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Recent Loss of Self-Incompatibility by Degradation of the Male Component in Allotetraploid


The evolutionary transition from outcrossing to self-fertilization (selfing) through the loss of self-incompatibility (SI) is one of the most prevalent events in flowering plants, and its genetic basis has been a major focus in evolutionary biology. In the Brassicaceae, the SI system consists of male and female specificity genes at the S-locus and of genes involved in the female downstream signaling pathway. During recent decades, much attention has been paid in particular to clarifying the genes responsible for the loss of SI. Here, we investigated the pattern of polymorphism and functionality of the female specificity gene, the S-locus receptor kinase (SRK), in allotetraploid Arabidopsis kamchatica. While its parental species, A. lyrata and A. halleri, are reported to be diploid and mainly self-incompatible, A. kamchatica is self-compatible. We identified five highly diverged SRK haplogroups, found their disomic inheritance and, for the first time in a wild allotetraploid species, surveyed the geographic distribution of SRK at the two homeologous S-loci across the species range. We found intact full-length SRK sequences in many accessions. Through interspecific crosses with the self-incompatible and diploid congener A. halleri, we found that the female components of the SI system, including SRK and the female downstream signaling pathway, are still functional in these accessions. Given the tight linkage and very rare recombination of the male and female components on the S-locus, this result suggests that the degradation of male components was responsible for the loss of SI in A. kamchatica. Recent extensive studies in multiple Brassicaceae species demonstrate that the loss of SI is often derived from mutations in the male component in wild populations, in contrast to cultivated populations. This is consistent with theoretical predictions that mutations disabling male specificity are expected to be more strongly selected than mutations disabling female specificity, or the female downstream signaling pathway.


Vyšlo v časopise: Recent Loss of Self-Incompatibility by Degradation of the Male Component in Allotetraploid. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002838
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002838

Souhrn

The evolutionary transition from outcrossing to self-fertilization (selfing) through the loss of self-incompatibility (SI) is one of the most prevalent events in flowering plants, and its genetic basis has been a major focus in evolutionary biology. In the Brassicaceae, the SI system consists of male and female specificity genes at the S-locus and of genes involved in the female downstream signaling pathway. During recent decades, much attention has been paid in particular to clarifying the genes responsible for the loss of SI. Here, we investigated the pattern of polymorphism and functionality of the female specificity gene, the S-locus receptor kinase (SRK), in allotetraploid Arabidopsis kamchatica. While its parental species, A. lyrata and A. halleri, are reported to be diploid and mainly self-incompatible, A. kamchatica is self-compatible. We identified five highly diverged SRK haplogroups, found their disomic inheritance and, for the first time in a wild allotetraploid species, surveyed the geographic distribution of SRK at the two homeologous S-loci across the species range. We found intact full-length SRK sequences in many accessions. Through interspecific crosses with the self-incompatible and diploid congener A. halleri, we found that the female components of the SI system, including SRK and the female downstream signaling pathway, are still functional in these accessions. Given the tight linkage and very rare recombination of the male and female components on the S-locus, this result suggests that the degradation of male components was responsible for the loss of SI in A. kamchatica. Recent extensive studies in multiple Brassicaceae species demonstrate that the loss of SI is often derived from mutations in the male component in wild populations, in contrast to cultivated populations. This is consistent with theoretical predictions that mutations disabling male specificity are expected to be more strongly selected than mutations disabling female specificity, or the female downstream signaling pathway.


Zdroje

1. StebbinsGL 1950 Variation and evolution in plants New York Columbia University Press 643

2. StebbinsGL 1974 Flowering plants: Evolution above the species level Cambridge Belknap Press 399

3. BarrettSCH 2002 The evolution of plant sexual diversity. Nat Rev Genet 3 274 284

4. IgicBLandeRKohnJR 2008 Loss of self-incompatibility and its evolutionary consequences. Int J Plant Sci 169 93 104

5. FisherRA 1941 Average excess and average effect of a gene substitution. Ann Eugen 11 53 63

6. GoodwillieCKaliszSEckertCG 2005 The evolutionary enigma of mixed mating systems in plants: Occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36 47 79

7. DarwinC 1876 The effects of cross and self fertilisation in the vegetable kingdom London J. Murray 487

8. KaliszSVoglerDWHanleyKM 2004 Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430 884 887

9. EckertCGSamisKEDartS 2006 Reproductive assurance and the evolution of uniparental reproduction in flowering plants. HarderLDBarrettSCH Ecology and evolution of flowers Oxford Oxford University Press 183 203

10. LandeRSchemskeDW 1985 The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39 24 40

11. CharlesworthDCharlesworthB 1987 Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18 237 268

12. de NettancourtD 2001 Incompatibility and incongruity in wild and cultivated plants, 2nd edn Berlin Springer 322

13. TakayamaSIsogaiA 2005 Self-incompatibility in plants. Annu Rev Plant Biol 56 467 489

14. Franklin-TongVE 2008 Self-incompatibility in flowering plants: Evolution, diversity, and mechanisms Berlin Springer 313

15. WrightS 1939 The distribution of self-sterility alleles in populations. Genetics 24 538 552

16. SchopferCRNasrallahMENasrallahJB 1999 The male determinant of self- incompatibility in Brassica. Science 286 1697 1700

17. TakasakiTHatakeyamaKSuzukiGWatanabeMIsogaiA 2000 The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403 913 916

18. TakayamaSShimosatoHShibaHFunatoMCheFS 2001 Direct ligand–receptor complex interaction controls Brassica self-incompatibility. Nature 413 534 538

19. SuzukiG 2009 Recent progress in plant reproduction research: The story of the male gametophyte through to successful fertilization. Plant Cell Physiol 50 1857 1864

20. ChapmanLAGoringDR 2010 Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J Exp Bot 61 1987 1999

21. GuTMazzurcoMSulamanWMatiasDDGoringDR 1998 Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci U S A 95 382 387

22. MazzurcoMSulamanWElinaHCockJMGoringDR 2001 Further analysis of the interactions between the Brassica S receptor kinase and three interacting proteins (ARC1, THL1 and THL2) in the yeast two-hybrid system. Plant Mol Biol 45 365 376

23. MuraseKShibaHIwanoMCheF-SWatanabeM 2004 A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303 1516 1519

24. CharlesworthDCharlesworthB 1979 The evolution and breakdown of S-allele systems. Heredity 43 41 55

25. UyenoyamaMKZhangYNewbiginE 2001 On the origin of self-incompatibility haplotypes: Transition through self-compatible intermediates. Genetics 157 1805 1817

26. MableBKRobertsonAVDartSDi BerardoCWithamL 2005 Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution 59 1437 1448

27. PorcherELandeR 2005 Loss of gametophytic self-incompatibility with evolution of inbreeding depression. Evolution 59 46 60

28. BuschJWSchoenDJ 2008 The evolution of self-incompatibility when mates are limiting. Trends Plant Sci 13 128 136

29. MableBK 2008 Genetic causes and consequences of the breakdown of self- incompatibility: Case studies in the Brassicaceae. Genet Res 90 47 60

30. KusabaMDwyerKHendershotJVrebalovJNasrallahJB 2001 Self-incompatibility in the genus Arabidopsis: Characterization of the S-locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13 627 643

31. NasrallahMELiuPNasrallahJB 2002 Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata. Science 297 247 249

32. ShimizuKK 2002 Ecology meets molecular genetics in Arabidopsis. Popul Ecol 44 221 233

33. NasrallahMELiuPSherman-BroylesSBoggsNANasrallahJB 2004 Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the evolution of selfing. Proc Natl Acad Sci U S A 101 16070 16074

34. ShimizuKKPuruggananMD 2005 Evolutionary and ecological genomics of Arabidopsis. Plant Physiol 138 578 584

35. LiuPSherman-BroylesSNasrallahMENasrallahJB 2007 A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol 17 734 740

36. Sherman-BroylesSBoggsNFarkasALiuPVrebalovJ 2007 S locus genes and the evolution of self-fertility in Arabidopsis thaliana. Plant Cell 19 94 106

37. TangCToomajianCSherman-BroylesSPlagnolVGuoYL 2007 The evolution of selfing in Arabidopsis thaliana. Science 317 1070 1072

38. ShimizuKKShimizu-InatsugiRTsuchimatsuTPuruggananMD 2008 Independent origins of self-compatibility in Arabidopsis thaliana. Mol Ecol 17 704 714

39. BoggsNANasrallahJBNasrallahME 2009 Independent S-locus mutations caused self-fertility in Arabidopsis thaliana. PLoS Genet 5 e1000426 doi:10.1371/journal.pgen.1000426

40. BoggsNADwyerKGShahPMcCullochAABechsgaardJS 2009 Expression of distinct self-incompatibility specificities in Arabidopsis thaliana. Genetics 182 1313 1321

41. TsuchimatsuTSuwabeKShimizu-InatsugiRIsokawaSPavlidisP 2010 Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464 1342 1346

42. ShimizuKKKudohHKobayashiMJ 2011 Plant sexual reproduction during climate change: gene function in natura studied by ecological and evolutionary systems biology. Ann Bot 108 777 787

43. GuoYLBechsgaardJSSlotteTNeufferBLascouxM 2009 Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc Natl Acad Sci U S A 106 5246 5251

44. BuschJWJolySSchoenDJ 2011 Demographic signatures accompanying the evolution of selfing in Leavenworthia alabamica. Mol Biol Evol 28 1717 1729

45. TantikanjanaTRizviNNasrallahMENasrallahJB 2009 A dual role for the S-locus receptor kinase in self-incompatibility and pistil development revealed by an Arabidopsis rdr6 mutation. Plant Cell 21 2642 2654

46. ShimizuKKFujiiSMarholdKWatanabeKKudohH 2005 Arabidopsis kamchatica (Fisch. ex DC.) K. Shimizu & Kudoh and A. kamchatica subsp. kawasakiana (Makino) K. Shimizu & Kudoh, new combinations. Acta Phytotax Geobot 56 165 174

47. SugisakaJKudohH 2008 Breeding system of the annual Cruciferae, Arabidopsis kamchatica subsp. kawasakiana. J Plant Res 121 65 68

48. Shimizu-InatsugiRLihováJIwanagaHKudohHMarholdK 2009 The allopolyploid Arabidopsis kamchatica originated from multiple individuals of Arabidopsis lyrata and Arabidopsis halleri. Mol Ecol 18 4024 4048

49. SchmicklRJørgensenMHBrystingAKKochMA 2010 The evolutionary history of the Arabidopsis lyrata complex: A hybrid in the amphi-Beringian area closes a large distribution gap and builds up a genetic barrier. BMC Evol Biol 10 98

50. FujimotoRKinoshitaYKawabeAKinoshitaTTakashimaK 2008 Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet 4 e1000048 doi:10.1371/journal.pgen.1000048

51. HigashiHIkedaHSetoguchiH 2012 Population fragmentation causes randomly fixed genotypes in populations of Arabidopsis kamchatica in the Japanese Archipelago. J Plant Res 125 223 233

52. SchierupMHMableBKAwadallaPCharlesworthD 2001 Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics 158 387 399

53. CharlesworthDBartoloméCSchierupMHMableBK 2003 Haplotype structure of the stigmatic self-incompatibility gene in natural populations of Arabidopsis lyrata. Mol Biol Evol 20 1741 1753

54. CharlesworthDMableBKSchierupMHBartoloméCAwadallaP 2003 Diversity and linkage of genes in the self-incompatibility gene family in Arabidopsis lyrata. Genetics 164 1519 1535

55. MableBKSchierupMHCharlesworthD 2003 Estimating the number, frequency, and dominance of S-alleles in a natural population of Arabidopsis lyrata (Brassicaceae) with sporophytic control of self-incompatibility. Heredity 90 422 431

56. CastricVVekemansX 2004 Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances. Mol Ecol 13 2873 2889

57. MableBKBelandJDi BerardoC 2004 Inheritance and dominance of self-incompatibility alleles in polyploid Arabidopsis lyrata. Heredity 93 476 486

58. CastricVVekemansX 2007 Evolution under strong balancing selection: How many codons determine specificity at the female self-incompatibility gene SRK in Brassicaceae? BMC Evol Biol 7 132

59. CastricVBechsgaardJSchierupMHVekemansX 2008 Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet 4 e1000168 doi:10.1371/journal.pgen.1000168

60. LlaurensVBilliardSLeducqJBCastricVKleinEK 2008 Does frequency-dependent selection with complex dominance interactions accurately predict allelic frequencies at the self-incompatibility locus in Arabidopsis halleri? Evolution 62 2545 2557

61. CastricVBechsgaardJSGrenierSNoureddineRSchierupMH 2010 Molecular evolution within and between self-incompatibility specificities. Mol Biol Evol 27 11 20

62. BechsgaardJSCastricVCharlesworthDVekemansXSchierupMH 2006 The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr. Mol Biol Evol 23 1741 1750

63. GuoYLZhaoXLanzCWeigelD 2011 Evolution of the S-locus region in Arabidopsis relatives. Plant Physiol 157 937 946

64. SchierupMHBechsgaardJSChristiansenFB 2008 Selection at work in self-incompatible Arabidopsis lyrata. II. Spatial distribution of S haplotypes in Iceland. Genetics 180 1051 1059

65. BarringerBC 2007 Polyploidy and self-fertilization in flowering plants. Amer J Bot 94 1527 1533

66. MableBK 2004 Polyploidy and self-compatibility: Is there an association? New Phytol 162 803 811

67. LevinDA 1975 Minority cytotype exclusion in local plant populations. Taxon 24 35 43

68. FelberF 1991 Establishment of a tetraploid cytotype in a diploid population: Effect of relative fitness of cytotypes. J Evol Biol 4 194 207

69. RodríguezDJ 1996 A model for the establishment of polyploidy in plants. Amer Nat 147 33 46

70. MillerJSVenableDL 2000 Polyploidy and the evolution of gender dimorphism in plants. Science 289 2335 2338

71. HedrickPW 1987 Genetic load and the mating system in homosporous ferns. Evolution 41 1282 1289

72. RonfortJ 1999 The mutation load under tetrasomic inheritance and its consequences for the evolution of the selfing rate in autotetraploid species. Genet Res 74 31 42

73. FoxeJPSlotteTStahlEANeufferBHurkaH 2009 Recent speciation associated with the evolution of selfing in Capsella. Proc Natl Acad Sci U S A 106 5241 5245

74. VekemansXSlatkinM 1994 Gene and allelic genealogies at a gametophytic self-incompatibility locus. Genetics 137 1157 1165

75. KochMAHauboldBMitchell-OldsT 2000 Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis and related genera (Brassicaceae). Mol Biol Evol 17 1483 1498

76. OssowskiSSchneebergerKLucas-LledóJIWarthmannNClarkRM 2010 The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327 92 94

77. KusabaMNishioTSattaYHinataKOckendonD 1997 Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: Implications for the evolution and recognition mechanism. Proc Natl Acad Sci U S A 94 7673 7678

78. NaithaniSChookajornTRipollDRNasrallahJB 2007 Structural modules for receptor dimerization in the S-locus receptor kinase extracellular domain. Proc Natl Acad Sci U S A 104 12211 12216

79. GoringDRGlavinTLSchaferURothsteinSJ 1993 An S receptor kinase gene in self-compatible Brassica napus has a 1-bp deletion. Plant Cell 5 531 539

80. OkamotoSOdashimaMFujimotoRSatoYKitashibaH 2007 Self-compatibility in Brassica napus is caused by independent mutations in S-locus genes. Plant J 50 391 400

81. de la ChauxNTsuchimatsuTShimizuKKWagnerA 2012 The predominantly selfing plant Arabidopsis thaliana experienced a recent reduction in transposable element abundance compared to its outcrossing relative Arabidopsis lyrata. Mob DNA 3 2

82. HewittG 2000 The genetic legacy of the Quaternary ice ages. Nature 405 907 913

83. NordborgMHuTTIshinoYJhaveriJToomajianC 2005 The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3 e196 doi:10.1371/journal.pbio.0030196

84. BeckJBSchmuthsHSchaalBA 2008 Native range genetic variation in Arabidopsis thaliana is strongly geographically structured and reflects Pleistocene glacial dynamics. Mol Ecol 17 902 915

85. FrançoisOBlumMGJakobssonMRosenbergNA 2008 Demographic history of European populations of Arabidopsis thaliana. PLoS Genet 4 e1000075 doi:10.1371/journal.pgen.1000075

86. FoxeJPStiftMTedderAHaudryAWrightSI 2010 Reconstructing origins of loss of self-incompatibility and selfing in North American Arabidopsis lyrata: A population genetic context. Evolution 64 3495 3510

87. HoebePNStiftMTedderAMableBK 2009 Multiple losses of self-incompatibility in North American Arabidopsis lyrata: Phylogeographic context and population genetic consequences. Mol Ecol 18 4924 4939

88. TedderAHoebePHAnsellSWMableBK 2010 Using chloroplast trnF pseudogenes for phylogeography in Arabidopsis lyrata. Diversity 2 653 678

89. Ramos-OnsinsSEStrangerBEMitchell-OldsTAguadéM 2004 Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166 373 388

90. BakerHG 1955 Self-compatibility and establishment after “long-distance” dispersal. Evolution 9 347 349

91. BakerHG 1967 Support for Baker's law—as a rule. Evolution 21 853 856

92. PannellJRBarrettSCH 1998 Baker's law revisited: Reproductive assurance in a metapopulation. Evolution 52 657 668

93. PujolBZhouSRSanchez VilasJPannellJR 2009 Reduced inbreeding depression after species range expansion. Proc Natl Acad Sci U S A 106 15379 15383

94. BataillonTKirkpatrickM 2000 Inbreeding depression due to mildly deleterious mutations in finite populations: Size does matter. Genet Res 75 75 81

95. GleminS 2003 How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57 2678 2687

96. BuschJWDelphLF 2011 The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann Bot In press

97. McClureB 2009 Darwin's foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI. J Exp Bot 60 1069 1081

98. RobertsonKGoldbergEEIgicB 2011 Comparative evidence for the correlated evolution of polyploidy and self-compatibility in Solanaceae. Evolution 65 139 155

99. NasrallahJBLiuPSherman-BroylesSSchmidtRNasrallahME 2007 Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids. Genetics 175 1965 1973

100. BatemanAJ 1952 Self-incompatibility systems in angiosperms. 1. Theory. Heredity 6 285 310

101. ShibaHIwanoMEntaniTIshimotoKShimosatoH 2002 The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14 491 504

102. KusabaMTungCWNasrallahMENasrallahJB 2002 Monoallelic expression and dominance interactions in anthers of self-incompatible Arabidopsis lyrata. Plant Physiol 128 17 20

103. PrigodaNLNassuthAMableBK 2005 Phenotypic and genotypic expression of self-incompatibility haplotypes in Arabidopsis lyrata suggests unique origin of alleles in different dominance classes. Mol Biol Evol 22 1609 1620

104. FujimotoRSugimuraTFukaiENishioT 2006 Suppression of gene expression of a recessive SP11/SCR allele by an untranscribed SP11/SCR allele in Brassica self-incompatibility. Plant Mol Biol 61 577 587

105. SchierupMHVekemansXChristiansenFB 1997 Evolutionary dynamics of sporophytic self-incompatibility alleles in plants. Genetics 147 835 846

106. BilliardSCastricVVekemansX 2007 A general model to explore complex dominance patterns in plant sporophytic self-incompatibility systems. Genetics 175 1351 1369

107. ShibaHKakizakiTIwanoMTarutaniYWatanabeM 2006 Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat Genet 38 297 299

108. TarutaniYShibaHIwanoMKakizakiTSuzukiG 2010 Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466 983 986

109. VekemansXSchierupMHChristiansenFB 1998 Mate availability and fecundity selection in multi-allelic self-incompatibility systems in plants. Evolution 52 19 29

110. BuschJWUrbanL 2011 Insights gained from 50 years of studying the evolution of self-compatibility in Leavenworthia (Brassicaceae). Evol Biol 38 15 27

111. NasrallahJBRundleandSJNasrallahME 1994 Genetic evidence for the requirement of the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J 5 373 384

112. FujimotoRSugimuraTNishioT 2006 Gene conversion from SLG to SRK resulting in self-compatibility in Brassica rapa. FEBS Lett 580 425 430

113. HallTA 1999 BIOEDIT: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41 95 98

114. TamuraKPetersonDPetersonNStecherGNeiM 2011 MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28 2731 2739

115. GaoHWilliamsonSBustamanteCD 2007 A Markov chain Monte Carlo approach for joint inference of population structure and inbreeding rates from multilocus genotype data. Genetics 176 1635 1651

116. JakobssonMRosenbergNA 2007 CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23 1801 1806

117. RosenbergNA 2004 DISTRUCT: A program for the graphical display of population structure. Mol Ecol Notes 4 137 138

118. EvannoGRegnautSGoudetJ 2005 Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol 14 2611 2620

119. PritchardJKStephensMDonnellyP 2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959

120. CramerH 1946 Mathematical method of statistics Princeton Princeton University Press 575

121. SokalRRRohlfFJ 1995 Biometry: The principles and practice of statistics in biological research, 3rd ed New York W. H. Freeman 880

122. R Development Core Team 2009 R: A language and environment for statistical computing Vienna (Austria) R Foundation for Statistical Computing Available from http://www.R-project.org

123. JukesTHCantorCR 1969 Evolution of protein molecules. MunroHN Mammalian protein metabolism New York Academic Press 32 132

124. NeiMKumarS 2000 Molecular evolution and phylogenetics Oxford Oxford University Press 336

125. CharruauPFernandesCOrozco-TerwengelPPetersJHunterL 2011 Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: Evidence for long-term geographic isolates. Mol Ecol 20 706 724

126. StoneACBattistuzziFUKubatkoLSPerryGHJrTrudeauE 2010 More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure. Phil Trans R Soc Lond B Biol Sci 365 3277 3288

127. DrummondAJHoSYPhillipsMJRambautA 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 e88 doi:10.1371/journal.pbio.0040088

128. OhwiJ 1953 Flora of Japan Washington Smithsonian Institution 1067

129. ShimizuKKOkadaK 2000 Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127 4511 4518

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