Genetic Resources and Crop Evolution

, Volume 58, Issue 1, pp 101–114 | Cite as

New data and phylogenetic placement of the enigmatic Old World lupin: Lupinus mariae-josephi H. Pascual

  • Frédéric Mahé
  • Higinio Pascual
  • Olivier Coriton
  • Virginie Huteau
  • Albert Navarro Perris
  • Marie-Thérèse Misset
  • Abdelkader AïnoucheEmail author
Research Article


Lupinus mariae-josephi H. Pascual is an intriguing lupin species recently discovered in the Mediterranean region. New data from seed coat micromorphology, cytology, and DNA sequences were generated in order to extend our knowledge on this species and to examine its evolutionary relationships within Lupinus. This species shows morphological similarities with the Mediterranean smooth seeded species of sections Micranthi and Lutei. It shares the same chromosome number 2n = 52 with the latter Old World taxa, but also with unifoliolate lupins from Florida. Besides, L. mariae-josephi exhibited a seed coat micromorphology “intermediate” between the rough and the smooth seed coat types. Phylogenetic analyses using ITS and ETS nrDNA spacers, and the LEGCYC1A locus supported L. mariae-josephi as a distinct Old World line, placed out of the Scabrispermae, but without clear placement amongst the Mediterranean smooth-seeded lineages. Unexpectedly, LEGCYC1A data revealed phylogenetic affinities between L. mariae-josephi and L. villosus, a unifoliolate North American lupin that might have experienced a reticulated evolutionary process. All together, the data underline the phylogenetic interest of L. mariae-josephi in Lupinus and the need of additional investigations in order to definitely elucidate its enigmatic status. Moreover, as L. mariae-josephi is one of the rare Old World lupins strictly restricted to poor basic soils, it opens new perspectives of ecological and agronomic interests in the wide areas of poor calcareous soils in the Mediterranean region.


Chromosome number Lupinus mariae-josephi Old World lupins Phylogenetic placement Seed coat microstructure 


  1. Aïnouche A (1998) Diversité et évolution du genre Lupinus L. (Fabaceae). Dissertation, Université de Rennes 1, FranceGoogle Scholar
  2. Aïnouche A, Bayer RJ (1999) Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Am J Bot 86:590–607CrossRefPubMedGoogle Scholar
  3. Aïnouche A, Bayer RJ (2000) Genetic evidence supports the new Anatolian lupin accession, Lupinus anatolicus, as an old world “rough-seeded” lupin (section Scabrispermae) related to L. pilosus. Folia Geobot 35:83–95. doi: 10.1007/BF02803088 CrossRefGoogle Scholar
  4. Aïnouche A, Greinwald R, Witte L, Huon A (1996) Seed alkaloid composition of Lupinus tassilicus Maire (Fabaceae: Genisteae) and comparison with its related rough seeded lupin species. Biochem Syst Ecol 24:405–414. doi: 10.1016/0305-1978(96)00034-8 CrossRefGoogle Scholar
  5. Aïnouche A, Bayer RJ, Cubas P, Misset M (2003) Phylogenetic relationships within tribe Genisteae (Papilionoideae) with special reference to genus Ulex. In: Klitgaard BB, Bruneau A (eds) Advances in legume systematics. Part 10. Higher level systematics. Royal Botanic Gardens, Kew, United Kingdom, pp 239–252Google Scholar
  6. Aïnouche A, Bayer RJ, Misset M (2004) Molecular phylogeny, diversification and character evolution in Lupinus (Fabaceae) with special attention to Mediterranean and African lupins. Plant Syst Evol 246:211–222. doi: 10.1007/s00606-004-0149-8 CrossRefGoogle Scholar
  7. Álvarez I, Wendel JF (2003) Ribosomal ITS sequences and plant phylogenetic inference. Mol Phylogenet Evol 29:417–434. doi: 10.1016/S1055-7903(03)00208-2 CrossRefPubMedGoogle Scholar
  8. Baldwin BG, Markos S (1998) Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: Congruence of ETS and ITS trees of Calycadenia (Compositae). Mol Phylogenet Evol 10:449–463. doi: 10.1006/mpev.1998.0545 CrossRefPubMedGoogle Scholar
  9. Baldwin BG, Sanderson MJ, Porter JM, Wojciechowski MF, Campbell CS, Donoghue MJ (1995) The ITS region of nuclear ribosomal DNA: a valuable source of evidence on angiosperm phylogeny. Ann MO Bot Gard 82:247–277. doi: 10.2307/2399880 CrossRefGoogle Scholar
  10. Bragg LH (1983) Seed coats of some Lupinus species. Scan Electron Micros 4:1739–1745Google Scholar
  11. Carstairs SA, Buirchell BJ, Cowling WA (1992) Chromosome number, size and interspecific crossing ability of three Old World lupins, Lupinus princei Harms, L. atlanticus Gladstones and L. digitatus Forskal, and implications for cyto-systematic relationships among the rough-seeded lupins. J R Soc West Aust 75:83–88Google Scholar
  12. Castroviejo S, Pascual H (1999) Lupinus L. In: Talavera S, Aedo C, Castroviejo S, Romero Zarco C, Sáez L, Salgueiro FJ, Velayos M (eds) Flora Iberica—Plantas vasculares de la Península Ibérica e Islas Baleares, vol VII (I). Real Jardín Botánico, CSIC, Madrid, Spain, pp 251–260Google Scholar
  13. Chandler GT, Bayer RJ, Crisp MD (2001) A molecular phylogeny of the endemic Australian genus Gastrolobium (Fabaceae: Mirbelieae) and allied genera using chloroplast and nuclear markers. Am J Bot 88:1675–1687. doi: 10.2307/3558413 CrossRefGoogle Scholar
  14. Citerne HL (2005) A Primer Set for Specific Amplification of Two Cycloidea-Like Genes in the Genistoid Clade of Leguminosae Subfam. Papilionoideae. Edinb J Bot 62:119–126. doi: 10.1017/S0960428606000126 CrossRefGoogle Scholar
  15. Citerne HL, Luo D, Pennington RT, Coen E, Cronk QC (2003) A Phylogenomic Investigation of CYCLOIDEA-Like TCP Genes in the Leguminosae. Plant Physiol 131:1042–1053. doi: 10.1104/pp.102.016311 CrossRefPubMedGoogle Scholar
  16. Clements JC, Buirchell BJ, Cowling WA (1996) Relationship between morphological variation and geographical origin or selection history in Lupinus pilosus. Plant Breed 115:16–22. doi: 10.1111/j.1439-0523.1996.tb00864.x CrossRefGoogle Scholar
  17. Conterato IF, Schifino-Wittmann MT (2006) New chromosome numbers, meiotic behaviour and pollen fertility in American taxa of Lupinus (Leguminosae): contributions to taxonomic and evolutionary studies. Bot J Linn Soc 150:229–240. doi: 10.1111/j.1095-8339.2006.00443.x CrossRefGoogle Scholar
  18. Cowling W, Buirchell BJ, and Tapia ME (1998) Lupin—Lupinus L.—Promoting the conservation and use of underutilized and neglected crops. No 23, IPBGRI, Rome, Gatersleben, 105 pGoogle Scholar
  19. Cristofolini G (1989) A serological contribution to the systematics of the genus Lupinus (Fabaceae). Plant Syst Evol 166:265–278. doi: 10.1007/BF00935955 CrossRefGoogle Scholar
  20. Drummond CS (2008) Diversification of Lupinus (Leguminosae) in the western New World: derived evolution of perennial life history and colonization of montane habitats. Mol Phylogenet Evol 48:408–421. doi: 10.1016/j.ympev.2008.03.009 CrossRefPubMedGoogle Scholar
  21. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi: 10.2307/2408678 CrossRefGoogle Scholar
  22. Gladstones JS (1974) Lupins of the Mediterranean region and Africa. Western Australian Department of Agriculture. Tech Bull 26:1–48Google Scholar
  23. Gladstones JS (1984) Present situation and potential of mediterranean/african Lupinus for crop production. In: Proceedings of the third international lupin conference. International Lupin Association, La Rochelle, France, pp 67–85Google Scholar
  24. Gladstones JS (1998) Distribution, origin, taxonomy, history and importance. In: Gladstones JS, Atkins CA, Hamblin J (eds) Lupins as crop plants: biology, production and utilization. CABI, Wallingford, United Kingdom, pp 1–37Google Scholar
  25. Guillon F, Champ MM (2002) Carbohydrate fractions of Legumes: uses in human nutrition and potential for health. Br J Nutr 88:293–306. doi: 10.1079/BJN2002720 CrossRefGoogle Scholar
  26. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi: 10.1080/10635150390235520 CrossRefPubMedGoogle Scholar
  27. Gupta S, Buirchell BJ, Cowling WA (1996) Interspecific reproductive barriers and genomic similarity among the rough-seeded Lupinus species. Plant Breed 115:123–127. doi: 10.1111/j.1439-0523.1996.tb00886.x CrossRefGoogle Scholar
  28. Hanelt P (1960) Lupinen. zur Geschichte und Verwendung landwirtschaftlich wichtiger Lupinenarten. Ziemsen-Verlag, WittenbergGoogle Scholar
  29. Harrison CJ, Langdale JA (2006) A step by step guide to phylogeny reconstruction. Plant J 45:561–572. doi: 10.1111/j.1365-313X.2005.02611.x CrossRefPubMedGoogle Scholar
  30. Heyn CC, Herrnstadt I (1977) Seed coat structure of Old World Lupinus species. Botaniska Notiser 130:427–435Google Scholar
  31. Howieson JG, Fillery IRP, Legocki A, Sikorski MM, Stępkowski T, Minchin FR, Dilworth MJ (1998) Nodulation, nitrogen fixation and nitrogen balance. In: Gladstones JS, Atkins CA, Hamblin J (eds) Lupins as crop plants: biology, production and utilization. CABI, Wallingford, United Kingdom, pp 149–180Google Scholar
  32. Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. P Natl Acad Sci USA 103:10334–10339. doi: 10.1073/pnas.0601928103 CrossRefGoogle Scholar
  33. Käss E, Wink M (1997) Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbcL gene and ITS 1 + 2 regions of rDNA. Plant Syst Evol 208:139–167. doi: 10.1007/BF00985439 CrossRefGoogle Scholar
  34. Maciel HS, Schifino-Wittmann MT (2002) First chromosome number determinations in south-eastern South American species of Lupinus L. (Leguminosae). Bot J Linn Soc 139:395–400. doi: 10.1046/j.1095-8339.2002.00071.x CrossRefGoogle Scholar
  35. Magni C, Sessa F, Accardo E, Vanoni M, Morazzoni P, Scarafoni A, Duranti M (2004) Conglutin γ, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels of hyperglycemic rats. J Nutr Biochem 15:646–650. doi: 10.1016/j.jnutbio.2004.06.009 CrossRefPubMedGoogle Scholar
  36. Monteiro R (1987) Seed testa pattern of unifoliolate species of Lupinus L. (Leguminosae). Salusvita 6:20–31Google Scholar
  37. Moretti S, Armougom F, Wallace IM, Higgins DG, Jongeneel CV, Notredame C (2007) The M-Coffee web server: a meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res 35:W645–W648. doi: 10.1093/nar/gkm333 CrossRefPubMedGoogle Scholar
  38. Müller K (2005) SeqState: primer design and sequence statistics for phylogenetic DNA datasets. Appl Bioinformatics 4:65–69CrossRefPubMedGoogle Scholar
  39. Müller K (2006) Incorporating information from length-mutational events into phylogenetic analysis. Mol Phylogenet Evol 38:667–676. doi: 10.1016/j.ympev.2005.07.011 CrossRefPubMedGoogle Scholar
  40. Naganowska B, Wolko B, Śliwińska E, Kaczmarek Z (2003) Nuclear DNA content variation and species relationships in the genus Lupinus (Fabaceae). Ann Bot 92:349–355. doi: 10.1093/aob/mcg145 CrossRefPubMedGoogle Scholar
  41. Navarro Perris AJ, Fos Martín S, Ferrando Pardo I, Laguna Lumbreras E (2006) Localizacíon del endemismo aparentemente extinto Lupinus mariae-josephi. Flora Montiberica 33:59–63Google Scholar
  42. Pascual H (2004) Lupinus mariae-josephi (Fabaceae), nueva y sorprendente especie descubierta en España. An Jard Bot Madrid 61:69–72Google Scholar
  43. Pilvi TK, Jauhiainen T, Cheng ZJ, Mervaala EM, Vapaatalo H, Korpela R (2006) Lupin protein attenuates the development of hypertension and normalises the vascular function of NaCl-loaded Goto-Kakizaki rats. J Physiol Pharmacol 57:167–176PubMedGoogle Scholar
  44. Plitmann U, Pazy B (1984) Cytogeographical distribution of the Old World Lupinus. Webbia 38:531–539Google Scholar
  45. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. doi: 10.1080/10635150490522304 CrossRefPubMedGoogle Scholar
  46. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi: 10.1093/bioinformatics/14.9.817 CrossRefPubMedGoogle Scholar
  47. Przybylska J, Zimniak-Przybylska Z (1995) Electrophoretic patterns of seed globulins in the Old-World Lupinus species. Genet Resour Crop Evol 42:69–75. doi: 10.1007/BF02310686 CrossRefGoogle Scholar
  48. Ree RH, Citerne HL, Lavin M, Cronk QCB (2004) Heterogeneous selection on LEGCYC paralogs in relation to flower morphology and the phylogeny of Lupinus (Leguminosae). Mol Biol Evol 21:321–331. doi: 10.1093/molbev/msh022 CrossRefPubMedGoogle Scholar
  49. Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381. doi: 10.1080/10635159950173889 CrossRefPubMedGoogle Scholar
  50. Soltis DE, Soltis PS (1998) Choosing an approach and an appropriate gene for phylogenetic analysis. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer Academic Publishers, Boston, Massachusetts, USA, pp 1–42Google Scholar
  51. Soltis DE, Mavrodiev EV, Doyle JJ, Rauscher J, Soltis PS (2008) ITS and ETS sequence data and phylogeny reconstruction in allopolyploids and hybrids. Syst Bot 33:7–20. doi: 10.1600/036364408783887401 CrossRefGoogle Scholar
  52. Suárez-Santiago VN, Salinas MJ, Garcia-Jacas N, Soltis PS, Soltis DE, Blanca G (2007) Reticulate evolution in the Acrolophus subgroup (Centaurea L., Compositae) from the western mediterranean: origin and diversification of section Willkommia Blanca. Mol Phylogenet Evol 43:156–172. doi: 10.1016/j.ympev.2006.08.006 CrossRefPubMedGoogle Scholar
  53. Święcicki W, Święcicki WK, Wolko B (1996) Lupinus anatolicus—a new lupin species of the Old World. Genet Resour Crop Evol 43:109–117. doi: 10.1007/BF00126753 CrossRefGoogle Scholar
  54. Swofford DL (2003) Phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland, Massachussets, USAGoogle Scholar
  55. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  56. Wallace IM, O’Sullivan O, Higgins DG, Notredame C (2006) M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 34:1692–1699. doi: 10.1093/nar/gkl091 CrossRefPubMedGoogle Scholar
  57. Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer Academic Publishers, Boston, Massachusetts, USA, pp 265–296Google Scholar
  58. Williams CA, Demissie A, Harborne JB (1983) Flavonoids as taxonomic markers in Old World Lupinus species. Biochem Syst Ecol 11:221–231. doi: 10.1016/0305-1978(83)90058-3 CrossRefGoogle Scholar
  59. Wink M (1992) The role of quinolizidine alkaloids in plant–insect interactions. In: Bernays EA (ed) Insect–plant interactions, vol 4. CRC Press, Boca Raton, Florida, USA, pp 131–166Google Scholar
  60. Wink M, Meißner C, Witte L (1995) Patterns of quinolizidine alkaloids in 56 species of the genus Lupinus. Phytochemistry 38:139–153. doi: 10.1016/0031-9422(95)91890-D CrossRefGoogle Scholar
  61. Wolko B, Weeden NF (1990a) Isozyme number as an indicator of phylogeny in lupins. Genet Pol 31:179–187Google Scholar
  62. Wolko B, Weeden NF (1990b) Relationships among lupin species as reflected by isozyme phenotype. Genet Pol 31:189–197Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Frédéric Mahé
    • 1
  • Higinio Pascual
    • 2
  • Olivier Coriton
    • 3
  • Virginie Huteau
    • 3
  • Albert Navarro Perris
    • 4
  • Marie-Thérèse Misset
    • 1
  • Abdelkader Aïnouche
    • 1
    Email author
  1. 1.UMR CNRS 6553 EcobioRennes cedexFrance
  2. 2.Instituto Madrileño de Investigación Agraria y Alimentaria (IMIA)Alcalá de HenaresSpain
  3. 3.UMR118 INRA-AgroCampus Rennes INRA Centre de Rennes BP 35327Le Rheu CedexFrance
  4. 4.Centro de Investigación y Experimentación Forestal (CIEF)Quart de PobletSpain

Personalised recommendations