Host species and habitat affect nodulation by specific Frankia genotypes in two species of Alnus in interior Alaska

Oecologia

Volumn 160, Issue 4, 2009, Pages 619-630

  Anderson, Michael Damon ^a   Ruess, Roger W ^a   Myrold, David D ^b   Taylor, D Lee ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Actinorhizal; Boreal; Distribution; Nitrogen fixation; Symbiosis

Indexed keywords

NITROGEN;

ACTINORHIZA; BACTERIUM; DECIDUOUS TREE; GENETIC STRUCTURE; GENOTYPE; HOST-SYMBIONT INTERACTION; NITROGEN FIXATION; NODULATION; SYMPATRY;

ALDER; ARTICLE; COMPARATIVE STUDY; ECOSYSTEM; FRANKIA; GENETICS; GENOTYPE; METABOLISM; MICROBIOLOGY; NODULATION; PHYSIOLOGY; PLANT LEAF; PRINCIPAL COMPONENT ANALYSIS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SYMBIOSIS; UNITED STATES;

ALASKA; ALNUS; ECOSYSTEM; FRANKIA; GENOTYPE; NITROGEN; PLANT LEAVES; PLANT ROOT NODULATION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; PRINCIPAL COMPONENT ANALYSIS; SYMBIOSIS;

ALASKA; NORTH AMERICA; UNITED STATES;

ALNUS; ALNUS TENUIFOLIA; ALNUS VIRIDIS; BACTERIA (MICROORGANISMS); FRANKIA;

EID: 67649236677     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-009-1330-0     Document Type: Article

References (74)

1. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389 3402 (Pubitemid 27359211)
2. 2 uptake Ecoscience 11 102 112 (Pubitemid 38462678)
3. JM Batzli JF Zimpfer V Huguet CA Smyth M Fernandez JO Dawson 2004 Distribution and abundance of infective, soilborne Frankia and host symbionts Shepherdia, Alnus, and Myrica in a sand dune ecosystem Can J Bot 82 700 709 (Pubitemid 39017300)
4. DR Benson JO Dawson 2007 Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants Physiol Plant 130 318 330 (Pubitemid 46906295)
5. DR Benson WB Silvester 1993 Biology of Frankia strains, actinomycete symbionts of actinorhizal plants Microbiol Rev 57 293 319
6. SH Burleigh JO Dawson 1994 Desiccation tolerance and trehalose production in Frankia hyphae Soil Biol Biochem 26 593 598
7. SH Burleigh JO Dawson 1994 Occurrence of Myrica nodulating Frankia in Hawaiian volcanic soils Plant Soil 164 283 289 (Pubitemid 2165467)
8. S Burleigh JG Torrey 1990 Effectiveness of different Frankia cell types as inocula for the actinorhizal plant Casuarina Appl Environ Microbiol 56 2565 2567 (Pubitemid 20235707)
9. FS Chapin III LR Walker CL Fastie LC Sharman 1994 Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska Ecol Monographs 64 149 175
10. Z Chen J Li 2004 Phylogenetics and biogeography of Alnus (Betulaceae) inferred from sequences of nuclear ribosomal DNA ITS region Int J Plant Sci 165 325 335 (Pubitemid 38791406)
11. WK Crannell Y Tanaka DD Myrold 1994 Calcium and pH interaction on root nodulation of nursery-grown red alder (Alnus rubra Bong.) seedlings by Frankia Soil Biol Biochem 26 607 614
12. YM Dai XY He CG Zhang ZZ Zhang 2004 Characterization of genetic diversity of Frankia strains in nodules of Alnus nepalensis (D. Don) from the Hengduan Mountains on the basis of PCR-RFLP analysis of the nifD-nifK IGS Plant Soil 267 207 212 (Pubitemid 40306949)
13. Y Dai C Zhang Z Xiong Z Zhang 2005 Correlations between the ages of Alnus host species and the genetic diversity of associated endosymbiotic Frankia strains from nodules Sci China C Life Sci 48S 76 81 (Pubitemid 44898301)
14. JO Dawson JC Gordon 1979 Nitrogen fixation in relation to photosynthesis in Alnus glutinosa Bot Gaz 140S S70 S75
15. JO Dawson S-H Sun 1981 The effect of Frankia isolates from Comptonia peregrina and Alnus crispa on the growth of Alnus glutinosa, A cordata, and A. incana clones Can J For Res 11 758 762
16. JO Dawson DG Kowalski PJ Dart 1989 Variation with soil depth, topographic position and host species in the capacity of soils from an Australian locale to nodulate Casuarina and Allocasuarina seedlings Plant Soil 118 1 11
17. RF Denison ET Kiers 2004 Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis FEMS Microbiol Lett 237 187 193 (Pubitemid 39091952)
18. JT Dillon D Baker 1982 Variations in nitrogenase activity among pure-cultured Frankia strains tested on actinorhizal plants as an indication of symbiotic compatibility New Phyt 92 215 219
19. D Du DD Baker 1992 Actinorhizal host-specificity of Chinese Frankia strains Plant Soil 144 113 116 (Pubitemid 23401487)
20. TA Hall 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp Ser 41 95 98
21. RM Holman CR Schwintzer 1987 Distribution of spore-positive and spore-negative nodules of Alnus incana ssp rugosa in Maine, USA Plant Soil 104 103 111
22. JE Hooker CT Wheeler 1987 The effectivity of Frankia for nodulation and nitrogen fixation in Alnus rubra and A. glutinosa Physiol Plant 70 333 341
23. V Huguet JM Batzli JF Zimpfer F Gourbière JO Dawson MP Fernandez 2004 Nodular symbionts of Shepherdia, Alnus, and Myrica from a sand dune ecosystem: trends in occurrence of soilborne Frankia genotypes Can J Bot 82 691 699 (Pubitemid 39017299)
24. V Huguet M Mergeay E Cervantes MP Fernandez 2004 Diversity of Frankia strains associated to Myrica gale in Western Europe: impact of host plant (Myrica vs. Alnus) and of edaphic factors Environ Microbiol 6 1032 1041 (Pubitemid 39275257)
25. V Huguet M Gouy P Normand JF Zimpfer MP Fernandez 2005 Molecular phylogeny of Myricaceae: a reexamination of host-symbiont specificity Mol Phylogenet Evol 34 557 568 (Pubitemid 40427967)
26. K Huss-Danell D Uliassi I Renberg 1997 River and lake sediments as sources of infective Frankia (Alnus) Plant Soil 197 35 39 (Pubitemid 28012419)
27. Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge
28. JM Igual A Valverde E Valázquez I Santa Regina C Rodríguez-Barrueco 2006 Natural diversity of nodular microsymbionts of Alnus glutinosa in the Tormes River basin Plant Soil 280 373 383 (Pubitemid 43310322)
29. S-C Jeong DD Myrold 2001 Population size and diversity of Frankia in soils of Ceanothus velutinus and Douglas-fir stands Soil Biol Biochem 33 931 941 (Pubitemid 32533114)
30. JMP version 7.0 (1989-2007) SAS Institute, Cary, NC
31. A Kahn DD Myrold AK Misra 2007 Distribution of Frankia genotypes occupying Alnus nepalensis nodules with respect to altitude and soil characteristics in the Sikkim Himalayas Physiol Plant 130 364 371 (Pubitemid 46906287)
32. ET Kiers RA Rousseau SA West RF Denison 2003 Host sanctions and the legume-rhizobium mutualism Nature 425 78 81 (Pubitemid 37101720)
33. - Frankia strain in Alnus incana Soil Biol Biochem 22 57 64
34. J Markham CP Chanway 1998 Alnus rubra (Bong.) nodule spore type distribution in southwestern British Columbia Plant Ecol 135 197 205 (Pubitemid 28181316)
35. KJ Martin NJ Posavatz DD Myrold 2003 Nodulation potential of soils from red alder stands covering a wide age range Plant Soil 254 187 192 (Pubitemid 37078268)
36. L Maunuksela K Zepp T Koivula J Zeyer K Haahtela D Hahn 1999 Analysis of Frankia populations in three soils devoid of actinorhizal plants FEMS Microbiol Ecol 28 11 21 (Pubitemid 29062909)
37. Mitchell JS (2006) Patterns and controls over N inputs by green alder (Alnus viridis) to a secondary successional chronosequence in interior Alaska. MS Thesis, University of Alaska Fairbanks
38. KB Mullis FA Faloona S Scharf RK Saiki G Horn HA Erlich 1986 Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction Cold Spring Harb Symp Quant Biol 51 263 273 (Pubitemid 17076711)
39. DD Myrold K Huss-Danell 1994 Population dynamics of Alnus-infective Frankia in a forest soil with and without host trees Soil Biol Biochem 26 533 540
40. 2-fixing activity of Frankia strains in relation to soil depth Physiol Plant 99 732 738 (Pubitemid 27195163)
41. E Navarro J Bousquet A Moirod A Munive D Piou P Normand 2003 Molecular phylogeny of Alnus (Betulaceae), inferred from nuclear ribosomal DNA ITS sequences Plant Soil 254 207 217 (Pubitemid 37078269)
42. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill, Boston
43. MW Paschke JO Dawson 1993 Avian dispersal of Frankia Can J Bot 71 1128 1131 (Pubitemid 24410014)
44. MW Paschke JO Dawson BM Condon 1994 Frankia in prairie, forest, and cultivated soils of central Illinois, USA Pedobiologia 38 546 551
45. D Prat 1989 Effects of some pure and mixed Frankia strains on seedling growth in different Alnus species Plant Soil 113 31 38
46. C Rouvier Y Prin P Reddell P Normand P Simonet 1996 Genetic diversity among Frankia strains nodulating members of the family Casuarinaceae in Australia revealed by PCR and restriction fragment length polymorphism analysis with crushed root nodules Appl Environ Microbiol 62 979 985 (Pubitemid 26071468)
47. SAS Institute (2001) The SAS system for Windows. Version 8.2. SAS Institute, Cary, NC
48. WF Sayed CT Wheeler HH Zahran AAM Shoreit 1997 Effect of temperature and soil moisture on the survival and symbiotic effectiveness of Frankia spp Biol Fertil Soils 25 349 353 (Pubitemid 27491035)
49. A Sellstedt K Huss-Danell A-S Ahlqvist 1986 Nitrogen fixation and biomass production in symbioses between Alnus incana and Frankia strains with different hydrogen metabolism Physiol Plant 66 99 107
50. LJ Sheppard JE Hooker CT Wheeler RI Smith 1988 Glasshouse evaluation of the growth of Alnus rubra and Alnus glutinosa on peat and acid brown earth soils when inoculated with four sources of Frankia Plant Soil 110 187 198
51. EL Simms DL Taylor J Povich RP Shefferson JL Sachs M Urbina Y Tausczik 2006 An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction Proc Biol Sci 273 77 81 (Pubitemid 46768048)
52. P Simonet E Navarro C Rouvier P Reddell J Zimpfer Y Dommergues R Bardin P Combarro J Hamelin A-M Domenach Prin Y Gourbière JO Dawson P Normand 1999 Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal Environ Microbiol 1 525 533 (Pubitemid 129640066)
53. A Smolander 1990 Frankia populations in soils under different tree species-with special emphasis on soils under Betula pendula Plant Soil 121 1 10
54. A Smolander V Sundman 1987 Frankia in acid soils of forests devoid of actinorhizal plants Physiol Plant 70 297 303
55. DD Uliassi RW Ruess 2002 Limitations to symbiotic nitrogen fixation in primary succession on the Tanana river floodplain Ecology 83 88 103 (Pubitemid 34067681)
56. M Valdés N-O Pérez P Estrada-de los Santos J Caballero-Mellado JJ Peña-Cabriales P Normand AM Hirsch 2005 Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen Appl Environ Microbiol 71 460 466 (Pubitemid 40116302)
57. Van Cleve K, Viereck LA (1981) Forest succession in relation to nutrient cycling in the boreal forest of Alaska. In: West DC, Shugart HH, Botkin DB (eds) Forest succession: concepts and application. Springer-Verlag, New York, pp 179-211
58. K Van Cleve LA Viereck RL Schlentner 1971 Accumulation of nitrogen in alder (Alnus) ecosystems near Fairbanks, Alaska Arc Alp Res 3 101 114
59. K Van Cleve CT Dyrness GM Marion R Erickson 1993 Control of soil development on the Tanana River floodplain, interior Alaska Can J For Res 23 941 955
60. K Van Cleve LA Viereck CT Dyrness 1996 State factor control of soils and forest succession along the Tanana River in interior Alaska, USA Arc Alp Res 28 388 400
61. C van Dijk A Sluimer 1994 Resistance to an ineffective Frankia strain type in Alnus glutinosa (L.) Gaertn New Phyt 128 497 504
62. C van Dijk A Sluimer A Weber 1988 Host range differentiation of spore-positive and spore-negative strain types of Frankia in stands of Alnus glutinosa and Alnus incana in Finland Physiol Plant 72 349 358
63. JG Vogel ST Gower 1998 Carbon and nitrogen dynamics of boreal Jack pine stands with and without a green alder understory Ecosystems 1 386 400 (Pubitemid 128663391)
64. LR Walker FS Chapin III 1986 Physiological controls over seedling growth in primary succession on an Alaskan floodplain Ecology 67 1508 1523 (Pubitemid 18285538)
65. LG Wall 2000 The actinorhizal symbiosis J Plant Growth Regul 19 167 182 (Pubitemid 30827371)
66. A Weber 1986 Distribution of spore-positive and spore-negative nodules in stands of Alnus glutinosa and Alnus incana in Finland Plant Soil 96 205 213
67. A Weber 1990 Host specificity and efficiency of nitrogenase activity of Frankia strains from Alnus incana and Alnus glutinosa Symbiosis 8 47 60
68. A Weber E-L Nurmiaho-Lassila V Sundman 1987 Features of the intrageneric Alnus-Frankia specificity Physiol Plant 70 289 296
69. SA West ET Kiers EL Simms RF Denison 2002 Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc Lond Biol Sci 269 685 694 (Pubitemid 34407375)
70. DJ Wolters C van Dijk EG Zoetendal DL Akkermans 1997 Phylogenetic characterization of ineffective Frankia in Alnus glutinosa (L.) Gaertn. nodules from wetland soil inoculants Mol Ecol 6 971 981 (Pubitemid 27447142)
71. TL Wurtz 1995 Understory alder in three boreal forests of Alaska: local distribution and effects on soil fertility Can J For Res 25 987 996 (Pubitemid 26440238)
72. DR Young E Sande GA Peters 1992 Spatial relationships of Frankia and Myrica cerifera on a Virginia, USA barrier island Symbiosis 12 209 220
73. JF Zimpfer GJ Kennedy CA Smyth J Hamelin E Navarro JO Dawson 1999 Localization of Casuarina-infective Frankia near Casuarina cunninghamiana trees in Jamaica Can J Bot 77 1248 1256 (Pubitemid 30144226)
74. SF Zitzer JO Dawson 1992 Soil properties and actinorhizal vegetation influence nodulation of Alnus glutinosa and Elaeagnus angustifolia by Frankia Plant Soil 140 197 204 (Pubitemid 23397581)