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Combined phylogenetic and morphological studies of true morels (Pezizales, Ascomycota) in Cyprus reveal significant diversity, including Morchella arbutiphila and M. disparilis spp. nov.

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Abstract

A detailed account of the genus Morchella in the island of Cyprus is presented, based on integrative phylogenetic, morphoanatomical, ecological, and chorological analyses. Eleven species are molecularly confirmed, nine of them previously unreported from the island. Notably, four species are recognized as new to science, including one species in Sect. Morchella and three in Sect. Distantes. Two of these are here newly described, as Morchella arbutiphila and Morchella disparilis, respectively, whilst the other two are provisionally assigned the phylogenetic codes Mes-28 and Mel-38. Following careful re-examination of the Morchella vulgaris clade, two closely related sister species are revealed, and the taxon Morchella dunensis is revived to accommodate Mes-17. A description for the widespread, yet poorly known Mediterranean species Morchella dunalii is further provided, and a detailed polythetic approach is introduced in systematics, to overcome the inherent difficulties associated with the morphological recognition of phylogenetically confirmed species. The presence on the island of five species of transcontinental distribution, accounting for nearly half of the total number of species recorded, sheds new light on the genus biogeography, questioning the hypothesis of recent anthropogenic dispersals of morel species. Overall, our results place Cyprus as a worldwide hotspot of Morchella diversity, establishing the island as a place of special interest in future studies aiming to decipher the evolutionary history and ecological trends within this iconic genus.

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References

  • Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552

    Article  PubMed  Google Scholar 

  • Anisimova M, Gil M, Dufayard JF, Dessimoz C, Gascuel O (2011) Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 60:685–699

    Article  PubMed  PubMed Central  Google Scholar 

  • Baral H-O (1992) Vital versus herbarium taxonomy: morphological differences between living and dead cells of Ascomycetes, and their taxonomic implications. Mycotaxon 44(2):333–390

    Google Scholar 

  • Barseghyan GS, Kosakyan A, Isikhuemhe OS, Didukh M, Wasser SP (2012) Phylogenetic analysis within genera Morchella (Ascomycota, Pezizales) and Macrolepiota (Basidiomycota, Agaricales) inferred from rDNA ITS and EF-1a Sequences. In: Misra JK, Tewari JP, Deshmukh SK (eds) Systipeatics and Evolution of Fungi. Science Publishers, USA, 422 pp

    Google Scholar 

  • Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant-fungal mutualism associated with fire. Fungal Biol 116(1):133–144

    Article  PubMed  Google Scholar 

  • Behrens A, Georgiev A, Carraro M (2010) Future Impacts of Climate Change across Europe. Working Document No. 324, Centre for European Policy Studies (CEPS), Brussels

  • Bellanger J-M, Moreau P-A, Corriol G, Bidaud A, Chalange R, Dudova Z, Richard F (2015) Plunging hands into the mushroom jar: a phylogenetic framework for Lyophyllaceae (Agaricales, Basidiomycota). Genetica 143:169–194. doi:10.1007/s10709-015-9823-8

  • Boudier E (1897) Révision analytique des morilles de France. Bull Soc Mycol Fr 13:130–150

    Google Scholar 

  • Boudier E (1909) Icones mycologicae ou iconographie des champignons de France principalement discomycètes avec texte descriptif. Tome II, pl. 194–421. Librairie des Sciences Naturelles, Paris

  • Bresadola G (1932) Iconographia Mycologica, vol 24. Societa Botanica italiana, pl, Trento, pp 1151–1200

    Google Scholar 

  • Buscot F (1992) Mycorrhizal succession and morel biology. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystipes. CAB International, Wallingford, pp 220–224

    Google Scholar 

  • Buscot F, Roux J (1987) Association between living roots and ascocarps of Morchella rotunda. Trans Br Mycol Soc 89(2):249–252

    Article  Google Scholar 

  • Castañera V, Moreno G (1996) Una Morchella (Morchella esculenta forma dunensis f. nov.) frecuente en las dunas de Cantabria. Yesca, Rev Soc Micólogica de Cántabria 8:27

    Google Scholar 

  • Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

    Article  CAS  PubMed  Google Scholar 

  • Chen J-Y, Liu P-G (2005) A new species of Morchella (Pezizales, Ascomycota) from southwestern China. Mycotaxon 93:89–93

    Google Scholar 

  • Chevenet F, Brun C, Bañuls AL, Jacq B, Christen R (2006) TreeByn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinf 7:439. doi:10.1186/1471-2105-7-439

    Article  Google Scholar 

  • Clowez P (1997) Morchella dunensis (Boud.) Clowez (stat. et comb. nov. ad int.). Une bonne espèce pour un mystère nomenclatural. Doc Mycol 26(104):13–20

    Google Scholar 

  • Clowez P (2012) (‘2010’) Les morilles: Une nouvelle approche mondiale du genre Morchella. Bull Trimest Soc Mycol Fr 126(3–4):199–376

  • Clowez P, Alvarado P, Becerra M, Bilbao T, Moreau P-A (2014) Morchella fluvialis sp. nov. (Ascomycota, Pezizales): a new but widespread morel in Spain. Bol Soc Micol Madrid 38(2):251–260

    Google Scholar 

  • Сухомилин ММ, Куткова ОВ, Панiна ЗО (2007) Morchella steppicola Zer.: морфологiчнi особливостi, ультраструктура та поширення в пiвденно-схiднiй Украïнi [Morchella steppicola Zer.: morphological peculiarities, ultrastructure and distribution in southeastern Ukraine] (in Russian). Ukr Bot J 64(6):867–874

  • Dahlstrom JL, Smith JE, Weber NS (2000) Mycorrhiza-like interaction by Morchella with species of the Pinaceae in pure culture synthesis. Mycorrhiza 9(5):279–285

    Article  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(Web Server issue):W465–W469. doi:10.1093/nar/gkn180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du X-H, Zhao Q, O’Donnell K, Rooney AP, Yang ZL (2012a) Multigene molecular phylogenetics reveals true morels (Morchella) are especially species-rich in China. Fungal Genet Biol 49:455–469

    Article  CAS  PubMed  Google Scholar 

  • Du X-H, Zhao Q, Yang ZL, Hansen K, Taşkın H, Büyükalaca S, Dewsbury D, Moncalvo J-M, Douhan GW, Robert VARG, Crous PW, Rehner SA, Rooney AP, Sink S, O’Donnell K (2012b) How well do ITS rDNA sequences differentiate species of true morels (Morchella)? Mycologia 104:1351–1368

    Article  PubMed  Google Scholar 

  • Du X-H, Zhao Q, Yang ZL (2015) A review on research advances, issues, and perspectives of morels. Mycology: An International Journal on Fungal Biology. doi:10.1080/21501203.2015.1016561

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BioMed Cen Bioinform 5:113. doi:10.1186/1471-2105-5-113

    Article  Google Scholar 

  • Elliott TF, Bougher NL, O’Donnell K, Trappe JM (2014) Morchella australiana sp. nov., an apparent Australian endemic from New South Wales and Victoria. Mycologia 106:113–118

    Article  PubMed  Google Scholar 

  • Fries EM (1849) Summa Vegetabilum Scandinaviae. Section Posterior 346:259–572

    Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodríguez-Sánchez F, Dobrowski SZ, Hampe A, Hu F-S, Ashcroft MB, Bartlein PJ, Blois JL, Carstens BC, Davis EB, De Lafontaine G, Edwards ME, Fernandez MC, Henne PD, Herring EM, Holden ZA, Kong WS, Liu J, Magri D, Matzke NJ, McGlone MS, Saltré F, Stigall AL, Tsai Y-HE, Williams JW (2014) Climate refugia: Joint inference from fossil records, species distribution models, and phylogeography. New Phytol 204:37–54

    Article  PubMed  Google Scholar 

  • Giorgi F (2006) Climate change hot-spots. Geophys Res Lett 330(8). doi:10.1029/2006GL025734

  • Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36(Web Server issue):W465–W469. doi:10.1093/nar/gkn180

    PubMed  PubMed Central  Google Scholar 

  • Guzmán G, Tapia F (1998) The known Morels in Mexico, a description of a new blushing species, Morchella rufobrunnea and new data on M. guatemalensis. Mycologia 90:705–714

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2007) The Physical Science Basis, Working Group I Contribution to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Isiloglu M, Alli H, Spooner BM, Solak MH (2010) Morchella anatolica (Ascomycota), a new species from southwestern Anatolia, Turkey. Mycologia 102(2):455–468

    Article  PubMed  Google Scholar 

  • Jacquetant E (1984) Les Morilles. La Bibliothèque des Arts, Paris, 114 p

  • Kuo M (2008) Morchella tomentosa, a new species from western North America and notes on M. rufobrunnea. Mycotaxon 105:441–446

    Google Scholar 

  • Kuo M, Dewsbury DR, O’Donnell K, Carter MC, Rehner SA, Moore JD, Moncalvo J-M, Canfield SA, Stephenson SL, Methven AS, Volk TJ (2012) Taxonomic revision of true morels (Morchella) in Canada and the United States. Mycologia 104:1159–1177

    Article  PubMed  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808

    Article  CAS  PubMed  Google Scholar 

  • Loizides M (2011) Morchella rufobrunnea, η μορχέλλα της πόλης [Morchella rufobrunnea, the urban morel] (in Greek). Μυκητολόγος [Mycologist] 5:10–13

  • Loizides M, Kyriakou T, Tziakouris A (2011) Edible & Toxic Fungi of Cyprus (in Greek & English), Published by the authors: 222–229 ISBN: 978-9963-7380-0-7

  • Loizides M, Alvarado P, Clowez P, Moreau P-A, Romero L, Palazón A (2015) Morchella tridentina, M. rufobrunnea and M. kakiicolor: A study of three poorly known Mediterranean morels, with nomenclatural updates in section Distantes. Mycol Prog 14:13

    Article  Google Scholar 

  • Malloch D (1973) Ascospore sculpturing in Morchella (Ascomycetes: Pezizales). Can J Bot 51:1519–1520

    Article  Google Scholar 

  • Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). Am J Bot 89:688–698

    Article  CAS  PubMed  Google Scholar 

  • Masaphy S, Zabari L, Goldberg D (2009) New long-season ecotype of Morchella rufobrunnea from northern Israel. Micología Aplicada Internacional 21(2):45–55

    Google Scholar 

  • Médail F, Diademal K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean basin. J Biogeogr 36(7):1333–1345

  • Médail F, Myers N (2004) Mediterranean Basin in Hotspots revisited. Cemex. Conservation International. University of Virginia, pp 144–147

  • 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 

  • Medardi G (2006) Atlante fortografico degli Ascomiceti d’Italia. Grafica Sette, Bagnolo mella, Brescia, Italia, p 678

  • Moreau P-A, Hériveau P, Bourgade V, Bellanger J-M, Courtecuisse R, Fons F, Rapior S (2011) Redécouverte et typification des champignons de la région de Montpellier illustrés par Michel-Félix Dunal et Alire Raffeneau-Delile. Cryptogram Mycol 32:255–276

    Article  Google Scholar 

  • Myers N (1990) The biodiversity challenge: expanded hot-spots analysis. Environmentalist 10:243–256

    Article  CAS  PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Norstedt G, Bader P, Ericson L (2001) Polypores as indicators of conservation value in Corsican pine forests. Biol Conserv 99:347–354

    Article  Google Scholar 

  • O’Donnell K, Rooney AP, Mills GL, Kuo M, Weber NS, Rehner SA (2011) Phylogeny and historical biogeography of true Morels (Morchella) reveals an early Cretaceous origin and high continental endemism and provincialism in the Holarctic. Fungal Genet Biol 48:252–265

    Article  PubMed  Google Scholar 

  • Persoon CH (1794) Neue Versuch einer Systemtischen Einsteilung der Schwämme. Neues Mag Bot 1:63–128

    Google Scholar 

  • Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98

    Article  CAS  PubMed  Google Scholar 

  • Richard F, Bellanger J-M, Clowez P, Hansen K, O’Donnell K, Urban A, Sauve M, Courtecuisse R, Moreau P-A (2015) True morels (Morchella, Pezizales) of Europe and North America: Evolutionary relationships inferred from multilocus data and a unified taxonomy. Mycologia 107(2):359–382

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577

    Article  CAS  PubMed  Google Scholar 

  • Taşkın H, Büyükalaca S, Hüseyin H, Rehner S, O’Donnel K (2010) A multigene molecular phylogenetic assessment of true morels (Morchella). Fungal Genet Biol 47:672–682

    Article  PubMed  Google Scholar 

  • Taşkın H, Büyükalaca S, Hansen K, O’Donnell K (2012) Multilocus phylogenetic analysis of true morels (Morchella) reveals high levels of endemics in Turkey relative to other regions of Europe. Mycologia 104:446–461

    Article  PubMed  Google Scholar 

  • Taşkın H, Doğan H, Büyükalaca S, Hüseyin H (2015) Morchella galilaea, an autumn species from Turkey. Mycotaxon 130(1):215–221

    Article  Google Scholar 

  • Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263

    Article  PubMed  Google Scholar 

  • Viney DE (2005) An illustrated introduction to the larger fungi of north Cyprus. Published by the author. ISBN: 0-85546-109-8

  • Voitk A, Beug MW, O’Donnell K, Burzynski M (2015) Two new species of true morels from Newfoundland and Labrador: cosmopolitan Morchella eohespera and parochial M. laurentiana. Mycologia 108(1):31–37. doi:10.3852/15-149

  • Willimott SG (1933) Some edible and poisonous fungi of Cyprus: an investigation of their habitat, uses, nutritive value, toxicology, cases of poisoning and treatment. The Cyprus Government, Nicosia, p 24

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Acknowledgments

We are indebted to our friend Pablo Alvarado, for generating and analyzing many of the sequences cited in this work; to Marcel Lecomte for his advice on staining chemicals for microscopy; to Yiangos Yiangou, for his valuable field observations and image of Morchella cf galilaea (Fig. 16l); to Father Savvas Michaelides, for his continuous support and collection of M. dunensis (Moutoullas); to Daniel Markides, for his collections of M. disparilis (Prastio) and M. dunensis (Amiantos); to Michalis Georgiades, for his collection of M. rufobrunnea (Ayia Fila); and to Michalis Chelides, for his collections of M. dunalii and M. tridentina (Lythrodontas). We are further grateful to Boris Assyov (Bulgaria), John Karagkiozis (Greece), Kostas Manatakis (Greece), Evgenia Tziava (Greece), Antonio Palazón (Spain), and Olga Godorova (Israel), for kindly providing us with information on the ecology and distribution of morel species outside Cyprus. Last but not least, our gratitude extends to Prof. Gabriel Moreno, for making the holotype and isoparatype of M. dunensis available to us for molecular analysis.

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Loizides, M., Bellanger, JM., Clowez, P. et al. Combined phylogenetic and morphological studies of true morels (Pezizales, Ascomycota) in Cyprus reveal significant diversity, including Morchella arbutiphila and M. disparilis spp. nov.. Mycol Progress 15, 39 (2016). https://doi.org/10.1007/s11557-016-1180-1

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