Planta (2018) 247:289–300 https://doi.org/10.1007/s00425-017-2825-2 REVIEW Cistus ladanifer (Cistaceae): a natural resource in Mediterranean‑type ecosystems David F. Frazão1 · Joana R. Raimundo1 · Joana L. Domingues1 · Celestino Quintela‑Sabarís2 · José C. Gonçalves1,3,4 · Fernanda Delgado1,3,4 Received: 26 July 2017 / Accepted: 27 November 2017 / Published online: 7 December 2017 © Springer-Verlag GmbH Germany, part of Springer Nature 2017 Abstract Main conclusion Cistus ladanifer has a well-defned taxonomic identity. 2,2,6-trimethylcyclohexanone may be an authenticity and taxonomic marker. Its traits and applications make it a possible economic resource ftted for Medi- terranean 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 diferent aspects of this species is summarized, from its taxonomy to its chemical charac- terisation or its competitive traits. There are no doubts about the taxonomic entity of C. ladanifer, although the recognition of infraspecifc taxa deserves more attention. Given that the fragrant exudate of C. ladanifer holds a very specifc composition, one species specifc 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 fnding 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. Keywords Rockrose · Labdanum · 2,2,6-Trimethylcyclohexanone · Taxonomy · Competitive traits Introduction Cistus ladanifer L. (Cistaceae), also known as rockrose, and called “esteva” (Portuguese) or “jara” (Spanish), is a res- * Fernanda Delgado inous and fragrant evergreen shrub, very abundant among [email protected] other wild species in the forest and uncultivated areas of the western Mediterranean region (Portugal, Spain, south of 1 CBPBI, Centro de Biotecnologia de Plantas da Beira France, north of Morocco). This plant is frequently associ- Interior, Quinta da Senhora de Mércules, Apartado 119, 6001‑909 Castelo Branco, Portugal ated to negative impacts, such as agroecosystems occupation and competition, as well as fre promotion. Knowledge about 2 Laboratoire Sols et Environnement (UMR 1120, INRA-Univ. Lorraine), ENSAIA, the shrub’s survival mechanisms may constitute a way either 2 Av. de la Forêt de Haye, TSA 40602 54518 V​and​oeu​vre​‑lè​ to fght and control it or to exploit it. Cistaceae plants have s‑N​ancy, France gained high biological interest, both at the level of rapid 3 IPCB-ESA, Escola Superior Agrária, Instituto Politécnico de colonization of burnt and poor agricultural areas, as well as Castelo Branco, Quinta da Senhora de Mércules, Apartado revegetation of metal-polluted sites, and at the level of phy- 119, 6001‑909 Castelo Branco, Portugal totoxic and symbiotic interactions with the ecosystem, which 4 CERNAS/IPCB, Centro de Estudos de Recursos Naturais, consequently highlights its relevant aromatic and pharmaco- Ambiente e Sociedade/Instituto Politécnico de Castelo logical potential applications (Dias et al. 2005; Martín-Pinto Branco, Castelo Branco, Portugal Vol.:(0123456789)1 3 290 Planta (2018) 247:289–300 et al. 2006; Papaefthimiou et al. 2014; Santos et al. 2016). along three subgenera (Fig. 1). However, frequent hybridi- This shrub produces a resin, called labdanum, rich in valu- sations have been registered in the genus (Demoly and able compounds, which have been extracted in countries Montserrat 1993). Within C. ladanifer three subspecies are such as France, Spain and Portugal, mainly to be used in the recognized (Fig. 1). perfume industry due to its fxative and aromatic properties Morphological diferences of Cistus genus have been (Moyler and Clery 1997). In Spain, C. ladanifer labdanum clarifed by the application of DNA sequencing and molecu- has been exported to some Arabic countries, where it is used lar markers, allowing a more complete taxonomic classifca- as incense (Papaefthimiou et al. 2014). Moreover, some tion. In these studies, many authors used universal primers labdanum compounds constitute an important alternative to for non-coded regions of the chloroplast DNA since these ambergris, which is a rare ingredient obtained from a pro- are structurally stable, haploid and heritability is maternal tected animal source (sperm whale), and provides starting (Fernández-Mazuecos and Vargas 2010; Guzmán and Var- materials for the manufacturing of synthetic ambers (Groom gas 2005, 2010; Hamilton 1999; Johnson and Soltis 1994; 1997). Essential oils are valuable products obtained from Taberlet et al. 1991). Sequencing of the Internal Transcribed plants. Although in rockrose it has a low yield extraction Spacer region (Sun et al. 1994; White et al. 1990) from the of around 0.1%, essential oil has a potential use in medi- nuclear genome has also been used at the level of Cistus cal, cosmetic (Papaefthimiou et al. 2014) and food industry genus, but showed to be less useful for species identifca- (Barrajón-Catalán et al. 2016). tion than plastid sequences. Apart from sequence analyses, Most of the current labdanum exploitation is based on nuclear markers such as RAPDs (Williams et al. 1990), wild C. ladanifer populations, although possibilities are AFLPs (Vos et al. 1995) and ISSRs (Zietkiewicz et al. 1994) emerging of cultivation this species on derelict land, such and sets of primers for plastid microsatellites (Sebastiani as low-productive agricultural felds or mine tailings (San- et al. 2004; Weising and Gardner 1999) have been applied tos et al. 2017). However, in order to develop C. ladanifer to the study of phylogeography and population genetics in cultivation, knowledge on the ecology of the species, its C. ladanifer (Quintela-Sabarís et al. 2005, 2011, 2012) or reproductive biology, or inherent variability in secondary in C. ladanifer. ssp. sulcatus, Halimium halimifolium and compounds is needed. several other Cistus species from south of Portugal (Carlier To fulfl this task, this study compiled and reviewed the et al. 2008). existing scientifc literature on C. ladanifer, focusing on its taxonomy, phylogeny, and phylogeography, its morphology and distribution, its reproductive biology and its chemical characterisation. The natural advantages of this species are also evidenced as competitive traits versus others species and/or as environmental responses. Taxonomy, phylogeny and phylogeography Cistaceae family comprises eight genera, five of which (Cistus, Fumana, Halimium, Helianthemum and Xolantha) are present in the Mediterranean area, and about 180 spe- cies. After several taxonomic re-evaluations, about twenty one species of Cistus are now recognized, spreading within white and pink-flowered lineages (Guzmán and Vargas 2005). These taxonomic changes have been mainly based on morphological characters. However, the type of pollen, specifc genetic characteristics and chemical characteriza- tion of plants belonging to the genus Cistus have also been taken into account for taxonomy and phylogenetic divisions (Barrajón-Catalán et al. 2011). Ellul et al. (2002) reported signifcant diferences in DNA content between pink-fow- ered species (subgenus Cistus) and white-fowered ones Fig. 1 Cistus (subgenera Leucocistus and Halimioides). Phylogenetic tree of species in Flora Iberica, where A— subgenus Cistus, B—subgenus Leucocistus, C—subgenus Halimi- Currently, twelve Cistus species are recognised in the oides (adapted from Guzmán and Vargas 2005). Cistus ladanifer and Flora Iberica (Demoly and Montserrat 1993) distributed its subspecies are marked in bold type 1 3 Planta (2018) 247:289–300 291 The taxonomic identity of C. ladanifer has been con- sulcatus (Carlier et al. 2008). However, more recent analy- frmed by Guzmán and Vargas (2005) on the basis of nuclear ses using cpSSRs and AFLPs (Quintela-Sabarís et al. 2011, and plastid genetic sequence data. A later study done by 2012) showed no diferentiation between subspecies ladani- Guzmán and Vargas (2009), using also nuclear and plastid fer and sulcatus, and also indicated that Betic populations DNA sequences, dated the origin of C. ladanifer and the of C. ladanifer (identifed as subspecies ladanifer on the divergence of its diferent subspecies in the Upper Pleisto- basis of leaf morphology) formed an unusual cluster both cene, well after the onset of the Mediterranean climate and at the chloroplast and nuclear level. Therefore, contrasting the fooding of the Strait of Gibraltar. Therefore, the current results between diferent studies, as well as the incongru- species range in northern Africa and southwest Europe is the ence between morphology and genetic data pointed out the result of recent natural long distance dispersal events across need for a taxonomic revision at the intraspecifc level in that sea barrier (Guzmán and Vargas 2009). These data were these species. further confrmed by Quintela-Sabarís et al. (2011) who, using chloroplast microsatellites (cpSSRs),