Genetic diversity and population structure in natural populations of Moroccan Atlas cedar (Cedrus atlantica; Pinaceae) determined with cpSSR markers

American Journal of Botany

Volumn 93, Issue 9, 2006, Pages 1274-1280

  Terrab, Anass ^a,b   Paun, Ovidiu ^a   Talavera, Salvador ^b   Tremetsberger, Karin ^a   Arista, Montserrat ^b   Stuessy, Tod F ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Cedrus atlantica; Chloroplast microsatellites; Conservation; Morocco; Pinaceae; Population genetics

Indexed keywords

BIODIVERSITY; BIOMARKER; CHLOROPLAST; CLUSTER ANALYSIS; CONIFEROUS TREE; CONSERVATION GENETICS; ENDANGERED SPECIES; GENETIC ANALYSIS; GENETIC VARIATION; POPULATION STRUCTURE;

AFRICA; MOROCCO; NORTH AFRICA;

ATLAS CEDAR; CEDRUS; CEDRUS ATLANTICA; CONIFEROPHYTA; GYMNOSPERMAE; MAGNOLIOPHYTA; PINACEAE;

EID: 33749441432     PISSN: 00029122     EISSN: 00029122     Source Type: Journal    
DOI: 10.3732/ajb.93.9.1274     Document Type: Article

References (65)

1. AEFCS (ADMINISTRATION DES EAUX ET FORÊTS ET DE LA CONSERVATION DES SOLS). 1995. Bilan de la compagne des reboisements, 1994-1995. Ministère de l'Agriculture et de la Réforme Agraire, Rabat, Morocco.
2. BENABID, A. 2000. Flore et cosystèmes du Maroc. Éditions Ibis Press, Paris, France.
3. BENABID, A., AND M. FENNANE. 1994. Connaissances sur la végétation du Maroc: phytogégraphie, phytosociologie et sèries de végétation. Lazaroa 14: 21-97.
4. CATO, S. A., AND T. E. RICHARDSON. 1996. Inter- and intraspecific polymorphism at chloroplast SSR loci and the inheritance of plastids in Pinus radiata D. Don. Theoretical and Applied Genetics 93: 587-592.
5. CHEDDADI, R., H. F. LAMB, J. GUIOT, AND S. VAN DER KAARS. 1998. Holocene climatic change in Morocco: a quantitative reconstruction from pollen data. Climate Dynamics 14: 883-890.
6. CLARK, C. M., T. R. WENTWORTH, AND D. M. O'MALLEY. 2000. Genetic discontinuity revealed by chloroplast microsatellites in eastern North American Abies (Pinaceae). American Journal of Botany 87: 774-782.
7. CLEGG, M. T., AND G. ZURAWSKI. 1992. Chloroplast DNA and the study of plant phylogeny: present status and future prospects. In P. E. Soltis, D. E. Soltis, and J. J. Doyle [eds.], Molecular systematics of plants, 1-13. Chapman and Hall, New York, New York, USA.
8. CUENCA, A., A. E. ESCALANTE, AND D. PIÑERO. 2003. Long-distance colonization, isolation by distance, and historical demography in a relictual Mexican pinyon pine (Pinus nelsonii Shaw) as revealed by paternally inherited genetic markers (cpSSRs). Molecular Ecology 12: 2087-2097.
9. CULLINGS, K. W. 1992. Design and testing of a plant-specific PCR primer for ecological and evolutionary studies. Molecular Ecology 1: 233-240.
10. DE BEAULIEU, J. L., AND M. REILLE. 1973. L'interprétation des spectres polliniques de périodes froides: à propos du cèdre au Quaternaire en Europe, supplément, Bulletin de l'Association Française pour l'Etude du Quaternaire 36: 198-199.
11. DUPANLOUP, I., S. SCHNEIDER, AND L. EXCOFFIER. 2002. A simulated annealing approach to define genetic structure of populations. Molecular Ecology 11: 2571-2581.
12. ECHT, C., L. DE VERNOL, M. ANZIDEI, AND G. G. VENDRAMIN. 1998. Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Molecular Ecology 7: 307-316.
13. EL AMMARI, A. 1996. Étude de rendement en sciage du cèdre du Moyen Atlas central. Mémoire de 3ème cycle. ENFI, Rabat, Morocco.
14. ESTOUP, A., P. JARNE, AND J. M. CORNUET. 2002. Homoplasy and mutation model at microsatellite loci and their consequences for population genetic analysis. Molecular Ecology 11: 1591-1604.
15. EXCOFFIER, L., P. E. SMOUSE, AND J. M. QUATTRO. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
16. FADY, B. 2005. Is there really more biodiversity in Mediterranean forest ecosystems? Taxon 54: 905-910.
17. FADY, B., F. LEVÈVRE, M. REYNAUD, G. G. VENDRAMIN, M. BOU DAGHERKHARRAT, M. ANZIDEI, R. PASTORELLI, A. SAVOURÉ , AND M. BARITEAU. 2003. Gene flow among different taxonomic units: evidence from nuclear and cytoplasmic markers in Cedrus plantation forests. Theoretical and Applied Genetics 107: 1132-1138.
18. FALLOUR, D., B. FADY, AND F. LEFÈVRE. 2001. Evidence of variation in segregation patterns within a Cedrus population. Journal of Heredity 92: 260-266.
19. GOLDSTEIN, D. B., A. RUIZ LINARES, L. L. CAVALLI-SFORZA, AND M. W. FELDMAN. 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463-471.
20. GÓMEZ, A., S. C. GONZÁLEZ-MARTÍNEZ, C. COLLADA, J. CLIMENT, AND L. GIL. 2003. Complex population genetic structure in the endemic Canary Island pine revealed using chloroplast microsatellite markers. Theoretical and Applied Genetics 107: 1123-1131.
21. HAMRICK, J. L., M. J. W. GODT, AND S. L. SHERMAN-BROYLES. 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests 6: 95-124.
22. HANSEN, O. K., E. D. KJAER, AND G. G. VENDRAMIN. 2005. Chloroplast microsatellite variation in Abies nordmanniana and simulation of causes for low differentiation among populations. Tree Genetics & Genomes 1: 116-123.
23. HARDY, O. J., N. CHARBONNEL, H. FREVILLE, AND M. HEUERTZ. 2003. Microsatellite allele size: a simple test to assess their significance in genetic differentiation. Genetics 163: 1467-1482.
24. HARDY, O. J., AND X. VEKEMANS. 2002. SPAGeDi : a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618-620.
25. HARTL, D. L., AND A. G. CLARK. 1997. Principles of population genetics. Sinauer, Sunderland, Massachusetts, USA.
26. HUSON, D. H. 1998. SplitsTree: a program for analyzing and visualizing evolutionary data. Bioinformatics 14: 68-73.
27. LAMB, H. F., AND S. VAN DER KAARS. 1995. Vegetational response to Holocene climatic change: pollen and palaeolimnologic data from the Middle Atlas, Morocco. Holocene 5: 400-408.
28. LEFÈVRE, F., B. FADY, D. FALLOUR-RUBIO, D. GHOSN, AND M. BARITEAU. 2004. Impact of founder population, drift and selection on the genetic diversity of a recently translocated tree population. Heredity 93: 542-550.
29. MAGRI, D., AND I. PARRA. 2002. Late quaternary western Mediterranean pollen records and African winds. Earth and Planetary Science Letters 200: 401-408.
30. MABBERLY, D. J. 1990. The plant-book. Cambridge University Press, Cambridge, UK.
31. MCCAULEY, D. E. 1995. The use of chloroplast DNA polymorphism in studies of gene flow in plants. Trends in Ecology & Evolution 10: 198-202.
32. MORGANTE, M., N. FELICE, AND G. G. VENDRAMIN. 1998. Analysis of hypervariable chloroplast microsatellites in Pinus halepensis reveals a dramatic genetic bottleneck. In A. Karp, P. G. Isaac, and D. S. Ingram [eds.], Molecular tools for screening biodiversity: plants and animals, 407-412. Chapman and Hall, London, UK.
33. NEALE, D. B., AND R. R. SEDEROFF. 1989. Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in lobololly pine. Theoretical and Applied Genetics 77: 212-216.
34. NEALE, D. B., N. C. WHEELER, AND R. W. ALLARD. 1986. Paternal inheritance of chloroplast DNA in Douglas fir. Canadian Journal of Forest Research 16: 1152-1154.
35. NEI, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
36. NEI, M., F. TAJIMA, AND Y. TATENO. 1983. Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. Journal of Molecular Evolution 19: 153-170.
37. NEWTON, A. C., T. R. ALLNUTT, A. C. M. GILLIES, A. J. LOWE, AND R. A. ENNOS. 1999. Molecular phylogeography, intraspecific variation and the conservation of tree species. Trends in Ecology & Evolution 14: 140-145.
38. NYBOM, H., AND I. V. BARTISH. 2000. Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspectives in Plant Ecology, Evolution and Systematics 3: 93-114.
39. PANETSOS, K. P., A. CHRISTOU, AND A. SCALSOYIANNES. 1992. First analysis on allozymes variation in Cedar species (Cedrus sp.). Silvae Genetica 41: 339-342.
40. PANETSOS, K. P., A. SCALSOYIANNES, AND M. TSAKTSIRA. 1994. Genetic variation in allozymes of Cedrus libani A. Rich and Cedrus atlantica Manneti. Annales de la Recherche forestière au Maroc 27: 420-434.
41. PARDUCCI, L., A. E. SZMIDT, A. MADAGHIELE, M. ANZIEI, AND G. G. VENDRAMIN. 2001. Genetic variation at chloroplast microsatellites (cpSSRs) in Abies nebrodensis (Lojac.) Mattei and three neighboring Abies species. Theoretical and Applied Genetics 102: 733-740.
42. POWELL, W., M. MORGANTE, C. ANDRE, J. W. MCNICOL, G. C. MACHRAY, J. J. DOYLE, S. V. TINGEY, AND J. A. RAFALSKI. 1995. Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Current Biology 5: 1023-1029.
43. PROVAN, J., N. SORANZO, N. WILSON, D. B. GOLDSTEIN, AND W. POWELL. 1999. A low mutational rate for chloroplast microsatellites. Genetics 153: 943-947.
44. QUÉZEL, P. 1981. Les hautes montagnes du Maghreb et du Proche Orient: essai de mise en parallèle des caractères phytogéographiques. Actas III Congreso Optima. Anales del Jardín Botánico de Madrid 37: 353-372.
45. RENAU-MORATA, B., S. G. NEBAUER, E. SALES, J. ALLAINGUILLAUME, P. CALIGARI, AND J. SEGURA. 2005. Genetic diversity and structure of natural and managed populations of Cedrus atlantica (Pinaceae) assessed using random amplified polymorphic DNA. American Journal of Botany 92: 875-884.
46. REILLE, M. 1990. La tourbière de La Borde (Pyrénées orientales, France): un site clé pour l'étude du Tardiglaciaire sudeuropéen. Comptes Rendus de l'Académie des Sciences Paris Series, II 310: 823-829.
47. RIBEIRO, M. M., C. PLOMION, R. PETIT, G. G. VENDRAMIN, AND A. E. SZMIDT. 2001. Variation in chloroplast single-sequence repeats in Portuguese maritime pine (Pinus pinaster Ait.). Theoretical and Applied Genetics 102: 97-103.
48. ROHLF, F. J. 1997. NTSYS: numerical taxonomy and multivariate analysis system, version 2.0. Exeter Software, Setauket, New York, USA.
49. SAITOU, N., AND M. NEI. 1987. The neighbour-joining method: a new model for reconstructing phylogenetic trees. Molecular Biology & Evolution 4: 406-425.
50. SALVADOR, L., R. ALÍA, D. AGÚNDEZ, AND L. GIL. 2000. Genetic variation and migration pathways of maritime pine (Pinus pinaster Ait) in the Iberian Peninsula. Theoretical and Applied Genetics 100: 89-95.
51. SCALTSOYIANNES, A. 1999. Allozyme differentiation and phylogeny of cedar species. Silvae Genetica 48: 61-68.
52. SCHNEIDER, S., D. ROESSLI, AND L. EXCOFFIER. 2000. Arlequin v.2.000: a software for population genetics data analysis. User manual: ver. 2.000. Genetics and Biometry Laboratory, University of Geneva, Geneva, Switzerland.
53. SEDEROFF, R. R., S. LEVINGS III, D. H. TIMOTHY, AND W. W. L. HU. 1981. Evolution of DNA sequence organization in mitochondrial genomes of Zea. Proceedings of the National Academy of Sciences, USA 78: 5953-5957.
54. SLATKIN, M. 1995. A measure of population subdivision based on microsatellites allele frequency. Genetics 139: 457-462.
55. STRAUSS, S. H., Y-P. HONG, AND V. D. HIPKINS. 1993. High levels of population differentiation for mitochondrial DNA haplotypes in Pinus radiata, muricata, and attenuata. Theoretical and Applied Genetics 86: 605-611.
56. TAKEZAKI, N., AND M. NEI. 1996. Genetic distance and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144: 389-399.
57. TSUMURA, Y., AND Y. SUYAMA. 1998. Differentiation of mitochondrial DNA polymorphism in a population of five Japanese Abies species. Evolution 52: 1031-1042.
58. VENDRAMIN, G. G., M. ANZIDEI, A. MADAGHIELE, AND G. BUCCI. 1998. Distribution of genetic diversity in Pinus pinaster Ait. as revealed by chloroplast microsatellites. Theoretical and Applied Genetics 97: 456-463.
59. VENDRAMIN, G. G., B. DEGEN, R. J. PETIT, M. ANZIDEI, A. MADAGHIELE, AND B. ZIEGENHAGEN. 1999. High level of variation at Abies alba chloroplast microsatellites loci in Europe. Molecular Ecology 8: 1117-1126.
60. VENDRAMIN, G. G., L. LELLI, P. ROSSI, AND M. MORGANTE. 1996. A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Molecular Ecology 5: 595-598.
61. VENDRAMIN, G. G., AND B. ZIEGENHAGEN. 1997. Characterization and inheritance of polymorphic plastid microsatellites in Abies. Genome 40: 857-864.
62. WAKASUGI, T., S. I. TSUDZUKI, M. SHIBATA, AND M. SUGIURA. 1994. A physical map and clone bank of the black pine (Pinus thunbergii) chloroplast genome. Plant Molecular Biology Reporter 12: 227-241.
63. WRIGHT, S. 1965. The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395-420.
64. WU, J. W., K. V. KRUTOVSKII, AND S. H. STRAUSS. 1998. Abundant mitochondrial genome diversity, population differentiation and convergent evolution in pines. Genetics 150: 1605-1614.
65. ZIEGENHAGEN, B., F. SCHOLZ, A. MADAGHIELE, AND G. G. VENDRAMIN. 1998. Chloroplast microsatellites as markers for paternity analysis in Abies alba. Canadian Journal of Forest Research 28: 317-321.