The responses of Vitreoscilla hemoglobin-expressing hybrid aspen (Populus tremula × tremuloides) exposed to 24-h herbivory: Expression of hemoglobin and stress-related genes in exposed and nonorthostichous leaves

Journal of Plant Research

Volumn 126, Issue 6, 2013, Pages 795-809

  Sutela, Suvi ^a   Ylioja, Tiina ^b   Jokipii Lukkari, Soile ^a   Anttila, Anna Kaisa ^a   Julkunen Tiitto, Riitta ^c   Niemi, Karoliina ^d   Mölläri, Tiina ^a   Kallio, Pauli T ^e   Häggman, Hely ^a  

^a UNIVERSITY OF OULU   (Finland)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d Finnish Forest Industries Federation   (Finland)

^e ETH ZURICH   (Switzerland)

Author keywords

Hybrid aspen; Non symbiotic hemoglobins; RGR; Truncated hemoglobin; vhb

Indexed keywords

CONISTRA; ECTROPIS CREPUSCULARIA; ORGYIA ANTIQUA; ORTHOSIA GOTHICA; POPULUS; POPULUS TREMULA; POPULUS TREMULOIDES; VITREOSCILLA;

BACTERIAL PROTEIN; HEMOGLOBIN PROTEIN, VITREOSCILLA; HYDROXYBENZOIC ACID DERIVATIVE; MESSENGER RNA; PHENOLIC ACID; PLANT RNA; TRANSCRIPTOME; TRUNCATED HEMOGLOBIN; VEGETABLE PROTEIN;

ANIMAL; ARTICLE; CHIMERA; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HERBIVORY; INSECT; LARVA; PARASITOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; POPULUS; TRANSGENIC PLANT;

ANIMALS; BACTERIAL PROTEINS; CHIMERA; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; HYDROXYBENZOATES; INSECTS; LARVA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT LEAVES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POPULUS; RNA, MESSENGER; RNA, PLANT; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; TRUNCATED HEMOGLOBINS;

EID: 84886720258     PISSN: 09189440     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10265-013-0569-z     Document Type: Article

References (79)

1. Appleby C (1984) Leghemoglobin and Rhizobium respiration. Annu Rev Plant Physiol Plant Mol Biol 35: 443-478. doi: 10. 1146/annurev. pp. 35. 060184. 002303.
2. Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130: 585-593. doi: 10. 1007/s00442-001-0839-7.
3. Babst BA, Ferrieri RA, Thorpe MR, Orians CM (2008) Lymantria dispar herbivory induces rapid changes in carbon transport and partitioning in Populus nigra. Entomol Exp Appl 128: 117-125. doi: 10. 1111/j. 1570-7458. 2008. 00698. x.
4. Babst BA, Sjödin A, Jansson S, Orians CM (2009) Local and systemic transcriptome responses to herbivory and jasmonic acid in Populus. Tree Genet Genomes 5: 459-474. doi: 10. 1007/s11295-009-0200-6.
5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57: 289-300. doi: 10. 2307/2346101.
6. Boerman SJ, Webster DA (1982) Control of heme content in Vitreoscilla by oxygen. J Gen Appl Microbiol 28: 35-43.
7. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43: 545-580. doi: 10. 1146/annurev. phyto. 41. 052002. 095505.
8. Brosché M, Vinocur B, Alatalo ER, Lamminmäki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot MB, Altman A, Polle A, Dreyer E, Rudd S, Lars P, Auvinen P, Kangasjärvi J (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6: R101. doi: 10. 1186/gb-2005-6-12-r101.
9. Bustos-Sanmamed P, Tovar-Méndez A, Crespi M, Sato S, Tabata S, Becana M (2011) Regulation of nonsymbiotic and truncated hemoglobin genes of Lotus japonicus in plant organs and in response to nitric oxide and hormones. New Phytol 189: 765-776. doi: 10. 1111/j. 1469-8137. 2010. 03527. x.
10. Chen M (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15: 101-114. doi: 10. 1111/j. 1744-7917. 2008. 00190. x.
11. Chen F, Liu C, Tschaplinski TJ, Zhao N (2009) Genomics of secondary metabolism in Populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28: 375-392. doi: 10. 1080/07352680903241279.
12. Chi P, Webster DA, Stark BC (2009) Vitreoscilla hemoglobin aids respiration under hypoxic conditions in its native host. Microbiol Res 164: 267-275. doi: 10. 1016/j. micres. 2006. 11. 018.
13. Christopher ME, Miranda M, Major IT, Constabel CP (2004) Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219: 936-947. doi: 10. 1007/s00425-004-1297-3.
14. Clausen TP, Reichardt PB, Bryant JP, Werner RA, Post K, Frisby K (1989) Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J Chem Ecol 15: 2335-2346. doi: 10. 1007/BF01012085.
15. Constabel CP, Major IT (2005) Molecular biology and biochemistry of induced insect defense in Populus. In: Romeo J (ed) Recent advances in phytochemistry, vol. 39. Chemical Ecology and Phytochemistry of Forest Ecosystems. Elsevier Academic Press, Amsterdam, pp. 119-143.
16. Cooke JEK, Weih M (2005) Nitrogen storage and seasonal nitrogen cycling in Populus: bridging molecular physiology and ecophysiology. New Phytol 167: 19-30. doi: 10. 1111/j. 1469-8137. 2005. 01451. x.
17. Dikshit KL, Dikshit RP, Webster DA (1990) Study of Vitreoscilla globin (vgb) gene expression and promoter activity in E. coli through transcriptional fusion. Nucleic Acids Res 18: 4149-4155. doi: 10. 1093/nar/18. 14. 4149.
18. Dordas C, Hasinoff BB, Igamberdiev AU, Manac'h N, Rivoal J, Hill RD (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35: 763-770. doi: 10. 1046/j. 1365-313X. 2003. 01846. x.
19. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210. doi: 10. 1093/nar/30. 1. 207.
20. Fox J (2005) The R commander: a basic-statistics graphical user interface to R. J Stat Softw 14: 1-42.
21. Frey AD, Kallio PT (2003) Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol Rev 27: 525-545. doi: 10. 1016/S0168-6445(03)00056-1.
22. Frey AD, Farrés J, Bollinger CJT, Kallio PT (2002) Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli. Appl Environ Microbiol 68: 4835-4840. doi: 10. 1128/AEM. 68. 10. 4835-4840. 2002.
23. 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 Biotech J 2: 221-231. doi: 10. 1111/j. 1467-7652. 2004. 00066. x.
24. Frey AD, Shepherd M, Jokipii-Lukkari S, Häggman H, Kallio PT (2011) The single-domain globin of Vitreoscilla: augmentation of aerobic metabolism for biotechnological applications. Adv Microb Physiol 58: 81-139. doi: 10. 1016/B978-0-12-381043-4. 00003-9.
25. Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57: 507-516. doi: 10. 1093/jxb/erj053.
26. Gupta KJ, Hebelstrup KH, Mur LAJ, Igamberdiev AU (2011) Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett 585: 3843-3849. doi: 10. 1016/j. febslet. 2011. 10. 036.
27. Häggman H, Frey AD, Ryynänen L, Aronen T, Julkunen-Tiitto R, Tiimonen H, Pihakaski-Maunsbach K, Jokipii S, Chen XW, Kallio PT (2003) Expression of Vitreoscilla haemoglobin in hybrid aspen (Populus tremula × tremuloides). Plant Biotech J 1: 287-300. doi: 10. 1046/j. 1467-7652. 2003. 00027. x.
28. Holmberg N, Lilius G, Bailey JE, Bülow L (1997) Transgenic tobacco expressing Vitreoscilla hemoglobin exhibits enhanced growth and altered metabolite production. Nat Biotechnol 15: 244-247. doi: 10. 1038/nbt0397-244.
29. Hoy JA, Hargrove MS (2008) The structure and function of plant hemoglobins. Plant Physiol Biochem 46: 371-379. doi: 10. 1016/j. plaphy. 2007. 12. 016.
30. Igamberdiev AU, Bykova NV, Shah JK, Hill RD (2010) Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiol Plantarum 138: 393-404. doi: 10. 1111/j. 1399-3054. 2009. 01314. x.
31. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5: 299-314.
32. Jokipii S, Häggman H, Brader G, Kallio PT, Niemi K (2008) Endogenous PttHb1 and PttTrHb, and heterologous Vitreoscilla vhb haemoglobin gene expression in hybrid aspen roots with ectomycorrhizal interaction. J Exp Bot 59: 2449-2459. doi: 10. 1093/jxb/ern107.
33. Jokipii-Lukkari S, Frey AD, Kallio PT, Häggman H (2009) Intrinsic non-symbiotic and truncated haemoglobins and heterologous Vitreoscilla haemoglobin expression in plants. J Exp Bot 60: 409-422. doi: 10. 1093/jxb/ern320.
34. Jones C, Hopper R, Coleman J, Krischik V (1993) Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93: 452-456. doi: 10. 1007/BF00317892.
35. Julkunen-Tiitto R, Sorsa S (2001) Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J Chem Ecol 27: 779-789.
36. Kallio PT, Kim DJ, Tsai PS, Bailey JE (1994) Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur J Biochem 219: 201-208. doi: 10. 1021/bp950065j.
37. Kaur R, Pathania R, Sharma V, Mande SC, Dikshit KL (2002) Chimeric Vitreoscilla hemoglobin (VHb) carrying a flavoreductase domain relieves nitrosative stress in Escherichia coli: new insight into the functional role of VHb. Appl Environ Microbiol 68: 152-160. doi: 10. 1128/AEM. 68. 1. 152-160. 2002.
38. Kosmachevskaya OV, Topunov AF (2009) Hemoglobins: diversity of structures and functions. Appl Biochem Microbiol 45: 563-587. doi: 10. 1134/S0003683809060015.
39. Kvist M, Ryabova ES, Nordlander E, Bülow L (2007) An investigation of the peroxidase activity of Vitreoscilla hemoglobin. J Biol Inorg Chem 12: 324-334. doi: 10. 1007/s00775-006-0190-x.
40. Lee H, Kim H, An C (2004) Cloning and expression analysis of 2-on-2 hemoglobin from soybean. J Plant Biol 47: 92-98. doi: 10. 1007/BF03030637.
41. Li X, Peng R, Fan H, Xiong A, Yao Q, Cheng Z, Li Y (2005) Vitreoscilla hemoglobin overexpression increases submergence tolerance in cabbage. Plant Cell Rep 23: 710-715. doi: 10. 1007/s00299-004-0872-1.
42. Maffei ME, Mithöfer A, Boland W (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68: 2946-2959. doi: 10. 1016/j. phytochem. 2007. 07. 016.
43. Major IT, Constabel CP (2006) Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytol 172: 617-635. doi: 10. 1111/j. 1469-8137. 2006. 01877. x.
44. Major IT, Constabel CP (2007) Shoot-root defense signaling and activation of root defense by leaf damage in poplar. Can J Bot Rev Can Bot 85: 1171-1181. doi: 10. 1139/B07-090.
45. Mao Z, Hu Y, Zhong J, Wang L, Guo J, Lin Z (2003) Improvement of the hydroponic growth and waterlogging tolerance of petunias by the introduction of vhb gene. Acta Bot Sin 45: 205-210.
46. Millard P, Grelet G (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30: 1083-1095. doi: 10. 1093/treephys/tpq042.
47. Mur LAJ, Sivakumaran A, Mandon J, Cristescu SM, Harren FJM, Hebelstrup KH (2012) Haemoglobin modulates salicylate and jasmonate/ethylene-mediated resistance mechanisms against pathogens. J Exp Bot 63: 4375-4387. doi: 10. 1093/jxb/ers116.
48. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum 15: 473-497.
49. Núñez-Farfán J, Fornoni J, Luis Valverde P (2007) The evolution of resistance and tolerance to herbivores. Annu Rev Ecol Evol Syst 38: 541-566. doi: 10. 1146/annurev. ecolsys. 38. 091206. 095822.
50. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27: 1289-1313. doi: 10. 1023/A: 1010352307301.
51. Osier TL, Lindroth RL (2004) Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: plant growth, phytochemistry and insect performance. Oecologia 139: 55-65. doi: 10. 1007/s00442-003-1481-3.
52. Park K, Kim K, Howard AJ, Stark BC, Webster DA (2002) Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases. J Biol Chem 277: 33334-33337. doi: 10. 1074/jbc. M203820200.
53. Pawlowski K, Jacobsen KR, Alloisio N, Denison RF, Klein M, Tjepkema JD, Winzer T, Sirrenberg A, Guan C, Berry AM (2007) Truncated hemoglobins in actinorhizal nodules of Datisca glomerata. Plant Biol 9: 776-785. doi: 10. 1055/s-2007-965258.
54. Peters DJ, Constabel CP (2002) Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32: 701-712. doi: 10. 1046/j. 1365-313X. 2002. 01458. x.
55. Philippe RN, Bohlmann J (2007) Poplar defense against insect herbivores. Can J Bot Rev Can Bot 85: 1111-1126. doi: 10. 1139/B07-109.
56. Philippe RN, Ralph SG, Mansfield SD, Bohlmann J (2010) Transcriptome profiles of hybrid poplar (Populus trichocarpa × deltoides) reveal rapid changes in undamaged, systemic sink leaves after simulated feeding by forest tent caterpillar (Malacosoma disstria). New Phytol 188: 787-802. doi: 10. 1111/j. 1469-8137. 2010. 03392. x.
57. Qu Z, Zhong N, Wang H, Chen A, Jian G, Xia G (2006) Ectopic expression of the cotton non-symbiotic hemoglobin gene GhHb1 triggers defense responses and increases disease tolerance in Arabidopsis. Plant Cell Physiol 47: 1058-1068. doi: 10. 1093/pcp/pcj076.
58. Ralph SG (2009) Studying Populus defenses against insect herbivores in the post-genomic era. Crit Rev Plant Sci 28: 335-345. doi: 10. 1080/07352680903241139.
59. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D, Ritland CE, Benoit F, Rigby T, Nantel A, Butterfield YSN, Kirkpatrick R, Chun E, Liu J, Palmquist D, Wynhoven B, Stott J, Yang G, Barber S, Holt RA, Siddiqui A, Jones SJM, Marra MA, Ellis BE, Douglas CJ, Ritland K, Bohlmann J (2006) Genomics of hybrid poplar (Populus trichocarpa × deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15: 1275-1297. doi: 10. 1111/j. 1365-294X. 2006. 02824. x.
60. Ramandeep, Hwang KW, Raje M, Kim K, Stark BC, Dikshit KL, Webster DA (2001) Vitreoscilla hemoglobin-intracellular localization and binding to membranes. J Biol Chem 276: 24781-24789. doi: 10. 1074/jbc. M009808200.
61. Seregélyes C, Igamberdiev A, Maassen A, Hennig J, Dudits D, Hill R (2004) NO-degradation by alfalfa class 1 hemoglobin (Mhb 1): a possible link to PR-1a gene expression in Mhb1-overproducing tobacco plants. FEBS Lett 571: 61-66. doi: 10. 1016/j. febslet. 2004. 06. 05.
62. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W (eds) Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York.
63. Spyrakis F, Bruno S, Bidon-Chanal A, Javier Luque F, Abbruzzetti S, Viappiani C, Dominici P, Mozzarelli A (2011) Oxygen binding to Arabidopsis thaliana AHb2 nonsymbiotic hemoglobin: evidence for a role in oxygen transport. IUBMB Life 63: 355-362. doi: 10. 1002/iub. 470.
64. Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145: 298-306. doi: 10. 1007/s00442-005-0128-y.
65. Su X, Chu Y, Li H, Hou Y, Zhang B, Huang Q, Hu Z, Huang R, Tian Y (2011) Expression of multiple resistance genes enhances tolerance to environmental stressors in transgenic poplar (Populus × euramericana 'Guariento'). PLoS One 6: e24614. doi: 10. 1371/journal. pone. 0024614.
66. Sutela S, Niemi K, Edesi J, Laakso T, Saranpää P, Vuosku J, Mäkela R, Tiimonen H, Chiang VL, Koskimäki J, Suorsa M, Julkunen-Tiitto R, Häggman H (2009) Phenolic compounds in ectomycorrhizal interaction of lignin modified silver birch. BMC Plant Biol 9: 124. doi: 10. 1186/1471-2229-9-124.
67. Tiso M, Tejero J, Kenney C, Frizzell S, Gladwin MT (2012) Nitrite reductase activity of nonsymbiotic hemoglobins from Arabidopsis thaliana. Biochemistry 51: 5285-5292. doi: 10. 1021/bi300570v.
68. 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. Biotechnol Bioeng 49: 151-160. doi: 10. 1002/(SICI)1097-0290(19960120)49: 2<151: AID-BIT4>3. 0. CO;2-P.
69. Vázquez-Limón C, Hoogewijs D, Vinogradov SN, Arredondo-Peter R (2012) The evolution of land plant hemoglobins. Plant Sci 191: 71-81. doi: 10. 1016/j. plantsci. 2012. 04. 013.
70. Vieweg M, 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. doi: 10. 1007/s00425-004-1397-0.
71. 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 Physiol 155: 1435-1444. doi: 10. 1104/pp. 110. 166462.
72. Vinogradov SN, Moens L (2008) Diversity of globin function: enzymatic, transport, storage, and sensing. J Biol Chem 283: 8773-8777. doi: 10. 1074/jbc. R700029200.
73. Wakabayashi S, Matsubara H, Webster DA (1986) Primary sequence of a dimeric bacterial hemoglobin from Vitreoscilla. Nature 322: 481-483.
74. Wang Y, Guo S (2010) Insect-resistance and high-yield transgenic tobacco obtained by molecular breeding technology. Afr J Biotechnol 9: 6626-6631. doi: 10. 5897/AJB09. 1605.
75. Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2009) Functional expression of Vitreoscilla hemoglobin (VHb) in Arabidopsis relieves submergence, nitrosative, photo-oxidative stress and enhances antioxidants metabolism. Plant Sci 176: 66-77. doi: 10. 1016/j. plantsci. 2008. 09. 011.
76. Wildhagen H, Duerr J, Ehlting B, Rennenberg H (2010) Seasonal nitrogen cycling in the bark of field-grown Grey poplar is correlated with meteorological factors and gene expression of bark storage proteins. Tree Physiol 30: 1096-1110. doi: 10. 1093/treephys/tpq018.
77. Wu J, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32: 1161-1174. doi: 10. 1111/j. 1365-3040. 2009. 01943. x.
78. 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. Mol Breed 17: 201-216. doi: 10. 1007/s11032-005-5295-3.
79. Zhang L, Li Y, Wang Z, Xia Y, Chen W, Tang K (2007) Recent developments and future prospects of Vitreoscilla hemoglobin application in metabolic engineering. Biotechnol Adv 25: 123-136. doi: 10. 1016/j. biotechadv. 2006. 11. 001.