Plant Biol (Stuttg) 2007; 9(6): 776-785
DOI: 10.1055/s-2007-965258
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Truncated Hemoglobins in Actinorhizal Nodules of Datisca glomerata

K. Pawlowski1 , 2 , 6 , K. R. Jacobsen3 , N. Alloisio4 , R. Ford Denison3 , 7 , M. Klein3 , 8 , J. D. Tjepkema5 , T. Winzer1 , A. Sirrenberg1 , 9 , C. Guan2 , 10 , A. M. Berry3
  • 1Albrecht von Haller Institute for Plant Sciences, Department of Plant Biochemistry, Göttingen University, 37077 Göttingen, Germany
  • 2Department of Molecular Biology, Wageningen University, 6703 HA Wageningen, The Netherlands
  • 3Department of Plant Sciences, University of California, Davis, CA 95616, USA
  • 4Laboratoire d'Ecologie Microbienne, UMR CNRS 5557, Université Claude Bernard Lyon 1, 69622 Villeurbanne Cedex, France
  • 5Department of Biological Sciences, University of Maine, Orono, ME 04469-5722, USA
  • 6Present address: Department of Botany, Stockholm University, 10691 Stockholm, Sweden
  • 7Present address: Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108, USA
  • 8Present address: Department of Plant Biology, Cornell University, Ithaca, NY 14850, USA
  • 9Present address: Molecular Phytopathology, Göttingen University, 37077 Göttingen, Germany
  • 10Present address: Department of Plant Pathology, University of Wisconsin-Madison, Madison, WI 53706, USA
Further Information

Publication History

Received: November 2, 2006

Accepted: March 28, 2007

Publication Date:
07 August 2007 (online)

Abstract

Three types of hemoglobins exist in higher plants, symbiotic, non-symbiotic, and truncated hemoglobins. Symbiotic (class II) hemoglobins play a role in oxygen supply to intracellular nitrogen-fixing symbionts in legume root nodules, and in one case (Parasponia sp.), a non-symbiotic (class I) hemoglobin has been recruited for this function. Here we report the induction of a host gene, dgtrHb1, encoding a truncated hemoglobin in Frankia-induced nodules of the actinorhizal plant Datisca glomerata. Induction takes place specifically in cells infected by the microsymbiont, prior to the onset of bacterial nitrogen fixation. A bacterial gene (Frankia trHbO) encoding a truncated hemoglobin with O2-binding kinetics suitable for the facilitation of O2 diffusion ([Tjepkema et al., 2002]) is also expressed in symbiosis. Nodule oximetry confirms the presence of a molecule that binds oxygen reversibly in D. glomerata nodules, but indicates a low overall hemoglobin concentration suggesting a local function. Frankia TrHbO is likely to be responsible for this activity. The function of the D. glomerata truncated hemoglobin is unknown; a possible role in nitric oxide detoxification is suggested.

References

  • 1 Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J.. Basic local alignment search tool.  Journal of Molecular Biology. (1990);  215 403-410
  • 2 Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J.. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.  Nucleic Acids Research. (1997);  25 3389-3402
  • 3 Andersson C. R., Llewellyn D. J., Peacock W. J., Dennis E. S.. Cell-specific expression of the promoters of two nonlegume hemoglobin genes in a transgenic legume, Lotus corniculatus.  Plant Physiology. (1997);  113 45-57
  • 4 Appleby C. A.. Leghemoglobin and Rhizobium respiration.  Annual Review of Plant Physiology and Plant Molecular Biology. (1984);  35 443-478
  • 5 Appleby C. A.. The origin and functions of haemoglobin in plants.  Science Progress. (1992);  76 365-398
  • 6 Barnett M. J., Fisher R. F., Jones T., Komp C., Abola A. P., Barloy-Hubler F., Bowser L., Capela D., Galibert F., Gouzy J., Gurjal M., Hong A., Huizar L., Hyman R. W., Kahn D., Kahn M. L., Kalman S., Keating D. H., Palm C., Peck M. C., Surzycki R., Wells D. H., Yeh K. C., Davis R. W., Federspiel N. A., Long S. R.. Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 9883-9888
  • 7 Beckwith J., Tjepkema J. D., Cashon R. E., Schwintzer C. R., Tisa L. S.. Hemoglobin in five genetically diverse Frankia strains.  Canadian Journal of Microbiology. (2002);  48 1048-1055
  • 8 Berg R. H., McDowell L.. Endophyte differentiation in Casuarina actinorhizae.  Protoplasma. (1987);  136 104-117
  • 9 Berg R. H., McDowell L.. Cytochemistry of the wall of infected Casuarina actinorhizae.  Canadian Journal of Botany. (1988);  66 2038-2047
  • 10 Berg R. H., Langenstein B., Silvester W. B.. Development in the D. glomerata-Coriaria nodule type.  Canadian Journal of Botany. (1999);  77 1334-1350
  • 11 Berry A. M., Harriott O. T., Moreau R. A., Osman S. F., Benson D. R., Jones A. D.. Hopanoid lipids compose the Frankia vesicle envelope, presumptive barrier of oxygen diffusion to nitrogenase.  Proceedings of the National Academy of Sciences of the USA. (1993);  90 6091-6094
  • 12 Cheng J., Hipkin C. R., Gallon J. R.. Effects of inorganic nitrogen compounds on the activity and synthesis of nitrogenase in Gloeothece (Nägeli) sp. ATCC 27152.  New Phytologist. (1999);  141 61-70
  • 13 Clawson M. L., Bourret A., Benson D. R.. Assessing the phylogeny of Frankia-actinorhizal plant nitrogen-fixing root nodule symbioses with Frankia 16S rRNA and glutamine synthetase gene sequences.  Molecular Phylogenetics and Evolution. (2004);  31 131-138
  • 14 Corpet F., Gouzy J., Kahn D.. The ProDom database of protein domain families.  Nucleic Acids Research. (1998);  26 323-326
  • 15 Correa-Aragunde N., Graziano M., Lamattina L.. Nitric oxide plays a central role in determining lateral root development in tomato.  Planta. (2004);  218 900-905
  • 16 Cueto M., Hernández-Perera O., Martín R., Bentura M. L., Rodrigo J., Lamas S., Golvano M. P.. Presence of nitric oxide synthase activity in roots and root nodules of Lupinus albus. .  FEBS Letters. (1996);  398 159-164
  • 17 Denison R. F., Layzell D. B.. Measurement of legume nodule respiration and O2 permeability by noninvasive spectrophotometry of leghemoglobin.  Plant Physiology. (1991);  96 137-143
  • 18 Denison R. F., Hunt S., Layzell D. B.. Nitrogenase activity, nodule respiration, and O2 permeability following detopping of alfalfa and birdsfoot trefoil.  Plant Physiology. (1992 a);  98 894-900
  • 19 Denison R. F., Witty J. F., Minchin F. R.. Reversible O2 inhibition of nitrogenase activity in attached soybean nodules.  Plant Physiology. (1992 b);  100 1863-1868
  • 20 Dordas C., Rivoal J., Hill R. D.. Plant haemoglobins, nitric oxide and hypoxic stress.  Annals of Botany. (2003);  91 173-178
  • 21 Elvers K. T., Wu G., Gilberthorpe N. J., Poole R. K., Park S. F.. Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli.  Journal of Bacteriology. (2004);  186 5332-5341
  • 22 Fabozzi G., Ascenzi P., Renzi S. D., Visca P.. Truncated hemoglobin GlbO from Mycobacterium leprae alleviates nitric oxide toxicity.  Microbial Pathogenesis. (2006);  40 211-220
  • 23 Ferguson B. J., Mathesius U.. Signaling interactions during nodule development.  Journal of Plant Growth Regulation. (2004);  22 47-72
  • 24 Galibert F., Finan T. M., Long S. R., Pühler A., Abola P., Ampe F., Barloy-Hubler F., Barnett M. J., Becker A., Boistard P., Bothe G., Boutry M., Bowser L., Buhrmester J., Cadieu E., Capela D., Chain P., Cowie A., Davis R. W., Dreano S., Federspiel N. A., Fisher R. F., Gloux S., Godrie T., Goffeau A., Golding B., Gouzy J., Gurjal M., Hernandez-Lucas I., Hong A., Huizar L., Hyman R. W., Jones T., Kahn D., Kahn M. L., Kalman S., Keating D. H., Kiss E., Komp C., Lelaure V., Masuy D., Palm C., Peck M. C., Pohl T. M., Portetelle D., Purnelle B., Ramsperger U., Surzycki R., Thebault P., Vandenbol M., Vorholter F. J., Weidner S., Wells D. H., Wong K., Yeh K. C., Batut J.. The composite genome of the legume symbiont Sinorhizobium meliloti. .  Science. (2001);  293 668-672
  • 25 Gherbi H., Duhoux E., Franche C., Pawlowski K., Berry A. M., Bogusz D.. Cloning of a full-length symbiotic hemoglobin cDNA and in situ localization of the corresponding mRNA in Casuarina glauca root nodule.  Physiologia Plantarum. (1997);  99 608-616
  • 26 Gish W., States D. J.. Identification of protein coding regions by database similarity search.  Nature Genetics. (1993);  3 266-272
  • 27 Guo F. Q., Okamoto M., Crawford N. M.. Identification of a plant nitric oxide synthase gene involved in hormonal signaling.  Science. (2003);  302 100-103
  • 28 Hafeez F., Akkermans A. D. L., Chaudhary A. H.. Observations on the ultrastructure of Frankia sp. in root nodules of Datisca cannabina L.  Plant and Soil. (1984);  79 383-402
  • 29 Harris S., Silvester W. B.. Acetylene-induced and argon-induced declines in nitrogenase activity in Coriaria arborea. .  Soil Biology and Biochemistry. (1994);  26 641-648
  • 30 Herold S., Puppo A.. Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules?.  Journal of Biological Inorganic Chemistry. (2005);  10 935-945
  • 31 Hoagland D. R., Arnon D. T.. The water-culture method for growing plants without soil. California Agriculture Experimental Station Circular 347. (1938)
  • 32 Hunt P. W., Watts R. A., Trevaskis B., Llewelyn D. J., Burnell J., Dennis E. S., Peacock W. J.. Expression and evolution of functionally distinct haemoglobin genes in plants.  Plant Molecular Biology. (2001);  47 677-692
  • 33 Hunt P. W., Klok E. J., Trevaskis B., Watts R. A., Ellis M. H., Peacock W. J., Dennis E. S.. Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. .  Proceedings of the National Academy of Sciences of the USA. (2002);  99 17197-17202
  • 34 Jackson D.. In situ hybridization in plants. Bowles, D. J., Gurr, S. F., and McPherson, M., eds. Molecular Plant Pathology: A Practical Approach. Oxford, UK; Oxford University Press (1991): 163-174
  • 35 Jacobsen-Lyon K., Jensen E. Ø., Jorgensen J. E., Marcker K. A., Peacock W. J., Dennis E. S.. Symbiotic hemoglobin genes of Casuarina glauca.  Plant Cell. (1995);  7 213-223
  • 36 Johansen D. A.. Plant Microtechnique. London, UK; McGraw-Hill Book Company (1940)
  • 37 Kaneko T., Nakamura Y., Sato S., Asamizu E., Kato T., Sasamoto S., Watanabe A., Idesawa K., Ishikawa A., Kawashima K., Kimura T., Kishida Y., Kiyokawa C., Kohara M., Matsumoto M., Matsuno A., Mochizuki Y., Nakayama S., Nakazaki N., Shimpo S., Sugimoto M., Takeuchi C., Yamada M., Tabata S.. Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti (supplement).  DNA Research. (2000);  7 381-406
  • 38 Kaneko T., Nakamura Y., Sato S., Minamisawa K., Uchiumi T., Sasamoto S., Watanabe A., Idesawa K., Iriguchi M., Kawashima K., Kohara M., Matsumoto M., Shimpo S., Tsuruoka H., Wada T., Yamada M., Tabata S.. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 (supplement).  DNA Research. (2002);  9 225-256
  • 39 Kleemann G., Alskog G., Berry A. M., Huss-Danell K.. Lipid composition and nitrogenase activity of symbiotic Frankia (Alnus incana) in response to different oxygen concentrations.  Protoplasma. (1994);  183 107-115
  • 40 Kouchi H., Hata S.. Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development.  Molecular and General Genetics. (1993);  238 106-119
  • 41 Lamattina L., Garcia-Mata C., Graziano M., Pagnussat G.. Nitric oxide: the versatility of an extensive signal molecule.  Annual Review of Plant Biology. (2003);  54 109-136
  • 42 Lee H. S., Kim H. J., An C. S.. Cloning and expression analysis of 2-on-2 hemoglobin from soybean.  Journal of Plant Biology. (2004);  47 92-98
  • 43 Liu C., He Y., Chang Z.. Truncated hemoglobin o of Mycobacterium tuberculosis: the oligomeric state change and the interaction with membrane components.  Biochemical and Biophysical Research Communications. (2004);  316 1163-1172
  • 44 Long J. A., Moan E. I., Medford J. I., Barton M. K.. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. .  Nature. (1996);  379 66-69
  • 45 Meesters T. M., van Vliet W. M., Akkermans A. D. L.. Nitrogenase is restricted to the vesicles in Frankia strain EANlpec.  Physiologia Plantarum. (1987);  70 267-271
  • 46 Mesa S., de Dios Alché J., Bedmar E., Delgado M. J.. Expression of nir, nor and nos denitrification genes from Bradyrhizobum japonicum in soybean root nodules.  Physiologia Plantarum. (2004);  120 205-211
  • 47 Meyer J.. Comparison of carbon monoxide, nitric oxide, and nitrite as inhibitors of the nitrogenase from Clostridium pasteurianum.  Archives of Biochemistry and Biophysics. (1981);  210 246-256
  • 48 Milani M., Pesce A., Ouellet H., Guertin M., Bolognesi M.. Truncated hemoglobins and nitric oxide action.  IUBMB Life. (2003);  55 623-627
  • 49 Minchin F. R.. Regulation of oxygen diffusion in legume nodules.  Soil Biology and Biochemistry. (1997);  29 881-888
  • 50 Nathan C., Shiloh M. U.. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens.  Proceedings of the National Academy of Sciences of the USA. (2000);  97 8841-8848
  • 51 Niemann J. M., Tjepkema J. D., Tisa L. S.. Identification of the truncated hemoglobin gene in Frankia. .  Symbiosis. (2005);  39 91-95
  • 52 Okubara P. A., Pawlowski K., Murphy T. M., Berry A. M.. Symbiotic root nodules of the actinorhizal plant Datisca glomerata express rubisco activase mRNA.  Plant Physiology. (1999);  120 411-420
  • 53 Ouellet H., Ouellet Y., Richard C., Labarre M., Wittenberg B., Wittenberg J., Guertin M.. Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide.  Proceedings of the National Academy of Sciences of the USA. (2002);  99 5902-5907
  • 54 Pagnussat G. C., Simontacchi M., Puntarulo S., Lamattina L.. Nitric oxide is required for root organogenesis.  Plant Physiology. (2002);  129 954-956
  • 55 Parsons R., Silvester W. B., Harris S., Gruiters W. T. M., Bullivant S.. Frankia vesicles provide inducible and absolute oxygen protection for nitrogenase.  Plant Physiology. (1987);  83 728-731
  • 56 Pathania R., Navani N. K., Rajamohan G., Dikshit K. L.. Mycobacterium tuberculosis hemoglobin HbO associates with membranes and stimulates cellular respiration of recombinant Escherichia coli.  Journal of Biological Chemistry. (2002);  277 15293-15302
  • 57 Pawlowski K., Kunze R., de Vries S., Bisseling T.. Isolation of total, poly(A) and polysomal RNA from plant tissues. Gelvin, S. B. and Schilperoort, R. A., eds. Plant Molecular Biology Manual, D5, 2nd ed. Dordrecht, The Netherlands; Kluwer Academic Publishers (1994): 1-13
  • 58 Perazzolli M., Romero-Puertas M. C., Delledonne M.. Modulation of nitric oxide bioactivity by plant haemoglobins.  Journal of Experimental Botany. (2006);  57 479-488
  • 59 Sambrook J., Fritsch E. F., Maniatis T.. Molecular Cloning: A Laboratory Manual, 2nd ed. Plainview, N.Y.; Cold Spring Harbor Laboratory (1989)
  • 60 Sasakura F., Uchiumi T., Shimoda Y., Suzuki A., Takenouchi K., Higashi S., Abe M.. A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide.  Molecular Plant-Microbe Interactions. (2006);  19 441-450
  • 61 Schwintzer C. R., Tjepkema J. D.. Effect of oxygen concentration on growth and hemoglobin production in Frankia. .  Symbiosis. (2005);  39 77-82
  • 62 Seregélyes C., Dudits D.. Phytoglobins and nitric oxide: new partners in an old signalling system in plants.  Acta Biologica Hungarica. (2003);  54 15-25
  • 63 Shimoda Y., Nagata M., Suzuki A., Abe M., Sato S., Kato T., Tabata S., Higashi S., Uchiumi T.. Symbiotic Rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. .  Plant and Cell Physiology. (2005);  46 99-107
  • 64 Silvester W. B., Harris S. L., Tjepkema J. D.. Oxygen regulation and hemoglobin. Schwintzer, C. R. and Tjepkema, J. D., eds. The Biology of Frankia and Actinorhizal Plants. San Diego, CA; Academic Press Inc. (1990): 157-193
  • 65 Silvester W. B., Langenstein B., Berg R. H.. Do mitochondria provide the oxygen diffusion barrier in root nodules of Coriaria and Datisca?.  Canadian Journal of Botany. (1999);  77 1358-1366
  • 66 Takagi T., Iwaasa H., Yuasa H., Shikama K., Takemasa T., Watanabe Y.. Primary structure of Tetrahymena hemoglobins.  Biochimica et Biophysica Acta. (1993);  1173 75-78
  • 67 Taylor E. R., Nie X. Z., MacGregor A. W., Hill R. D.. A cereal haemoglobin gene is expressed in seed and root tissues under anaerobic conditions.  Plant Molecular Biology. (1994);  24 853-862
  • 69 Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.  Nucleic Acids Research. (1997);  25 4876-4882
  • 68 Tjepkema J. D., Pathirana M. S., Zeng S.. The gas diffusion pathway and hemoglobin content in actinorhizal nodules. Bothe, H., de Bruijn, F. J., and Newton, W. E., eds. Nitrogen Fixation: Hundred Years After. Stuttgart, New York; Gustav Fischer (1988 a): 701
  • 70 Tjepkema J. D.. Oxygen relations in leguminous and actinorhizal nodules. Gordon, J. C., Wheeler, C. T., and Perry, D. A., eds. Symbiotic Nitrogen Fixation in the Management of Temperate Forests. Corvallis, OR; For. Res. Lab., Oregon State Univ. (1979): 175-186
  • 71 Tjepkema J. D., Asa D. J.. Total and carbon monoxide-reactive heme content of actinorhizal nodules and the roots of some non-nodulated plants.  Plant and Soil. (1987);  100 225-236
  • 72 Tjepkema J. D., Cashon R. E., Beckwich J., Schwintzer C. R.. Hemoglobin in Frankia, a nitrogen-fixing actinomycete.  Applied and Environmental Microbiology. (2002);  68 2629-2631
  • 73 Tjepkema J. D., Schwintzer C. R., Monz C. A.. Time course of acetylene reduction in nodules of five actinorhizal genera.  Plant Physiology. (1988 b);  86 581-583
  • 74 Tjepkema J. D.. Hemoglobins in the nitrogen-fixing root nodules of actinorhizal plants.  Canadian Journal of Botany. (1983);  61 2924-2929
  • 75 Tjepkema J. D., Du G., Schwintzer C. R.. Response of respiration and nitrogenase activity in D. glomerata (Presl.) Baill. to changes in pO2.  Canadian Journal of Botany. (1999);  77 1367-1372
  • 76 Trevaskis B., Watts R. A., Andersson C. R., Llewellyn D. J., Hargrove M. S., Olson J. S., Dennis E. S., Peacock W. J.. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 12230-12234
  • 77 Trinchant J.-C., Rigaud J.. Nitrite and nitric oxide as inhibitors of nitrogenase from soybean bacteroids.  Applied and Environmental Microbiology. (1982);  44 1385-1388
  • 78 Van de Wiel C., Scheres B., Franssen H., van Lierop M.-J., van Lammeren A., van Kammen A., Bisseling T.. The early nodulin transcript ENOD2 is located in the nodule parenchyma inner cortex of pea and soybean root nodules.  The EMBO Journal. (1990);  9 1-8
  • 79 Vieweg M. F., Hohnjec N., Küster H.. Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. .  Planta. (2005);  220 757-766
  • 80 Watts R. A., Hunt P. W., Hvitved A. N., Hargrove M. S., Peacock W. J., Dennis E. S.. A hemoglobin from plants homologous to truncated hemoglobins of microorganisms.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 10119-10124
  • 81 Wendehenne D., Pugin A., Klessig D. F., Durner J.. Nitric oxide: comparative synthesis and signaling in animal and plant cells.  Trends in Plant Science. (2001);  6 177-183
  • 82 Wittenberg J. B., Bolognesi M., Wittenberg B. A., Guertin M.. Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants.  Journal of Biological Chemistry. (2002);  277 871-874
  • 83 Wittenberg J. B., Wittenberg B. A.. Mechanisms of cytoplasmic hemoglobin and myoglobin function.  Annual Review of Biophysics and Biophysical Chemistry. (1990);  19 217-241
  • 84 Zeng S., Tjepkema J. D., Berg R. H.. Gas diffusion pathway in nodules of Casuarina cunninghamiana.  Plant and Soil. (1989);  118 119-124

K. Pawlowski

Albrecht von Haller Institute for Plant Sciences
Department of Plant Biochemistry
Göttingen University

37077 Göttingen

Germany

Email: pawlowski@botan.su.se

Editor: T. Bisseling

    >