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Cistus ladanifer (Cistaceae): a natural resource in Mediterranean-type ecosystems

Abstract

Main conclusion

Cistus ladanifer has a well-defined taxonomic identity. 2,2,6-trimethylcyclohexanone may be an authenticity and taxonomic marker. Its traits and applications make it a possible economic resource fitted for Mediterranean areas.

Cistus ladanifer is a dominant shrub species endemic to the western Mediterranean region. Due to its dominant nature and its potential ecological, aromatic or pharmacological applications, C. ladanifer has been the object of numerous studies. In this review current knowledge on different aspects of this species is summarized, from its taxonomy to its chemical characterisation or its competitive traits. There are no doubts about the taxonomic entity of C. ladanifer, although the recognition of infraspecific taxa deserves more attention. Given that the fragrant exudate of C. ladanifer holds a very specific composition, one species specific carotenoid, 2,2,6-trimethylcyclohexanone, derivative is proposed as an authenticity marker for uses of C. ladanifer in pharmacological or aromatic industries. Evidence is also gathered on the extreme adaptation of C. ladanifer to stressful conditions in the Mediterranean region, such as the ability to survive in low hydric and high solar exposition conditions, presistence in poor and contaminated soils, and growth inhibition of several other plants through the release of allelochemicals. Thus, the finding of potential applications for this plant may contribute to enhance the economic dimension of derelict lands, such as mine tailings or poor agricultural Mediterranean areas.

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References

  1. Aerts RJ, Snoeijer W, Meijden E, Verpoorte R (1991) Allelopathic inhibition of seed germination by Cinchona alkaloids? Phytochemistry 30(9):2947–2951. https://doi.org/10.1016/S0031-9422(00)98229-3

  2. Agra-Coelho C, Rosa ML, Moreira I (1980) Efeitos alelopáticos de Cistus ladanifer L. In: III Simpósio nacional de herbologia, pp 165–178

  3. Águeda B, Parladé J, Fernández-Toirán LM, Cisneros Ó, Miguel AM, Modrego MP, Martínez-Peña F, Pera J (2008) Mycorrhizal synthesis between Boletus edulis species complex and rockroses (Cistus sp.). Mycorrhiza 18(8):443–449. https://doi.org/10.1007/s00572-008-0192-3

  4. Alías JC, Sosa T, Escudero JC, Chaves N (2006) Autotoxicity against germination and seedling emergence in Cistus ladanifer L. Plant Soil 282(1–2):327–332. https://doi.org/10.1007/s11104-005-6066-y

  5. Alías JC, Sosa T, Valares C, Escudero JC, Chaves N (2012) Seasonal variation of Cistus ladanifer L. diterpenes. Plants 1(1):6–15. https://doi.org/10.3390/plants1010006

  6. Alvarenga PM, Araújo MF, Silva JAL (2004) Elemental uptake and root-leaves transfer in Cistus Ladanifer L. growing in a contaminated pyrite mining area (Aljustrel–Portugal). Water Air Soil Pollut 152(1–4):81–96. https://doi.org/10.1023/B:WATE.0000015333.24165.5e

  7. Anastasaki T, Demetzos C, Perdetzoglou D, Gazouli M, Loukis A, Harvala C (1999) Analysis of labdane-type diterpenes from Cistus creticus (subsp. creticus and subsp. eriocephalus), by GC and GC-MS. Planta Med 65(8):735–739. https://doi.org/10.1055/s-1999-14095

  8. Antonovics J (1975) Metal tolerance in plants: perfecting an evolutionary paradigm. In: Con PLL (ed) Heavy metals in the environment. University of Toronto, Toronto, pp 169–186

  9. Ascenção L, Pais MSS (1987) Morfologia e ocorréncia de tricomas glandulares em C. ladanifer L. 2as Jornadas nacionais de plantas aromáticas e óleos essenciais, Lisbon, p 197

  10. Ater M, Lefèbvre C, Gruber W, Meerts P (2000) A phytogeochemical survey of the flora of ultramafic and adjacent normal soils in north Morocco. Plant Soil 218(1–2):127–135. https://doi.org/10.1023/A:1014925007960

  11. Barrajón-Catalán E, Fernández-Arroyo S, Saura D, Guillén E, Fernández-Gutiérrez A, Segura-Carretero A, Micol V (2010) Cistaceae aqueous extracts containing ellagitannins show antioxidant and antimicrobial capacity, and cytotoxic activity against human cancer cells. Food Chem Toxicol 48(8–9):2273–2282. https://doi.org/10.1016/j.fct.2010.05.060

  12. Barrajón-Catalán E, Fernández-Arroyo S, Roldán C, Guillén E, Saura D, Segura-Carretero A, Micol V (2011) A systematic study of the polyphenolic composition of aqueous extracts deriving from several Cistus genus species: evolutionary relationship. Phytochem Anal 22(4):303–312. https://doi.org/10.1002/pca.1281

  13. Barrajón-Catalán E, Tomás-Menor L, Morales-Soto A, Martí N, Saura D, Carretero AS, Micol V (2016) Rockroses (Cistus sp.) oils. In: Preedy VE (ed) Essential oils in food preservation, flavor and safety. Elsevier Inc., Amsterdam, pp 649–658

  14. Barrio M, Teixido AL (2015) Sex-dependent selection on flower size in a large-flowered Mediterranean species: an experimental approach with Cistus ladanifer. Plant Syst Evol 301(1):113–124. https://doi.org/10.1007/s00606-014-1058-0

  15. Barros L, Dueñas M, Alves CT, Silva S, Henriques M, Santos-Buelga C, Ferreira ICFR (2013) Antifungal activity and detailed chemical characterization of Cistus ladanifer phenolic extracts. Ind Crop Prod 41:41–45. https://doi.org/10.1016/j.indcrop.2012.03.038

  16. Bastida F, Talavera S (2002) Temporal and spatial patterns of seed dispersal in two Cistus species (Cistaceae). Ann Bot 89(4):427–434 PMID: 12096803

  17. Bolaños MM, López EG (1949) Jarales y jaras (Cistografía hispánica). Ediciones Ares, Madrid

  18. Borges AEL (1987) Aspectos morfológicos dos tricomas do C. ladanifer L. (Cistaceae). 2as. Jornadas nacionais de plantas aromáticas e óleos essenciais, Lisbon, pp 75–80

  19. Borges AEL (1989) Contribuição para o estudo da anatomia da folha e caule de C. ladanifer L. Jornadas ibericas de plantas médicinales aromáticas y de aceites esenciales, Madrid

  20. Carlier J, Leitão JOS, Fonseca F (2008) Population genetic structure of Cistus ladanifer L. (Cistaceae) and genetic differentiation from co-occurring Cistus species. Plant Spec Biol 23(3):141–151. https://doi.org/10.1111/j.1442-1984.2008.00220.x

  21. Carro L, Mulas R, Pastor-Bueis R, Blanco D, Terrón A, González-Andrés F, Peix A, Velázquez E (2017) Delftia rhizosphaerae sp. nov. isolated from the rhizosphere of Cistus ladanifer. Int J Syst Evol Microbiol 67(6):1957–1960. https://doi.org/10.1099/ijsem.0.001892

  22. Chaves N, Escudero JC (1997) Allelopathic effect of Cistus ladanifer on seed germination. Funct Ecol 11(4):432–440. https://doi.org/10.1046/j.1365-2435.1997.00107.x

  23. Chaves N, Rı́os JJ, Gutierrez C, Escudero JC, Olı́as JM (1998) Analysis of secreted flavonoids of Cistus ladanifer L. by high-performance liquid chromatography–particle beam mass spectrometry. J Chromatogr A 799(1–2):111–115. https://doi.org/10.1016/S0021-9673(97)01042-X

  24. Chaves N, Escudero JC, Gutiérrez-Merino C (1993) Seasonal variation of exudate of Cistus ladanifer. J Chem Ecol 19(11):2577–2591 PMID: 24248712

  25. Chaves N, Escudero JC, Gutierrez-Merino C (1997a) Role of ecological variables in the seasonal variation of flavonoid content of Cistus ladanifer exudate. J Chem Ecol 23(3):579–603. https://doi.org/10.1023/B:JOEC.0000006398.79306.09

  26. Chaves N, Escudero JC, Gutiérrez-Merino C (1997b) Quantitative variation of flavonoids among individuals of a Cistus ladanifer population. Biochem Syst Ecol 25(5):429–435. https://doi.org/10.1016/S0305-1978(97)00019-7

  27. Chaves N, Sosa T, Alías JC, Escudero JC (2001) Identification and effects of interaction phytotoxic compounds from exudate of Cistus ladanifer leaves. J Chem Ecol 27(3):611–621. https://doi.org/10.1023/A:1010336921853

  28. Colpaert JV, Wevers JHL, Krznaric E, Adriaensen K (2011) How metal-tolerant ecotypes of ectomycorrhizal fungi protect plants from heavy metal pollution. Ann For Sci 68(1):17–24. https://doi.org/10.1007/s13595-010-0003-9

  29. Comandini O, Contu M, Rinaldi AC (2006) An overview of Cistus ectomycorrhizal fungi. Mycorrhiza 16(6):381–395. https://doi.org/10.1007/s00572-006-0047-8

  30. Delgado JA, Serrano JM, López F, Acosta FJ (2001) Heat shock, mass-dependent germination, and seed yield as related components of fitness in Cistus ladanifer. Environ Exp Bot 46(1):11–20. https://doi.org/10.1016/S0098-8472(01)00076-4

  31. Demetzos C, Dimas KS (2001) Labdane-type diterpenes: chemistry and biological activity. Stud Nat Prod Chem 25:235–292. https://doi.org/10.1016/S1572-5995(01)80009-0

  32. Demetzos C, Angelopoulou D, Perdetzoglou D (2002) A comparative study of the essential oils of Cistus salvifolios in several populations of Crete (Greece). Biochem Syst Ecol 30(7):651–665. https://doi.org/10.1016/S0305-1978(01)00145-4

  33. Demoly JP, Montserrat P (1993) Cistus. In: Castroviejo S (ed) Flora Ibérica. CSIC (Centro Superior Investigaciones Científica), Madrid, pp 319–337

  34. Dentinho MTP, Moreira OC, Pereira MS, Bessa RJB (2007) The use of a tannin crude extract from Cistus ladanifer L. to protect soya-bean protein from degradation in the rumen. Animal 1(5):645–650. https://doi.org/10.1017/S1751731107689745

  35. Dias LS (2001) Describing phytotoxic effects on cumulative germination. J Chem Ecol 27(2):411–418. https://doi.org/10.1023/A:1005644808956

  36. Dias AS, Costa CT, Dias LS (2005) Allelopathic plants. XVII. Cistus ladanifer L. Allelopathy J 16(1):1–15

  37. Díez-Méndez A, Rivas R, Mateos PF, Martínez-Molina E, Santín PJ, Sánchez-Rodríguez JA, Velázquez E (2017) Bacillus terrae sp. nov. isolated from Cistus ladanifer rhizosphere soil. Int J Syst Evol Microbiol 67:1478–1481. https://doi.org/10.1099/ijsem.0.001742

  38. Ellul P, Boscaiu M, Vicente O, Moreno V, Rosselló JA (2002) Intra- and interspecific variation in DNA content in Cistus (Cistaceae). Ann Bot 90(3):345–351. https://doi.org/10.1093/aob/mcf194

  39. Fernández-Arroyo S, Barrajón-Catalán E, Micol V, Segura-Carretero A, Fernández-Gutiérrez A (2010) High-performance liquid chromatography with diode array detection coupled to electrospray time-of-flight and ion-trap tandem mass spectrometry to identify phenolic compounds from a Cistus ladanifer aqueous extract. Phytochem Anal 21(4):307–313. https://doi.org/10.1002/pca.1200

  40. Fernández-Mazuecos M, Vargas P (2010) Ecological rather than geographical isolation dominates quaternary formation of Mediterranean Cistus species. Mol Ecol 19(7):1381–1395. https://doi.org/10.1111/j.1365-294X.2010.04549.x

  41. Fogel R, Trappe JM (1978) Fungus consumption (mycophagy) by small animals. Northwest Sci 52(1):1–31

  42. Friedman J (1995) Allelopathy, autotoxicity, and germination. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp 599–628

  43. Gaston KJ, Fuller RA (2009) The sizes of species geographic ranges. J Appl Ecol 46(1):1–9. https://doi.org/10.1111/j.1365-2664.2008.01596.x

  44. Gomes PB, Mata VG, Rodrigues AE (2005) Characterization of the portuguese-grown Cistus ladanifer essential oil. J Essent Oil Res 17(2):160–165. https://doi.org/10.1080/10412905.2005.9698864

  45. Greche H, Mrabet N, Zrira S, Ismaïli-Alaoui M, Benjilali B, Boukir A (2009) The volatiles of the leaf oil of Cistus ladanifer L. var. albiflorus and labdanum extracts of moroccan origin and their antimicrobial activities. J Essent Oil Res 21(2):166–173. https://doi.org/10.1080/10412905.2009.9700140

  46. Groom N (1997) The new perfume handbook. Blackie Academic and Professional, London

  47. Guimarães R, Barros L, Carvalho AM, Sousa MJ, Morais JS, Ferreira ICFR (2009) Aromatic plants as a source of important phytochemicals: vitamins, sugars and fatty acids in Cistus ladanifer, Cupressus lusitanica and Eucalyptus gunnii leaves. Ind Crop Prod 30(3):427–430. https://doi.org/10.1016/j.indcrop.2009.08.002

  48. Guimarães R, Sousa MJ, Ferreira ICFR (2010) Contribution of essential oils and phenolics to the antioxidant properties of aromatic plants. Ind Crop Prod 32(2):152–156. https://doi.org/10.1016/j.indcrop.2010.04.011

  49. Gulz PG (1984) The composition of terpene hydrocarbons in the essential oils from leaves of four Cistus species. Z Naturforsch 39(7–8):699–704. https://doi.org/10.1515/znc-1984-7-802

  50. Gulz PG, Herrmann T, Hangst K (1996) Leaf trichomes in the genus Cistus. Flora 191(1):85–104. https://doi.org/10.1016/S0367-2530(17)30692-8

  51. Gutterman Y (1994) Strategies of seed dispersal and germination in plants inhabiting deserts. Bot Rev 60:373–425. https://doi.org/10.1007/BF02857924

  52. 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(3):644–660. https://doi.org/10.1016/j.ympev.2005.04.026

  53. Guzmán B, Vargas P (2009) Long-distance colonization of the western Mediterranean by Cistus ladanifer (Cistaceae) despite the absence of special dispersal mechanisms. J Biogeogr 36(5):954–968. https://doi.org/10.1111/j.1365-2699.2008.02040.x

  54. Guzmán B, Vargas P (2010) Unexpected synchronous differentiation in Mediterranean and Canarian Cistus (Cistaceae). Perspect Plant Ecol 12(3):163–174. https://doi.org/10.1016/j.ppees.2009.09.002

  55. Guzmán B, Narbona E, Vargas P (2011) Similar reproductive success of the two petal colour polymorphisms of Cistus ladanifer (Cistaceae). Plant Biosyst 145(4):931–937. https://doi.org/10.1080/11263504.2011.633111

  56. Guzmán B, Narbona E, Vargas P (2015) Investigating reproductive incompatibility barriers in a Mediterranean rockrose (Cistus ladanifer). Plant Biosyst 149(1):1–6. https://doi.org/10.1080/11263504.2013.801369

  57. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(3):1–11. https://doi.org/10.1016/j.ppees.2009.09.002

  58. Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523 PMID: 10199016

  59. Hernández-Rodríguez M, Oria-de-Rueda JA, Martín-Pinto P (2013) Post-fire fungal succession in a Mediterranean ecosystem dominated by Cistus ladanifer L. For Ecol Manag 289:48–57. https://doi.org/10.1016/j.foreco.2012.10.009

  60. Herranz JM, Ferrandis P, Copete MA, Duro EM, Zalacaín A (2006) Effect of allelopathic compounds produced by Cistus ladanifer on germination of 20 Mediterranean taxa. Plant Ecol 184(2):259–272. https://doi.org/10.1007/s11258-005-9071-6

  61. Johnson LA, Soltis DE (1994) matK DNA sequences and phylogenetic reconstruction in Saxifragaceae s. str. Syst Bot 19(1):143–156. https://doi.org/10.2307/2419718

  62. Kigel J (1995) Seed germination in arid and semi-arid regions. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, New York, pp 645–699

  63. Kuuluvainen T (1994) Gap disturbance, ground microtopography, and the regeneration dynamics of boreal coniferous forests in Finland: a review. Ann Zool Fenn 31(1):35–51

  64. Lawrence BM (1999) Progress in essential oils. Perfum Flavor 24(4):31–50

  65. Lázaro JD, Kidd PS, Martínez CM (2006) A phytogeochemical study of the Trás-os-Montes region (NE Portugal): possible species for plant-based soil remediation technologies. Sci Total Environ 354(2–3):265–277. https://doi.org/10.1016/j.scitotenv.2005.01.001

  66. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Annu Rev Ecol Syst 27:237–277. https://doi.org/10.1146/annurev.ecolsys.27.1.237

  67. Macnair MR (1993) The genetics of metal tolerance in vascular plants. N Phytol 124(4):541–559. https://doi.org/10.1111/j.1469-8137.1993.tb03846.x

  68. Malato-Beliz J, Escudero JC, Buyolo T (1992) Application of traditional indices and of diversity to an ecotonal area of different biocoenes. The state of the art in vegetation science. International Association for Vegetation Science, Toledo

  69. Malo JE, Suárez F (1998) The dispersal of a dry-fruited shrub by red deer in a Mediterranean ecosystem. Ecography 21(2):204–211. https://doi.org/10.1111/j.1600-0587.1998.tb00673.x

  70. Manzano P, Malo JE, Peco B (2005) Sheep gut passage and survival of Mediterranean shrub seeds. Seed Sci Res 15(1):21–28. https://doi.org/10.1079/SSR2004192

  71. Mariotti JP, Tomi F, Casanova J, Costa J, Bernardini AF (1997) Composition of the essential oil of Cistus ladaniferus L. cultivated in Corsica (France). Flavour Frag J 12:147–151

  72. Martín-Pinto P, Vaquerizo H, Peñalver F, Olaizola J, Oria-de-Rueda JA (2006) Early effects of a wildfire on the diversity and production of fungal communities in Mediterranean vegetation types dominated by Cistus ladanifer and Pinus pinaster in Spain. Forest Ecol Manag 225(1–3):296–305. https://doi.org/10.1016/j.foreco.2006.01.006

  73. Masa CV, Díaz TS, Gallego JCA, Lobón NC (2016a) Quantitative variation of flavonoids and diterpenes in leaves and stems of Cistus ladanifer L. at different ages. Molecules 21(3):275. https://doi.org/10.3390/molecules21030275

  74. Masa CV, Gallego JCA, Lobón NC, Díaz TS (2016b) Intra-population variation of secondary metabolites in Cistus ladanifer L. Molecules 21(7):1–12. https://doi.org/10.3390/molecules21070945

  75. Mediavilla O, Olaizola J, Santos-del-Blanco L, Oria-de-Rueda JA, Martín-Pinto P (2016) Mycorrhization between Cistus ladanifer L. and Boletus edulis Bull. is enhanced by the mycorrhiza helper bacteria Pseudomonas fluorescens Migula. Mycorrhiza 26(2):161–168. https://doi.org/10.1007/s00572-015-0657-0

  76. Metcalfe DB, Kunin WE (2006) The effects of plant density upon pollination success, reproductive effort and fruit parasitism in Cistus ladanifer L. (Cistaceae). Plant Ecol 185:41. https://doi.org/10.1007/s11258-005-9082-3

  77. Moreno JM, Zuazua E, Pérez B, Luna B, Velasco A, Dios VRd (2011) Rainfall patterns after fire differentially affect the recruitment of three Mediterranean shrubs. Biogeosciences 8:3721–3732. https://doi.org/10.5194/bg-8-3721-2011

  78. Moyler DA, Clery RA (1997) The aromatic resins: their chemistry and uses. In: Swift KAD (ed) Flavours and fragrances. Royal Society of Chemistry, Great Britain, pp 96–115

  79. Muller WH, Muller CH (1956) Association patterns involving desert plants that contain toxic products. Am J Bot 43(5):354–361

  80. Narbona E, Guzmán B, Arroyo J, Vargas P (2010) Why are fruit traits of Cistus ladanifer (Cistaceae) so variable: a multi-level study across the western Mediterranean region. Perspect Plant Ecol 12(4):305–315. https://doi.org/10.1016/j.ppees.2010.06.001

  81. Nunez-Olivera E, Martinez-Abaigar J, Escudero JC (1996) Adaptability of leaves of Cistus ladanifer to widely varying environmental conditions. Funct Ecol 10(5):636–646. https://doi.org/10.2307/2390174

  82. Öğütveren M, Tetik SS (2004) Composition of the essential oil of Cistus laurifolius L. from Turkey. J Essent Oil Res 16(1):24–25. https://doi.org/10.1080/10412905.2004.9698641

  83. Oller-López JL, Rodríguez R, Cuerva JM, Oltra JE, Bazdi B, Dahdouh A, Lamarti A, Mansour AI (2005) Composition of the essential oils of Cistus ladaniferus and C. monspeliensis from Morocco. J Essent Oil Res 17(5):553–555. https://doi.org/10.1080/10412905.2005.9698992

  84. Paolini J, Falchi A, Quilichini Y, Desjobert J-M, Cian M-CD, 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(9):1146–1160. https://doi.org/10.1016/j.phytochem.2009.06.013

  85. Papaefthimiou D, Papanikolaou A, Falara V, Givanoudi S, Kostas S, Kanellis AK (2014) Genus Cistus: a model for exploring labdane-type diterpenes’ biosynthesis and a natural source of high value products with biological, aromatic, and pharmacological properties. Front Chem 2:35. https://doi.org/10.3389/fchem.2014.00035

  86. Pascual JTD, Bellido IS, Basabe P, Marcos IS, Ruano LF, Urones JG (1982) Labdane diterpenoids from Cistus ladaniferus. Phytochemistry 21(4):899–901. https://doi.org/10.1016/0031-9422(82)80089-7

  87. Pérez-Fernández MA, Rodríguez-Echeverría S (2003) Effect of smoke, charred wood, and nitrogenous compounds on seed germination of ten species from woodland in central-western Spain. J Chem Ecol 29:237–251. https://doi.org/10.1023/A:1021997118146

  88. Pérez-García F (1997) Germination of Cistus ladanifer seeds in relation to parent material. Plant Ecol 133(1):57–62. https://doi.org/10.1023/A:1009776910683

  89. Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21(6):539–566. https://doi.org/10.1080/0735-260291044359

  90. Proksch P, Gulz P (1980a) Phenylpropanolic acid esters in the essential oil of Cistus ladanifer L. (Cistaceae). Z Naturforsch 35(3–4):201–203. https://doi.org/10.1515/znc-1980-3-405

  91. Proksch P, Gulz P (1980b) Further oxygenated compounds in the essential oils of Cistus ladanifer L. (Cistaceae). Z Naturforsch 35(7–8):529–532. https://doi.org/10.1515/znc-1980-7-801

  92. Quintana JR, Cruz A, Fernández-González F, Moreno JM (2004) Time of germination and establishment success after fire of three obligate seeders in a Mediterranean shrubland of central Spain. J Biogeogr 31:241–249. https://doi.org/10.1111/j.1365-2699.2004.00955.x

  93. Quintela-Sabarís C (2012) Evolutionary origin and ecophysiology of metallicolous populations of Cistus ladanifer L. PhD Thesis, University of Santiago de Compostela, Spain

  94. Quintela-Sabarís C, Kidd PS, Fraga MI (2005) Identification of metalliferous ecotypes of Cistus ladanifer L. using RAPD markers. Z Naturforsch 60(3–4):229–235. https://doi.org/10.1515/znc-2005-3-408

  95. Quintela-Sabarís C, Vendramin GG, Castro-Fernández D, Isabel Fraga M (2010) Chloroplast microsatellites reveal that metallicolous populations of the Mediterranean shrub Cistus ladanifer L. have multiple origins. Plant Soil 334:161–174. https://doi.org/10.1007/s11104-010-0368-4

  96. Quintela-Sabarís C, Vendramin GG, Castro-Fernández D, Isabel Fraga M (2011) Chloroplast DNA phylogeography of the shrub Cistus ladanifer L. (Cistaceae) in the highly diverse western Mediterranean region. Plant Biol 13(2):391–400. https://doi.org/10.1111/j.1438-8677.2010.00371.x

  97. Quintela-Sabarís C, Ribeiro MM, Poncet B, Costa R, Castro-Fernández D, Fraga MI (2012) AFLP analysis of the pseudometallophyte Cistus ladanifer: comparison with cpSSRs and exploratory genome scan to investigate loci associated to soil variables. Plant Soil 359(1–2):397–413. https://doi.org/10.1007/s11104-012-1221-8

  98. Ramalho PS, Freitas VAP, Macedo A, Silva G, Silva AMS (1999) Volatile components of Cistus ladanifer leaves. Flavour Frag J 14:300–302

  99. Ribeiro S, Delgado F (2016) Cistus ladanifer L. subsp. ladanifer. In: Azevedo L (ed) Cardo. Norprint, Portugal, pp 52–53

  100. Rincón J, Lucas AD, Gracia I (2000) Isolation of rock rose essential oil using supercritical CO2 extraction. Sep Sci Technol 35(16):2745–2763. https://doi.org/10.1081/SS-100102366

  101. Rivas-Martínez S (1979) Brezales y jarales de Europa occidental (Revisión fitosociológica de las clases Calluno-Ulicetea y Cisto-Lavanduletea). Lazaroa 1:5–127

  102. Robles C, Bousquet-Mélou A, Garzino S, Bonin G (2003) Comparition of essential oil composition of two varieties of C. ladanifer. Biochem Syst Ecol 31:339–343. https://doi.org/10.1016/S0305-1978(02)00161-8

  103. Rouy G, Foucaud J (1895) Flore de France ou description des plantes qui croissent spontanément en France, en Corse et en Alsace-Lorraine. Imprimerie Deslis Frères, Tours. 2:254–279

  104. Sangswan NS, Farooqui AHA, Shabih F, Sangswan R (2011) Regulation of essential oil production in plants. Plant Growth Regul 34(1):3–21. https://doi.org/10.1023/A:1013386921596

  105. Santos ES, Abreu MM, Magalhães MCF (2016) Cistus ladanifer phytostabilizing soils contaminated with non-essential chemical elements. Ecol Eng 94:107–116. https://doi.org/10.1016/j.ecoleng.2016.05.072

  106. Santos ES, Balseiro-Romero M, Abreu MM, Macías F (2017) Bioextracts of Cistus ladanifer L. growing in São Domingos mine as source of valuable compounds. J Geochem Explor 174:84–90. https://doi.org/10.1016/j.gexplo.2016.07.004

  107. Sebastiani F, Carnevale S, Vendramin GG (2004) A new set of mono- and dinucleotide chloroplast microsatellites in Fagaceae. Mol Ecol Notes 4(2):259–261. https://doi.org/10.1111/j.1471-8286.2004.00635.x

  108. Solano B, Iglesia MTP, Probanza A, García JAL, Megías M, Mañero FJG (2007) Screening for PGPR to improve growth of Cistus ladanifer seedlings for reforestation of degraded mediterranean ecosystems. In: Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Springer, Dordrecht, pp 59–68

  109. Sosa T, Chaves N, Alias JC, Escudero JC, Henao F, Gutiérrez-Merino C (2004) Inhibition of mouth skeletal muscle relaxation by flavonoids of Cistus ladanifer L.: a plant defense mechanism against herbivores. J Chem Ecol 30(6):1087–1101. https://doi.org/10.1023/B:JOEC.0000030265.45127.08

  110. Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor Appl Genet 89(1):26–32. https://doi.org/10.1007/BF00226978

  111. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17(5):1105–1109. https://doi.org/10.1007/BF00037152

  112. Talavera S, Gibbs PE, Herrera J (1993) Reproductive biology of Cistus ladanifer (Cistaceae). Plant Syst Evol 186(3–4):123–134. https://doi.org/10.1007/BF00940792

  113. Teixeira S, Mendes A, Alves A, Santos L (2007) Simultaneous distillation–extraction of high-value volatile compounds from Cistus ladanifer L. Anal Chim Acta 584(2):439–446. https://doi.org/10.1016/j.aca.2006.11.054

  114. Thanos CA, Georghiou K, Pantazi C (1992) Cistaceae: a plant family with hard seeds. Israel J Bot 41:251–263. https://doi.org/10.1080/0021213X.1992.10677232

  115. Trabaud L, Oustric J (1989) Heat requirements for seed germination of three Cistus species in the Garrigue of southern France. Flora 183(3–4):321–325. https://doi.org/10.1016/S0367-2530(17)31557-8

  116. Valbuena L, Tarrega R, Luis E (1992) Influence of heat on seed germination of Cistus laurifolius and Cistus ladanifer. Int J Wildland Fire 2(1):15–20. https://doi.org/10.1071/WF9920015

  117. Verdeguer M, Blázquez MA, Boira H (2012) Chemical composition and herbicidal activity of the essential oil from a Cistus ladanifer L. population from Spain. Nat Prod Res 26(17):1602–1609. https://doi.org/10.1080/14786419.2011.592835

  118. Vieira M, Bessa LJ, Martins MR, Arantes S, Teixeira APS, Mendes Â, Costa PM, Belo ADF (2017) Chemical composition, antibacterial, antibiofilm and synergistic properties of essential oils from Eucalyptus globulus Labill. and seven mediterranean aromatic plants. Chem Biodivers. https://doi.org/10.1002/cbdv.201700006

  119. Vogt T, Proksch P, Gülz P-G (1987) Epicuticular flavonoid aglycones in the genus Cistus, Cistaceae. J Plant Physiol 131(1–2):25–36. https://doi.org/10.1016/S0176-1617(87)80264-X

  120. Vos P, Hogers R, Bleeker M, Reijans M, Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23(21):4407–4414. https://doi.org/10.1093/nar/23.21.4407

  121. Weising K, Gardner RC (1999) A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42(1):9–19. https://doi.org/10.1139/g98-104

  122. Weyerstahl P, Marschall H, Weirauch M, Thefeld K, Surburg H (1998) Constituents of commercial labdanum oil. Flavour Frag J 13(5):295–318. https://doi.org/10.1002/(SICI)1099-1026(1998090)13:5<295:AID-FFJ751>3.0.CO;2-I

  123. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Geldfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

  124. Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acid Res 18(22):6531–6535. https://doi.org/10.1093/nar/18.22.6531

  125. Wollenweber E, Mann K (1984) Flavonoid aglycones in the leaf resin of some Cistus species. Z Naturforsch C 39(3–4):303–306. https://doi.org/10.1515/znc-1984-3-418

  126. Zidane H, Elmiz M, Aouinti F, Tahani A, Wathelet J, Sindic M, Elbachiri A (2013) Chemical composition and antioxidant activity of essential oil, various organic extracts of Cistus ladanifer and Cistus libanotis growing in eastern Morocco. Afr J Biotechnol 12(34):5314–5320. https://doi.org/10.5897/AJB2013.12868

  127. Zietkiewicz E, Rafalski A, Labuda D (1994) Genome fingerprinting by simple sequence repeat (SSR)-anchored polymerase chain reaction amplification. Genomics 20(2):176–183. https://doi.org/10.1006/geno.1994.1151

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Correspondence to Fernanda Delgado.

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Frazão, D.F., Raimundo, J.R., Domingues, J.L. et al. Cistus ladanifer (Cistaceae): a natural resource in Mediterranean-type ecosystems. Planta 247, 289–300 (2018). https://doi.org/10.1007/s00425-017-2825-2

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Keywords

  • Rockrose
  • Labdanum
  • 2,2,6-Trimethylcyclohexanone
  • Taxonomy
  • Competitive traits