Advertisement

Genomes: Classical Era

  • David B. Neale
  • Nicholas C. Wheeler
Chapter

Abstract

The study of conifer genomes began in 1933 with the publication by Sax and Sax (1933) of chromosome numbers found in several conifer species. From 1933 until the beginning of the application of recombinant DNA technologies in the 1970s, the study of conifer genomes was done using classical cytogenetic techniques. From the 1970s until the late 1990s, a suite of developing DNA technologies was applied to the study of conifer genomes. We have labeled the years between 1933 and the late 1990s as the classical era in the study of conifer genomes. Beginning in the late 1990s, high-throughput DNA sequencing began to be applied. We have labeled this period as the modern era which will be covered in Chap.  3. In conifers, like all higher plants, there are three genomes; the nuclear genome (nDNA), the chloroplast genome (cpDNA), and the mitochondrial genome (mtDNA). In this chapter we will discuss what was learned about chromosome number, ploidy, karyotypes, genome size, and basic genome content in all three genomes during the classical era.

References

  1. Ahuja, M. R. (2005). Polyploidy in gymnosperms: revisited. Silvae Genetica, 54(2), 59–69.CrossRefGoogle Scholar
  2. Ahuja, M. R., & Neale, D. B. (2002). Origins of polyploidy in coast redwood (Sequoia sempervirens (D. Don) Endl.) and relationship of coast redwood to other genera of Taxodiaceae. Silvae Genetica, 51(2–3), 93–99.Google Scholar
  3. Ahuja, M. R., & Neale, D. B. (2005). Evolution of genome size in conifers. Silvae Genetica, 54(3), 126–137.CrossRefGoogle Scholar
  4. Ali, I. F., Neale, D. B., & Marshall, K. A. (1991). Chloroplast DNA restriction fragment length polymorphism in Sequoia sempervirens D. Don Endl., Pseudotsuga menziesii (Mirb.) Franco, Calocedrus decurrens (Torr.), and Pinus taeda L. Theoretical and Applied Genetics, 81(1), 83–89.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Amarasinghe, V., & Carlson, J. E. (1998). Physical mapping and characterization of 5S rRNA genes in Douglas-fir. Journal of Heredity, 89(6), 495–500.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bogunic, F., Muratovic, E., & Siljak-Yakovlev, S. (2006). Chromosomal differentiation between Pinus heldreichii and Pinus nigra. Annals of Forest Science, 63(3), 267–274.CrossRefGoogle Scholar
  7. Boscherini, G., Morgante, M., Rossi, P., & Vendramin, G. G. (1994). Allozyme and chloroplast DNA variation in Italian and Greek populations of Pinus leucodermis. Heredity, 73(3), 284–290.PubMedCrossRefGoogle Scholar
  8. Britten, R. J., & Kohne, D. E. (1968). Repeated sequences in DNA. Science, 161, 529–540.PubMedCrossRefGoogle Scholar
  9. Brown, G. R., & Carlson, J. E. (1997). Molecular cytogenetics of the genes encoding 18S-5.8 S-26S rRNA and 5S rRNA in two species of spruce (Picea). Theoretical and Applied Genetics, 95(1–2), 1–9.CrossRefGoogle Scholar
  10. Brown, G. R., Amarasinghe, V., Kiss, G., & Carlson, J. E. (1993). Preliminary karyotype and chromosomal localization of ribosomal DNA sites in white spruce using fluorescence in situ hybridization. Genome, 36(2), 310–316.PubMedCrossRefPubMedCentralGoogle Scholar
  11. Cai, Q., Zhang, D., Liu, Z. L., & Wang, X. R. (2006). Chromosomal localization of 5S and 18S rDNA in five species of subgenus Strobus and their implications for genome evolution of Pinus. Annals of Botany, 97(5), 715–722.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Dagher-Kharrat, M. B., Grenier, G., Bariteau, M., Brown, S., Siljak-Yakovlev, S., & Savouré, A. (2001). Karyotype analysis reveals interspecific differentiation in the genus Cedrus despite genome size and base composition constancy. Theoretical and Applied Genetics, 103(6–7), 846–854.CrossRefGoogle Scholar
  13. De Luc, A., Adams, R. A., & Zhang, M. (1999). Using random amplification of polymorphic DNA for taxonomic evaluation of Pfitzer junipers. Hortscience, 34, 1123–1125.CrossRefGoogle Scholar
  14. Deng, H. S., Zhang, D. M., Fu, C. X., & Hong, D. Y. (2008). Behavior of meiotic chromosomes in Pinus wallichiana, P. strobus and their hybrid and nrDNA localization in pollen mother cells of the hybrid by using FISH. Journal of Integrative Plant Biology, 50(3), 360–367.PubMedCrossRefPubMedCentralGoogle Scholar
  15. DeVerno, L. L., Charest, P. J., & Bonen, L. (1993). Inheritance of mitochondrial DNA in the conifer Larix. Theoretical and Applied Genetics, 86(2–3), 383–388.PubMedCrossRefPubMedCentralGoogle Scholar
  16. Dhillon, S. S., Berlyn, G. P., & Miksche, J. P. (1978). Nuclear DNA content in populations of Pinus rigida. American Journal of Botany, 65, 192–196.CrossRefGoogle Scholar
  17. Dhir, N. K., & Miksche, J. P. (1974). Intraspecific variation of nuclear DNA content in Pinus resinosa Ait. Canadian Journal of Genetics and Cytology, 16(1), 77–83.CrossRefGoogle Scholar
  18. Dong, J., & Wagner, D. B. (1993). Taxonomic and population differentiation of mitochondrial diversity in Pinus banksiana and Pinus contorta. Theoretical and Applied Genetics, 86(5), 573–578.PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dong, J., Wagner, D. B., Yanchuk, A. D., Carlson, M. R., Magnussen, S., Wang, X. R., & Szmidt, A. E. (1992). Paternal chloroplast DNA inheritance in Pinus consora and Pinus banksiana: independence of parenetal species or cross direction. Journal of Heredity, 83(6), 419–422.CrossRefGoogle Scholar
  20. Doudrick, R. L., Heslop-Harrison, J. S., Nelson, C. D., Schmidt, T., Nance, W. L., & Schwarzacher, T. (1995). Karyotype of slash pine (Pinus elliottii var. elliottii) using patterns of fluorescence in situ hybridization and fluorochrome banding. Journal of Heredity, 86(4), 289–296.CrossRefGoogle Scholar
  21. El-Lakany, M. H., & Sziklai, O. (1971). Intraspecific variation in nuclear characteristics of Douglas-fir. Advancing Frontiers of Plant Science, 28, 363–378.Google Scholar
  22. Ferguson, M. C. (1904). Contributions to the knowledge of the life history of Pinus with special reference to sporogenesis, the development of the gametophytes and fertilization (Vol. 6). The Academy.Google Scholar
  23. Guttenberger, H., Mueller, M., & Grill, D. (1996). Cytogenetic studies on Norway spruce (Picea abies (L.) Karst.). Phyton, 36, 147–154.Google Scholar
  24. Hair, J. B. (1968). The chromosomes of the Cupressaceae: 1. Tetraclineae and Actinostrobeae (Callitroideae). New Zealand Journal of Botany, 6(3), 277–284.CrossRefGoogle Scholar
  25. Hamberger, B., Hall, D., Yuen, M., Oddy, C., Hamberger, B., Keeling, C. I., et al. (2009). Targeted isolation, sequence assembly and characterization of two white spruce (Picea glauca) BAC clones for terpenoid synthase and cytochrome P450 genes involved in conifer defence reveal insights into a conifer genome. BMC Plant Biology, 9(1), 106.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Hipkins, V. D., Krutovsky, K. V., & Strauss, S. (1994). Organelle genomes in conifers: structure, evolution, and diversity. Forest Genetics, 1, 179–189.Google Scholar
  27. Hipkins, V. D., Marshall, K. A., Neale, D. B., Rottmann, W. H., & Strauss, S. H. (1995). A mutation hotspot in the chloroplast genome of a conifer (Douglas-fir: Pseudotsuga) is caused by variability in the number of direct repeats derived from a partially duplicated tRNA gene. Current Genetics, 27(6), 572–579.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hirayoshi, I., & Nakamura, Y. (1943). Chromosome number of Sequoia sempervirens. Advances in Zoology and Botany, 2, 73–75.Google Scholar
  29. Hizume, M. (2015a). Fluorescent band pattern of chromosomes in Pseudolarix amabilis, Pinaceae. Cytologia, 80(2), 151–157.CrossRefGoogle Scholar
  30. Hizume, M. (2015b). Fluorescent banding pattern in chromosomes of Tsuga forrestii and T. sieboldii, Pinaceae. Chromosome Botany, 10(3), 95–100.CrossRefGoogle Scholar
  31. Hizume, M., & Kan, M. (2015). Fluorescent banding pattern of chromosomes in Araucaria araucana, Araucariaceae. Cytologia, 80(4), 399–403.CrossRefGoogle Scholar
  32. Hizume, M., Shibata, F., Matsusaki, Y., & Garajova, Z. (2002). Chromosome identification and comparative karyotypic analyses of four Pinus species. Theoretical and Applied Genetics, 105(4), 491–497.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Hizume, M., Ohtaka, K. N., Takeda, K. M., Fujii, S., Yamasaki, Y., & Kondo, K. (2016). Chromosome banding in the genus Pinus IV. Fluorescent banding patterns of chromosomes in eight taxa of haploxylone pines. Chromosome Botany, 11(3), 61–71.CrossRefGoogle Scholar
  34. Hong, Y. P., Hipkins, V. D., & Strauss, S. H. (1993). Chloroplast DNA diversity among trees, populations and species in the California closed-cone pines (Pinus radiata, Pinus muricata and Pinus attenuata). Genetics, 135(4), 1187–1196.PubMedPubMedCentralGoogle Scholar
  35. Islam-Faridi, M. N., & Nelson, C. D. (2011). Cytogenetics. In C. Plomion, J. Bousquet, & C. Kole (Eds.), Genetics, genomics and breeding of conifers (pp. 128–140). Enfield: Science Publishers.Google Scholar
  36. Islam-Faridi, M. N., Nelson, C. D., & Kubisiak, T. L. (2007). Reference karyotype and cytomolecular map for loblolly pine (Pinus taeda L.). Genome, 50(2), 241–251.PubMedCrossRefGoogle Scholar
  37. Joyner, K. L., Wang, X. R., Johnston, J. S., Price, H. J., & Williams, C. G. (2001). DNA content for Asian pines parallels New World relatives. Canadian Journal of Botany, 79(2), 192–196.CrossRefGoogle Scholar
  38. Khoshoo, T. N. (1959). Polyploidy in gymnosperms. Evolution, 13(1), 24–39.CrossRefGoogle Scholar
  39. Khoshoo, T. N. (1961). Chromosome numbers in gymnosperms. Silvae Genetica, 10(1), 1–32.Google Scholar
  40. Kinlaw, C. S., & Neale, D. B. (1997). Complex gene families in pine genomes. Trends in Plant Science, 2(9), 356–359.CrossRefGoogle Scholar
  41. Korshikov, I. I., Tkacheva, Y. A., & Privalikhin, S. N. (2012). Cytogenetic abnormalities in Norway spruce (Picea abies (L.) Karst.) seedlings from natural populations and an introduction plantation. Cytology and Genetics, 46(5), 280–284.CrossRefGoogle Scholar
  42. Kovach, A., Wegrzyn, J. L., Parra, G., Holt, C., Bruening, G. E., Loopstra, C. A., et al. (2010). The Pinus taeda genome is characterized by diverse and highly diverged repetitive sequences. BMC Genomics, 11(1), 420.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kriebel, H. B. (1985). DNA sequence components of the Pinus strobus nuclear genome. Canadian Journal of Forest Research, 15(1), 1–4.CrossRefGoogle Scholar
  44. Lewis, I. M. (1908). The behaviour of the chromosomes in Pinus and Thuja. Annals of Botany, 22(88), 529–556.CrossRefGoogle Scholar
  45. Li, Z., Baniaga, A. E., Sessa, E. B., Scascitelli, M., Graham, S. W., Rieseberg, L. H., & Barker, M. S. (2015). Early genome duplications in conifers and other seed plants. Science Advances, 1(10), e1501084–e1501084.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Liu, Z. L., Zhang, D., Hong, D. Y., & Wang, X. R. (2003a). Chromosomal localization of 5S and 18S–5.8 S–25S ribosomal DNA sites in five Asian pines using fluorescence in situ hybridization. Theoretical and Applied Genetics, 106(2), 198–204.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Liu, W., Thummasuwan, S., Sehgal, S. K., Chouvarine, P., & Peterson, D. G. (2011a). Characterization of the genome of bald cypress. BMC Genomics, 12(1), 553.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lubaretz, O., Fuchs, J., Ahne, R., Meister, A., & Schubert, I. (1996). Karyotyping of three Pinaceae species via fluorescent in situ hybridization and computer-aided chromosome analysis. Theoretical and Applied Genetics, 92(3–4), 411–416.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Marshall, K. A., & Neale, D. B. (1992). The inheritance of mitochondrial DNA in Douglas-fir (Pseudotsuga menziesii). Canadian Journal of Forest Research, 22(1), 73–75.CrossRefGoogle Scholar
  50. Mehes-Smith, M., Nkongolo, K. K., & Kim, N. S. (2011). A comparative cytogenetic analysis of five pine species from North America, Pinus banksiana, P. contorta, P. monticola, P. resinosa, and P. strobus. Plant Systematics and Evolution, 292(3–4), 153–164.CrossRefGoogle Scholar
  51. Miksche, J. P. (1967). Variation in DNA content of several gymnosperms. Canadian Journal of Genetics and Cytology, 9(4), 717–722.CrossRefGoogle Scholar
  52. Miksche, J. P. (1968). Quantitative study of intraspecific variation of DNA per cell in Picea glauca and Pinus banksiana. Canadian Journal of Genetics and Cytology, 10(3), 590–600.CrossRefGoogle Scholar
  53. Murray, B. G. (1998). Nuclear DNA amounts in gymnosperms. Annals of Botany, 82(1), 3–15.CrossRefGoogle Scholar
  54. Neale, D. B., & Sederoff, R. R. (1989). Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theoretical and Applied Genetics, 77(2), 212–216.PubMedCrossRefPubMedCentralGoogle Scholar
  55. Neale, D. B., Wheeler, N. C., & Allard, R. W. (1986). Paternal inheritance of chloroplast DNA in Douglas-fir. Canadian Journal of Forest Research, 16(5), 1152–1154.CrossRefGoogle Scholar
  56. Neale, D. B., Marshall, K. A., & Sederoff, R. R. (1989). Chloroplast and mitochondrial DNA are paternally inherited in Sequoia sempervirens D. Don Endl. Proceedings of the National Academy of Sciences, 86(23), 9347–9349.CrossRefGoogle Scholar
  57. Neale, D. B., Marshall, K. A., & Harry, D. E. (1991). Inheritance of chloroplast and mitochondrial DNA in incense-cedar (Calocedrus decurrens). Canadian Journal of Forest Research, 21(5), 717–720.CrossRefGoogle Scholar
  58. Nelson, C. D., Nance, W. L., & Wagner, D. B. (1994). Chloroplast DNA variation among and within taxonomic varieties of Pinus caribaea and Pinus elliottii. Canadian Journal of Forest Research, 24(2), 424–426.CrossRefGoogle Scholar
  59. Nkongolo, K. K. (1996). Chromosome analysis and DNA homology in three Picea species, P. mariana, P. rubens, and P. glauca (Pinaceae). Plant Systematics and Evolution, 203(1), 27–40.CrossRefGoogle Scholar
  60. Nkongolo, K. K., & Klimaszewska, K. (1995). Cytological and molecular relationships between Larix decidua, L. leptolepis and Larix x eurolepis: identification of species-specific chromosoms and synchronization of mitotic cells. Theoretical and Applied Genetics, 90(6), 827–834.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Ohba, K., Iwakawa, M., Okada, Y., & Murai, M. (1971). Paternal transmission of a plastid anomaly in some reciprocal crosses of Sugi, Cryptomeria japonica D. Don. Silvae Genetica., 20, 101–107.Google Scholar
  62. Ohri, D., & Khoshoo, T. N. (1986). Genome size in gymnosperms. Plant Systematics and Evolution, 153(1), 119–132.CrossRefGoogle Scholar
  63. Owens, J. N. (1967). Chromosome aberrations in Douglas fir. Canadian Journal of Botany, 45(10), 1910–1913.CrossRefGoogle Scholar
  64. Pedrick, L. A. (1967). The structure and identification of the chromosomes of Pinus radiata D. Don. Silvae Genetica, 16, 69–77.Google Scholar
  65. Pedrick, L. A. (1968). Chromosome inversions in Pinus radiata. Silvae Genetica, 17, 22–26.Google Scholar
  66. Pedrick, L. A. (1970). Chromosome relationships between Pinus species. Silvae Genetica, 19, 171–180.Google Scholar
  67. Ponoy, B., Hong, Y. P., Woods, J., Jaquish, B., & Carlson, J. E. (1994). Chloroplast DNA diversity of Douglas-fir in British Columbia. Canadian Journal of Forest Research, 24(9), 1824–1834.CrossRefGoogle Scholar
  68. Rake, A. V., Miksche, J. P., Hall, R. B., & Hansen, K. M. (1980). DNA reassociation kinetics of four conifers. Canadian Journal of Genetics and Cytology, 22(1), 69–79.CrossRefGoogle Scholar
  69. Sax, K., & Sax, H. J. (1933). Chromosome number and morphology in the conifers. Journal of the Arnold Arboretum, 14(4), 356–375.CrossRefGoogle Scholar
  70. Saylor, L. C. (1961). A karyotypic analysis of selected species of Pinus. Silvae Genetica, 10, 77–83.Google Scholar
  71. Saylor, L. C. (1964). Karyotype Analysis of Pinus, Group Lariciones. Silvae Genetica, 13, 165–170.Google Scholar
  72. Saylor, L. C. (1972). Karyotype analysis of the genus Pinus-subgenus Pinus. Silvae Genetica, 21(5), 155–163.Google Scholar
  73. Schlarbaum, S. E., & Tsuchiya, T. (1975a). Chromosome study of giant sequoia, Sequoiadendron giganteum. Silvae Genetica, 24, 23–26.Google Scholar
  74. Schlarbaum, S. E., & Tsuchiya, T. (1975b). Chromosomes of incense cedar. Journal of Heredity, 66(1), 41–42.CrossRefGoogle Scholar
  75. Schlarbaum, S. T., & Tsuchiya, T. (1976). Chromosome study of Japanese umbrella pine. Journal of Heredity, 67(1), 65–67.CrossRefGoogle Scholar
  76. Schlarbaum, S. E., & Tsuchiya, T. (1984a). The Chromosomes of Cunninghamia konishii, C. lanceolata, and Taiwania cryptomerioides (Taxodiaceae). Plant Systematics and Evolution, 145(3), 169–181.CrossRefGoogle Scholar
  77. Schlarbaum, S. E., Johnson, L. C., & Tsuchiya, T. (1983). Chromosome studies of Metasequoia glyptostroboides and Taxodium distichum. Botanical Gazette, 144(4), 559–565.CrossRefGoogle Scholar
  78. Scott, A. D., Stenz, N. W., Ingvarsson, P. K., & Baum, D. A. (2016). Whole genome duplication in coast redwood (Sequoia sempervirens) and its implications for explaining the rarity of polyploidy in conifers. New Phytologist, 211(1), 186–193.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Sedelnikova, T. S., & Muratova, E. N. (2002). Specific karyological features of Siberian stone pine (Pinus sibirica Du Tour) in Western Siberian bogs. Russian Journal of Ecology, 33(5), 303–308.CrossRefGoogle Scholar
  80. Shibata, F., & Hizume, M. (2008). Comparative FISH karyotype analysis of 11 Picea species. Cytologia (Tokyo), 73(2), 203.CrossRefGoogle Scholar
  81. Shibata, F., Matsusaki, Y., & Hizume, M. (2005). AT-rich sequences containing Arabidopsis-type telomere sequence and their chromosomal distribution in Pinus densiflora. Theoretical and Applied Genetics, 110(7), 1253–1258.PubMedCrossRefPubMedCentralGoogle Scholar
  82. Soltis, D. E., Buggs, R. J., Doyle, J. J., & Soltis, P. S. (2010). What we still don't know about polyploidy. Taxon, 59(5), 1387–1403.CrossRefGoogle Scholar
  83. Stebbins, G. L. (1948). The chromosomes and relationships of Metasequoia and Sequoia. Science, 108(2796), 95–98.PubMedCrossRefPubMedCentralGoogle Scholar
  84. Stevens, K. A., Wegrzyn, J. L., Zimin, A., Puiu, D., Crepeau, M., Cardeno, C., et al. (2016). Sequence of the Sugar Pine Megagenome. Genetics, 204(4), 1613–1626.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Stine, M., & Keathley, D. E. (1990). Paternal inheritance of plastids in Engelmann spruce x blue spruce hybrids. Journal of Heredity, 81(6), 443–446.CrossRefGoogle Scholar
  86. Stine, M., Sears, B. B., & Keathley, D. E. (1989). Inheritance of plastids in interspecific hybrids of blue spruce and white spruce. Theoretical and Applied Genetics, 78(6), 768–774.PubMedCrossRefPubMedCentralGoogle Scholar
  87. Strauss, S. H., Palmer, J. D., Howe, G. T., & Doerksen, A. H. (1988). Chloroplast genomes of two conifers lack a large inverted repeat and are extensively rearranged. Proceedings of the National Academy of Sciences, 85(11), 3898–3902.CrossRefGoogle Scholar
  88. Strauss, S. H., Hong, Y. P., & Hipkins, V. D. (1993). High levels of population differentiation for mitochondrial DNA haplotypes in Pinus radiata, muricata, and attenuata. Theoretical and Applied Genetics, 86(5), 605–611.PubMedCrossRefPubMedCentralGoogle Scholar
  89. Sutton, B. C. S., Flanagan, D. J., & El-Kassaby, Y. A. (1991). A simple and rapid method for estimating representation of species in spruce seedlots using chloroplast DNA restriction fragment length polymorphism. Silvae genetica, 40(3–4), 119–123.Google Scholar
  90. Szmidt, A. E., Aldén, T., & Hällgren, J. E. (1987). Paternal inheritance of chloroplast DNA in Larix. Plant Molecular Biology, 9(1), 59–64.PubMedCrossRefPubMedCentralGoogle Scholar
  91. Szmidt, A. E., Sigurgeirsson, A., Wang, X. R., Haellgren, J. E., & Lindgren, D. (1988a). Genetic relationships among Pinus species based on chloroplast DNA polymorphism. In Hällgren, J.-E. (Ed.). Proc F. Kempe Symposium, Molecular genetics of forest trees, June 14–16, 1988. Umeå, Sweden, pp. 33–47.Google Scholar
  92. Tsudzuki, J., Nakashima, K., Tsudzuki, T., Hiratsuka, J., Shibata, M., Wakasugi, T., & Sugiura, M. (1992). Chloroplast DNA of black pine retains a residual inverted repeat lacking rRNA genes: nucleotide sequences of trnQ, trnK, psbA, trnI and trnH and the absence of rps16. Molecular and General Genetics MGG, 232(2), 206–214.PubMedPubMedCentralGoogle Scholar
  93. Tsumura, Y., Suyama, Y., & Yoshimura, K. (2000). Chloroplast DNA inversion polymorphism in populations of Abies and Tsuga. Molecular Biology and Evolution, 17(9), 1302–1312.PubMedCrossRefPubMedCentralGoogle Scholar
  94. Vischi, M., Jurman, I., Bianchi, G., & Morgante, M. (2003). Karyotype of Norway spruce by multicolor FISH. Theoretical and Applied Genetics, 107(4), 591–597.PubMedCrossRefPubMedCentralGoogle Scholar
  95. Wagner, D. B., Furnier, G. R., Saghai-Maroof, M. A., Williams, S. M., Dancik, B. P., & Allard, R. W. (1987). Chloroplast DNA polymorphisms in lodgepole and jack pines and their hybrids. Proceedings of the National Academy of Sciences, 84(7), 2097–2100.CrossRefGoogle Scholar
  96. Wagner, D. B., Govindaraju, D. R., Yeatman, C. W., & Pitel, J. A. (1989). Paternal chloroplast DNA inheritance in a diallel cross of jack pine (Pinus banksiana Lamb.). Journal of Heredity, 80(6), 483–485.CrossRefGoogle Scholar
  97. Wagner, D. B., Dong, J., Carlson, M. R., & Yanchuk, A. D. (1991a). Paternal leakage of mitochondrial DNA in Pinus. Theoretical and Applied Genetics, 82(4), 510–514.PubMedCrossRefPubMedCentralGoogle Scholar
  98. Wagner, D. B., Nance, W. L., Nelson, C. D., Li, T., Patel, R. N., & Govindaraju, D. R. (1992). Taxonomic patterns and inheritance of chloroplast DNA variation in a survey of Pinus echinata, Pinus elliottii, Pinus palustris, and Pinus taeda. Canadian Journal of Forest Research, 22(5), 683–689.CrossRefGoogle Scholar
  99. Wakamiya, I., Newton, R. J., Johnston, J. S., & Price, H. J. (1993). Genome size and environmental factors in the genus Pinus. American Journal of Botany, 80, 1235–1241.CrossRefGoogle Scholar
  100. Wakasugi, T., Tsudzuki, J., Ito, S., Nakashima, K., Tsudzuki, T., & Sugiura, M. (1994). Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proceedings of the National Academy of Sciences, 91(21), 9794–9798.CrossRefGoogle Scholar
  101. White, E. E. (1990). Chloroplast DNA in Pinus monticola. Theoretical and Applied Genetics, 79(1), 119–124.PubMedCrossRefPubMedCentralGoogle Scholar
  102. White, T. L., Adams, W. T., & Neale, D. B. (2007). Forest genetics. Wallingford: CABI Publisher.CrossRefGoogle Scholar
  103. Yang, Z.-Y., Ran, J.-H., & Wang, X.-Q. (2012). Three genome-based phylogeny of Cupressaceae s.l.: Further evidence for the evolution of gymnosperms and Southern Hemisphere biogeography. Molecular Phylogenetics and Evolution, 64(3), 452–470.PubMedCrossRefPubMedCentralGoogle Scholar
  104. Zonneveld, B. J. M. (2012). Conifer genome sizes of 172 species, covering 64 of 67 genera, range from 8 to 72 picogram. Nordic Journal of Botany, 30(4), 490–502.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • David B. Neale
    • 1
  • Nicholas C. Wheeler
    • 2
  1. 1.Department of Plant SciencesUniversity of California, DavisDavisUSA
  2. 2.ConsultantCentraliaUSA

Personalised recommendations