly increased, while ACS1, ACS3, IDH2, and IDH3 levels were reduced considerably in pgrl1 under high-light stress. The current study demonstrates both pgr5 and prgl1 showed a differential defense response to high-light stress at the primary metabolites and mRNA expression level, which can be added to the existing knowledge to explore molecular regulatory responses of prg5 and pgrl1 to high-light stress.
Identifiants
pubmed: 37751074
doi: 10.1007/s43630-023-00478-2
pii: 10.1007/s43630-023-00478-2
doi:
Substances chimiques
Photosystem I Protein Complex
0
Glycerol
PDC6A3C0OX
RNA, Messenger
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2635-2650Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR14964/BPA/118/137/2015
Organisme : University Grants Commission
ID : UoH/IoE/RC1/RC1-20-019
Informations de copyright
© 2023. The Author(s), under exclusive licence to European Photochemistry Association, European Society for Photobiology.
Références
Larkum, A. W., Ross, I. L., Kruse, O., & Hankamer, B. (2012). Selection, breeding and engineering of microalgae for bioenergy and biofuel production. Trends in Biotechnology, 30(4), 198–205. https://doi.org/10.1016/j.tibtech.2011.11.003
doi: 10.1016/j.tibtech.2011.11.003
pubmed: 22178650
Scranton, M. A., Ostrand, J. T., Fields, F. J., & Mayfield, S. P. (2015). Chlamydomonas as a model for biofuels and bio-products production. The Plant Journal : For Cell and Molecular Biology, 82(3), 523–531. https://doi.org/10.1111/tpj.12780
doi: 10.1111/tpj.12780
pubmed: 25641390
Chouhan, N., Devadasu, E., Yadav, R. M., & Subramanyam, R. (2022). Autophagy induced accumulation of lipids in pgrl1 and pgr5 of Chlamydomonas reinhardtii under high light. Frontiers in plant science, 12, 752634. https://doi.org/10.3389/fpls.2021.752634
doi: 10.3389/fpls.2021.752634
pubmed: 35145528
pmcid: 8821104
Rastogi, R. P., Madamwar, D., Nakamoto, H., & Incharoensakdi, A. (2020). Resilience and self-regulation processes of microalgae under UV radiation stress. Journal of Photochemistry and Photobiology C: Photochemistry Reviews, 43, 1389–5567.
doi: 10.1016/j.jphotochemrev.2019.100322
Foyer, C. H., & Noctor, G. (2009). Redox regulation in photosynthetic organisms: Signaling, acclimation, and practical implications. Antioxidants & redox signaling, 11(4), 861–905. https://doi.org/10.1089/ars.2008.2177
doi: 10.1089/ars.2008.2177
Wulff-Zottele, C., Gatzke, N., Kopka, J., Orellana, A., Hoefgen, R., Fisahn, J., & Hesse, H. (2010). Photosynthesis and metabolism interact during acclimation of Arabidopsis thaliana to high irradiance and sulphur depletion. Plant, Cell & Environment, 33(11), 1974–1988. https://doi.org/10.1111/j.1365-3040.2010.02199.x
doi: 10.1111/j.1365-3040.2010.02199.x
Post, A. F., Dubinsky, Z., Wyman, K. D., & Falkowski, P. G. (1985). Physiological responses of a marine planktonic diatom to transitions in growth irradiance. Marine EcologyProgress Series, 25, 141–149.
doi: 10.3354/meps025141
Davis, M. C., Fiehn, O., & Durnford, D. G. (2013). Metabolic acclimation to excess light intensity in Chlamydomonas reinhardtii. Plant, Cell & Environment, 36(7), 1391–1405. https://doi.org/10.1111/pce.12071
doi: 10.1111/pce.12071
Kolling, K., Müller, A., Flutsch, P., & Zeeman, S. C. (2013). A device for single leaf labelling with CO
doi: 10.1186/1746-4811-9-45
pubmed: 24252607
pmcid: 4177546
Post, W., Pastor, J., & Zinke, P. (1985). Global patterns of soil nitrogen storage. Nature, 317, 613–616. https://doi.org/10.1038/317613a0
doi: 10.1038/317613a0
Geigenberger, P., & Fernie, A. R. (2014). Metabolic control of redox and redox control of metabolism in plants. Antioxidants & Redox Signalling, 21(9), 1389–1421. https://doi.org/10.1089/ars.2014.6018
doi: 10.1089/ars.2014.6018
Matthew, T., Zhou, W., Rupprecht, J., Lim, L., Thomas-Hall, S. R., Doebbe, A., Kruse, O., Hankamer, B., Marx, U. C., Smith, S. M., & Schenk, P. M. (2009). The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H
doi: 10.1074/jbc.M109.003541
pubmed: 19478077
pmcid: 2749115
Doebbe, A., Keck, M., La Russa, M., Mussgnug, J. H., Hankamer, B., Tekçe, E., Niehaus, K., & Kruse, O. (2010). The interplay of proton, electron, and metabolite supply for photosynthetic H
doi: 10.1074/jbc.M110.122812
pubmed: 20581114
pmcid: 2943295
Renberg, L., Johansson, A. I., Shutova, T., Stenlund, H., Aksmann, A., Raven, J. A., Gardeström, P., Moritz, T., & Samuelsson, G. (2010). A metabolomic approach to study major metabolite changes during acclimation to limiting CO
doi: 10.1104/pp.110.157651
pubmed: 20634393
pmcid: 2938146
Bölling, C., & Fiehn, O. (2005). Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant physiology, 139(4), 1995–2005. https://doi.org/10.1104/pp.105.071589
doi: 10.1104/pp.105.071589
pubmed: 16306140
pmcid: 1310576
Hayat, S., Hayat, Q., Alyemeni, M. N., Wani, A. S., Pichtel, J., & Ahmad, A. (2012). Role of proline under changing environments: A review. Plant Signaling & Behavior, 7(11), 1456–1466. https://doi.org/10.4161/psb.21949
doi: 10.4161/psb.21949
Tolleter, D., Ghysels, B., Alric, J., Petroutsos, D., Tolstygina, I., Krawietz, D., Happe, T., Auroy, P., Adriano, J. M., Beyly, A., Cuiné, S., Plet, J., Reiter, I. M., Genty, B., Cournac, L., Hippler, M., & Peltier, G. (2011). Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. The Plant Cell, 23(7), 2619–2630. https://doi.org/10.1105/tpc.111.086876
doi: 10.1105/tpc.111.086876
pubmed: 21764992
pmcid: 3226202
Terashima, M., Petroutsos, D., Hüdig, M., Tolstygina, I., Trompelt, K., Gäbelein, P., Fufezan, C., Kudla, J., Weinl, S., Finazzi, G., & Hippler, M. (2012). Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proceedings of the National Academy Of Sciences of the United States of America, 109(43), 17717–17722. https://doi.org/10.1073/pnas.1207118109
doi: 10.1073/pnas.1207118109
pubmed: 23045639
pmcid: 3491457
Johnson, X., Steinbeck, J., Dent, R. M., Takahashi, H., Richaud, P., Ozawa, S., Houille-Vernes, L., Petroutsos, D., Rappaport, F., Grossman, A. R., Niyogi, K. K., Hippler, M., & Alric, J. (2014). Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: A study of ΔATpase pgr5 and ΔrbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiology, 165(1), 438–452. https://doi.org/10.1104/pp.113.233593
doi: 10.1104/pp.113.233593
pubmed: 24623849
pmcid: 4012601
Yadav, R. M., Aslam, S. M., Madireddi, S. K., Chouhan, N., & Subramanyam, R. (2020). Role of cyclic electron transport mutations pgrl1 and pgr5 in acclimation process to high light in Chlamydomonas reinhardtii. Photosynthesis Research, 146(1–3), 247–258. https://doi.org/10.1007/s11120-020-00751-w
doi: 10.1007/s11120-020-00751-w
pubmed: 32350701
Dang, K. V., Plet, J., Tolleter, D., Jokel, M., Cuiné, S., Carrier, P., Auroy, P., Richaud, P., Johnson, X., Alric, J., Allahverdiyeva, Y., & Peltier, G. (2014). Combined increases in mitochondrial cooperation and oxygen photoreduction compensate for deficiency in cyclic electron flow in Chlamydomonas reinhardtii. The Plant cell, 26(7), 3036–3050. https://doi.org/10.1105/tpc.114.126375
doi: 10.1105/tpc.114.126375
pubmed: 24989042
pmcid: 4145130
Wase, N., Tu, B., Allen, J. W., Black, P. N., & DiRusso, C. C. (2017). Identification and metabolite profiling of chemical activators of lipid accumulation in green algae. Plant physiology, 174(4), 2146–2165. https://doi.org/10.1104/pp.17.00433
doi: 10.1104/pp.17.00433
pubmed: 28652262
pmcid: 5543952
Gargouri, M., Park, J. J., Holguin, F. O., Kim, M. J., Wang, H., Deshpande, R. R., Shachar-Hill, Y., Hicks, L. M., & Gang, D. R. (2015). Identification of regulatory network hubs that control lipid metabolism in Chlamydomonas reinhardtii. Journal of Experimental Botany, 66(15), 4551–4566. https://doi.org/10.1093/jxb/erv217
doi: 10.1093/jxb/erv217
pubmed: 26022256
pmcid: 4507760
Ajjawi, I., Verruto, J., Aqui, M., Soriaga, L. B., Coppersmith, J., Kwok, K., Peach, L., Orchard, E., Kalb, R., Xu, W., Carlson, T. J., Francis, K., Konigsfeld, K., Bartalis, J., Schultz, A., Lambert, W., Schwartz, A. S., Brown, R., & Moellering, E. R. (2017). Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nature Biotechnology, 35(7), 647–652. https://doi.org/10.1038/nbt.3865
doi: 10.1038/nbt.3865
pubmed: 28628130
Neelam, S., & Subramanyam, R. (2013). Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells. Journal of Photochemical and Photobiology B: Biol., 124, 63–70. https://doi.org/10.1016/j.jphotobiol.2013.04.007
doi: 10.1016/j.jphotobiol.2013.04.007
Schauer, N., Zamir, D., & Fernie, A. R. (2005). Metabolic profiling of leaves and fruit ofwild species tomato: A survey of the Solanum lycopersicum complex. Journal of Experimental Botany, 56(410), 297–307. https://doi.org/10.1093/jxb/eri057
doi: 10.1093/jxb/eri057
pubmed: 15596477
Kundu, A., Mishra, S., & Vadassery, J. (2018). Spodoptera litura-mediated chemical defense is differentially modulated in older and younger systemic leaves of Solanum lycopersicum. Planta, 248(4), 981–997. https://doi.org/10.1007/s00425-018-2953-3
doi: 10.1007/s00425-018-2953-3
pubmed: 29987372
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., & Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1(1), 387–396. https://doi.org/10.1038/nprot.2006.59
doi: 10.1038/nprot.2006.59
pubmed: 17406261
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999
doi: 10.1006/abio.1976.9999
pubmed: 942051
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif.), 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
doi: 10.1006/meth.2001.1262
pubmed: 11846609
Marriboina, S., Sharma, K., Sengupta, D., Yadavalli, A. D., Sharma, R. P., & Reddy Attipalli, R. (2021). Evaluation of high salinity tolerance in Pongamia pinnata (L.) Pierre by a systematic analysis of hormone-metabolic network. Physiologia Plantarum, 173(4), 1514–1534. https://doi.org/10.1111/ppl.13486
doi: 10.1111/ppl.13486
pubmed: 34165187
Voss, I., Sunil, B., Scheibe, R., & Raghavendra, A. S. (2013). Emerging concept for the role of photorespiration as an important part of abiotic stress response. Plant Biology (Stuttgart, Germany), 15(4), 713–722. https://doi.org/10.1111/j.1438-8677.2012.00710.x
doi: 10.1111/j.1438-8677.2012.00710.x
pubmed: 23452019
Timm, S., Florian, A., Wittmiß, M., Jahnke, K., Hagemann, M., Fernie, A. R., & Bauwe, H. (2013). Serine acts as a metabolic signal for the transcriptional control of photorespiration-related genes in Arabidopsis. Plant physiology, 162(1), 379–389. https://doi.org/10.1104/pp.113.215970
doi: 10.1104/pp.113.215970
pubmed: 23471132
pmcid: 3641216
Hossain, M. S., Persicke, M., ElSayed, A. I., Kalinowski, J., & Dietz, K. J. (2017). Metabolite profiling at the cellular and subcellular level reveals metabolites associated with salinity tolerance in sugar beet. Journal of Experimental Botany, 68(21–22), 5961–5976. https://doi.org/10.1093/jxb/erx388
doi: 10.1093/jxb/erx388
pubmed: 29140437
pmcid: 5854137
Ufaz, S., & Galili, G. (2008). Improving the content of essential amino acids in crop plants: Goals and opportunities. Plant Physiology, 147(3), 954–961. https://doi.org/10.1104/pp.108.118091
doi: 10.1104/pp.108.118091
pubmed: 18612072
pmcid: 2442549
Huang, T., & Jander, G. (2017). Abscisic acid-regulated protein degradation causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana. Planta, 246(4), 737–747. https://doi.org/10.1007/s00425-017-2727-3
doi: 10.1007/s00425-017-2727-3
pubmed: 28668976
Hildebrandt, T. M. (2018). Synthesis versus degradation: Directions of amino acid metabolism during Arabidopsis abiotic stress response. Plant molecular biology, 98(1–2), 121–135. https://doi.org/10.1007/s11103-018-0767-0
doi: 10.1007/s11103-018-0767-0
pubmed: 30143990
Szabados, L., & Savoure, A. (2010). Proline: A multifunctional amino acid. Trends in Plant Science, 15(2), 89–97. https://doi.org/10.1016/j.tplants.2009.11.009
doi: 10.1016/j.tplants.2009.11.009
pubmed: 20036181
Ireland, R. J., & Lea, P. J. (1999). The enzymes of glutamine, glutamate, asparagine and aspartate metabolism. In B. Singh (Ed.), Plant amino acids : Biochemistry and biotechnology (pp. 49–109). Marcel Dekker Inc.
Chen, Q., Lan, Y., Li, Q., Kong, M., & Mi, H. (2023). Inactivation of photosynthetic cyclic electron transports upregulates photorespiration for compensation of efficient photosynthesis in Arabidopsis. Frontiers in plant science, 14, 1061434. https://doi.org/10.3389/fpls.2023.1061434
doi: 10.3389/fpls.2023.1061434
pubmed: 37123850
pmcid: 10130413
Johnson, X., & Alric, J. (2013). Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: Metabolic constraints for carbon partitioning between oil and starch. Eukaryotic cell, 12(6), 776–793. https://doi.org/10.1128/EC.00318-12
doi: 10.1128/EC.00318-12
pubmed: 23543671
pmcid: 3675994
De Wulf, P., & Vandamme, E. (2001). Microbial synthesis of D-ribose: screening, metabolic deregulation and fermentation optimisation. In: FAB-Symposium, 15th, Proceedings, part 1, 241–242. http://hdl.handle.net/1854/LU-147421
Bhattacharya, S., & Kundu, A. (2020). Sugars and sugar polyols in overcoming environmental stresses. In: Protective chemical agents in the amelioration of plant abiotic stress: Biochemical and molecular perspectives, 71–101. https://doi.org/10.1002/9781119552154.ch4 .
Debolt, S., Melino, V., & Ford, C. M. (2007). Ascorbate as a biosynthetic precursor in plants. Annals of botany, 99(1), 3–8. https://doi.org/10.1093/aob/mcl236
doi: 10.1093/aob/mcl236
pubmed: 17098753
Foyer, C. H. (2015). Redox homeostasis: Opening up ascorbate transport. Nat. Plants, 1, 14012. https://doi.org/10.1038/nplants.2014.12
doi: 10.1038/nplants.2014.12
pubmed: 27246058
Kytidou, K., Artola, M., Overkleeft, H. S., & Aerts, J. M. F. G. (2020). Plant glycosides and glycosidases: A treasure-trove for therapeutics. Frontiers in plant science, 11, 357. https://doi.org/10.3389/fpls.2020.00357
doi: 10.3389/fpls.2020.00357
pubmed: 32318081
pmcid: 7154165
Ke, J., Behal, R. H., Back, S. L., Nikolau, B. J., Wurtele, E. S., & Oliver, D. J. (2000). The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant physiology, 123(2), 497–508. https://doi.org/10.1104/pp.123.2.497
doi: 10.1104/pp.123.2.497
pubmed: 10859180
pmcid: 59018
Rengel, R., Smith, R. T., Haslam, R. P., Sayanova, O. V., Vila, M., & Leon, R. (2018). Overexpression of acetyl-CoA synthetase (ACS) enhances the biosynthesis of neutral lipids and starch in the green microalga Chlamydomonas reinhardtii. Algal Research., 31, 183–193. https://doi.org/10.1016/j.algal.2018.02.009
doi: 10.1016/j.algal.2018.02.009
You, W., Wei, L., Gong, Y., Hajjami, M. E., Xu, J., & Poetsch, A. (2020). Integration of proteome and transcriptome refines key molecular processes underlying oil production in Nannochloropsis oceanica. Biotechnology for biofuels, 13, 109. https://doi.org/10.1186/s13068-020-01748-2
doi: 10.1186/s13068-020-01748-2
pubmed: 32565907
pmcid: 7302151