期刊论文详细信息
Annals of Occupational and Environmental Medicine
Specialization-generalization trade-off in a Bradyrhizobium symbiosis with wild legume hosts
Martine Ehinger1  Toni J Mohr1  Juliana B Starcevich1  Joel L Sachs2  Stephanie S Porter1  Ellen L Simms1 
[1] Department of Integrative Biology, University of California, Berkeley, CA, USA
[2] Institute of Integrative Genomic Biology, University of California, Riverside, CA, USA
关键词: Rhizobia;    Legumes;    Alpha-proteobacteria;    Lotus;    Acmispon strigosus (strigose trefoil);    Lupinus bicolor (dove lupine);    Coevolution;    Specialization;    Symbiosis;    Mutualism;   
Others  :  834725
DOI  :  10.1186/1472-6785-14-8
 received in 2013-12-03, accepted in 2014-03-10,  发布年份 2014
【 摘 要 】

Background

Specialized interactions help structure communities, but persistence of specialized organisms is puzzling because a generalist can occupy more environments and partake in more beneficial interactions. The “Jack-of-all-trades is a master of none” hypothesis asserts that specialists persist because the fitness of a generalist utilizing a particular habitat is lower than that of a specialist adapted to that habitat. Yet, there are many reasons to expect that mutualists will generalize on partners.

Plant-soil feedbacks help to structure plant and microbial communities, but how frequently are soil-based symbiotic mutualistic interactions sufficiently specialized to influence species distributions and community composition? To address this question, we quantified realized partner richness and phylogenetic breadth of four wild-grown native legumes (Lupinus bicolor, L. arboreus, Acmispon strigosus and A. heermannii) and performed inoculation trials to test the ability of two hosts (L. bicolor and A. strigosus) to nodulate (fundamental partner richness), benefit from (response specificity), and provide benefit to (effect specificity) 31 Bradyrhizobium genotypes.

Results

In the wild, each Lupinus species hosted a broader genetic range of Bradyrhizobium than did either Acmispon species, suggesting that Acmispon species are more specialized. In the greenhouse, however, L. bicolor and A. strigosus did not differ in fundamental association specificity: all inoculated genotypes nodulated both hosts. Nevertheless, A. strigosus exhibited more specificity, i.e., greater variation in its response to, and effect on, Bradyrhizobium genotypes. Lupinus bicolor benefited from a broader range of genotypes but averaged less benefit from each. Both hosts obtained more fitness benefit from symbionts isolated from conspecific hosts; those symbionts in turn gained greater fitness benefit from hosts of the same species from which they were isolated.

Conclusions

This study affirmed two important tenets of evolutionary theory. First, as predicted by the Jack-of-all-trades is a master of none hypothesis, specialist A. strigosus obtained greater benefit from its beneficial symbionts than did generalist L. bicolor. Second, as predicted by coevolutionary theory, each test species performed better with partner genotypes isolated from conspecifics. Finally, positive fitness feedback between the tested hosts and symbionts suggests that positive plant-soil feedback could contribute to their patchy distributions in this system.

【 授权许可】

   
2014 Ehinger et al.; licensee BioMed Central Ltd.

【 参考文献 】
  • [1]Poisot T, Bever JD, Nemri A, Thrall PH, Hochberg ME: A conceptual framework for the evolution of ecological specialisation. Ecol Lett 2011, 14(9):841-851.
  • [2]Williams GC: Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton, New Jersey, USA: Princeton University Press; 1966.
  • [3]Kawecki TJ, Ebert D: Conceptual issues in local adaptation. Ecol Lett 2004, 7(12):1225-1241.
  • [4]Futuyma DJ, Moreno G: The evolution of ecological specialization. Annu Rev Ecol Syst 1988, 19:207-234.
  • [5]Wilson DS, Yoshimura J: On the coexistence of specialists and generalists. Am Nat 1994, 144(4):692-707.
  • [6]Burdon JJ, Gibson AH, Searle SD, Woods MJ, Brockwell J: Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian Acacia: within-species interactions. J Appl Ecol 1999, 36(3):398-408.
  • [7]Straub CS, Ives AR, Gratton C: Evidence for a trade-off between host-range breadth and host-use efficiency in Aphid parasitoids. Am Nat 2011, 177(3):389-395.
  • [8]Agrawal AA, Conner JK, Rasmann S: Tradeoffs and negative correlations in evolutionary ecology. In Evolution After Darwin: The First 150 Years. Edited by Bell MA, Futuyma DJ, Eanes WF, Levinton JS. Sunderland, MA, USA: Sinauer; 2010:243-268.
  • [9]Kassen R: The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 2002, 15:173-190.
  • [10]Levins R: Evolution in Changing Environments. Princeton, N.J.: Princeton University Press; 1968.
  • [11]MacArthur RH: Geographical Ecology: Patterns in the Distribution of Species. New York, USA: Harper & Row; 1972.
  • [12]Bever JD: Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecol Lett 1999, 2:52-61.
  • [13]van der Putten WH, Van Dijk C, Peters BAM: Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 1993, 362:53-56.
  • [14]Connell JH: On the Role of Natural Enemies in Preventing Competitive Exclusion in Some Marine Animals and in Rain Forest Trees. In Dynamics of Populations. Edited by Boer PJ, Gradwell GR. Wageningen: Centre for Agricultural Publications and Documentation; 1971:298-310.
  • [15]Janzen DH: Herbivores and the number of tree species in tropical forests. Am Nat 1970, 104:501-528.
  • [16]Augspurger CK: Seed dispersal of the tropical tree, Platypodium elegans, and the escape of its seedlings from fungal pathogens. J Ecol 1983, 71(3):759-771.
  • [17]Blomqvist MM, Olff H, Blaauw MB, Bongers T, Van Der Putten WH: Interactions between above- and belowground biota: importance for small-scale vegetation mosaics in a grassland ecosystem. Oikos 2000, 90(3):582-598.
  • [18]Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M: Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 2010, 25(8):468-478.
  • [19]Friesen ML, Porter SS, Stark SC, Wettberg EJ, Sachs JL, Martinez-Romero E: Microbially-mediated plant functional traits. Annu Rev Ecol Evol Syst 2011, 43:23-46.
  • [20]Bever JD, Broadhurst LM, Thrall PH: Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks. Ecol Lett 2013, 16(2):167-174.
  • [21]Klironomos JN: Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 2002, 417(6884):67-70.
  • [22]Kulmatiski A, Beard KH, Stevens JR, Cobbold SM: Plant–soil feedbacks: a meta-analytical review. Ecol Lett 2008, 11(9):980-992.
  • [23]Liu X, Liang M, Etienne RS, Wang Y, Staehelin C, Yu S: Experimental evidence for a phylogenetic Janzen–Connell effect in a subtropical forest. Ecol Lett 2012, 15(2):111-118.
  • [24]Li R, Yu S, Wang Y, Staehelin C, Zang R: Distance-dependent effects of soil-derived biota on seedling survival of the tropical tree legume Ormosia semicastrata. J Veg Sci 2009, 20(3):527-534.
  • [25]Florence RG: Decline of old-growth redwood forests in relation to some soil microbiological processes. Ecology 1965, 46(1/2):52-64.
  • [26]Webb LJ, Tracey JG, Haydock KP: A factor toxic to seedlings of the same species associated with living roots of the non-gregarious subtropical rain forest tree Grevillea robusta. J Appl Ecol 1967, 4(1):13-25.
  • [27]Mordecai EA: Pathogen impacts on plant communities: unifying theory, concepts, and empirical work. Ecol Monogr 2011, 81(3):429-441.
  • [28]Taylor DL, Bruns TD: Community structure of ectomycorrhizal fungi in a Pinus muricata forest: Minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 1999, 8(11):1837-1850.
  • [29]Law R: Evolution in a Mutualistic Environment. In The Biology of Mutualism: Ecology and Evolution. Edited by Boucher D. New York, NY: Oxford University Press; 1985.
  • [30]van der Pijl L: Ecological aspects of flower evolution. I. Phyletic evolution. Evolution 1960, 14(4):403-416.
  • [31]Pauw A: Collapse of a pollination web in small conservation areas. Ecology 2007, 88(7):1759-1769.
  • [32]Geerts S, Pauw A: The cost of being specialized: pollinator limitation in the endangered geophyte Brunsvigia litoralis (Amaryllidaceae) in the Cape Floristic Region of South Africa. S Afr J Bot 2012, 78:159-164.
  • [33]Fettell NA, O’Connor GE, Carpenter DJ, Evans J, Bamforth I, Oti-Boateng C, Hebb DM, Brockwell J: Nodulation studies on legumes exotic to Australia: the influence of soil populations and inocula of Rhizobium leguminosarum bv. viciae on nodulation and nitrogen fixation by field peas. Appl Soil Ecol 1997, 5(3):197-210.
  • [34]Coventry DR, Hirth JR, Reeves TG, Jones HR: Development of populations of rhizobium trifolii and nodulation of subterranean clover following the cropping phase in crop-pasture rotations in southeastern Australia. Soil Biol Biochem 1985, 17(1):17-22.
  • [35]Del Papa MF, Pistorio M, Balagué LJ, Draghi WO, Wegener C, Perticari A, Niehaus K, Lagares A: A microcosm study on the influence of pH and the host-plant on the soil persistence of two alfalfa-nodulating rhizobia with different saprophytic and symbiotic characteristics. Biol Fertil Soils 2003, 39(2):112-116.
  • [36]Hagen M, Puhler A, Selbitschka W: The persistence of bioluminescent Rhizobium meliloti strains L1 (RecA-) and L33 (RecA+) in non-sterile microcosms depends on the soil type, on the co-cultivation of the host legume alfalfa and on the presence of an indigenous R. meliloti population. Plant Soil 1997, 188:257-266.
  • [37]Simonet P, Navarro E, Rouvier C, Reddell P, Zimpfer J, Dommergues Y, Bardin R, Combarro P, Hamelin J, Domenach A-M, Gourbière F, Prin Y, Dawson JO, Normand P: Co-evolution between Frankia populations and host plants in the family Casuarinaceae and consequent patterns of global dispersal. Environ Microbiol 1999, 1(6):525-533.
  • [38]Béna G, Lyet A, Huguet T, Olivieri I: Medicago-Sinorhizobium symbiotic specificity evolution and the geographic expansion of Medicago. J Evol Biol 2005, 18(6):1547-1558.
  • [39]Parker MA: Mutualism as a constraint on invasion success for legumes and rhizobia. Divers Distrib 2001, 7:125-136.
  • [40]Parker MA, Malek W, Parker IM: Growth of an invasive legume is symbiont limited in newly occupied habitats. Divers Distrib 2006, 12(5):563-571.
  • [41]Rodríguez-Echeverría S, Crisóstomo JA, Nabais C, Freitas H: Belowground mutualists and the invasive ability of Acacia longifolia in coastal dunes of Portugal. Biol Invasions 2009, 11(3):651-661.
  • [42]Rodríguez-Echeverría S: Rhizobial hitchhikers from down under: invasional meltdown in a plant-bacteria mutualism? J Biogeog 2010, 37(8):1611-1622.
  • [43]Stanton-Geddes J, Anderson CG: Does a facultative mutualism limit species range expansion? Oecologia (Berlin) 2011, 167:149-155.
  • [44]Reinhart KO, Callaway RM: Soil biota and invasive plants. New Phytol 2006, 170(3):445-457.
  • [45]Douglas AE: Host benefit and the evolution of specialization in symbiosis. Heredity 1998, 81:599-603.
  • [46]Buddemeier RW, Fautin DG: Coral bleaching as an adaptive mechanism. Bioscience 1993, 43(5):320-326.
  • [47]Lundgren JG, Lehman RM: Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle. PLoS ONE 2010, 5(5):e10831.
  • [48]Mueller UG, Mikheyev AS, Hong E, Sen R, Warren DL, Solomon SE, Ishak HD, Cooper M, Miller JL, Shaffer KA, Juenger TE: Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant–fungus symbiosis. Proc Natl Acad Sci 2011, 108(10):4053-4056.
  • [49]Kiester AR, Lande R, Schemske DW: Models of coevolution and speciation in plants and their pollinators. Am Nat 1984, 124(2):220-243.
  • [50]Thompson JN: The Geographic Mosaic of Coevolution. Chicago: University of Chicago Press; 2005.
  • [51]Rathke B: Competition and Facilitation Among Plants for Pollination. In Pollination Biology. Edited by Real L. New York: Academic Press; 1983:305-329.
  • [52]Yoder JB, Nuismer SL: When does coevolution promote diversification? Am Nat 2010, 176(6):802-817.
  • [53]Fleming TH, Venable DL, Herrera LG: Opportunism vs specialization: the evolution of dispersal strategies in fleshy-fruited plants. Vegetatio 1993, 107/108:107-120.
  • [54]Waser NM, Chittka L, Price MV, Williams NM, Ollerton J: Generalization in pollination systems, and why it matters. Ecology 1996, 77(4):1043-1060.
  • [55]Barrett LG, Broadhurst LM, Thrall PH: Geographic adaptation in plant-soil mutualisms: tests using Acacia spp. and rhizobial bacteria. Funct Ecol 2011, 26(2):457-468.
  • [56]Bruns TD, Bidartondo MI, Taylor DL: Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol 2002, 42(2):352-359.
  • [57]Yang SM, Tang F, Gao MQ, Krishnan HB, Zhu HY: R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci U S A 2010, 107(43):18735-18740.
  • [58]Bull JJ, Rice WR: Distinguishing mechanisms for the evolution of cooperation. J Theor Biol 1991, 149(1):63-74.
  • [59]Noë R, Hammerstein P: Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol 1994, 35:1-11.
  • [60]Johnstone RA, Bshary R: From parasitism to mutualism: partner control in asymmetric interactions. Ecol Lett 2002, 5(5):634-639.
  • [61]Sachs JL, Mueller UG, Wilcox TP, Bull JJ: The evolution of cooperation. Q Rev Biol 2004, 79:135-160.
  • [62]Simms EL, Taylor DL: Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr Comp Biol 2002, 42(2):369-380.
  • [63]Bronstein JL: The exploitation of mutualisms. Ecol Lett 2001, 4(3):277-287.
  • [64]West SA, Kiers ET, Simms EL, Denison RF: Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc R Soc Lond Ser B 2002, 269(1492):685-694.
  • [65]Foster KR, Kokko H: Cheating can stabilize cooperation in mutualisms. Proc R Soc B Biol Sci 2006, 273(1598):2233-2239.
  • [66]Sachs JL, Ehinger MO, Simms EL: Origins of cheating and loss of symbiosis in wild Bradyrhizobium. J Evol Biol 2010, 23(5):1075-1089.
  • [67]Friesen ML: Widespread fitness alignment in the legume-rhizobium symbiosis. New Phytol 2012, 194(4):1096-1111.
  • [68]Tirichine L, De Billy F, Huguet T: Mtsym6, a gene conditioning Sinorhizobium strain-specific nitrogen fixation in Medicago truncatula. Plant Physiol (Rockville) 2000, 123(3):845-852.
  • [69]Paine RT: Food webs - Linkage, interaction strength and community infrastructure - the 3rd Tansley Lecture. J Anim Ecol 1980, 49(3):667-685.
  • [70]Berlow EL, Neutel A-M, Cohen JE, De Ruiter PC, Ebenman B, Emmerson M, Fox JW, Jansen VAA, Iwan Jones J, Kokkoris GD, Logofet DO, McKane AJ, Montoya JM, Petchey O: Interaction strengths in food webs: issues and opportunities. J Anim Ecol 2004, 73(3):585-598.
  • [71]Poisot T, Canard E, Mouquet N, Hochberg ME: A comparative study of ecological specialization estimators. Methods Ecol Evol 2012, 3(3):537-544.
  • [72]Schemske DW, Horvitz CC: Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 1984, 225:519-521.
  • [73]Reynolds HL, Vogelsang KM, Hartley AE, Bever JD, Schultz PA: Variable responses of old-field perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia 2006, 147(2):348-358.
  • [74]Harley JL, Smith SE: Mycorrhizal Symbiosis. New York, USA: Academic Press; 1983.
  • [75]Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, Venail P, Villéger S, Mouquet N: Defining and measuring ecological specialization. J Appl Ecol 2010, 47(1):15-25.
  • [76]Chase JM, Leibold MA: Ecological Niches: Linking Classical and Contemporary Approaches. Chicago, IL, USA: University of Chicago Press; 2003.
  • [77]Heath KD: Intergenomic epistasis and coevolutionary constrain in plants and rhizobia. Evolution 2009, 64(5):1446-1458.
  • [78]Sachs JL, Kembel SW, Lau AH, Simms EL: In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Appl Environ Microbiol 2009, 75(14):4727-4735.
  • [79]Stępkowski T, Hughes CE, Law IJ, Markiewicz L, Gurda D, Chlebicka A, Moulin L: Diversification of lupine Bradyrhizobium strains: evidence from nodulation gene trees. Appl Environ Microbiol 2007, 73(10):3254-3264.
  • [80]Jarabo-Lorenzo A, Perez-Galdona R, Donate-Correa J, Rivas R, Velazquez E, Hernandez M, Temprano F, Martinez-Molina E, Ruiz-Argueso T, Leon-Barrios M: Genetic diversity of bradyrhizobial populations from diverse geographic origins that nodulate Lupinus spp. and Ornithopus spp. Syst Appl Microbiol 2003, 26(4):611-623.
  • [81]Aguilar OM, Riva O, Peltzer E: Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc Natl Acad Sci U S A 2004, 101(37):13548-13553.
  • [82]Brockwell J, Bottomley PJ, Thies JE: Manipulation of rhizobia microflora for improving legume productivity and soil fertility: a critical assessment. Plant Soil 1995, 174(1–2):143-180.
  • [83]Rangin C, Brunel B, Cleyet-Marel J-C, Perrineau M-M, Béna G: Effects of Medicago truncatula genetic diversity, rhizobial competition, and strain effectiveness on the diversity of a natural Sinorhizobium species community. Appl Environ Microbiol 2008, 74(18):5653-5661.
  • [84]Saeki K: Rhizobial measures to evade host defense strategies and endogenous threats to persistent symbiotic nitrogen fixation: a focus on two legume-rhizobium model systems. Cell Mol Life Sci 2011, 68(8):1327-1339.
  • [85]Oldroyd GED, Murray JD, Poole PS, Downie JA: The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 2011, 45(1):119-144.
  • [86]Rousset F, Roze D: Constraints on the origin and maintenance of genetic kin recognition. Evolution 2007, 61(10):2320-2330.
  • [87]Sachs JL, Russell JE, Lii YE, Black KC, Lopez G, Patil AS: Host control over infection and proliferation of a cheater symbiont. J Evol Biol 2010, 23(9):1919-1927.
  • [88]Heath KD, Tiffin P: Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 2009, 63(3):652-662.
  • [89]Lie TA, Göktan D, Engin M, Pijnenborg J, Anlarsal E: Co-evolution of the legume-Rhizobium association. Plant Soil 1987, 100:171-181.
  • [90]Wielbo J: Rhizobial communities in symbiosis with legumes: genetic diversity, competition and interactions with host plants. Cent Eur J Biol 2012, 7(3):363-372.
  • [91]Robleto EA, Kmiecik K, Oplinger ES, Nienhuis J, Triplett EW: Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl Environ Microbiol 1998, 64(7):2630-2633.
  • [92]Bittinger MA, Milner JL, Saville BJ, Handelsman J: rosR, a determinant of nodulation competitiveness in Rhizobium etli. Mol Plant Microbe Interact 1997, 10(2):180-186.
  • [93]Wielbo J, Marek-Kozaczuk M, Kubik-Komar A, Skorupska A: Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Can J Microbiol 2007, 53(8):957-967.
  • [94]Hynes MF, Oconnell MP: Host plant effect on competition among strains of Rhizobium leguminosarum. Can J Microbiol 1990, 36(12):864-869.
  • [95]Chatel DL, Parker CA: The colonization of host-root and soil by Rhizobia—I. Species and strain differences in the field. Soil Biol Biochem 1973, 5(4):425-432.
  • [96]Wollum AG, Cassel DK: Spatial variability of Rhizobium japonicum in Two North Carolina Soils. Soil Sci Soc Am J 1984, 48(5):1082-1086.
  • [97]Vlassak KM, Vanderleyden J: Factors influencing nodule occupancy by inoculant rhizobia. Crit Rev Plant Sci 1997, 16(2):163-229.
  • [98]Parker MA: Mutualism in metapopulations of legumes and rhizobia. Am Nat 1999, 153:S48-S60.
  • [99]Orme AR, Tchakerian VP: Quaternary Dunes of the Pacific Coast of the Californias. In Aeolian Geomorphology Proceedings of the 17th Annual Binghamton Geomorphology Symposium, September 1986. Edited by Nickling WG. Boston: Allen & Unwin; 1986:149-175.
  • [100]Cooper WS: Coastal Dunes of California, Volume 104. Boulder, CO: Geological Society of America; 1967.
  • [101]Barbour MG, Craig RB, Drysdale FR, Ghiselin MT: Coastal Ecology: Bodega Head. Berkeley, CA: University of California Press; 1973.
  • [102]Wilkinson HH, Parker MA: Symbiotic specialization and the potential for genotypic coexistence in a plant-bacterial mutualism. Oecologia 1996, 108:361-367.
  • [103]Thrall PH, Burdon JJ, Woods MJ: Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian legumes: Interactions within and between genera. J Appl Ecol 2000, 37(1):52-65.
  • [104]Murray BR, Thrall PH, Woods MJ: Acacia species and rhizobial interactions: Implications for restoration of native vegetation. Ecol Manage Restor 2001, 2(3):213-219.
  • [105]Martinez-Romero E: Coevolution in rhizobium-legume symbiosis? DNA Cell Biol 2009, 28(8):361-370.
  • [106]Akçay E, Simms EL: Negotiation, sanctions, and context dependency in the legume-rhizobium mutualism. Am Nat 2011, 178(1):1-14.
  • [107]Bever JD: Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 2003, 157(3):465-473.
  • [108]Kisdi Ã: Dispersal: risk spreading versus local adaptation. Am Nat 2002, 159(6):579-596.
  • [109]Hastings A: Disturbance, coexistence, history, and competition for space. Theor Popul Biol 1980, 18(3):363-373.
  • [110]Buell AC, Pickart AJ, Stuart JD: Introduction history and invasion patterns of Ammophila arenaria on the North Coast of California. Conserv Biol 1995, 9(6):1587-1593.
  • [111]Danin A, Rae S, Barbour M, Jurjavcic N, Connors P, Uhlinger E: Early primary succession on dunes at bodega head. California. Madrono 1998, 45(2):101-109.
  • [112]Brouillet L: The taxonomy of North American loti (Fabaceae: Loteae): New names in Acmispon and Hosackia. J Bot Res Inst Tex 2008, 2(1):387-394.
  • [113]Wojciechowski MF, Lavin M, Sanderson MJ: A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family. Am J Bot 2004, 91(11):1846-1862.
  • [114]van Berkum P, Fuhrmann JJ: Evolutionary relationships among the soybean bradyrhizobia reconstructed from 16S rRNA gene and internally transcribed spacer region sequence divergence. Int J Syst Evol Microbiol 2000, 50:2165-2172.
  • [115]Parker MA: Divergent Bradyrhizobium symbionts on Tachigali versicolor from Barro Colorado Island, Panama. Syst Appl Microbiol 2000, 23(4):585-590.
  • [116]Katoh K, Misawa K, Kuma K, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30(14):3059-3066.
  • [117]Maddison DR, Maddison WP: MacClade 4: Analysis of Phylogeny and Character Evolution. Sunderland, MA: Sinauer Associates; 2008.
  • [118]Fox LR, Morrow PA: Specialization: species property or local phenomenon. Science 1981, 211(4485):887-893.
  • [119]Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006, 23(2):254-267.
  • [120]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14(9):817-818.
  • [121]Rodríguez F, Oliver JL, Marín A, Medina JR: The general stochastic model of nucleotide substitution. J Theor Biol 1990, 142(4):485-501.
  • [122]Hasegawa M, Kishino H, Yano T-a: Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 1985, 22(2):160-174.
  • [123]Parker MA, Lafay B, Burdon JJ, van Berkum P: Conflicting phylogeographic patterns in rRNA and nifD indicate regionally restricted gene transfer in Bradyrhizobium. Microbiology (UK) 2002, 148:2557-2565.
  • [124]Parker MA: Genetic markers for analysing symbiotic relationships and lateral gene transfer in Neotropical bradyrhizobia. Mol Ecol 2003, 12(9):2447-2455.
  • [125]Vinuesa P, Silva C, Werner D, Martínez-Romero E: Population genetics and phylogenetic inference in bacterial molecular systematics: the roles of migration and recombination in Bradyrhizobium species cohesion and delineation. Mol Phylogenet Evol 2005, 34:29-54.
  • [126]Posada D, Crandall KA: Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 2001, 98(24):13757-13762.
  • [127]Excoffier L, Smouse PE, Quattro JM: Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 1992, 131(2):479-491.
  • [128]Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform 2005, 1:47-50.
  • [129]Simms EL, Povich J, Shefferson RP, Taylor DL, Sachs JL, Tausczik Y, Urbina M: An empirical test of partner choice in a legume-rhizobium mutualism. Proc R Soc B Biol Sci 2006, 273:77-81.
  • [130]Somasegaran P, Hoben HJ: Handbook for Rhizobia: Methods in Legume-Rhizobium Technology. New York: Springer-Verlag; 1994.
  • [131]Abramoff MD, Magelhaes PJ, Ram SJ: Image processing with ImageJ. Biophoton Int 2004, 11(7):36-42.
  • [132]Kiers ET, Rousseau RA, West SA, Denison RF: Host sanctions and the legume-rhizobium mutualism. Nature 2003, 425(6953):78-81.
  • [133]Oono R, Denison RF, Kiers ET: Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol 2009, 183(4):967-979.
  • [134]Porter SS, Stanton ML, Rice KJ: Mutualism and adaptive divergence: co-invasion of a heterogeneous grassland by an exotic legume-rhizobium symbiosis. PLoS ONE 2011, 6(12):e27935.
  • [135]Friesen ML, Heath KD: One hundred years of solitude: integrating single-strain inoculations with community perspectives in the legume–rhizobium symbiosis. New Phytol 2013, 198(1):7-9.
  • [136]Heath KD, Tiffin P: Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc B Biol Sci 2007, 274(1620):1905-1912.
  • [137]Moawad M, Schmidt EL: Occurrence and nature of mixed infections in nodules of field-grown soybeans (Glycine max). Biol Fertil Soils 1987, 5(2):112-114.
  • [138]Laguerre G, Depret G, Bourion V, Duc G: Rhizobium leguminosarum bv. viciae genotypes interact with pea plants in developmental responses of nodules, roots and shoots. New Phytol 2007, 176(3):680-690.
  • [139]Ramsey PH, Ramsey PP: Power of pairwise comparisons in the equal variance and unequal sample size case. Br J Math Stat Psychol 2008, 61(1):115-131.
  • [140]Burnham KP, Anderson DR: Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd edition. Berlin: Springer-Verlag; 2002.
  • [141]Zar JH: Biostatistical Analysis. 4th edition. Englewood Cliffs, NJ: Prentice-Hall; 1999.
  • [142]R_Development_Core_Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2008.
  文献评价指标  
  下载次数:0次 浏览次数:2次