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

  • Physiological Ecology - Original Paper
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Abstract

Alders (Alnus spp.) are important components of northern ecosystems due to their ability to fix nitrogen (N) in symbiosis with Frankia bacteria. Availability of optimal Frankia may be a contributing factor in limiting the performance and ecological effects of Alnus, but the factors underlying distribution of Alnus-infective Frankia are not well understood. This study examined the genetic structure (nifD–K spacer RFLP haplotypes) of Frankia assemblages symbiotic with two species of Alnus (A. tenuifolia and A. viridis) in four successional habitats in interior Alaska. We used one habitat in which both hosts occurred to observe differences between host species independent of habitat, and we used replicate sites for each habitat and host to assess the consistency of symbiont structure related to both factors. We also measured leaf N content and specific N-fixation rate (SNF) of nodules (15N uptake) to determine whether either covaried with Frankia structure, and whether Frankia genotypes differed in SNF in situ. Frankia structure differed between sympatric hosts and among habitats, particularly for A. tenuifolia, and was largely consistent among replicate sites representing both factors. Leaf N differed between host species and among habitats for both hosts. SNF did not differ among habitats or host species, and little evidence for differences in SNF among Frankia genotypes was found, due largely to high variation in SNF. Consistency of Frankia structure among replicate sites suggests a consistent relationship between both host species and habitat among these sites. Correlations with specific environmental variables and possible underlying mechanisms are discussed.

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References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anderson MD, Ruess RW, Uliassi DD, Mitchell JS (2004) Estimating N2 fixation in two species of Alnus in interior Alaska using acetylene reduction and 15N2 uptake. Ecoscience 11:102–112

    Google Scholar 

  • Batzli JM, Zimpfer JF, Huguet V, Smyth CA, Fernandez M, Dawson JO (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

    Article  Google Scholar 

  • Benson DR, Dawson JO (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330

    Article  CAS  Google Scholar 

  • Benson DR, Silvester WB (1993) Biology of Frankia strains, actinomycete symbionts of actinorhizal plants. Microbiol Rev 57:293–319

    PubMed  CAS  Google Scholar 

  • Burleigh SH, Dawson JO (1994a) Desiccation tolerance and trehalose production in Frankia hyphae. Soil Biol Biochem 26:593–598

    Article  CAS  Google Scholar 

  • Burleigh SH, Dawson JO (1994b) Occurrence of Myrica nodulating Frankia in Hawaiian volcanic soils. Plant Soil 164:283–289

    Article  CAS  Google Scholar 

  • Burleigh S, Torrey JG (1990) Effectiveness of different Frankia cell types as inocula for the actinorhizal plant Casuarina. Appl Environ Microbiol 56:2565–2567

    PubMed  Google Scholar 

  • Chapin FS III, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monographs 64:149–175

    Article  Google Scholar 

  • Chen Z, Li J (2004) Phylogenetics and biogeography of Alnus (Betulaceae) inferred from sequences of nuclear ribosomal DNA ITS region. Int J Plant Sci 165:325–335

    Article  CAS  Google Scholar 

  • Crannell WK, Tanaka Y, Myrold DD (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

    Article  CAS  Google Scholar 

  • Dai YM, He XY, Zhang CG, Zhang ZZ (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

    Article  CAS  Google Scholar 

  • Dai Y, Zhang C, Xiong Z, Zhang Z (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

    Google Scholar 

  • Dawson JO, Gordon JC (1979) Nitrogen fixation in relation to photosynthesis in Alnus glutinosa. Bot Gaz 140S:S70–S75

    Article  Google Scholar 

  • Dawson JO, Sun S-H (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

    Article  Google Scholar 

  • Dawson JO, Kowalski DG, Dart PJ (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

    Article  Google Scholar 

  • Denison RF, Kiers ET (2004) Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol Lett 237:187–193

    Article  PubMed  CAS  Google Scholar 

  • Dillon JT, Baker D (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

    Article  Google Scholar 

  • Du D, Baker DD (1992) Actinorhizal host-specificity of Chinese Frankia strains. Plant Soil 144:113–116

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Holman RM, Schwintzer CR (1987) Distribution of spore-positive and spore-negative nodules of Alnus incana ssp rugosa in Maine, USA. Plant Soil 104:103–111

    Article  Google Scholar 

  • Hooker JE, Wheeler CT (1987) The effectivity of Frankia for nodulation and nitrogen fixation in Alnus rubra and A. glutinosa. Physiol Plant 70:333–341

    Article  CAS  Google Scholar 

  • Huguet V, Batzli JM, Zimpfer JF, Gourbière F, Dawson JO, Fernandez MP (2004a) 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

    Article  CAS  Google Scholar 

  • Huguet V, Mergeay M, Cervantes E, Fernandez MP (2004b) 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

    Article  PubMed  CAS  Google Scholar 

  • Huguet V, Gouy M, Normand P, Zimpfer JF, Fernandez MP (2005) Molecular phylogeny of Myricaceae: a reexamination of host-symbiont specificity. Mol Phylogenet Evol 34:557–568

    Article  PubMed  CAS  Google Scholar 

  • Huss-Danell K, Uliassi D, Renberg I (1997) River and lake sediments as sources of infective Frankia (Alnus). Plant Soil 197:35–39

    Article  CAS  Google Scholar 

  • Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge

    Google Scholar 

  • Igual JM, Valverde A, Valázquez E, Santa Regina I, Rodríguez-Barrueco C (2006) Natural diversity of nodular microsymbionts of Alnus glutinosa in the Tormes River basin. Plant Soil 280:373–383

    Article  CAS  Google Scholar 

  • Jeong S-C, Myrold DD (2001) Population size and diversity of Frankia in soils of Ceanothus velutinus and Douglas-fir stands. Soil Biol Biochem 33:931–941

    Article  CAS  Google Scholar 

  • JMP version 7.0 (1989-2007) SAS Institute, Cary, NC

  • Kahn A, Myrold DD, Misra AK (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

    Article  CAS  Google Scholar 

  • Kiers ET, Rousseau RA, West SA, Denison RF (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425:78–81

    Article  PubMed  CAS  Google Scholar 

  • Kurdali F, Rinaudo G, Moiroud A, Domenach AM (1990) Competition for nodulation and 15N2-fixation between a Sp+ and a Sp− Frankia strain in Alnus incana. Soil Biol Biochem 22:57–64

    Article  CAS  Google Scholar 

  • Markham J, Chanway CP (1998) Alnus rubra (Bong.) nodule spore type distribution in southwestern British Columbia. Plant Ecol 135:197–205

    Article  Google Scholar 

  • Martin KJ, Posavatz NJ, Myrold DD (2003) Nodulation potential of soils from red alder stands covering a wide age range. Plant Soil 254:187–192

    Article  CAS  Google Scholar 

  • Maunuksela L, Zepp K, Koivula T, Zeyer J, Haahtela K, Hahn D (1999) Analysis of Frankia populations in three soils devoid of actinorhizal plants. FEMS Microbiol Ecol 28:11–21

    Article  CAS  Google Scholar 

  • 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

  • Mullis KB, Faloona FA, Scharf S, Saiki RK, Horn G, Erlich HA (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol 51:263–273

    PubMed  CAS  Google Scholar 

  • Myrold DD, Huss-Danell K (1994) Population dynamics of Alnus-infective Frankia in a forest soil with and without host trees. Soil Biol Biochem 26:533–540

    Article  Google Scholar 

  • Nalin R, Normand P, Domenach A-M (1997) Distribution and N2-fixing activity of Frankia strains in relation to soil depth. Physiol Plant 99:732–738

    Article  CAS  Google Scholar 

  • Navarro E, Bousquet J, Moirod A, Munive A, Piou D, Normand P (2003) Molecular phylogeny of Alnus (Betulaceae), inferred from nuclear ribosomal DNA ITS sequences. Plant Soil 254:207–217

    Article  CAS  Google Scholar 

  • Neter J, Kutner MH, Nachtsheim CJ, Wasserman W (1996) Applied linear statistical models, 4th edn. McGraw-Hill, Boston

    Google Scholar 

  • Paschke MW, Dawson JO (1993) Avian dispersal of Frankia. Can J Bot 71:1128–1131

    Google Scholar 

  • Paschke MW, Dawson JO, Condon BM (1994) Frankia in prairie, forest, and cultivated soils of central Illinois, USA. Pedobiologia 38:546–551

    Google Scholar 

  • Prat D (1989) Effects of some pure and mixed Frankia strains on seedling growth in different Alnus species. Plant Soil 113:31–38

    Article  Google Scholar 

  • Rouvier C, Prin Y, Reddell P, Normand P, Simonet P (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

    PubMed  CAS  Google Scholar 

  • SAS Institute (2001) The SAS system for Windows. Version 8.2. SAS Institute, Cary, NC

  • Sayed WF, Wheeler CT, Zahran HH, Shoreit AAM (1997) Effect of temperature and soil moisture on the survival and symbiotic effectiveness of Frankia spp. Biol Fertil Soils 25:349–353

    Article  Google Scholar 

  • Sellstedt A, Huss-Danell K, Ahlqvist A-S (1986) Nitrogen fixation and biomass production in symbioses between Alnus incana and Frankia strains with different hydrogen metabolism. Physiol Plant 66:99–107

    Article  CAS  Google Scholar 

  • Sheppard LJ, Hooker JE, Wheeler CT, Smith RI (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

    Article  Google Scholar 

  • Simms EL, Taylor DL, Povich J, Shefferson RP, Sachs JL, Urbina M, Tausczik Y (2006) An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc Biol Sci 273:77–81

    Article  PubMed  Google Scholar 

  • Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach A-M, Gourbière Prin Y, Dawson JO, Normand P (1999) Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1:525–533

    Article  PubMed  CAS  Google Scholar 

  • Smolander A (1990) Frankia populations in soils under different tree species–with special emphasis on soils under Betula pendula. Plant Soil 121:1–10

    Article  Google Scholar 

  • Smolander A, Sundman V (1987) Frankia in acid soils of forests devoid of actinorhizal plants. Physiol Plant 70:297–303

    Article  Google Scholar 

  • Uliassi DD, Ruess RW (2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana river floodplain. Ecology 83:88–103

    Article  Google Scholar 

  • Valdés M, Pérez N-O, Estrada-de los Santos P, Caballero-Mellado J, Peña-Cabriales JJ, Normand P, Hirsch AM (2005) Non-Frankia actinomycetes isolated from surface-sterilized roots of Casuarina equisetifolia fix nitrogen. Appl Environ Microbiol 71:460–466

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Van Cleve K, Viereck LA, Schlentner RL (1971) Accumulation of nitrogen in alder (Alnus) ecosystems near Fairbanks, Alaska. Arc Alp Res 3:101–114

    Article  Google Scholar 

  • Van Cleve K, Dyrness CT, Marion GM, Erickson R (1993) Control of soil development on the Tanana River floodplain, interior Alaska. Can J For Res 23:941–955

    Article  Google Scholar 

  • Van Cleve K, Viereck LA, Dyrness CT (1996) State factor control of soils and forest succession along the Tanana River in interior Alaska, USA. Arc Alp Res 28:388–400

    Article  Google Scholar 

  • van Dijk C, Sluimer A (1994) Resistance to an ineffective Frankia strain type in Alnus glutinosa (L.) Gaertn. New Phyt 128:497–504

    Article  Google Scholar 

  • van Dijk C, Sluimer A, Weber A (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

    Article  Google Scholar 

  • Vogel JG, Gower ST (1998) Carbon and nitrogen dynamics of boreal Jack pine stands with and without a green alder understory. Ecosystems 1:386–400

    Article  CAS  Google Scholar 

  • Walker LR, Chapin FS III (1986) Physiological controls over seedling growth in primary succession on an Alaskan floodplain. Ecology 67:1508–1523

    Article  Google Scholar 

  • Wall LG (2000) The actinorhizal symbiosis. J Plant Growth Regul 19:167–182

    PubMed  CAS  Google Scholar 

  • Weber A (1986) Distribution of spore-positive and spore-negative nodules in stands of Alnus glutinosa and Alnus incana in Finland. Plant Soil 96:205–213

    Article  Google Scholar 

  • Weber A (1990) Host specificity and efficiency of nitrogenase activity of Frankia strains from Alnus incana and Alnus glutinosa. Symbiosis 8:47–60

    CAS  Google Scholar 

  • Weber A, Nurmiaho-Lassila E-L, Sundman V (1987) Features of the intrageneric Alnus-Frankia specificity. Physiol Plant 70:289–296

    Article  Google Scholar 

  • West SA, Kiers ET, Simms EL, Denison RF (2002) Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc Lond Biol Sci 269:685–694

    Article  Google Scholar 

  • Wolters DJ, van Dijk C, Zoetendal EG, Akkermans DL (1997) Phylogenetic characterization of ineffective Frankia in Alnus glutinosa (L.) Gaertn. nodules from wetland soil inoculants. Mol Ecol 6:971–981

    Article  PubMed  CAS  Google Scholar 

  • Wurtz TL (1995) Understory alder in three boreal forests of Alaska: local distribution and effects on soil fertility. Can J For Res 25:987–996

    Article  Google Scholar 

  • Young DR, Sande E, Peters GA (1992) Spatial relationships of Frankia and Myrica cerifera on a Virginia, USA barrier island. Symbiosis 12:209–220

    Google Scholar 

  • Zimpfer JF, Kennedy GJ, Smyth CA, Hamelin J, Navarro E, Dawson JO (1999) Localization of Casuarina-infective Frankia near Casuarina cunninghamiana trees in Jamaica. Can J Bot 77:1248–1256

    Article  Google Scholar 

  • Zitzer SF, Dawson JO (1992) Soil properties and actinorhizal vegetation influence nodulation of Alnus glutinosa and Elaeagnus angustifolia by Frankia. Plant Soil 140:197–204

    Article  Google Scholar 

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Acknowledgments

We thank Lola Oliver of the UAF Forest Soils Laboratory for providing resources and expertise for mass spec analysis, and Jason Schneider for field support. This manuscript benefited greatly from the suggestions of Dr. Christa Mulder and Dr. Naoki Takebayashi. We also thank four anonymous reviewers for providing suggestions which substantially improved this manuscript. Funding was provided by the Bonanza Creek Long-Term Ecological Research program (funded jointly by NSF grant DEB-0423442 and USDA Forest Service, Pacific Northwest Research Station grant PNW01-JV11261952-231). The research conducted in this study is in compliance with all applicable US laws.

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Authors and Affiliations

  1. Institute of Arctic Biology, University of Alaska, Fairbanks, Fairbanks, AK, 99775, USA

    Michael Damon Anderson, Roger W. Ruess & D. Lee Taylor

  2. Department of Crop and Soil Science, Oregon State University, Corvallis, OR, 97331, USA

    David D. Myrold

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  1. Michael Damon Anderson
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  2. Roger W. Ruess
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Correspondence to Michael Damon Anderson.

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Communicated by Andrea Polle.

Nomenclature: Flora of North America (http://hua.huh.harvard.edu/FNA/).

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Anderson, M.D., Ruess, R.W., Myrold, D.D. et al. Host species and habitat affect nodulation by specific Frankia genotypes in two species of Alnus in interior Alaska. Oecologia 160, 619–630 (2009). https://doi.org/10.1007/s00442-009-1330-0

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