Aconitase: To Be or not to Be Inside Plant Glyoxysomes, That Is the Question
Abstract
1. Introduction
2. The Glyoxysome Story
3. Aconitase Gene Families in Plants
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Breidenbach, R.W.; Beevers, H. Association of the glyoxylate cycle enzymes in a novel subcellular particle from castor bean endosperm. Biochem. Biophys. Res. Commun. 1967, 27, 462–469. [Google Scholar] [CrossRef]
- Breidenbach, R.W.; Kahn, A.; Beevers, H. Characterization of glyoxysomes from castor bean endosperm. Plant Physiol. 1968, 43, 705–713. [Google Scholar] [CrossRef]
- De Duve, C.; Baudhuin, P. Peroxisomes (microbodies and related particles). Physiol. Rev. 1966, 46, 323–357. [Google Scholar] [CrossRef]
- Cooper, T.G.; Beevers, H. Mitochondria and Glyoxysomes from Castor Bean Endosperm. J. Biol. Chem. 1969, 244, 3507–3513. [Google Scholar] [CrossRef] [PubMed]
- Pracharoenwattana, I.; Smith, S.M. When is a peroxisome not a peroxisome? Trends Plant Sci. 2008, 13, 522–525. [Google Scholar] [CrossRef] [PubMed]
- Courtois-Verniquet, F.; Douce, R. Lack of aconitase in glyoxysomes and peroxisomes. Biochem. J. 1993, 294, 103–107. [Google Scholar] [CrossRef]
- De Bellis, L.; Hayashi, M.; Biagi, P.P.; Hara-Nishimura, I.; Alpi, A.; Nishimura, M. Immunological analysis of aconitase in pumpkin cotyledons: The absence of aconitase in glyoxysomes. Physiol. Plant. 1994, 90, 757–762. [Google Scholar] [CrossRef]
- De Bellis, L.; Hayashi, M.; Nishimura, M.; Alpi, A. Subcellular and developmental changes in distribution of aconitase isoforms in pumpkin cotyledons. Planta 1995, 195, 464–468. [Google Scholar] [CrossRef]
- Hayashi, M.; De Bellis, L.; Alpi, A.; Nishimura, M. Cytosolic Aconitase Participates in the Glyoxylate Cycle in Etiolated Pumpkin Cotyledons. Plant Cell Physiol. 1995, 36, 669–680. [Google Scholar] [CrossRef]
- Maa, Z.; Bykovac, N.V.; Igamberdieva, A.U. Cell signaling mechanisms and metabolic regulation of germination and dormancy in barley seeds. Crop J. 2017, 5, 459–477. [Google Scholar] [CrossRef]
- Dong, H.; Bai, L.; Zhang, Y.; Zhang, G.; Mao, Y.; Min, L.; Xiang, F.; Qian, D.; Zhu, X.; Song, C.P. Modulation of Guard Cell Turgor and Drought Tolerance by a Peroxisomal Acetate-Malate Shunt. Mol. Plant 2018, 11, 1278–1291. [Google Scholar] [CrossRef]
- Sandalio, L.M.; Gotor, C.; Romero, L.C.; Romero-Puertas, M.C. Multilevel Regulation of Peroxisomal Proteome by Post-Translational Modifications. Int. J. Mol. Sci. 2019, 20, 4881. [Google Scholar] [CrossRef]
- Hwang, J.H.; Yu, S.I.; Lee, B.H.; Lee, D.H. Modulation of Energy Metabolism Is Important for Low-Oxygen Stress Adaptation in Brassicaceae Species. Int. J. Mol. Sci. 2020, 21, 1787. [Google Scholar] [CrossRef]
- Hewitt, S.L.; Ghogare, R.; Dhingra, A. Glyoxylic acid overcomes 1-MCP-induced blockage of fruit ripening in Pyrus communis L. var. ‘D’Anjou’. Sci. Rep. 2020, 10, 7084. [Google Scholar] [CrossRef] [PubMed]
- Pan, R.; Liu, J.; Hu, J. Peroxisomes in plant reproduction and seed-related development. J. Integr. Plant Biol. 2019, 61, 784–802. [Google Scholar] [CrossRef] [PubMed]
- Pan, R.; Liu, J.; Wang, S.; Hu, J. Peroxisomes: Versatile organelles with diverse roles in plants. New Phytol. 2020, 225, 1410–1427. [Google Scholar] [CrossRef]
- Schnarrenberger, C.; Oeser, A.; Tolbert, N.E. Development of Microbodies in Sunflower Cotyledons and Castor Bean Endosperm during Germination. Plant Physiol. 1971, 48, 566–574. [Google Scholar] [CrossRef] [PubMed]
- Tolbert, N.E. Microbodies-Peroxisomes and Glyoxysomes. Ann. Rev. Plant Physiol. 1971, 22, 45–74. [Google Scholar] [CrossRef]
- Beevers, H. Microbodies in higher plants. Ann. Rev. Plant Physiol. 1979, 30, 159–193. [Google Scholar] [CrossRef]
- Tolbert, N.E. Metabolic Pathways in Peroxisomes and Glyoxysomes. Ann. Rev. Biochem. 1981, 50, 133–157. [Google Scholar] [CrossRef]
- Beevers, H. Glyoxysomes in higher plants. Ann. N. Y. Acad. Sci. 1982, 386, 243–251. [Google Scholar] [CrossRef]
- Huang, A.H.C.; Trelease, R.N.; Moore, T.S. Plant Peroxisomes, American Society of Plant Physiologists; Academic Press: New York, NY, USA, 1983. [Google Scholar]
- Trelease, R.N. Biogenesis of Glyoxysomes. Ann. Rev. Plant Physiol. 1984, 35, 321–347. [Google Scholar] [CrossRef]
- Gut, H.; Matile, P. Apparent induction of key enzymes of the glyoxylic acid cycle in senescent barley leaves. Planta 1988, 176, 548–550. [Google Scholar] [CrossRef] [PubMed]
- De Bellis, L.; Picciarelli, P.; Pistelli, L.; Alpi, A. Localization of glyoxylate-cycle marker enzymes in peroxisomes of senescent leaves and green cotyledons. Planta 1990, 180, 435–439. [Google Scholar] [CrossRef]
- De Bellis, L.; Tsugeki, R.; Nishimura, M. Glyoxylate cycle enzymes in peroxisomes isolated from petals of pumpkin (Cucurbita sp.) during senescence. Plant Cell Physiol. 1991, 32, 1227–1235. [Google Scholar]
- Pistelli, L.; De Bellis, L.; Alpi, A. Peroxisomal enzyme activities in attached senescing leaves. Planta 1991, 184, 151–153. [Google Scholar] [CrossRef]
- Vicentini, F.; Matile, P. Gerontosomes, a Multifunctional Type of Peroxisome in Senescent Leaves. J. Plant Physiol. 1993, 142, 50–56. [Google Scholar] [CrossRef]
- Nishimura, M.; Takeuchi, Y.; De Bellis, L.; Hara-Nishimura, I. Leaf peroxisomes are directly transformed to glyoxysomes during senescence of pumpkin cotyledons. Protoplasma 1993, 175, 131–137. [Google Scholar] [CrossRef]
- Brouquisse, R.; Gaillard, J.; Douce, R. Electron Paramagnetic Resonance Characterization of Membrane Bound Iron-Sulfur Clusters and Aconitase in Plant Mitochondria. Plant Physiol. 1986, 81, 247–252. [Google Scholar] [CrossRef]
- Brouquisse, R.; Nishimura, M.; Gaillard, J.; Douce, R. Characterization of a Cytosolic Aconitase in Higher Plant Cells. Plant Physiol. 1987, 84, 1402–1407. [Google Scholar] [CrossRef]
- Verniquet, F.; Gaillard, J.; Neoburger, M.; Douce, R. Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem. J. 1991, 276, 643–648. [Google Scholar] [CrossRef] [PubMed]
- De Bellis, L.; Tsugeki, R.; Alpi, A.; Nishimura, M. Purification and characterization of aconitase isoforms from etiolated pumpkin cotyledons. Physiol. Plant. 1993, 88, 485–492. [Google Scholar] [CrossRef]
- Pistelli, L.; De Bellis, L.; Alpi, A. Evidences of glyoxylate cycle in peroxisomes of senescent cotyledons. Plant Sci. 1995, 109, 13–21. [Google Scholar] [CrossRef]
- Arnaud, N.; Ravet, K.; Borlotti, A.; Touraine, B.; Boucherez, J.; Fizames, C.; Briat, J.F.; Cellier, F.; Gaymard, F. The iron-responsive element (IRE)/iron-regulatory protein 1 (IRP1)–cytosolic aconitase iron-regulatory switch does not operate in plants. Biochem. J. 2007, 405, 523–531. [Google Scholar] [CrossRef]
- Hayashi, H.; De Bellis, L.; Ciurli, A.; Kondo, M.; Hayashi, M.; Nishimura, M. A Novel Acyl-CoA Oxidase That Can Oxidize Short-chain Acyl-CoA in Plant Peroxisomes. J. Biol. Chem. 1999, 274, 12715–12721. [Google Scholar] [CrossRef]
- Hayashi, H.; De Bellis, L.; Hayashi, Y.; Nito, K.; Kato, A.; Hayashi, M.; Hara-Nishimura, I.; Nishimura, M. Molecular Characterization of an Arabidopsis Acyl-Coenzyme A Synthetase Localized on Glyoxysomal Membranes. Plant Physiol. 2002, 130, 2019–2026. [Google Scholar] [CrossRef][Green Version]
- Rylott, E.L.; Rogers, C.A.; Gilday, A.D.; Edgell, T.; Larson, T.R.; Graham, I.A. Arabidopsis Mutants in Short- and Medium-chain Acyl-CoA Oxidase Activities Accumulate Acyl-CoAs and Reveal That Fatty Acid β-Oxidation Is Essential for Embryo Development. J. Biol. Chem. 2003, 278, 21370–21377. [Google Scholar] [CrossRef]
- Hayashi, M.; Nishimura, M. Arabidopsis thaliana—A model organism to study plant peroxisomes. Biochim. Biophys. Acta 2006, 1763, 1382–1391. [Google Scholar] [CrossRef]
- Graham, I.A. Seed Storage Oil Mobilization. Annu. Rev. Plant Biol. 2008, 59, 115–142. [Google Scholar] [CrossRef]
- Navarre, D.A.; Wendehenne, D.; Durner, J.; Noad, R.; Klessig, D.F. Nitric Oxide Modulates the Activity of Tobacco Aconitase. Plant Physiol. 2000, 122, 573–582. [Google Scholar] [CrossRef]
- Carrari, F.; Nunes-Nesi, A.; Gibon, Y.; Lytovchenko, A.; Loureiro, M.E.; Fernie, A.R. Reduced Expression of Aconitase Results in an Enhanced Rate of Photosynthesis and Marked Shifts in Carbon Partitioning in Illuminated Leaves of Wild Species Tomato. Plant Physiol. 2003, 133, 1322–1335. [Google Scholar] [CrossRef]
- Moeder, W.; del Pozo, O.; Navarre, D.A.; Martin, G.B.; Klessig, D.F. Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol. Biol. 2007, 63, 273–287. [Google Scholar] [CrossRef] [PubMed]
- Mettler, I.J.; Beevers, H. Oxidation of NADH in glyoxysomes by a malate-aspartate shuttle. Plant Physiol. 1980, 66, 555–560. [Google Scholar] [CrossRef] [PubMed]
- Donaldson, R.P. Nicotinamide cofactors (NAD and NADP) in glyoxysomes, mitochondria and plastids isolated from castor bean endosperm. Arch. Biochem. Biophys. 1982, 215, 274–279. [Google Scholar] [CrossRef]
- van Roermund, C.W.; Elgersma, Y.; Singh, N.; Wanders, R.J.; Tabak, H.F. The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 1995, 14, 3480–3486. [Google Scholar] [CrossRef]
- McAlister-Henn, L.; Steffan, J.S.; Minard, K.I.; Anderson, S.L. Expression and function of a mislocalized form of peroxisomal malate dehydrogenase (MDH3) in yeast. J. Biol. Chem. 1995, 270, 21220–21225. [Google Scholar] [CrossRef]
- Minard, K.I.; McAlister-Henn, L. Isolation, nucleotide sequence analysis, and disruption of the MDH2 gene from Saccharomyces cerevisiae: Evidence for three isozymes of yeast malate dehydrogenase. Mol. Cell. Biol. 1991, 11, 370–380. [Google Scholar] [CrossRef]
- Pracharoenwattana, I.; Cornah, J.E.; Smith, S.M. Arabidopsis peroxisomal malate dehydrogenase functions in β-oxidation but not in the glyoxylate cycle. Plant J. 2007, 50, 381–390. [Google Scholar] [CrossRef]
- Reumann, S. Specification of the peroxisome targeting signals type 1 and type 2 of plant peroxisomes by bioinformatics analyses. Plant Physiol. 2004, 135, 783–800. [Google Scholar] [CrossRef]
- Wang, Y.M.; Yang, Q.; Liu, Y.J.; Yang, H.L. Molecular Evolution and Expression Divergence of the Aconitase (ACO) Gene Family in Land Plants. Front. Plant Sci. 2016, 7, 1879. [Google Scholar] [CrossRef]
- Peyrett, P.; Perez, P.; Alrich, M. Structure, Genomic Organization, and Expression of the Arabidopsis thaliana Aconitase Gene—Plant aconitase show significant homology with mammalian iron-responsive-element-binding protein. J. Biol. Chem. 1995, 270, 8131–8137. [Google Scholar] [CrossRef] [PubMed]
- Millar, A.H.; Sweetlove, L.J.; Giegé, P.; Leaver, C.J. Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 2001, 127, 1711–1727. [Google Scholar] [CrossRef]
- Terol, J.; Soler, G.; Talon, M.; Cercos, M. The aconitate hydratase family from Citrus. BMC Plant Biol. 2010, 10, 222. [Google Scholar] [CrossRef] [PubMed]
- Kruft, V.; Eubel, H.; Jansch, L.; Werhahn, W.; Braun, H.P. Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol. 2001, 127, 1694–1710. [Google Scholar] [CrossRef] [PubMed]
- Heazlewood, J.L.; Tonti-Filippini, J.S.; Gout, A.M.; Day, D.A.; Whelan, J.; Millar, A.H. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 2004, 16, 241–256. [Google Scholar] [CrossRef] [PubMed]
- Cots, J.; Widmer, F. Germination, senescence and pathogenic attack in soybean (Glycine max L.): Identification of the cytosolic aconitase participating in the glyoxylate cycle. Plant Sci. 1999, 149, 95–104. [Google Scholar] [CrossRef]
- Eprintsev, A.T.; Fedorin, D.N.; Cherkasskikh, M.V.; Igamberdiev, A.U. Regulation of expression of the mitochondrial and cytosolic forms of aconitase in maize leaves via phytochrome. Plant Physiol. Biochem. 2020, 146, 157–162. [Google Scholar] [CrossRef]
- Bernard, D.G.; Cheng, Y.; Zhao, Y.; Balk, J. An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol. 2009, 151, 590–602. [Google Scholar] [CrossRef]
- Hooks, M.A.; Allwood, J.W.; Harrison, J.K.; Kopka, J.; Erban, A.; Goodacre, R.; Balk, J. Selective induction and subcellular distribution of ACONITASE 3 reveal the importance of cytosolic citrate metabolism during lipid mobilization in Arabidopsis. Biochem. J. 2014, 463, 309–317. [Google Scholar] [CrossRef]
- Eprintsev, A.T.; Fedorin, D.N.; Nikitina, M.V.; Igamberdiev, A.U. Expression and properties of the mitochondrial and cytosolic forms of aconitase in maize scutellum. J. Plant Physiol. 2015, 181, 14–19. [Google Scholar] [CrossRef]
- Li, Y.; Beisson, F.; Pollard, M.; Ohlrogge, J. Oil content of Arabidopsis seeds: The influence of seed anatomy, light and plant-to-plant variation. Phytochemistry 2006, 67, 904–915. [Google Scholar] [CrossRef] [PubMed]
- Badouin, H.; Gouzy, J.; Grassa, C.J.; Murat, F.; Staton, S.E.; Cottret, L.; Lelandais-Brire, C.; Owens, G.L.; Carrre, S.; Mayjonade, B.; et al. The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature 2017, 546, 148–152. [Google Scholar] [CrossRef] [PubMed]
- ePlant Sunflower. Available online: http://bar.utoronto.ca/eplant_sunflower/ (accessed on 15 May 2020).
- Brito, D.S.; Agrimi, G.; Charton, L.; Brilhaus, D.; Bitetto, M.G.; Lana-Costa, J.; Messina, E.; Nascimento, C.P.; Feitosa-Araújo, E.; Pires, M.V.; et al. Biochemical and functional characterization of a mitochondrial citrate carrier in Arabidopsis thaliana. Biochem. J. 2020, 477, 1759–1777. [Google Scholar] [CrossRef] [PubMed]
Database/Program | ACO1 * (At4g35830) | ACO2 * (At4g26970) | ACO3 * (At2g05710) |
---|---|---|---|
The Plant Proteome Database (https://ppdb.tc.cornell.edu) | mitochondria; cytosol | mitochondria | mitochondria; cytosol |
SUBcellular localisation database for Arabidopsis proteins—SUBA (https://suba.plantenergy.uwa.edu.au) | mitochondria; cytosol | mitochondria | mitochondria |
Protein Localization Database (https://www.rostlab.org/services/locDB/index.php) | mitochondria; cytosol | mitochondria | mitochondria |
Organelle DB (http://labs.mcdb.lsa.umich.edu/organelledb/index.php) | mitochondria | mitochondria | mitochondria |
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De Bellis, L.; Luvisi, A.; Alpi, A. Aconitase: To Be or not to Be Inside Plant Glyoxysomes, That Is the Question. Biology 2020, 9, 162. https://doi.org/10.3390/biology9070162
De Bellis L, Luvisi A, Alpi A. Aconitase: To Be or not to Be Inside Plant Glyoxysomes, That Is the Question. Biology. 2020; 9(7):162. https://doi.org/10.3390/biology9070162
Chicago/Turabian StyleDe Bellis, Luigi, Andrea Luvisi, and Amedeo Alpi. 2020. "Aconitase: To Be or not to Be Inside Plant Glyoxysomes, That Is the Question" Biology 9, no. 7: 162. https://doi.org/10.3390/biology9070162
APA StyleDe Bellis, L., Luvisi, A., & Alpi, A. (2020). Aconitase: To Be or not to Be Inside Plant Glyoxysomes, That Is the Question. Biology, 9(7), 162. https://doi.org/10.3390/biology9070162