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Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress

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Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress

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Sainz, M.; Pérez-Rontomé, C.; Ramos, J.; Mulet Salort, JM.; James, EK.; Bhattacharjee, U.; Petrich, JW.... (2013). Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. The Plant Journal. 76(5):875-887. https://doi.org/10.1111/tpj.12340

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Title: Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress
Author: Sainz, Martha Pérez-Rontomé, Carmen Ramos, Javier Mulet Salort, José Miguel James, Euan K. Bhattacharjee, Ujjal Petrich, Jacob W. Becana, Manuel
UPV Unit: Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia
Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes
Issued date:
Abstract:
The heme of bacteria, plant and animal hemoglobins (Hbs) must be in the ferrous state to bind O2 and other physiological ligands. Here we have characterized the full set of non-symbiotic (class 1 and 2) and truncated ...[+]
Subjects: Lotus japonicus , Plant hemoglobins , Flavins , Legume nodules , Nitrosative stress , Oxidative stress
Copyrigths: Reserva de todos los derechos
Source:
The Plant Journal. (issn: 0960-7412 ) (eissn: 1365-313X )
DOI: 10.1111/tpj.12340
Publisher:
Wiley-Blackwell
Publisher version: http://dx.doi.org/10.1111/tpj.12340
Project ID:
info:eu-repo/grantAgreement/MICINN//AGL2011-24524/ES/SEÑALIZACION POR ESPECIES REACTIVAS DE OXIGENO%2FNITROGENO Y ANTIOXIDANTES EN LA SIMBIOSIS FIJADORA DE NITROGENO RHIZOBIUM-LEGUMINOSA/
Government of Aragon/Fondo Social Europeo [A53]
Junta de Ampliacion de Estudios/Consejo Superior de Investigaciones Cientificas
Description: This is the accepted version of the following article: Sainz, M., Pérez-Rontomé, C., Ramos, J., Mulet, J. M., James, E. K., Bhattacharjee, U., Petrich, J. W. and Becana, M. (2013), Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. Plant J, 76: 875–887, which has been published in final form at http://dx.doi.org/10.1111/tpj.12340.
Thanks:
We are grateful to Ryan Sturms and Mark Hargrove (Department of Biochemistry and Molecular Biology, Iowa State University, Ames, IA) for help with stopped-flow measurements, and to Raul Arredondo-Peter (Laboratorio de ...[+]
Type: Artículo

References

Angelo, M., Hausladen, A., Singel, D. J., & Stamler, J. S. (2008). Interactions of NO with Hemoglobin: From Microbes to Man. Globins and Other Nitric Oxide-Reactive Proteins, Part A, 131-168. doi:10.1016/s0076-6879(08)36008-x

Appleby, C. A. (1984). Leghemoglobin and Rhizobium Respiration. Annual Review of Plant Physiology, 35(1), 443-478. doi:10.1146/annurev.pp.35.060184.002303

Baudouin, E. (2003). A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules. Journal of Experimental Botany, 55(394), 43-47. doi:10.1093/jxb/erh020 [+]
Angelo, M., Hausladen, A., Singel, D. J., & Stamler, J. S. (2008). Interactions of NO with Hemoglobin: From Microbes to Man. Globins and Other Nitric Oxide-Reactive Proteins, Part A, 131-168. doi:10.1016/s0076-6879(08)36008-x

Appleby, C. A. (1984). Leghemoglobin and Rhizobium Respiration. Annual Review of Plant Physiology, 35(1), 443-478. doi:10.1146/annurev.pp.35.060184.002303

Baudouin, E. (2003). A Medicago sativa haem oxygenase gene is preferentially expressed in root nodules. Journal of Experimental Botany, 55(394), 43-47. doi:10.1093/jxb/erh020

Becana, M., & Klucas, R. V. (1990). Enzymatic and nonenzymatic mechanisms for ferric leghemoglobin reduction in legume root nodules. Proceedings of the National Academy of Sciences, 87(18), 7295-7299. doi:10.1073/pnas.87.18.7295

Becana, M., Matamoros, M. A., Udvardi, M., & Dalton, D. A. (2010). Recent insights into antioxidant defenses of legume root nodules. New Phytologist, 188(4), 960-976. doi:10.1111/j.1469-8137.2010.03512.x

Bruno, S., Faggiano, S., Spyrakis, F., Mozzarelli, A., Abbruzzetti, S., Grandi, E., … Dominici, P. (2007). The Reactivity with CO of AHb1 and AHb2 fromArabidopsisthalianais Controlled by the Distal HisE7 and Internal Hydrophobic Cavities. Journal of the American Chemical Society, 129(10), 2880-2889. doi:10.1021/ja066638d

Bustos-Sanmamed, P., Tovar-Méndez, A., Crespi, M., Sato, S., Tabata, S., & Becana, M. (2010). Regulation of nonsymbiotic and truncated hemoglobin genes of Lotus japonicus in plant organs and in response to nitric oxide and hormones. New Phytologist, 189(3), 765-776. doi:10.1111/j.1469-8137.2010.03527.x

Bykova, N. V., Igamberdiev, A. U., Ens, W., & Hill, R. D. (2006). Identification of an intermolecular disulfide bond in barley hemoglobin. Biochemical and Biophysical Research Communications, 347(1), 301-309. doi:10.1016/j.bbrc.2006.06.091

Cochemé, H. M., & Murphy, M. P. (2007). Complex I Is the Major Site of Mitochondrial Superoxide Production by Paraquat. Journal of Biological Chemistry, 283(4), 1786-1798. doi:10.1074/jbc.m708597200

Dalton, D. A., Baird, L. M., Langeberg, L., Taugher, C. Y., Anyan, W. R., Vance, C. P., & Sarath, G. (1993). Subcellular Localization of Oxygen Defense Enzymes in Soybean (Glycine max [L.] Merr.) Root Nodules. Plant Physiology, 102(2), 481-489. doi:10.1104/pp.102.2.481

DORDAS, C. (2003). Plant Haemoglobins, Nitric Oxide and Hypoxic Stress. Annals of Botany, 91(2), 173-178. doi:10.1093/aob/mcf115

Duff, S. M. G., Wittenberg, J. B., & Hill, R. D. (1997). Expression, Purification, and Properties of Recombinant Barley (Hordeumsp.) Hemoglobin. Journal of Biological Chemistry, 272(27), 16746-16752. doi:10.1074/jbc.272.27.16746

Folta, K. M., & Kaufman, L. S. (2000). Preparation of transcriptionally active nuclei from etiolated Arabidopsis thaliana. Plant Cell Reports, 19(5), 504-510. doi:10.1007/s002990050764

Gardner, P. R. (2012). Hemoglobin: A Nitric-Oxide Dioxygenase. Scientifica, 2012, 1-34. doi:10.6064/2012/683729

Daniel Gietz, R., & Woods, R. A. (2002). Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods in Enzymology, 87-96. doi:10.1016/s0076-6879(02)50957-5

Gladwin, M. T., Ognibene, F. P., Pannell, L. K., Nichols, J. S., Pease-Fye, M. E., Shelhamer, J. H., & Schechter, A. N. (2000). Relative role of heme nitrosylation and beta -cysteine 93 nitrosation in the transport and metabolism of nitric oxide by hemoglobin in the human circulation. Proceedings of the National Academy of Sciences, 97(18), 9943-9948. doi:10.1073/pnas.180155397

Gupta, K. J., Fernie, A. R., Kaiser, W. M., & van Dongen, J. T. (2011). On the origins of nitric oxide. Trends in Plant Science, 16(3), 160-168. doi:10.1016/j.tplants.2010.11.007

Hargrove, M. S. (2000). A Flash Photolysis Method to Characterize Hexacoordinate Hemoglobin Kinetics. Biophysical Journal, 79(5), 2733-2738. doi:10.1016/s0006-3495(00)76512-x

Hebelstrup, K. H., & Jensen, E. Ø. (2007). Expression of NO scavenging hemoglobin is involved in the timing of bolting in Arabidopsis thaliana. Planta, 227(4), 917-927. doi:10.1007/s00425-007-0667-z

Hebelstrup, K. H., Igamberdiev, A. U., & Hill, R. D. (2007). Metabolic effects of hemoglobin gene expression in plants. Gene, 398(1-2), 86-93. doi:10.1016/j.gene.2007.01.039

Hebelstrup, K. H., Shah, J. K., & Igamberdiev, A. U. (2013). The role of nitric oxide and hemoglobin in plant development and morphogenesis. Physiologia Plantarum, 148(4), 457-469. doi:10.1111/ppl.12062

Hill, R. D. (2012). Non-symbiotic haemoglobins—What’s happening beyond nitric oxide scavenging? AoB PLANTS, 2012. doi:10.1093/aobpla/pls004

Hunt, P. W., Watts, R. A., Trevaskis, B., Llewelyn, D. J., Burnell, J., Dennis, E. S., & Peacock, W. J. (2001). Plant Molecular Biology, 47(5), 677-692. doi:10.1023/a:1012440926982

Hunt, P. W., Klok, E. J., Trevaskis, B., Watts, R. A., Ellis, M. H., Peacock, W. J., & Dennis, E. S. (2002). Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 99(26), 17197-17202. doi:10.1073/pnas.212648799

Igamberdiev, A. U., Bykova, N. V., & Hill, R. D. (2005). Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta, 223(5), 1033-1040. doi:10.1007/s00425-005-0146-3

Igamberdiev, A. U., Bykova, N. V., Shah, J. K., & Hill, R. D. (2010). Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiologia Plantarum, 138(4), 393-404. doi:10.1111/j.1399-3054.2009.01314.x

Ioanitescu, A. I., Dewilde, S., Kiger, L., Marden, M. C., Moens, L., & Van Doorslaer, S. (2005). Characterization of Nonsymbiotic Tomato Hemoglobin. Biophysical Journal, 89(4), 2628-2639. doi:10.1529/biophysj.105.060582

Kakar, S., Hoffman, F. G., Storz, J. F., Fabian, M., & Hargrove, M. S. (2010). Structure and reactivity of hexacoordinate hemoglobins. Biophysical Chemistry, 152(1-3), 1-14. doi:10.1016/j.bpc.2010.08.008

Kim, D. Y., Hong, M. J., Lee, Y. J., Lee, M. B., & Seo, Y. W. (2012). Wheat truncated hemoglobin interacts with photosystem I PSK-I subunit and photosystem II subunit PsbS1. Biologia Plantarum, 57(2), 281-290. doi:10.1007/s10535-012-0268-y

Lee, H., Kim, H., & An, C. S. (2004). Cloning and expression analysis of 2-on-2 hemoglobin from soybean. Journal of Plant Biology, 47(2), 92-98. doi:10.1007/bf03030637

Miyake, C., Schreiber, U., Hormann, H., Sano, S., & Kozi, A. (1998). The FAD-Enzyme Monodehydroascorbate Radical Reductase Mediates Photoproduction of Superoxide Radicals in Spinach Thylakoid Membranes. Plant and Cell Physiology, 39(8), 821-829. doi:10.1093/oxfordjournals.pcp.a029440

Moran, J. F., Sun, Z., Sarath, G., Arredondo-Peter, R., James, E. K., Becana, M., & Klucas, R. V. (2002). Molecular Cloning, Functional Characterization, and Subcellular Localization of Soybean Nodule Dihydrolipoamide Reductase. Plant Physiology, 128(1), 300-313. doi:10.1104/pp.010505

Mulet, J. M., Alemany, B., Ros, R., Calvete, J. J., & Serrano, R. (2004). Expression of a plant serine O-acetyltransferase inSaccharomyces cerevisiae confers osmotic tolerance and creates an alternative pathway for cysteine biosynthesis. Yeast, 21(4), 303-312. doi:10.1002/yea.1076

Mur, L. A. J., Mandon, J., Persijn, S., Cristescu, S. M., Moshkov, I. E., Novikova, G. V., … Gupta, K. J. (2012). Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants, 5(0), pls052-pls052. doi:10.1093/aobpla/pls052

Pankhurst, C. E., Schwinghamer, E. A., Thorne, S. W., & Bergersen, F. J. (1974). The Flavin Content of Clovers Relative to Symbiosis with a Riboflavin-requiring Mutant of Rhizobium trifoli. Plant Physiology, 53(2), 198-205. doi:10.1104/pp.53.2.198

Perazzolli, M., Dominici, P., Romero-Puertas, M. C., Zago, E., Zeier, J., Sonoda, M., … Delledonne, M. (2004). Arabidopsis Nonsymbiotic Hemoglobin AHb1 Modulates Nitric Oxide Bioactivity. The Plant Cell, 16(10), 2785-2794. doi:10.1105/tpc.104.025379

Qu, Z.-L., Wang, H.-Y., & Xia, G.-X. (2005). GhHb1: A nonsymbiotic hemoglobin gene of cotton responsive to infection by Verticillium dahliae. Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, 1730(2), 103-113. doi:10.1016/j.bbaexp.2005.06.009

Ríos, G., Cabedo, M., Rull, B., Yenush, L., Serrano, R., & Mulet, J. M. (2013). Role of the yeast multidrug transporter Qdr2 in cation homeostasis and the oxidative stress response. FEMS Yeast Research, 13(1), 97-106. doi:10.1111/1567-1364.12013

Rodríguez-Celma, J., Vázquez-Reina, S., Orduna, J., Abadía, A., Abadía, J., Álvarez-Fernández, A., & López-Millán, A.-F. (2011). Characterization of Flavins in Roots of Fe-Deficient Strategy I Plants, with a Focus on Medicago truncatula. Plant and Cell Physiology, 52(12), 2173-2189. doi:10.1093/pcp/pcr149

Ross, E. J. H., Shearman, L., Mathiesen, M., Zhou, Y. J., Arredondo-Peter, R., Sarath, G., & Klucas, R. V. (2001). Nonsymbiotic hemoglobins in rice are synthesized during germination and in differentiating cell types. Protoplasma, 218(3-4), 125-133. doi:10.1007/bf01306602

Rubio, M. C., Becana, M., Kanematsu, S., Ushimaru, T., & James, E. K. (2009). Immunolocalization of antioxidant enzymes in high-pressure frozen root and stem nodules of Sesbania rostrata. New Phytologist, 183(2), 395-407. doi:10.1111/j.1469-8137.2009.02866.x

Seregélyes, C., Mustárdy, L., Ayaydin, F., Sass, L., Kovács, L., Endre, G., … Dudits, D. (2000). Nuclear localization of a hypoxia-inducible novel non-symbiotic hemoglobin in cultured alfalfa cells1. FEBS Letters, 482(1-2), 125-130. doi:10.1016/s0014-5793(00)02049-4

Smagghe, B. J., Blervacq, A.-S., Blassiau, C., Decottignies, J.-P., Jacquot, J.-P., Hargrove, M. S., & Hilbert, J.-L. (2007). Immunolocalization of Non-Symbiotic Hemoglobins During Somatic Embryogenesis in Chicory. Plant Signaling & Behavior, 2(1), 43-49. doi:10.4161/psb.2.1.3812

Smagghe, B. J., Hoy, J. A., Percifield, R., Kundu, S., Hargrove, M. S., Sarath, G., … Appleby, C. A. (2009). Review: Correlations between oxygen affinity and sequence classifications of plant hemoglobins. Biopolymers, 91(12), 1083-1096. doi:10.1002/bip.21256

Spyrakis, F., Bruno, S., Bidon-Chanal, A., Luque, F. J., Abbruzzetti, S., Viappiani, C., … Mozzarelli, A. (2011). Oxygen binding to Arabidopsis thaliana AHb2 nonsymbiotic hemoglobin: evidence for a role in oxygen transport. IUBMB Life, 63(5), 355-362. doi:10.1002/iub.470

Sturms, R., Kakar, S., Trent, J., & Hargrove, M. S. (2010). TremaandParasponiaHemoglobins Reveal Convergent Evolution of Oxygen Transport in Plants. Biochemistry, 49(19), 4085-4093. doi:10.1021/bi1002844

Taylor, E. R., Nie, X. Z., MacGregor, A. W., & Hill, R. D. (1994). A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Molecular Biology, 24(6), 853-862. doi:10.1007/bf00014440

Trent, J. T., Watts, R. A., & Hargrove, M. S. (2001). Human Neuroglobin, a Hexacoordinate Hemoglobin That Reversibly Binds Oxygen. Journal of Biological Chemistry, 276(32), 30106-30110. doi:10.1074/jbc.c100300200

Trevaskis, B., Watts, R. A., Andersson, C. R., Llewellyn, D. J., Hargrove, M. S., Olson, J. S., … Peacock, W. J. (1997). Two hemoglobin genes in Arabidopsis thaliana: The evolutionary origins of leghemoglobins. Proceedings of the National Academy of Sciences, 94(22), 12230-12234. doi:10.1073/pnas.94.22.12230

Uchiumi, T., Shimoda, Y., Tsuruta, T., Mukoyoshi, Y., Suzuki, A., Senoo, K., … Abe, M. (2002). Expression of Symbiotic and Nonsymbiotic Globin Genes Responding to Microsymbionts on Lotus japonicus. Plant and Cell Physiology, 43(11), 1351-1358. doi:10.1093/pcp/pcf165

Vieweg, M. F., Hohnjec, N., & K�ster, H. (2004). Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta, 220(5), 757-766. doi:10.1007/s00425-004-1397-0

Vigeolas, H., Hühn, D., & Geigenberger, P. (2011). Nonsymbiotic Hemoglobin-2 Leads to an Elevated Energy State and to a Combined Increase in Polyunsaturated Fatty Acids and Total Oil Content When Overexpressed in Developing Seeds of Transgenic Arabidopsis Plants. Plant Physiology, 155(3), 1435-1444. doi:10.1104/pp.110.166462

Vinogradov, S. N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Guertin, M., Gough, J., … Vanfleteren, J. R. (2005). Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life. Proceedings of the National Academy of Sciences, 102(32), 11385-11389. doi:10.1073/pnas.0502103102

Wang, Y., Elhiti, M., Hebelstrup, K. H., Hill, R. D., & Stasolla, C. (2011). Manipulation of hemoglobin expression affects Arabidopsis shoot organogenesis. Plant Physiology and Biochemistry, 49(10), 1108-1116. doi:10.1016/j.plaphy.2011.06.005

Watts, R. A., Hunt, P. W., Hvitved, A. N., Hargrove, M. S., Peacock, W. J., & Dennis, E. S. (2001). A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proceedings of the National Academy of Sciences, 98(18), 10119-10124. doi:10.1073/pnas.191349198

Weber, R. E., & Vinogradov, S. N. (2001). Nonvertebrate Hemoglobins: Functions and Molecular Adaptations. Physiological Reviews, 81(2), 569-628. doi:10.1152/physrev.2001.81.2.569

Zhang, L., Onda, K., Imai, R., Fukuda, R., Horiuchi, H., & Ohta, A. (2003). Growth temperature downshift induces antioxidant response in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications, 307(2), 308-314. doi:10.1016/s0006-291x(03)01168-9

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