Current Genetics

, Volume 14, Issue 1, pp 65–74 | Cite as

Evolutionary significance of inversions in legume chloroplast DNAs

  • Jeffrey D. Palmer
  • Bernardita Osorio
  • William F. Thompson
Original Articles


Cloned genes from tobacco, spinach, and pea were used as hybridization probes to localize 36 protein genes on the chloroplast chromosomes of four legumes — mung bean, common bean, soybean, and pea. The first three chloroplast DNAs (cpDNAs), all of which retain a large inverted repeat, have an identical gene order with but one exception. A 78 kb segment encompassing nearly the entire large single copy region is inverted in mung bean and common bean relative to soybean and non-legumes. The simplest evolutionary explanation for this difference is a 78 kb inversion, with one endpoint between rps8 and infA and the second between psbA and rpl2. However, we can not rule out a two-step re-arrangement (consisting of successive expansion and contraction of the inverted repeat) leading to the relocation of a block of six ribosomal protein genes (rps19-rps8) from one end of the large single copy region to the other. Analysis of gene locations in pea cpDNA, which lacks the large inverted repeat, combined with cross-hybridization studies using 59 clones covering the mung bean genome, leads to a refined picture of the position and nature of the numerous rearrangements previously described in the pea genome. A minimum of eight large inversions are postulated to account for these rearrangements. None of these inversions disrupt groups of genes that are transcriptionally linked in angiosperm cpDNA. Rather, the end-points of inversions are associated with relatively spacer-rich segments of the genome, many of which contain tRNA genes. All of the pea-specific inversions are shown to be positionally distinct from those recently described in a closely related legume, broad bean.

Key words

Gene mapping Rearrangements Chloroplast DNA evolution Inverted repeat 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alt J, Morris J, Westhoff P, Herrmann RG (1984) Curr Genet 8:597–606Google Scholar
  2. Berends T, Kubicek Q, Mullet JE (1986) Plant Mol Biol 6:125–134Google Scholar
  3. Birnboim HC, Doly J (1979) Nucleic Acids Res 7:1513–1523Google Scholar
  4. Bookjans G, Stummann BM, Rasmussen OF, Henningsen (1986) Plant Mol Biol 6:359–366Google Scholar
  5. Cantatore P, Gadaletta MN, Roberti R, Saccone C, Wilson AC (1987) Nature 329:853–855Google Scholar
  6. Courtice GRM, Bowman CM, Dyer TA, Gray JC (1985) Cuff Genet 10:329–333Google Scholar
  7. Cozens AL, Walker JE (1986) Biochem J 236:453–460Google Scholar
  8. Cozens AL, Walker JE, Phillips AL, Huttly AK, Gray JC (1986) EMBO 5:217–222Google Scholar
  9. Fromm H, Edelman M, Koller B, Goloubinoff P, Galun E (1986) Nucleic Acids Res 14:883–898Google Scholar
  10. Heinemeyer W, Alt J, Herrmann RB (1984) Curr Genet 8:543–549Google Scholar
  11. Herrmann RG, Alt J, Schiller B, Widger WR, Cramer WA (1984) FEBS Lett 176:239–244Google Scholar
  12. Howe CJ (1985) Curr Genet 10:139–145Google Scholar
  13. Howe CJ, Barker RF, Bowman CM, Dyer TA (1988) Curt Genet 13:343–349Google Scholar
  14. Hudson GS, Mason JG, Holton TA, Koller B, Cox GB, Whitfeld PR, Bottomley W (1987) J Mol Biol 196:283–298Google Scholar
  15. Hudson GS, Holton TA, Whitfeld PR, Bottomley W (1988) J Mol Biol 200:639–654Google Scholar
  16. Jansen RK, Palmer JD (1987) Curr Genet 11:553–564Google Scholar
  17. Kirsch W, Seyer P, Herrmann RG (1986) Curr Genet 10:843–855Google Scholar
  18. Ko K, Orfanides AG, Straus NA (1987) Theor Appl Genet 74:125–139Google Scholar
  19. Koller B, Delius H (1980) Mol Gen Genet 178:261–269Google Scholar
  20. Koller B, Fromm H, Galun E, Edelman (1987) Cell 48:111–119Google Scholar
  21. Kolodner R, Tewari KK (1975) Biochem Biophy Acta 401:372–390Google Scholar
  22. Lehmbeck J, Rasmussen OF, Bookjans BG, Jepsen BR, Stummann BM, Henningsen KW (1986) Plant Mol Biol 7:3–10Google Scholar
  23. Lehmbeck J, Stummann BM, Henningsen KW (1987) Nucleic Acids Res 15:3630Google Scholar
  24. Michalowski C, Breunig KD, Bohnert HJ (1987) Curr Genet 11:265–274Google Scholar
  25. Moritz C, Brown WM (1987) Proc Natl Acad Sci USA 84:7183–7187Google Scholar
  26. Morris J, Herrmann RG (1984) Nucleic Acids Res 12:2837–2850Google Scholar
  27. Mubumbila M, Gordon KHJ, Crouse EJ, Burkard G, Weil JH (1983) Gene 21:257–266Google Scholar
  28. Neuhaus H, Link G (1987) Curr Genet 11:251–257Google Scholar
  29. Ohme M, Tanaka M, Chunwongse J, Shinozaki K, Sugiura M (1986) FEBS Lett 200:87–90Google Scholar
  30. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H, Ozeki H (1986) Nature 322:572–574Google Scholar
  31. Oishi KK, Shapiro DR, Tewari KK (1984) Mol Cell Biol 4:2556–2563Google Scholar
  32. Palmer JD (1983) Nature 301:92–93Google Scholar
  33. Palmer JD (1985) Annu Rev Genet 19:325–354Google Scholar
  34. Palmer JD (1986) Methods Enzymol 118:167–186Google Scholar
  35. Palmer JD, Stein DB (1986) Curr Genet 10:823–833Google Scholar
  36. Palmer JD, Thompson WF (1981a) Proc Natl Acad Sci USA 78:5533–5537Google Scholar
  37. Palmer JD, Thompson WF (1981b) Gene 15:21–26Google Scholar
  38. Palmer JD, Thompson WF (1982) Cell 29:537–550Google Scholar
  39. Palmer JD, Edwards H, Jorgensen RA, Thompson WF (1982) Nucleic Acids Res 10:6819–6832Google Scholar
  40. Palmer JD, Singh GP, Pillay DTN (1983) Mol Gen Genet 190:13–19Google Scholar
  41. Palmer JD, Osorio B, Watson JC, Edwards H, Dodd J, Thompson WF (1984) In: Thornber JP, Staehelin LA, Hallick RB (eds) Biosynthesis of the photosynthetic apparatus: molecular biology, development and regulation. New York, pp 273–283Google Scholar
  42. Palmer JD, Boynton JE, Gillham NW, Harris EH (1985a) In: Steinback KE, Bonitz S, Arntzen CJ, Bogorad L (eds) Molecular biology of the photosynthetic apparatus. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp 269–278Google Scholar
  43. Palmer JD, Jorgensen RA, Thompson WF (1985b) Genetics 109: 195–213Google Scholar
  44. Palmer JD, Osorio B, Aldrich J, Thompson WF (1987a) Curr Genet 11:275–286Google Scholar
  45. Palmer JD, Nugent JM, Herbon LA (1987b) Proc Natl Acad Sci USA 84:769–773Google Scholar
  46. Phillips AL, Gray JC (1984) Mol Gen Genet 194:477–484Google Scholar
  47. Polhill RM, Raven PH (1981) Advances in legume systematics, Part 1. Royal Botanic Gardens, KewGoogle Scholar
  48. Posno M, Torenvliet DJ, Lustig H, van Noort M, Groot GSP (1985) Curr Genet 9:211–219Google Scholar
  49. Purton S, Gray JC (1987) Nucleic Acids Res 15:1873Google Scholar
  50. Quigley F, Weil JH (1985) Curr Genet 9:495–503Google Scholar
  51. Rasmussen OF, Bookjans G, Stummann BM, Henningsen KW (1984a) Plant Mol Biol 3:191–199Google Scholar
  52. Rasmussen OF, Stummann BM, Henningsen KW (1984b) Nucleic Acids Res 12:9143–9153Google Scholar
  53. Rasmussen O, Jepsen B, Stummann B, Henningsen KW (1987) Nucleic Acids Res 15:854Google Scholar
  54. Reed KC, Mann DA (1985) Nucleic Acids Res 13:7207–7221Google Scholar
  55. Shapiro DR, Tewari KK (1986) Plant Mol Biol 6:1–12Google Scholar
  56. Shen GF, Chen K, Wu M, Kung SD (1982) Mol Gen Genet 187:12–18Google Scholar
  57. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse K, Obokata J, Yamaguchi-Shiozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) EMBO 5:2043–2049Google Scholar
  58. Sijben-Muller G, Hallick RB, Alt J, Westhoff P, Herrmann RG (1986) Nucleic Acids Res 14:1029–1044Google Scholar
  59. Singh GP, Wallen DG, Pillay DTN (1985) Plant Mol Biol 4:87–93Google Scholar
  60. Smith AG, Gray JC (1984) Mol Gen Genet 194:471–476Google Scholar
  61. Smith GE, Summers MD (1980) Anal Biochem 109:123–129Google Scholar
  62. Spielmann A, Ortiz W, Stutz E (1983) Mol Gen Genet 190:5–12Google Scholar
  63. Spielmann A, Stutz E (1983) Nucleic Acids Res 11:7157–7167Google Scholar
  64. Stummann BM, Lehmbeck J, Bookjans G, Henningsen KW (1988) Physiol Plant 72:139–146Google Scholar
  65. Sugita M, Kato A, Shimada H, Sugiura M (1984) Mol Gen Genet 19:200–205Google Scholar
  66. Sugita M, Shinozaki K, Sugiura M (1985) Proc Natl Acad Sci USA 82:3557–3561Google Scholar
  67. Sugiura M, Shinozaki K, Zaita N, Kusuda M, Kumano M (1986) Plant Sci 44:211–216Google Scholar
  68. Tanaka M, Wakasugi T, Sugita M, Shinozaki K, Sugiura M (1986) Proc Natl Acad Sci USA 83:6030–6034Google Scholar
  69. Turker MS, Domenico JM, Cummings DJ (1987) J Mol Biol 198:171–185Google Scholar
  70. von Allmen JM, Stutz E (1987) Nucleic Acids Res 15:2387Google Scholar
  71. Westhoff P, Farchaus JW, Herrmann RG (1986) Curr Genet 11:165–169Google Scholar
  72. Westhoff P, Grune H, Schrubar H, Oswald A, Streubel M, Ljungberg U, Herrmann RG (1988) In: Scheer H, Schneider S (eds) Photosynthetic light-harvesting systems: structure and function. de Gruyter, Berlin (in press)Google Scholar
  73. Willey DL, Auffret AD, Gray JC (1984) Cell 36:555–562Google Scholar
  74. Woodbury NW, Roberts LL, Palmer JD, Thompson (1988) Curr Genet 14:75–89Google Scholar
  75. Zurawski G, Bottomley W, Whitfeld PR (1982) Proc Natl Acad Sci USA 79:6260–6264Google Scholar
  76. Zurawski G, Bottomley W, Whitfeld PR (1984) Nucleic Acids Res 12:6547–6558Google Scholar
  77. Zurawski G, Bottomley W, Whitfeld PR (1986a) Nucleic Acids Res 14:3974Google Scholar
  78. Zurawski G, Bottomley W, Whitfeld PR (1986b) Nucleic Acids Res 14:3975Google Scholar

Copyright information

© Springer-Verlag 1988

Authors and Affiliations

  • Jeffrey D. Palmer
    • 1
  • Bernardita Osorio
    • 2
  • William F. Thompson
    • 3
  1. 1.Department of BiologyUniversity of MichiganAnn ArborUSA
  2. 2.StaffordUSA
  3. 3.Department of BotanyNorth Carolina State UniversityRaleighUSA

Personalised recommendations