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The endangered Saharan cypress (Cupressus dupreziana): do not let it get into Charon’s boat

Abstract

Main conclusion

The current state-of-the-art creates a sound basis for the preservation of unique species Cupressus dupreziana provided that targeted effort and care is devoted to the accomplishment of multiplication protocols.

Abstract

This review is to summarize known data on Cupressus dupreziana-specific characteristics, including abiotic stress resistance, and natural reproduction, and estimates the possibilities of ex situ conservation with an emphasis on the cultivation in vitro of this endangered species. As there is only limited information about the cultivation of C. dupreziana in vitro, we have included relevant data on the related species Cupressus sempervirens, where micropropagation techniques are well established, along with other information on species with similar fates and life strategies—Saharan olive Olea europaea subsp. laperrinei and myrtle Myrthus nivellei. The aim of this work is to enhance general understanding and to promote an interest in this relict plant species to contribute to more wide-ranging studies and to increase its chance of preservation. Besides others, reducing the number of species threatened with extinction is an essential and immediate task as high genetic variability of ecosystems is crucial for their stability under changing climatic conditions.

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source of primary explants for cultivation in vitro). Bar represents 10 cm

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References

  1. Abdoun F, Beddiaf M (2002) Cupressus dupreziana A. Camus: distribution, decline and regeneration on the Tassili n'Aijer. Central Sahara C R Biol 325:617–627

  2. Abdoun F, Gardner M (2013) Cupressus dupreziana var. dupreziana. In: The IUCN red list of threatened species 2013: e.T44046A2991873. https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T44046A2991873.en. Accessed 10 Aug 2019

  3. Abdoun F, Jull AJT, Guibal F, Thinon M (2005) Radial growth of the Sahara’s oldest trees: Cupressus dupreziana A. Camus Trees-Struct Funct 19:661–670. https://doi.org/10.1007/s00468-005-0430-7

  4. Alifriqui M, M’Hirit O, Peltier JP, Tessier L (1996) Analyse comparée de la croissance radiale du pin d’Alep et du Cyprès de l’Atlas dans le Haut Atlas Occidental Marocain. Dendrochronologia 14:71–87

  5. Anthelme F, Mato MW, Maley J (2008) Elevation and local refuges ensure persistence of mountain specific vegetation in the Nigerien Sahara. J Arid Environ 72:2232–2242. https://doi.org/10.1016/j.jaridenv.2008.07.003

  6. Baali-Cherif D, Besnard G (2005) High genetic diversity and clonal growth in relict populations of Olea europaea subsp laperrinei (Oleaceae) from Hoggar, Algeria. Ann Bot 96:823–830. https://doi.org/10.1093/aob/mci232

  7. Baali-Cherif D, Bouguedoura N, Besnard G, Bouhired L (2007) Etudes des populations d’olivier de Laperrine (Olea europaea subsp. laperrinei Batt. and Trab.) du Sahara central algérien (Hoggar et Tassili): aspects biologiques et caractérisation moléculaire. Ann Inst Natl Agron El-Harrach 28:35–73

  8. Barberini S, Danti R, Lambardi M (2016) Somatic plant regeneration from selected common cypress (Cupressus sempervirens L.) clones resistant to the bark canker disease. Plant Cell Tiss Organ Cult 124:393–403. https://doi.org/10.1007/s11240-015-0902-4

  9. Benamar D, Bouguedoura N (2000) Essai de germination del’Olivier Laperrine (Olea laperrinei) Batt. et Trab. La foret Algerienne 5:15–18

  10. Benhouhou SS, Boucheneb N, Kerzabi Q, Sassi O (2003) Plant communities of several wadi types in the Tassili N'Ajjer, Central Sahara, Algeria. Phytocoenologia 33:49–69. https://doi.org/10.1127/0340-269X/2003/0033-0049

  11. Benmazari N (2008) Recherche des conditions adéquates pour la micropropagation du cyprès du Tassili Cupressus dupreziana A. In: CAMUS et étude préliminaire des mycorhizes. Université Mouloud Mammeri, Algeria https://dl.ummto.dz/handle/ummto/112. Accessed 7 Apr 2019

  12. Bertazza G, Baraldi R, Predieri S (1995) Light effects on in vitro rooting of pear cultivars of different rhizogenic ability. Plant Cell Tiss Organ Cult 41:139–143. https://doi.org/10.1007/BF00051582

  13. Besnard G, Baali-Cherif D (2009) Coexistence of diploids and triploids in a Saharan relict olive: evidence from nuclear microsatellite and flow cytometry analyses. C R Biol 332:1115–1120. https://doi.org/10.1016/j.crvi.2009.09.014

  14. Besnard G, Anthelme F, Baali-Cherif D (2012) The Laperrine’s olive tree (Oleaceae): a wild genetic resource of the cultivated olive and a model-species for studying the biogeography of the Saharan Mountains. Acta Bot Gallica 159:319–328. https://doi.org/10.1080/12538078.2012.724281

  15. Borchert R (1967) The cultivation of tissues of Cupressus lusitanica in vitro. Physiol Plant 20:608–616

  16. Capuana M, Giannini R (1997) Micropropagation of young and adult plants of cypress (Cupressus sempervirens L.). J Hortic Sci 72:453–460. https://doi.org/10.1080/14620316.1997.11515533

  17. Cremaschi M, Pelfini M, Santilli M (2006) Cupressus dupreziana: a dendroclimatic record for the middle-late Holocene in the central Sahara. Holocene 16:293–303. https://doi.org/10.1191/0959683606hl926rr

  18. Dalichaouch N (1997) Vegetative multiplication of Cupressus dupreziana A. In: Camus by softwood cutting, grafting and attempts of in vitro propagation on the Tassili n' Ajjers, Algeria. Mediterranean Agronomic Institute of Chania

  19. Danti R, Della Rocca G, Panconesi A (2013a) Cypress canker. In: Nicolotti G, Gonthier P (eds) Infectious forest disease. CABI Press, Wallingford, pp 359–375

  20. Danti R, Di Lonardo V, Pecchioli A, Della Rocca G (2013b) ‘Le Crete 1’ and ‘Le Crete 2’: two newly patented Seiridium cardinale cankerresistant cultivars of Cupressus sempervirens. Forest Pathol 43:204–210. https://doi.org/10.1111/efp.12016

  21. de Witte LC, Stöcklin J (2010) Longevity of clonal plants: why it matters and how to measure it. Ann Bot 106:859–870. https://doi.org/10.1093/aob/mcq191

  22. Di Paola LM, Fossi D, Tognoni F, Nuti Ronchi V (1987) Adventitous bud induction in vitro from juvenile leaves of Cupressus arizonica Green. Plant Cell Tiss Organ Cult 10:3–10. https://doi.org/10.1007/BF00037491

  23. El Maâtaoui M, Pichot C (2001) Microsporogenesis in the endangered species Cupressus dupreziana A. Camus: evidence for meiotic defects yielding unreduced and abortive pollen. Planta 213:543–549

  24. Farjon A (2017) A handbook of the world’s conifers, 2nd edn. Brill, Leiden, Boston

  25. Frankham R, Ralls K (1998) Inbreeding leads to extinction. Nature 392:441–442

  26. García D, Zamora R (2003) Persistence, multiple demographic strategies and conservation in long-lived Mediterranean plants. J Veg Sci 14:921–926. https://doi.org/10.1111/j.1654-1103.2003.tb02227.x

  27. Gardner M, Griffiths A (2013) Cupressus dupreziana var. atlantica (errata version published in 2016). In: The IUCN Red List of Threatened Species 2013: e.T44045A102618349. https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T44045A2991752.en. Accessed 10 Aug 2019

  28. Giovanelli A, De Carlo A (2007) Micropropagation of mediterranean cypress (Cupressus sempervirens L.). In: Mohan Jain S, Haggman H (eds) Protocols for micropropagation of woody trees and fruits. Springer, The Netherlands, pp 93–105

  29. Goffner D, Sinare H, Gordon LJ (2019) The Great Green Wall for the Sahara and the Sahel Initiative as an opportunity to enhance resilience in Sahelian landscapes and livelihoods. Reg Environ Change 19:1417–1428. https://doi.org/10.1007/s10113-019-01481-z

  30. Gösslová M, Svobodová H, Lipavská H, Albrechtová J, Vreugdenhil D (2001) Comparing carbohydrate status during Norway spruce seed development and somatic embryo maturation. Vitro Cell Dev Biol Plant 37:24–28. https://doi.org/10.1007/s11627-001-0005-2

  31. Griffiths AJK (1998) Taxonomic and conservation status of Cupressus atlantica. In: Dissertation, University of Reading

  32. Gross K, Cardinale BJ, Fox JW, Gonzalez A, Loreau M, Polley HW, Reich PB, Ruijven A (2014) Species richness and the tem-poral stability of biomass production: a new analysis of recent biodiversity experiments. Am Nat 183:1–12. https://doi.org/10.1086/673915

  33. Gupta PK, Durzan DJ (1985) Shoot multiplication from mature trees of Douglas-fir (Pseudotsuga menziesii) and sugar pine (Pinus tambertiana). Plant Cell Rep 4:177–179

  34. Haddad B, Carra A, Saadi A, Haddad N, Mercati F, Gristina AS, Boukhalfa S, Djillali A, Carimi F (2018) In vitro propagation of the relict laperinne’s olive (Olea europaea L. subsp. Laperrinei). Plant Biosys 152:621–630. https://doi.org/10.1080/11263504.2017.1306002

  35. Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route or route to extinction? Oikos 108:427–432. https://doi.org/10.1111/j.0030-1299.2005.13569.x

  36. Hřib J, Dobrý J (1984) An explant culture of Tassilian cypress Cupressus dupreziana (A. Camus). Forest Ecol Manag 8:235–242

  37. Hudec L, Konrádová H, Hašková A, Lipavská H (2016) Norway spruce embryogenesis: changes in carbohydrate profile, structural development and response to polyethylene glycol. Tree Physiol 36:548–561. https://doi.org/10.1093/treephys/tpw016

  38. Iacona C, Muleo R (2010) Light quality affects in vitro adventitious rooting and ex vitro performance of cherry rootstock Colt. Sci Hortic 125:630–636. https://doi.org/10.1016/j.scienta.2010.05.018

  39. Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. https://doi.org/10.1038/nature10282

  40. Kamthan A, Chaudhuri A, Kamthan M, Datta A (2016) Genetically modified (GM) crops: milestones and new advances in crop improvement. Theor Appl Genet 129:1639–1655. https://doi.org/10.1007/s00122-016-2747-6

  41. Khamushi M, Dehestani-Ardakani M, Zarei A, Kamali Aliabad K (2019) An efficient protocol for micropropagation of old cypress of Abarkuh (Cupressus sempervirens var. horizontalis [Mill.]) under in vitro condition. Plant Cell Tiss Organ Cult 138:597–601. https://doi.org/10.1007/s11240-019-01645-z

  42. Kohler F, Holland TG, Kotiaho JS, Desrousseaux M, Potts MD (2014) Embracing diverse worldviews to share planet Earth. Conservation Biol 33:1014–1022. https://doi.org/10.1111/cobi.13304

  43. Lambardi M (2000) Somatic embryogenesis in cypress (Cupressus sempervirens L.). In: Mohan Jain S, Gupta P, Newton R (eds) Somatic embryogenesis in woody plants, vol 6. Kluver Academic Publishers, Boston, pp 553–567

  44. Lambardi M, Harry IS, Menabeni D, Thorpe TA (1995) Organogenesis and somatic embryogenesis in Cupressus sempervirens. Plant Cell Tiss Org 40:179–182. https://doi.org/10.1007/BF00037672

  45. Lambardi M, Ozudogru EA, Barberini S, Danti R (2018) Strategies for fast multiplication and conservation of forest trees by somatic embryogenesis and cryopreservation: a case study with cypress (Cupressus sempervirens L.). Not Bot Horti Agrob 46:32–38. https://doi.org/10.15835/nbha46111011

  46. Lipavská H, Svobodová H, Albrechtová J (2000) Annual dynamics of the content of non-structural saccharides in the context of structural development of vegetative buds of Norway spruce. J Plant Physiol 157:365–373. https://doi.org/10.1016/S0176-1617(00)80021-8

  47. Little DP (2006) Evolution and circumscription of the true cypresses (Cupressaceae: Cupressus). Syst Bot 31:461–480. https://doi.org/10.1043/05-33.1

  48. Maruyama TE, Hosoi Y (2012) Post-maturation treatment improves and synchronizes somatic embryo germination of three species of Japanese pines. Plant Cell Tissue Organ Cult 110:45–52. https://doi.org/10.1007/s11240-012-0128-7

  49. May MR, Provance MC, Sanders AC, Ellstrand NC, Ross-Ibarra J (2009) A Pleistocene clone of Palmer’s Oak persisting in Southern California. PLoS One 4:e8346. https://doi.org/10.1371/journal.pone.0008346

  50. Médial F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 36:1333–1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x

  51. Meilhac J, Durand J-L, Beguier V, Litrico I (2019) Increasing the benefits of species diversity in multispecies temporary grasslands by increasing within-species diversity. Ann Bot 123:891–900. https://doi.org/10.1093/aob/mcy227

  52. Mercuri A, Trevisan Grandi G (2001) Palynological analyses of the late Pleistocene, Early and Middle Holocene layers. In: Garcea E (ed) Uan Tabu in the settlement history of the Lybian Sahara. Arid zone archeology 2. All'Insegna del Giglio, Sesto Fiorentino, Italy, pp 161–188

  53. Migliore J, Baumel A, Juin M, Fady B, Roig A, Duong N, Médail F (2013) Surviving in mountain climate Refugia: new insights from the genetic diversity and structure of the relict shrub Myrtus nivellei (Myrtaceae) in the Sahara desert. PLoS One 8:e73795. https://doi.org/10.1371/journal.pone.0073795

  54. Mullins VV (1987) Micropropagation of chestnut (Castanea sativa Mill.). Acta Hortic 212:525–530

  55. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–479

  56. Nava JLR, Buonamici A, Vendramin GG, Pichot C (2010) Molecular evidence for the natural production of homozygous Cupressus sempervirens L. lines by Cupressus dupreziana seed trees. Heredity 104:185–190. https://doi.org/10.1038/hdy.2009.112

  57. Nicholson R, Bibiana G, McDaniel B, MacRay C (1999) Observations on the propagation of Cupressus dupreziana, an endemic conifer of the Sahara Desert. Botanic Garden Conserv News 3:49–50 https://www.bgci.org/resources/article/0150/. Accessed 7 Apr 2019

  58. Pichot C, Borrut A, El Maâtaoui M (1998) Unexpected DNA content in the endosperm of Cupressus dupreziana A. Camus seeds and its implications in the reproductive process. Sex Plant Reprod 11:148–152. https://doi.org/10.1007/s004970050132

  59. Pichot C, Fady B, Hochu I (2000) Lack of mother tree alleles in zymograms of Cupressus dupreziana A. Camus embryos Ann For Sci 57:17–22. https://doi.org/10.1051/forest:2000108

  60. Pichot C, El Maâtaoui M, Raddi S, Raddi P (2001) Surrogate mother for endangered Cupressus. Nature 412:39. https://doi.org/10.1038/35083687

  61. Pichot C, Liens B, Rivera Nava JL, Bachelier JB, El Maâtaoui M (2008) Cypress surrogate mother produces haploid progeny from alien pollen. Genetics 178:379–383. https://doi.org/10.1534/genetics.107.080572

  62. Prieto I, Violle C, Barre P, Durand JL, Ghesquiere M, Litrico I (2015) Complementary effects of species and genetic diversity on productivity and stability of sown grasslands. Nature Plants 1:15033. https://doi.org/10.1038/nplants.2015.33

  63. Primack RB (2003) Genetic piracy: a newly discovered marvel of the plant world. Arnoldia, pp 62–2. https://arnoldia.arboretum.harvard.edu/pdf/articles/2003-62-2-genetic-piracy-a-newly-discovered-marvel-of-the-plant-world.pdf. Accessed 7 Jul 2019

  64. Quézel P (1997) High mountains of the Central Sahara: dispersal, speciation, origin and conservation of the flora. In: Barakat HN, Hegazy AK (eds) Reviews in ecology: desert conservation and development, Metropole, Cairo, Egypt, pp 159–175

  65. Quoirin M, Lepoivre P (1977) Études de milieux adaptes aux cultures in vitro de Prunus. Acta Hortic 78:437–442

  66. Raddi P, Panconesi A (1981) Cypress canker disease in Italy—biology, control possibilities and genetic improvement for resistance. Eur J Forest Pathol 11:340–347

  67. Ramdani M, Lograda T, Chalard P, Figueredo G, Chalchat JC, Zeraib A (2012) Essential oil variability in natural Hahadjerine population of Cupressus dupreziana in Tassili N'Ajjer (Algeria). J Forest Res Open Access 1:101. https://doi.org/10.4172/2168-9776.1000101

  68. Razmogolov VP (1973) Tissue culture from the generative cell of the pollen grain of Cupressus spp. Bull Torrey Bot Club 100:18–22

  69. Rejšková A, Patková L, Stodůlková E, Lipavská H (2007) The effect of abiotic stresses on carbohydrate status of olive shoots (Olea europaea L.) under in vitro conditions. J Plant Physiol 164:174–184. https://doi.org/10.1016/j.jplph.2005.09.011

  70. Risser PG, White PR (1964) Nutritional requirements of spruce tumor cells in vitro. Physiol Plant 17:620–635

  71. Ruedell CM, de Almeida MR, Schwambach J, Posenato C, Fett-Neto AG (2013) Pre and post-severance effects of light quality on carbohydrate dynamics and microcutting adventitious rooting of two Eucalyptus species of contrasting recalcitrance. Plant Growth Regul 69:235–245. https://doi.org/10.1007/s10725-012-9766-3

  72. Rushforth K, Adams RP, Zhong M, Ma XQ, Pandley RN (2003) Variation among Cupressus species from the eastern hemisphere based on random amplified polymorphic dans (RAPDs). Biochem Syst Ecol 31:17–24. https://doi.org/10.1016/S0305-1978(02)00073-X

  73. Sallandrouze A, Faurobert M, El-Maataoui M, Espagnac H (1999) Two-dimensional electrophoretic analysis of proteins associated with somatic embryogenesis development in Cupressus sempervirens L. Electrophoresis 20:1109–1119

  74. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Botany 50:199–204

  75. Schwander T, Oldroyd BP (2016) Androgenesis: where males hijack eggs to clone themselves. Phil Trans R Soc B 371:20150534. https://doi.org/10.1098/rstb.2015.0534

  76. Sękiewicz K, Sękiewicz M, Romo A, Didukh Y, Fennane M, Boratyński A (2014) Chorological and conservation status of the endemic cypress, Cupressus atlantica Gaussen, in the High Atlas (Morocco). Dendrobiology 71:3–13. https://doi.org/10.12657/denbio.071.001

  77. Sękiewicz K, Dering M, Romo A, Dagher-Kharrat MB, Boratyńska K, Ok T, Boratyński A (2018) Phylogenetic and biogeographic insights into long-lived Mediterranean Cupressus taxa with a schizo-endemic distribution and Tertiary origin. Bot J Linn Soc 188:190–212. https://doi.org/10.1093/botlinnean/boy049

  78. Singh H (1978) Embryology of gymnosperms. Gebrüder Bomtraeger, Berlin

  79. Spanos KA, Pirrie A, Woodward S (1997) Micropropagation of Cupressus sempervirens L. and Chamaecyparis lawsoniana (A. MURR.) PAR. Silvae Genet 46:291–295

  80. Stewart P (1969) Cupressus dupreziana, threatened conifer of the Sahara. Biol Conserv 2:10–12

  81. Stewart PJ (1976) Cupressus dupreziana Fiches de renseignements sur les essences dont le patrimoine génétique s'appauvrit. Bull Ressourc Génet Forest Numéro 5:42

  82. Svobodová H, Albrechtová J, Kumstýřová L, Lipavská H, Vágner M, Vondráková Z (1999) Somatic embryogenesis in Norway spruce: anatomical study of embryo development and influence of polyethylene glycol on maturation process. Plant Physiol Biochem 37:209–221. https://doi.org/10.1016/S0981-9428(99)80036-9

  83. Wade TI, Ndiaye O, Mauclaire M, Mbaye B, Sagna M, Guissé A, Goffner D (2018) Biodiversity field trials to inform reforestation and natural resource management strategies along the African Great Green Wall in Senegal. New Forest 49:341–362. https://doi.org/10.1007/s11056-017-9623-3

  84. Werner L, Bubriski K (2007) A cypress in the Sahara. Saudi Aramco World 58:32–39. https://archive.aramcoworld.com/issue/200705/a.cypress.in.the.sahara.htm. Accessed 7 Jul 2019

  85. Wickens GE (1976) Speculations on long distance dispersal and the flora of Jebel Marra (Sudan). Kew Bull 31:105–150

  86. Yani A, Baradat P, Bernard-Dagan C (1990) Chemotaxonomy of Cupressus species. In: Ponchet J (ed) Progress in EEC research on cypress diseases, Luxembourg: Commission of the European Communities, pp 29–38

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Acknowledgements

The authors are very thankful to ing. Ladislav Pavlata, Head of Botanical Garden of the Faculty of Science, Charles University, Prague, for plant material and encouragement, Matěj Lipavský, MgA for art work and Prof. John D. Brooker for proofreading the article. This work was supported by the Czech Ministry of Education, Youth and Sports—Project LO1417.

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Correspondence to Hana Konrádová.

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Lábusová, J., Konrádová, H. & Lipavská, H. The endangered Saharan cypress (Cupressus dupreziana): do not let it get into Charon’s boat. Planta 251, 63 (2020). https://doi.org/10.1007/s00425-020-03358-6

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Keywords

  • Saharan relict plant species
  • Duprez´cypress
  • Olea europaea subsp. laperrinei
  • Micropropagation
  • Cultivation in vitro