Endogenous PttHb1 and PttTrHb, and heterologous Vitreoscilla vhb haemoglobin gene expression in hybrid aspen roots with ectomycorrhizal interaction

Journal of Experimental Botany

Volumn 59, Issue 9, 2008, Pages 2449-2459

  Jokipii, Soile ^a   Häggman, Hely ^a   Brader, Günter ^b   Kallio, Pauli T ^c   Niemi, Karoliina ^b  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c ETH ZURICH   (Switzerland)

Author keywords

Ectomycorrhizas; Non symbiotic haemoglobin; Populus tremulaxtremuloides; Real time PCR; Truncated haemoglobin; Vitreoscilla haemoglobin (VHb)

Indexed keywords

FUNGI; LECCINUM POPULINUM; POPULUS; VITREOSCILLA; XEROCOMUS SUBTOMENTOSUS;

BACTERIAL PROTEIN; HEMOGLOBIN; HEMOGLOBIN PROTEIN, VITREOSCILLA; TRUNCATED HEMOGLOBIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ASPEN; BASIDIOMYCETES; CHEMISTRY; COMPARATIVE STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; PHYSIOLOGY; PLANT ROOT; SEQUENCE ALIGNMENT; SYMBIOSIS; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASIDIOMYCOTA; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; HEMOGLOBINS; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; POPULUS; SEQUENCE ALIGNMENT; SYMBIOSIS; TRUNCATED HEMOGLOBINS;

EID: 48649096661     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ern107     Document Type: Article

References (61)

1. Altman DG. 1991. Practical statistics for medical research. London: Chapman and Hall.
2. Appleby CA. 1984. Leghemoglobin and Rhizobium respiration. Annual Review of Plant Physiology 35, 443-478.
3. Aronen T, Häggman H. 1995. Differences in Agrobacterium infections in silver birch and Scots pine. European Journal of Forest Pathology 25, 197-213.
4. Béguiristain T, Lapeyrie F. 1997. Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytologist 136, 525-532.
5. Brunner AM, Yakovlev IA, Strauss SH. 2004. Validating internal controls for quantitative plant gene expression studies. BMC Plant Biology 4, 14.
6. Cao MX, Huang JQ, Wei ZM, Yao QH, Wan CZ, Lu JA. 2004. Engineering higher yield and herbicide resistance in rice by Agrobacterium-mediated multiple gene transformation. Crop Science 44, 2206-2213.
7. Chang S, Puryear J, Cairney J. 1993. A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113-116.
8. Correa-Aragunde N, Graziano M, Lamattina L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218, 900-905.
9. Delledonne M. 2005. NO news is good news for plants. Current Opinion in Plant Biology 8, 390-396.
10. Dordas C, Rivoal J, Hill RD. 2003. Plant haemoglobins, nitric oxide and hypoxic stress. Annals of Botany 91, 173-178.
11. Doyle JJ, Doyle JL. 1990. Isolation of plant DNA from fresh tissue. BRL Focus 12, 13-15.
12. Farrés J, Kallio PT. 2002. Improved cell growth in tobacco suspension cultures expressing Vitreoscilla hemoglobin. Biotechnology Progress 18, 229-233.
13. Frey AD, Farrés J, Bollinger CJT, Kallio PT. 2002. Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli. Applied and Environmental Microbiology 68, 4835-4840.
14. Frey AD, Kallio PT. 2003. Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiology Reviews 27, 525-545.
15. Frey AD, Kallio PT. 2005. Nitric oxide detoxification - a new era for bacterial globins in biotechnology? Trends in Biotechnology 23, 69-73.
16. Frey AD, Oberle BT, Farrés J, Kallio PT. 2004. Expression of Vitreoscilla haemoglobin in tobacco cell cultures relieves nitrosative stress in vivo and protects from NO in vitro. Plant Biotechnology Journal 2, 221-231.
17. Gardner PR. 2005. Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. Journal of Inorganic Biochemistry 99, 247-266.
18. Godbout C, Fortin JA. 1985. Synthesized ectomycorrhizae of aspen: fungal genus level of structural characterization. Canadian Journal of Botany 63, 252-262.
19. Guldner E, Desmarais E, Galtier N, Godelle B. 2004. Molecular evolution of plant haemoglobin: two haemoglobin genes in nymphaeaceae Euryale ferox. Journal of Evolutionary Biology 17, 48-54.
20. Häggman H, Frey AD, Ryynänen L, Aronen T, Julkunen-Tiitto R, Tiimonen H, Pihakaski-Maunsbach K, Jokipii S, Chen X, Kallio PT. 2003. Expression of Vitreoscilla haemoglobin in hybrid aspen (Populus tremulaxtremuloides). Plant Biotechnology Journal 1, 287-300.
21. Hebelstrup KH, Hunt P, Dennis E, Bjerregaard Jensen S, Østergaard Jensen E. 2006. Hemoglobin is essential for normal growth of Arabidopsis organs. Physiologia Plantarum 127, 157-166.
22. Holmberg N, Lilius G, Bailey JE, Bülow L. 1997. Transgenic tobacco expressing Vitreoscilla haemoglobin exhibits enhanced growth and altered metabolite production. Nature Biotechnology 15, 244-247.
23. Hoy JA, Hargrove MS. 2008. The structure and function of plant hemoglobins. Plant Physiology and Biochemistry 46, 371-379.
24. Hunt PW, Klok EJ, Trevaskis B, Watts RA, Ellis MH, Peacock WJ, Dennis ES. 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, USA 99, 17197-17202.
25. Hunt PW, Watts RA, Trevaskis B, Llewelyn DJ, Burnell J, Dennis ES, Peacock WJ. 2001. Expression and evolution of functionally distinct haemoglobin genes in plants. Plant Molecular Biology 47, 677-692.
26. Igamberdiev AU, Baron K, Manac'H-Little N, Stoimenova M, Hill RD. 2005. The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Annals of Botany 96, 557-564.
27. Jaakola L, Pirttilä AM, Halonen M, Hohtola A. 2001. Isolation of high quality RNA from bilberry (Vaccinium myrtillus L.) fruit. Molecular Biotechnology 19, 201-203.
28. Kallio PT, Kim D-J, Tsai PS, Bailey JE. 1994. Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. European Journal of Biochemistry 219, 201-208.
29. Karabaghli-Degron C, Sotta B, Bonnet M, Gay G, Le Tacon F. 1998. The auxin transport inhibitor 2,3,5-triiodobenzoic acid (TIBA) inhibits the stimulation of in vitro lateral root formation and the colonization of the tap-root cortex of Norway spruce (Picea abies) seedlings by the ectomycorrhizal fungus Laccaria bicolor. New Phytologist 140, 723-733.
30. Lira-Ruan V, Sarath G, Klucas RV, Arredondo-Peter R. 2001. Synthesis of hemoglobins in rice (Oryza sativa var. Jackson) plants growing in normal and stress conditions. Plant Science 161, 279-287.
31. Marx DH. 1969. The influence of ectotrophic fungi on the resistance of pine roots to pathogenic infections. I. Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathology 59, 153-163.
32. Modess O. 1941. Zur Kentniss der Mycorrhizabildner von Kiefer und Fichte. Symbolae Botanicae Upsaliensis 5, 1-147.
33. Mur LAJ, Carver TLW, Prats R. 2006. NO way to live; the various roles of nitric oxide in plant-pathogen interactions. Journal of Experimental Botany 57, 489-505.
34. Murashige T, Skoog F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473-497.
35. Neville J, Tessier JL, Morrison I, Scarratt J, Canning B, Klironomos JN. 2002. Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Applied Soil Ecology 19, 209-216.
36. Niemi K, Häggman H. 2002. Pisolithus tinctorius promotes germination and forms mycorrhizal structures in Scots pine somatic embryos in vitro. Mycorrhiza 12, 263-267.
37. Niemi K, Salonen M, Ernstsen A, Heinonen-Tanski H, Häggman H. 2000. Application of ectomycorrhizal fungi in rooting of Scots pine fascicular shoots. Canadian Journal of Forest Research 30, 1221-1230.
38. Niemi K, Scagel C, Häggman H. 2004. Application of ectomycorrhizal fungi in vegetative propagation of conifers. Plant Cell, Tissue and Organ Culture 78, 83-91.
39. Niemi K, Vuorinen T, Ernstsen A, Häggman H. 2002. Ectomycorrhizal fungi and exogenous auxins influence root and mycorrhiza formation of Scots pine hypocotyl cuttings in vitro. Tree Physiology 22, 1231-1239.
40. Ohwaki Y, Kawagishi-Kobayashi M, Wakasa K, Fujihara S, Yoneyama T. 2005. Induction of class-1 non-symbiotic hemoglobin genes by nitrate, nitrite and nitric oxide in cultured rice cells. Plant and Cell Physiology 46, 324-331.
41. Ouellet H, Ouellet Y, Richard C, Labarre M, Wittenberg B, Wittenberg J, Guertin M. 2002. Truncated hemoglobin HbN protects Mycobacterium bovis from nitric oxide. Proceedings of the National Academy of Sciences, USA 99, 5902-5907.
42. Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L. 2002. Nitric oxide is required for root organogenesis. Plant Physiology 129, 954-956.
43. Perazzolli M, Romero-Puertas MC, Delledonne M. 2006. Modulation of nitric oxide bioactivity by plant haemoglobins. Journal of Experimental Botany 57, 479-488.
44. Ross EJH, Stone JM, Elowsky CG, Arredondo-Peter R, Klucas RV, Sarath G. 2004. Activation of the Oryza sativa non-symbiotic haemoglobin-2 promoter by the cytokinin-regulated transcription factor, ARR1. Journal of Experimental Botany 55, 1721-1731.
45. Ryynänen L. 1991. Micropropagation of hybrid aspen (Populus tremulaxtremuloides). Reports from the Foundation for Forest Tree Breeding 1, 61-68.
46. Sakamoto A, Sakurao S, Fukunaga K, Matsubara T, Ueda-Hashimoto M, Tsukamoto S, Takahashi M, Morikawa H. 2004. Three distinct Arabidopsis hemoglobins exhibit peroxidase-like activity and differentially mediate nitrite-dependent protein nitration. FEBS Letters 572, 27-32.
47. Sasakura F, Uchiumi T, Shimoda Y, Suzuki A, Takenouchi K, Higashi S, Abe M. 2006. A class 1 hemoglobin gene from Alnus firma functions in symbiotic and nonsymbiotic tissues to detoxify nitric oxide. Molecular Plant-Microbe Interactions 19, 441-450.
48. Shimoda Y, Nagata M, Suzuki A, Abe M, Sato S, Kato T, Tabata S, Higashi S, Uchiumi T. 2005. Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus jabonicus. Plant and Cell Physiology 46, 99-107.
49. Smith SE, Read DJ. 1997. Mycorrhizal symbiosis, 2nd edn. Cambridge, UK: Academic Press.
50. Tranvan H, Habricot Y, Jeannette E, Gay G, Sotta B. 2000. Dynamics of symbiotic establishment between an IAA-overproducing mutant of the ectomycorrhizal fungus Hebeloma cylindrosporum and Pinus pinaster. Tree Physiology 20, 123-129.
51. Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ. 1997. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proceedings of the National Academy of Sciences, USA 94, 12230-12234.
52. Tsai PS, Nägeli M, Bailey JE. 1996. Intracellular expression of Vitreoscilla hemoglobin modifies microaerobic Escherichia coli metabolism through elevated concentration and specific activity of cytochrome o. Biotechnology and Bioengineering 49, 151-160.
53. Vieweg MF, Hohnjec N, Küster H. 2005. Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 220, 757-766.
54. Vinogradov SN, Hoogewijs D, Bailly X, Arredondo-Peter R, Gough J, Dewilde S, Moens L, Vanfleteren JR. 2006. A phylogenomic profile of globins. BMC Evolutionary Biology 6, 31.
55. Vuosku J, Jaakola L, Jokipii S, Karppinen K, Kämäräinen T, Pelkonen V-P, Jokela A, Sarjala T, Hohtola A, Häggman H. 2004. Does extraction of DNA and RNA by magnetic fishing work for diverse plant species? Molecular Biotechnology 27, 209-215.
56. Wang R, Guegler K, LaBrie ST, Crawford NM. 2000. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. The Plant Cell 12, 1491-1509.
57. Wang Y-H, Kochian LV, Doyle JJ, Garvin DF. 2003. Two tomato non-symbiotic haemoglobin genes are differentially expressed in response to diverse changes in mineral nutrient status. Plant, Cell and Environment 26, 673-680.
58. Watts RA, Hunt PW, Hvitved AN, Hargrove MS, Peacock WJ, Dennis ES. 2001. A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proceedings of the National Academy of Sciences, USA 98, 10119-10124.
59. Wilhelmson A, Kallio PT, Oksman-Caldentey K-M, Nuutila AM. 2005. Expression of Vitreoscilla hemoglobin enhances growth of Hyoscyamus muticus hairy root cultures. Planta Medica 71, 48-53.
60. Zar JH. 1984. Biostatistical analyses, 2nd edn. Englewood Cliffs, NJ: Prentice-Hall.
61. Zelasco S, Reggi S, Calligari P, Balestrazzi A, Bongiorni C, Quattrini E, Delia G, Bisoffi S, Fogher C, Confalonieri M. 2006. Expression of the Vitreoscilla hemoglobin (VHb)-encoding gene in transgenic white poplar: plant growth and biomass production, biochemical characterization and cell survival under submergence, oxidative and nitrosative stress conditions. Molecular Breeding 17, 201-216.