Intergenomic epistasis and coevolutionary constraint in plants and rhizobia

Evolution

Volumn 64, Issue 5, 2010, Pages 1446-1458

  Heath, Katy D ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

G G; Genetic correlation; Genotype genotype interaction; Local adaptation; Medicago truncatula; Sinorhizobium

Indexed keywords

PRIMER DNA;

COEVOLUTION; EPISTASIS; FITNESS; GENOTYPE; LEGUME; LOCAL ADAPTATION; MUTUALISM; RHIZOBACTERIUM; TRADE-OFF;

ANALYSIS OF VARIANCE; ARTICLE; EVOLUTION; GENETIC EPISTASIS; GENETICS; GENOTYPE; NUCLEOTIDE SEQUENCE; PLANT; PLANT GENOME; RHIZOBIUM; EPISTASIS;

ANALYSIS OF VARIANCE; BASE SEQUENCE; DNA PRIMERS; EPISTASIS, GENETIC; EVOLUTION; GENOME, PLANT; GENOTYPE; PLANTS; RHIZOBIUM; BIOLOGICAL EVOLUTION;

MEDICAGO TRUNCATULA; RHIZOBIACEAE; RHIZOBIUM; SINORHIZOBIUM;

EID: 77953731497     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00913.x     Document Type: Article

References (72)

1. Agrawal A F, Stinchcombe J R. How much do genetic covariances alter the rate of adaptation?. Proc. R Soc. Lond. B 2009, 276:1183-1191.
2. Bailly X, Olivieri I, De Mita S, Cleyet-Marel J C, Bena G. Recombination and selection shape the molecular diversity pattern of nitrogen-fixing Sinorhizobium sp. associated to Medicago. Mol. Ecol. 2006, 15:2719-2734.
3. Bever J D. Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecol. Lett. 1999, 2:52-61.
4. Bever J D. Negative feedback within a mutualism: host-specific growth of myxorrhizal fungi reduces plant benefit. Proc. R. Soc. Lond. B 2002, 274:1905-1912.
5. Blows M W. A tale of two matrices: multivariate approaches in evolutionary biology. J. Evol. Biol. 2007, 20:1-8.
6. Blows M, Chenoweth S, Hine E. Orientation of the genetic variance-covariance matrix and the fitness surface for multiple male sexually selected traits. Am. Nat. 2004, 163:329-340.
7. Bonnin I, Huguet T, Gherardi M, Prosperi J M, Olivieri I. High level of polymorphism and spatial structure in a selfing plant species, Medicago truncatula (Leguminosae), shown using RAPD markers. Am. J. Bot. 1996, 83:843-855.
8. Bonnin I, Ronfort J, Wozniak F, Olivieri I. Spatial effects and rare outcrossing events in Medicago truncatula (Fabaceae). Mol. Ecol. 2001, 10:1371-1383.
9. Brodie E D, Ridenhour B J, Brodie E D. The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 2002, 56:2067-2082.
10. Bull J J, Rice W R. Distinguishing mechanisms for the evolution of co-operation. J. Theor. Biol. 1991, 149:63-74.
11. Cassell D L. A randomized-test wrapper for SAS PROCs. 2002, 1-4. Pages, , SAS Institute, Cary, NC
12. Day T, Nagel L, van Oppen M J H, Caley M J. Factors affecting the evolution of bleaching resistance in corals. Am. Nat. 2008, 171:E72-E88.
13. Denison R F. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 2000, 156:567-576.
14. Denison R, Kiers E. Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis. FEMS Microbiol. Lett. 2004, 237:187-193.
15. Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 2005, 1:47-50.
16. Fred E B, Baldwin I L, McCoy E. Root nodule bacteria and leguminous plants 1932, Univ. of Wisconsin Press, Madison, WI
17. Fry J D. The general vigor problem-can antagonistic pleiotropy be detected when genetic covariances are positive. Evolution 1993, 47:327-333.
18. Garau G, Reeve W, Brau L, Deiana P, Yates R, James D, Tiwari R, O'Hara G, Howieson J. The symbiotic requirements of different Medicago spp. suggest the evolution of Sinorhizobium meliloti and S-Medicae with hosts differentially adapted to soil pH. Plant Soil 2005, 276:263-277.
19. Gomulkiewicz R, Nuismer S L, Thompson J N. Coevolution in variable mutualisms. American Naturalist 2003, 162:S80-S93.
20. Heath K D, Tiffin P. Context dependence in the coevolution of plant and rhizobial mutualists. Proc. R. Soc. Lond. B 2007, 274:1905-1912.
21. Heath K D, Tiffin P. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 2009, 63:652-662.
22. Herre E A, West S A. Conflict of interest in a mutualism: documenting the elusive fig wasp/seed trade-off. Proc. R. Soc. Lond. B 1997, 264:1501-1507.
23. Hoeksema J D, Thompson J N. Geographic structure in a widespread plant-mycorrhizal interaction: pines and false truffles. J. Evol. Biol. 2007, 20:1148-1163.
24. Johnson N C, Graham J H, Smith F A. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 1997, 135:575-585.
25. Kiers E T, Rousseau R A, West S A, Denison R F. Host sanctions and the legume-rhizobium mutualism. Nature 2003, 425:78-81.
26. Kirkpatrick M. Patterns of quantitative genetic variation in multiple dimensions. Genetica 2008, 1-14.
27. Lande R. Quantitative genetic-analysis of multivariate evolution, applied to brain-body size allometry. Evolution 1979, 33:402-416.
28. Lau J A. Evolutionary responses of native plants to novel community members. Evolution 2006, 60:56-63.
29. Law R. Evolution in a mutualistic environment. The biology of mutualism: ecology and evolution 1985, 145-170. Boucher D H. Pages, , ed, Oxford Univ. Press, New York, NY
30. Lesins K, Lesins I. Genus Medicago (Leguminosae): a taxogenetic study 1979, Dr. W. Junk bv Publishers, The Hague, Netherlands
31. Littell R C, Milliken G A, Stroup W W, Wolfinger R D. SAS system for mixed models 1996, SAS Institute, Cary, NC
32. Lupski J R, Weinstock G M. Short, interspersed repetitive DNA-sequences in prokaryotic genomes. J. Bacteriol. 1992, 174:4525-4529.
33. Messina F J, Fry J D. Environment-dependent reversal of a life history trade-off in the seed beetle Callosobruchus maculatus. J. Evol. Biol. 2003, 16:501-509.
34. Mhadhbi H, Jebara M, Limam F, Huguet T, Aouani M. Interaction between Medicago truncatula lines and Sinorhizobium meliloti strains for symbiotic efficiency and nodule antioxidant activities. Physiol. Plant. 2005, 124:4-11.
35. Molofsky J, Bever J, Antonovics J. Coexistence under positive frequency dependence. Proc. R. Soc. Lond. B 2001, 268:273-277.
36. Mytton L R, Jones D G. The response to selection for increased nodule tissue in white clover (Trifolium repens L.). Plant Soil Special Volume 1971, 17-25.
37. Neuhauser C, Fargione J. A mutualism-parasitism continuum model and its application to plant-mycorrhizae interactions. Ecol. Model. 2004, 177:337-352.
38. Nuismer S, Doebeli M. Genetic correlations and the coevolutionary dynamics of three-species systems. Evolution 2004, 58:1165-1177.
39. Parker M A. Plant fitness variation caused by different mutualist genotypes. Ecology 1995, 76:1525-1535.
40. Penmetsa R, Cook D. A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 1997, 275:527-530.
41. Penmetsa R, Frugoli J, Smith L, Long S, Cook D. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiol. 2003, 131:998-1008.
42. Rademaker J L W, de Bruijn F J. Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer assisted pattern analysis. DNA markers: protocols, applications, and overviews 1997, 151-171. Caetano-Anolles G, Gresshoff P M. Pages, , eds, Wiley-Liss, NY
43. Ratcliff W C, Denison R F. Rhizobitoxine producers gain more poly-3-hydroxybutyrate in symbiosis than do competing rhizobia, but reduce plant growth. Isme J. 2009, 3:870-872.
44. Ratcliff W C, Kadam S V, Denison R F. Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiol. Ecol. 2008, 65:391-399.
45. Reed D H, Frankham R. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 2001, 55:1095-1103.
46. Robinson K, Beyene D, van Berkum P, Knight-Mason R, Bhardwaj H. Variability in plant-microbe interaction between Lupinus lines and Bradyrhizobium strains. Plant. Sci. 2000, 159:257-264.
47. Rome S, Brunel B, Normand P, Cleyet-Marel J C. Evidence that two genomic species of Rhizobium are associated with Medicago truncatula. Arch. Microbiol. 1996, 165:285-288.
48. Roumiantseva M L, Yakutkina V V, Damman-Kalinowski T, Sharypova L A, Keller M, Simarov B V. Comparative analyses if structural organization of the genome in alfalfa nodule bacteria Sinorhizobium medicae and Sinorhizobium meliloti. Russian J. Genet. 1999, 35:128-135.
49. Rudgers J A, Strauss S Y. A selection mosaic in the facultative mutualism between ants and wild cotton. Proc. R. Soc. Lond. B 2004, 271:2481-2488.
50. Sachs J L, Mueller U G, Wilcox T P, Bull J J. The evolution of cooperation. Q. Rev. Biol. 2004, 79:135-160.
51. Salvaudon L, Héraudet V, Shykoff J A. Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system. Evolution 2005, 59:2518-2524.
52. Schnabel E, Kulikova O, Penmetsa R, Bisseling T, Cook D, Frugoli J. An integrated physical, genetic and cytogenetic map around the sunn locus of Medicago truncatula. Genome 2003, 46:665-672.
53. Service P M, Rose M R. Genetic covariance among life-history components: the effect of novel environments. Evolution 1985, 39:943-945.
54. Shapiro S S, Wilk M B. An analysis of variance test for normality (complete samples). Biometrika 1965, 52:591-611.
55. Shaw R G. Response to density in a wild population of the perennial herb Salvia lyrata: variation among families. Evolution 1986, 40:492-505.
56. Simms E L, Taylor D L, Povich J, Shefferson R P, Sachs J L, Urbina M, Tausczik Y. And empirical test of partner choice mechanisms in a wild legume-rhizobium mutualism. Proc. R. Soc. Lond. B 2005, 273:77-81.
57. Smith R A, Rausher M D. Selection for character displacement is constrained by the genetic architecture of floral traits in the ivyleaf morning glory. Evolution 2008, 62:2829-2841.
58. Steven J C, Delph L F, Brodie E D. Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia. Evolution 2007, 61:42-57.
59. Stinchcombe J R, Rausher M. Diffuse selection on resistance to deer herbivory in the ivyleaf morning glory, Ipomoea hederacea. Am. Nat. 2001, 158:376-388.
60. Swofford D L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) 2000, Version 4, Sinauer Associates, Sunderland, MA
61. Thompson J N. The coevolutionary process 1994, Univ. of Chicago Press, Chicago, IL
62. Thompson J N, Cunningham B M. Geographic structure and dynamics of coevolutionary selection. Nature 2002, 417:735-738.
63. Trivers R L. The evolution of reciprocal altruism. Q. Rev. Biol. 1971, 46:35-57.
64. van Berkum P. Evidence for a third uptake hydrogenase phenotype among the soybean bradyrhizobia. Appl. Environ. Microbiol. 1990, 56:3835-3841.
65. Versalovic J, Koeuth T, Lupski J R. Distribution of repetitive DNA-sequences in Eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res. 1991, 19:6823-6831.
66. Via S, Lande R. Genotype-environment interactions and the evolution of phenotypic plasticity. Evolution 1985, 39:505-522.
67. Vincent J M. A manual for the practical study of root-nodule bacteria 1970, Oxford and Edinburgh, UK, Blackwell Scientific Publications
68. Wade M J. Epistasis as a genetic constraint within populations and an accelerant of adaptive divergence among them. Epistasis and the evolutionary process 2000, 213-231. Wolf J BBrodie E DWade M J. Pp., , eds, Oxford Univ. Press, NY
69. Wade M J. The co-evolutionary genetics of ecological interactions. Nat. Rev. Genet. 2007, 8:185-195.
70. West S A, Kiers E T, Pen I, Denison R F. Sanctions and mutualism stability: when should less beneficial mutualists be tolerated?. J. Evol. Biol. 2002, 15:830-837.
71. Wolf J B. Indirect genetic effects and gene interactions. Epistasis and the evolutionary process 2000, 158-176. Wolf J BBrodie E DWade M J. Pp., , eds, Oxford Univ. Press, NY
72. Young N D, Cannon S B, Sato S, Kim D, Cook D R, Town C D, Roe B A, Tabata S. Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiol. 2005, 137:1174-1181.