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Molecular systematics, character evolution, and pollen morphology of Cistus and Halimium (Cistaceae)

Plant Systematics and Evolution volume 295, pages 23–54 (2011)Cite this article

Abstract

Pollen analysis and parsimony-based phylogenetic analyses of the genera Cistus and Halimium, two Mediterranean shrubs typical of Mediterranean vegetation, were undertaken, on the basis of cpDNA sequence data from the trnL-trnF, and trnS-trnG regions, to evaluate limits between the genera. Neither of the two genera examined formed a monophyletic group. Several monophyletic clades were recognized for the ingroup. (1) The “white and whitish pink Cistus”, where most of the Cistus sections were present, with very diverse pollen ornamentations ranging from striato-reticulate to largely reticulate, sometimes with supratectal elements; (2) The “purple pink Cistus” clade grouping all the species with purple pink flowers belonging to the Macrostylia and Cistus sections, with rugulate or microreticulate pollen. Within this clade, the pink-flowered endemic Canarian species formed a monophyletic group, but with weak support. (3) Three Halimium clades were recovered, each with 100% bootstrap support; all Halimium species had striato-reticulate pollen. Two Halimium clades were characterized by yellow flowers, and the other by white flowers.

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References

  • Alverson WS, Karol KG, Baum DA, Chase MW, Swensen SM, Mccourt R, Sytsma KJ (1998) Circumscription of the Malvales and relationships to other Rosidae: evidence from rbcL sequence data. Am J Bot 85:876–887

    Article  PubMed  CAS  Google Scholar 

  • Arrington JM, Kubitzki K (2003) Cistaceae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants. Malvales, Capparales and non-betalain Caryophyllales, vol 5. Springer, Berlin

  • Ball J (1877) Spicilegium Florae Marocannae. J Linn Soc Bot 16:343–348

    Article  Google Scholar 

  • Bañares Á, Blanca G, Güemes J, Moreno JC, Ortiz S (eds) (2008) Atlas y Libro Rojo de la Flora Vascular Amenazada de España. Adenda 2008. Dirección General de Medio Natural y Política Forestal (Ministerio de Medio Ambiente, y Medio Rural y Marino-Sociedad Española de Biología de la Conservación de Plantas). Madrid

  • Barquín-Diez E, Voggenreiter V (1988) Prodromus del atlas fitocorológico de las Canarias occidentales. Parte I: Flora autóctona y especies de interés general

  • Batista F, Bañares A, Caujapé-Castells J, Carqué E, Marrero-Gómez M, Sosa PA (2001) Allozyme diversity in three endemic species of Cistus (Cistaceae) from the Canary Islands: intraspecific and interspecific comparisons and implications for genetic conservation. Am J Bot 88:1582–1592

    Article  PubMed  CAS  Google Scholar 

  • Bayer C, Chase MW, Fay MF (1998) Muntingiaceae, a new family of dicotyledons with malvalean affinities. Taxon 47:37–42

    Article  Google Scholar 

  • Borsch T, Quandt D (2009) Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Syst Evol 282:169–199

    Article  CAS  Google Scholar 

  • Civeyrel L, Le Thomas A, Ferguson IK, Chase MW (1998) Critical reexamination of palynological characters used to delimit Asclepiadaceae in comparison to the molecular phylogeny obtained from plastid matK sequences. Mol Phylogenet Evol 9:517–527

    Article  PubMed  CAS  Google Scholar 

  • Clegg MT, Zurawski G (1992) Chloroplast DNA and the study of plant phylogeny: present status and future prospects. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, pp 1–13

  • Dansereau P (1939) Monographie du genre Cistus. Boissiera 4:1–90

    Google Scholar 

  • Dansereau P (1940) Études sur les hybrides de Cistes. Ann Épiphyt 6 (Ser. 2):7–26

  • Dansereau P (1941) Etudes sur les hybrides de cistes—IV. Corrélation des caractères du C. salviifolius L: VI. Introgression dans la section Ladanium. Anim Biodivers Conserv 38:59–67

    Google Scholar 

  • Demoly JP (1996) Les hybrides binaires rares du genre Cistus L. (Cistaceae). Anales Jard Bot Madrid 54:241–254

    Google Scholar 

  • Demoly JP (1998) Notes taxonomiques sur le nothogenre × Halimiocistus Janch. (Cistaceae). J Bot Soc Bot France 6:31–38 (× Halimiocistus humilis Demoly)

    Google Scholar 

  • Demoly JP (2004) Description d une espèce confondue dans le passé avec Cistus symphytifolius Lam. et, parfois, avec C. ocreatus Chr. Sm. Acta Bot Gallica 151:231–232

    Google Scholar 

  • Demoly JP, Montserrat P (1993) Cistus. In: Castroviejo S et al (eds) Flora Iberica, vol 3, pp 319–337. Consejo de Investigaciones Cientifícas, Madrid

  • Dercourt J, Bassoullet JP, Baud A, Butterlin J, Camoin G, Cavelier C, Cecca F, Enay R, Fourcade E, Guiraud R, Lorenz C, Marcoux J, Masse JP, Orszag F, Philip J (1992) Paeloenvironmental atlas of the Tethys from Permian to recent. In: 29th International geological congress, Kyoto, Japan

  • Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, pp 14–35

  • Emerson BC (2003) Genes, geology and biodiversity: faunal and floral diversity on the island of Gran Canaria. Anim Biodivers Conserv 26:707–716

    Google Scholar 

  • Erdtman G (1943) An introduction to pollen analysis. Waltham, Massachusetts

  • Erdtman G (1952) Pollen morphology and plant taxonomy, angiosperms. Almqvist and Wiksell, Stockholm

    Google Scholar 

  • Erdtman G (1960) The acetolysis method. A revised description. Svensk Bot Tidskr 54:561–564

    Google Scholar 

  • Falchi A, Paolini J, Desjobert JM, Melis A, Costa J, Varesi L (2009) Phylogeography of Cistus creticus L. on Corsica and Sardinia inferred by the trnL-F and rpl32-trnL sequences of cpDNA. Mol Phylogenet Evol 52:538–543

  • Farris JS (1969) A successive approximations approach to character weighting. Syst Zool 18:374–385

    Article  Google Scholar 

  • Fennane M, Ibn Tattou M, Mathez J, Ouyahya A, El Oualidi J (eds) (1999) Flore Pratique du Maroc, vol 1. Trav Inst Sci 36:I–XV

  • García-Talavera F (1999) La Macaronesia. Consideraciones geológicas, biogegráficas y paleoecológicas. In: Fernández-Palacios JM, Bacallado JJ, Belmonte JA (eds) Ecología y cultura en Canarias, 39–64. Museo de la Ciencia, Cabildo Insular de Tenerife, Santa Cruz de Tenerife, Canary Islands, Spain

  • Gaskin JF, Schaal BA (2003) Molecular phylogenetic investigation of US invasive Tamarix. Syst Bot 28:86–95

    Google Scholar 

  • Grant OM, McNeilly T, Incoll LD (2006) Genetic diversity of Cistus albidus in south-east Spain does not relate to mesoclimate. Funct Pl Biol 33:247–255

    Article  Google Scholar 

  • Greuter W, Raus T (2000) Med-Checklist Notulae, 19. Willdenowia 30:232

    Google Scholar 

  • Greuter W, Burdet HM, Long G (1984) Med Checklist. A critical inventory of vascular plants of the circum-Mediterranean countries. Conservatoire et Jardin Botanique de la Ville de Genève, Genève

  • Grosser W (1903) Cistaceae. In: Engler A (éd) Das Pflanzenreieh, Regni vegetabilis conspectus. vol 14, p 161

  • Guzmán B, Vargas P (2005) Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnL-trnF, and matK sequences. Mol Phylogenet Evol 37:644–660

  • Guzmán B, Vargas P (2009) Historical biogeography and character evolution of Cistaceae (Malvales) based on analysis of plastid rbcL and trnL-trnF sequences. Org Divers Evol 9:83–99

    Google Scholar 

  • Guzmán B, Lledó MD, Vargas P (2009) Adaptive radiation in mediterranean Cistus (Cistaceae). PLoS ONE 4(7):e6362. doi:10.1371/journal.pone.0006362

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    PubMed  CAS  Google Scholar 

  • Hesse M, Halbritter H, Zetter R, Weber M, Buchner R, Frosch-Radivo A, Ulrich S (2009) Pollen terminology. An illustrated handbook, VI. Springer, Wien

  • Heydacker F (1963) Les types polliniques de la famille des Cistaceae. Pollen Spores 5:41–50

    Google Scholar 

  • Hoernle K, Tilton G, Schminke HU (1991) Sr–Nd–Pb isotopic evolution of Gran Canaria: evidence for shallow enriched mantle beneath the Canary Islands. Earth Planet Sci Lett 106:44–63

    Article  CAS  Google Scholar 

  • Iversen J, Troels Smith J (1950) Pollenmorfologiske definitioner og typer. Danmarks Geol Unders 3:1–54

    Google Scholar 

  • Janchen E (1925) Cistaceae. In: Engler A, Prantl K (eds) Die Naturlichen Pflanzenfamilien, 2nd edn., Bd. 21:289–313. W Engelmann, Leipzig

  • Jean MT, Pons A (1962) Une clef de détermination palynologique pour les Cistacées de la flore de France. Naturalia MonspFasc 14:87–92

    Google Scholar 

  • Jean MT, Pons A (1963) Contibution à l’étude palynologique des Cistacées de la flore de France. Ann Sci Nat Bot Paris 4:159–204

    Google Scholar 

  • Jiménez-Albarrán MJ (1984) Estudio palinologico del Genero Halimium (Dun.) Spach (Cistaceae). Anal Asoc Pal Lengua Esp 1:21–29

    Google Scholar 

  • Kress WJ, Prince LM, Williams KJ (2002) The phylogeny and a new classification of the gingers (Zingiberaceae): evidence from molecular data. Am J Bot 89:1682–1696

    Article  PubMed  CAS  Google Scholar 

  • Lahaye R, Klackenberg J, Källersjö M, Van Campo E, Civeyrel L (2007) Phylogenetic relationships within Secamonoideae (Apocynaceae s.l.) based on four chloroplast sequences. Ann Mo Bot Gard 94:378–396

    Article  Google Scholar 

  • Márquez J, Diaz-Losada E, Rodríguez-Gracia V, Suàrez-Cervera M (1996) Cistaceae. In: Atlas de Polen de Galicia, pp 113–127, Ourense

  • Marrero-Rodríguez Á, Almeida R, Ríos C (2008) Cistus grancanariae sp. nov. (Cistaceae) una nueva especie para Gran Canaria (Islas Canarias). Bot Macaronésica 27:73–88

    Google Scholar 

  • Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the mediterranean basin. Ann Mo Bot Gard 84:112–127

    Article  Google Scholar 

  • Moreno JC (coord) (2008) Lista Roja 2008 de la flora vascular española. Dirección General de Medio Natural y Política Forestal (Ministerio de Medio Ambiente, y Medio Rural y Marino, y Sociedad Española de Biología de la Conservación de Plantas), Madrid

  • Mort ME, Archibald JK, Randle CP, Levsen ND, O’Leary TR, Topalov K, Wiegand CM, Crawford DJ (2007) Inferring phylogeny at low taxonomic levels: utility of rapidly evolving cpDNA and nuclear ITS loci. Am J Bot 94:173–183

    Article  PubMed  Google Scholar 

  • Nandi OI (1998) Floral development and systematics of Cistaceae. Plant Syst Evol 212:107–134

    Article  Google Scholar 

  • Olson ME (2002) Intergeneric relationships within the Caricaceae-Moringaceae clade (Brassicales) and potential morphological synapomorphies of the clade and its families. Int J Plant Sci 163:51–65

    Article  CAS  Google Scholar 

  • Palacios-Chávez R, Quiroz-García DL, Arreguín-Sánchez MDLL (1999) Morfología de los granos de polen de la familia Cistaceae de México. Acta Botanica Mexicana 49:1–14

    Google Scholar 

  • Paolini J, Falchi A, Quilichini Y, Desjobert JM, Cian MC, Varesi L, Costa J (2009) Morphological, chemical and genetic differentiation of two subspecies of Cistus creticus L. (C. creticus subsp. eriocephalus and C. creticus subsp. corsicus). Phytochemistry 70:1146–1160

    Article  PubMed  CAS  Google Scholar 

  • Punt W, Blackmore S, Nilsson S, Le Thomas A (1994) Glossary of pollen and spore terminology. LPP Foundation (Laboratory of Paleobotany and Palynology), Utrecht

  • Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynology 143:1–81

    Article  Google Scholar 

  • Quandt D, Müller K, Stech M, Hilu KW, Frey W, Frahm JP, Borsch T (2004) Molecular evolution of the chloroplast trnL-F region in land plants. Monogr Syst Bot Mo Bot Gard 98:13–37

    Google Scholar 

  • Raynaud C (1992) Cistaceae. In: Fennane M, Mathez J (eds) Elements pour la Flore pratique du Maroc. Naturalia Monsp, sér. Bot. 56:154–158, 171–220

  • Reille M (1990) Leçons de Palynologie et d’Analyse pollinique. Editions du CNRS, Paris

    Google Scholar 

  • Saenz De Rivas C (1979) Pollen morphology of Spanish Cistaceae. Grana 18:91–98

    Article  Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu WS, Miller J, Siripin KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    Article  PubMed  CAS  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    Google Scholar 

  • Swofford DL (2002) PAUP: phylogenetic analysis using parsimony. Version 4.0b10 for Macintosh. Sinauer Associates, Sunderland

    Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of the chloroplast DNA. Pl Mol Biol 17:1105–1109

    Article  CAS  Google Scholar 

  • Tan K, Iatrou G (2001) Endemic plants of Greece—the Peloponnese (Halimium voldii). Gads Forlag, Copenhagen, pp 215–217

  • Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walters SM, Webb DA (1968) Flora Europaea, vol 2. Rosaceae to Umbelliferae. Cambridge University Press, Cambridge

  • Ukraintseva VV (1991) The palynological study of the genus Cistus (Cistaceae). Bot J (St. Peterburg). 76:969–985

    Google Scholar 

  • Ukraintseva VV (1993) Pollen morphology of the family Cistaceae in relation to its taxonomy. Grana 2:33–36

    Article  Google Scholar 

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Acknowledgments

We are most grateful to curators or keepers of the herbaria G, K, MPU, and P for permitting the examination of specimens and removal of pollen samples. We should like to thank Peter Biggins from CIRAD for revising the English, and also all colleagues of the palynology unit at the R. B. G. Kew for their assistance, the Conservatoire Botanique National de Brest and Robert Page for their help, and Olivier Filippi for cultivating our plants collected on field trips, especially from Morocco and the Canary Islands. We also wish to thank Elise Van Campo, Laurent Chibret, and Renaud Lahaye for their support.

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  1. Laboratoire Ecologie Fonctionnelle et Environnement, Université de Toulouse, UPS, 31062, Toulouse Cedex 9, France

    Laure Civeyrel, Yannick Agnan, Céline Pélissier & Thierry Otto

  2. UMR DAP, CIRAD, TA A-96/03, Avenue Agropolis, 34398, Montpellier Cedex 5, France

    Julie Leclercq

  3. APBF, 15 bis rue de Marignan, 75008, Paris, France

    Jean-Pierre Demoly

  4. ETH Zentrum, IBZ, Universitätstrasse 16, CHN-G35.1, 8092, Zurich, Switzerland

    Nicolas Quèbre

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  1. Laure Civeyrel
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Correspondence to Laure Civeyrel.

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Civeyrel, L., Leclercq, J., Demoly, JP. et al. Molecular systematics, character evolution, and pollen morphology of Cistus and Halimium (Cistaceae). Plant Syst Evol 295, 23–54 (2011). https://doi.org/10.1007/s00606-011-0458-7

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