Two new species of Entoloma (Entolomataceae) from Khyber Pakhtunkhwa, Pakistan

AIMAN IZHAR; MUHAMMAD USMAN; MUNAZZA KIRAN; ABDUL NASIR KHALID

doi:10.11646/phytotaxa.574.3.2

Issue: Vol. 574 No. 3: 30 November 2022

Type: Article

Published: 2022-11-30

DOI: 10.11646/phytotaxa.574.3.2

Page range: 226-240

Abstract views: 84

PDF downloaded: 1

**Two new species of Entoloma (Entolomataceae) from Khyber Pakhtunkhwa, Pakistan**

AIMAN IZHAR⁺⁻
MUHAMMAD USMAN⁺⁻
MUNAZZA KIRAN⁺⁻
ABDUL NASIR KHALID⁺⁻

Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan.

Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan. Department of Botany, Division of Science & Technology, University of Education, Lahore, 54500, Pakistan.

Fungal Biology and Systematics Research Laboratory, Institute of Botany, University of the Punjab, Quaid-e-Azam Campus, Lahore 54590, Pakistan.

Cyanula macrofungi phylogenetic affinities taxonomy Fungi

Requires Subscription or Fee PDF (10MB)

Abstract

Cedar towering forests of Kumrat Valley, Khyber Pakhtunkhwa, Pakistan were visited on several occasions to collect mushrooms and this resulted in the discovery of two novel species of Entoloma. Entoloma kumraticus is characterized by bluish-brown, centrally depressed pileus, serrulate lamellar edge, bluish-violet fibrillose stipe, dense clusters of cheilocystidia, and presence of abundant grayish-brown intracellular pigments in the terminal cells of pileipellis, and cheilocystidia. Entoloma dirensis is characterized by brownish olive to dull violet, finely fibrillose striate pileus with a violet-blue margin, slightly twisted violet-blue stipe, and blackish-brown lamellar edge, with groups of cheilocystidia which are often septate. The new species are presented based on the morphological and molecular study. Entoloma kumraticus and E. dirensis formed distinct phylogenetic lineages based on the sequences of nuclear ribosomal ITS and LSU gene regions. A key to the Pakistani species in sect. Cyanula is also provided.

References

Ahmad, S. (1962) Further contributions to the fungi of Pakistan. II. Biologia 8: 123‒150.
Ahmad, S., Iqbal, S.H. & Khalid, A.N. (1997) Fungi of Pakistan. Sultan Ahmad Mycological Society of Pakistan, Lahore.
Ahmad, S., Ahmad, A. & Moazzam, N.S. (2014) Assessment of Biomass Expansion Factor of Picea Smithiana (WA-LL) Boiss. International Journal of Scientific and Engineering Research 5 (11): 1232.
Ahmad, A., Amir, M., Mannan, A., Saeed, S., Shah, S., Ullah, S., Uddin, R. & Liu, Q. (2018) The carbon sinks and mitigation potential of deodar (Cedrus deodara) forest ecosystem at different altitude in Kumrat Valley, Pakistan. Open Journal of Forestry 8 (04): 553.
Aman, N., Khalid, A.N. & Moncalvo, J-M. (2022) A compendium of macrofungi of Pakistan by ecoregions. MycoKeys 89: 171–233. https://doi.org/10.3897/mycokeys.89.81148
Amir, M., Xiaodong, L., Saeed, S., Ahmad, A., Mannan, A., Nabi, M., Khan, D., Rehman, A.U., Badshah, M.T., Khan, M.A. & Muneer, M.A. (2019) Soil carbon storage potential in deodar (Cedrus deodara) Forest of Kumrat Valley, Pakistan. International Journal of Biosciences 14 (3): 92–99.
Blanco-Dios, J.B. (2017) Notas sobre el género Entoloma sl en el noroeste de la peninsula Ibérica (IX): Entoloma nesophilum, sp. nov. y algunas combinaciones y nombres nuevos. Tarrelos 19: 24–31.
Bruns, T.D. (1995) Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. The significance and regulation of soil biodiversity, Springer Netherlands, pp. 63–73. http://dx.doi.org/10.1007/978-94-011-0479-1_5
Castellano, M.A., Trappe, J.M. & Vernes, K. (2011) Australian species of Elaphomyces (Elaphomycetaceae, Eurotiales, Ascomycota). Australian Systematic Botany 24: 32–57.
Co-David, D., Langeveld, D. & Noordeloos, M.E. (2009) Molecular phylogeny and spore evolution of Entolomataceae. Persoonia 23: 147–176.
Courtecuisse, R. (1986) Notes de nomenclature concernant les hyménomycètes. IV: Sur quelques épithètes spécifiques préoccupés. 3. Mycotaxon 27: 127–145.
Crous, P.W., Wingfield, M.J., Burgess, T.I., Carnegie, A.J., Hardy, G.E.S.J., Smith, D., Summerell, B.A., Cano-Lira, J.F., Guarro, J., Houbraken, J., Lombard, L., Martin, M.P., Sandoval-Denis, M., Alexandrova, A.V., Barnes, C.W., Baseia, I.G., Bezerra, J.D.P., Guarnaccia, V., May, T.W., Hernandez-Restrepo, M., Stchigel, A.M., Miller, A.N., Ordonez, M.E., Abreu, V.P., Accioly, T., Agnello, C., Agustin Colman, A., Albuquerque, C.C., Alfredo, D.S., Alvarado, P., Araujo-Magalhaes, G.R., Arauzo, S., Atkinson, T., Barili, A., Barreto, R.W., Bezerra, J.L., Cabral, T.S., Camello Rodriguez, F., Cruz, R.H.S.F., Daniels, P.P., da Silva, B.D.B., de Almeida, D.A.C., de Carvalho Junior, A.A., Decock, C.A., Delgat, L., Denman, S., Dimitrov, R.A., Edwards, J., Fedosova, A.G., Ferreira, R.J., Firmino, A.L., Flores, J.A., Garcia, D., Gene, J., Giraldo, A., Gois, J.S., Gomes, A.A.M., Goncalves, C.M., Gouliamova, D.E., Groenewald, M., Gueorguiev, B.V., Guevara-Suarez, M., Gusmao, L.F.P., Hosaka, K., Hubka, V., Huhndorf, S.M., Jadan, M., Jurjevic, Z., Kraak, B., Kucera, V., Kumar, T.K.A., Kusan, I., Lacerda, S.R., Lamlertthon, S., Lisboa, W.S., Loizides, M., Luangsa-Ard, J.J., Lyskova, P., Mac Cormack, W.P., Macedo, D.M., Machado, A.R., Malysheva, E.F., Marinho, P., Matocec, N., Meijer, M., Mesic, A., Mongkolsamrit, S., Moreira, K.A., Morozova, O.V., Nair, K.U., Nakamura, N., Noisripoom, W., Olariaga, I., Oliveira,R.J.V., Paiva, L.M., Pawar, P., Pereira, O.L., Peterson, S.W., Prieto, M., Rodriguez-Andrade, E., Rojo De Blas, C., Roy, M., Santos, E.S., Sharma, R., Silva, G.A., Souza-Motta, C.M., Takeuchi-Kaneko, Y., Tanaka, C., Thakur, A., Smith, M.T., Tkalcec, Z., Valenzuela-Lopez, N., van der Kleij, P., Verbeken, A., Viana, M.G., Wang, X.W. & Groenewald, J.Z. (2017) Fungal Planet description sheets: 625–715. Persoonia 39: 270–467. https://doi.org/10.3767/persoonia.2017.39.11
Crous, P.W., Carnegie, A.J., Wingfield, M.J., Sharma, R., Mughini, G., Noordeloos, M.E., Santini, A., Shouche, Y.S., Bezerra, J.D.P., Dima, B., Guarnaccia, V., Imrefi, I., Jurjević, Ž., Knapp, D.G., Kovács, G.M., Magistà, D., Perrone, G., Rämä, T., Rebriev, Y.A., Shivas, R.G., Singh, S.M., Souza-Motta, C.M., Thangavel, R., Adhapure, N.N., Alexandrova, A.V., Alfenas, A.C., Alfenas, R.F., Alvarado, P., Alves, A.L., Andrade, D.A., Andrade, J.P., Barbosa, R.N., Barili, A., Barnes, C.W., Baseia, I.G., Bellanger, J.M., Berlanas, C., Bessette, A.E., Bessette, A.R., Biketova, A.Y., Bomfim, F.S., Brandrud, T.E., Bransgrove, K., Brito, A.C.Q., Cano-Lira, J.F., Cantillo, T., Cavalcanti, A.D., Cheewangkoon, R., Chikowski, R.S., Conforto, C., Cordeiro, T.R.L., Craine, J.D., Cruz, R., Damm, U., de Oliveira, R.J.V., de Souza, J.T., de Souza, H.G., Dearnaley, J.D.W., Dimitrov, R.A., Dovana, F., Erhard, A., Esteve-Raventós, F., Félix, C.R., Ferisin, G., Fernandes, R.A., Ferreira, R.J., Ferro, L.O., Figueiredo, C.N., Frank, J.L., Freire, K.T.L.S., García, D., Gené, J., Gêsiorska, A., Gibertoni, T.B., Gondra, R.A.G., Gouliamova, D.E., Gramaje, D., Guard, F., Gusmão, L.F.P., Haitook, S., Hirooka, Y., Houbraken, J., Hubka, V., Inamdar, A., Iturriaga, T., Iturrieta-González, I., Jadan, M., Jiang, N., Justo, A., Kachalkin, A.V., Kapitonov, V.I., Karadelev, M., Karakehian, J., Kasuya, T., Kautmanová, I., Kruse, J., Kušan, I., Kuznetsova, T.A., Landell, M.F., Larsson, K.H., Lee, H.B., Lima, D.X., Lira, C.R.S., Machado, A.R., Madrid, H., Magalhães, O.M.C., Majerova, H., Malysheva, E.F., Mapperson, R.R., Marbach, P.A.S., Martín, M.P., Martín-Sanz, A., Matočec, N., McTaggart, A.R., Mello, J.F., Melo, R.F.R., Mešić, A., Michereff, S.J., Miller, A.N., Minoshima, A., Molinero-Ruiz, L., Morozova, O.V., Mosoh, D., Nabe, M., Naik, R., Nara, K., Nascimento, S.S., Neves, R.P., Olariaga, I., Oliveira, R.L., Oliveira, T.G.L., Ono, T., Ordoñez, M.E., Ottoni, A.M., Paiva, L.M., Pancorbo, F., Pant, B., Pawłowska, J., Peterson, S.W., Raudabaugh, D.B., Rodríguez-Andrade, E., Rubio, E., Rusevska, K., Santiago, A.L.C.M.A., Santos, A.C.S., Santos, C., Sazanova, N.A., Shah, S., Sharma, J., Silva, B.D.B., Siquier, J.L., Sonawane, M.S., Stchigel, A.M., Svetasheva, T., Tamakeaw, N., Telleria, M.T., Tiago, P.V., Tian, C.M., Tkalčec, Z., Tomashevskaya, M.A., Truong, H.H., Vecherskii, M.V., Visagie, C.M., Vizzini, A., Yilmaz, N., Zmitrovich, I.V., Zvyagina, E.A., Boekhout, T., Kehlet, T., Læssøe, T., Groenewald, J.Z.  (2019) Fungal planet description sheets: 868–950. Persoonia 42: 291–473.  https://doi.org/10.3767/persoonia.2019.42.11
Dennis, R.W.G. (1953) Les Agaricales de l’Ile de la Trinité. Rhodosporae-Ochrosporae. Bulletin de la Société Mycologique de France 69: 145–198.
Dima, B., Brandrud, T.E., Corriol, G., Jansen, G.M., Jordal, J.B., Khalid, A.N., Larsson, E., Lorås, J., Morozova, O.V., Naseer, A., Noordeloos, M.E., Rossi, W., Santamaria, S., Sarwar, S., Sesli, E., Usman, M., Afshan, N.S., Ahmad, I., Banerjee, A., Banerjee, K., Bendiksen, E., Rodrigues Da Silva Colombo, D., De Kesel, A., Dovana, F., Ferisin, G., Hussain, S., Islam, S., Jesus, A.L., Kaygusuz, O., Krisai-Greilhuber, I., Mahammad, S., Mishra, D.K., Nath, P.S., De Oliveira Da Paixã, S.C., Panja, B., Papp, V., Amorim Pires-Zottarelli, C.L., Radnóti, A., Rana, D., Saha, R., Türkekul, I. & Haelewaters, D. (2021) Fungal Systematics and Evolution: FUSE 7. Sydowia 73: 271–340. https://doi.org/10.12905/0380.sydowia73-2021-0271
Elliott, T.F., Nelsen, D.J., Karunarathna, S.C. & Stephenson, S.L. (2020) Entoloma sequestratum, a new species from northern Thailand, and a worldwide key to sequestrate taxa of Entoloma (Entolomataceae). FUSE 6: 253–263.  https://doi.org/10.3114/fuse.2020.06.12. 
Fries, E.M. (1838) Epicrisis Systematis Mycologici. Typographia Academica, Uppsala, 610 pp.
Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae rusts. Molecular Ecology 2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gates, G.M. & Noordeloos, M. (2007) Preliminary studies in the genus Entoloma in Tasmania. Persoonia 19: 157–226. 
Haelewaters, D., Dima, B., Abdel-Hafiz, A.I., Abdel-Wahab, M.A., Abul-Ezz, S.R., Acar, I., Aguirre-Acosta, E., Aime, M.C., Aldemir, S., Ali, M., Ayala-Vásquez, O., Bakhit, M.S., Bashir, H., Battistin, E., Bendiksen, E., Castro-Rivera, R., Çolak, Ö.F., De Kesel, A., de la Fuente, J.I., Dizkýrýcý, A., Hussain, S., Jansen, G.M., Kaygusuz, O., Khalid, A.N., Khan, J., Kiyashko, A.A., Larsson, E., Martínez-González, C.R., Morozova, O.V., Niazi, A.R., Noordeloos, M.E., Pham, T.H.G., Popov, E.S., Psurtseva, N.V., Schoutteten, N., She, H., Türkekul, Ý., Verbeken, A., Ahmad, H., Afshan, N.S., Christe, P., Fiaz, M., Glaizot, O., Liu, J., Majeed, J., Markotter, W., Nagy, A., Nawaz, H., Papp, V., Péter, Á., Pfliegler, W.P., Qasim, T., Riaz, M., Sándor, A.D., Szentiványi, T., Voglmayr, H., Yousaf, N. & Krisai-Greilhuber, I. (2020) Fungal systematics and evolution. Fungal Systematics and Evolution 6. Sydowia 72: 231–356. https://doi.org/10.12905/0380.sydowia72-2020-0271
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98. https://doi.org/10.1073/pnas.1117018109
He, X-L., Li, T-H., Peng, W-H. & Gan, B-C. (2016) Four new Chinese records of Entoloma from northeast China. Mycosystem 35: 222–228. https://doi.org/10.13346/j.mycosystema.140237
He, X-L., Wang, D., Peng, W-H. & Gan, B-C. (2017) Two new Entoloma s.l. species with serrulatum-type lamellar edge from Changbai Mountains, Northeast China. Mycological Progress 16: 761–768. https://doi.org/10.1007/s11557-017-1313-1
Hesler, L.R. (1967) Entoloma in Southeastern North America. Beihefte zur Nova Hedwigia 23: 1–196.
Horak, E. (1980) Entoloma (Agaricales) in Indomalaya and Australasia. Beihefte zur Nova Hedwigia 65: 1–352. 
Karstedt, F. & Capelari, M. (2013) Inocephalus (Entolomataceae, Agaricales) from São Paulo State, Brazil. Nova Hedwigia 96: 279–308. https://doi.org/10.1127/0029-5035/2012/0055
Khalid, A.N. (2022) A Checklist of Macrofungi of Pakistan published from 1998–2020. Pakistan Journal of Botany 54: 1947–1962. http://dx.doi.org/10.30848/PJB2022-5(23)
Kondo, K., Nakamura, K., Ishigaki, T., Sakata, K., Obitsu, S., Noguchi, A., Fukuda, N., Nagasawa, E., Teshima, R. & Nishimaki-Mogami, T. (2017) Molecular phylogenetic analysis of new Entoloma rhodopolium-related species in Japan and its identification method using PCR-RFLP. Scientific reports 7: 1–12. https://doi.org/10.1038/s41598-017-14466-x
Kummer, P. (1871) Der Führer in die Pilzkunde. C. Luppe, Zerbst, 146 pp.
Lorås, J., Weholt, Ø. & Eidissen, S.E. (2014) Entoloma gomerense Wölfel & Noordel. - a new species to Northern Europe. Agarica 35: 19–24.
Largent, D.L. (1994) Entolomatoid fungi of the western United States and Alaska. Mad River Press, Eureka, California.
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway computing environments workshop (GCE). New Orleans, Louisiana, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129.
Moser, M. (1978) Die Röhrlinge und Blätterpilze (in Gams, h., Kleine Kryptogamenflora, Bd.II b/2, Jena, Stuttgart 206 pp.
Morozova, O.V., Noordeloos, M.E., Popov, E.S. & Alexandrova, A.V. (2018) Three new species within the genus Entoloma (Basidiomycota, Agaricales) with clamped basidia and a serrulatum-type lamellae edge, and their phylogenetic position. Mycological Progress 17: 381–392. https://doi.org/10.1007/s11557-017-1364-3
Noordeloos, M.E. (1980) Entoloma subgenus Nolanea in the Netherlands and adjacent regions with a reconnaissance of its remaining taxa in Europe. Persoonia 10: 427–534.
Noordeloos, M.E. (1981) Introduction to the taxonomy of the genus Entoloma sensu lato (Agaricales). Persoonia 11: 121–151.
Noordeloos, M.E. (1982) Notes on Entoloma. New and rare species of Entoloma from Scandinavia. New names and combinations. Nordic Journal of Botany 2: 155–162.
Noordeloos, M.E. (1984) Studies in Entoloma 10–13. Persoonia 12: 195–223.
Noordeloos, M.E. & Liiv, V. (1992) New taxa of Entoloma (Basidiomycetes, Agaricales) from Estonia and Karelia. Persoonia 15: 23–31.
Noordeloos, M.E. (1988) Entoloma in North America. Gustav Fischer Verlag, Stuttgart, New York.
Noordeloos, M.E. (1995a) Bestimmungsschlüssel zu den Arten der Gattung Entoloma (Rötlinge) in Europa. IHW-Verlag. Eching. Zeitschrift für Mykologie 61: 183–196.
Noordeloos, M.E., Wölfel, G. & Hausknecht, A. (1995b) Über neue, kritische oder seltene Rötlinge aus dem östlichen Österreich.  4: 119–136.
Noordeloos, M.E. (2004) Entoloma s.l. Fungi Europaei 5a: 761–1378.
Noordeloos, M.E. & Hausknecht, A. (2007) The genus Entoloma (Basidiomycetes, Agaricales) of the Mascarenes and Seychelles. Fungal Diversity 27: 111–144.
Noordeloos, M.E. & Morozova, O.V. (2010) New and noteworthy Entoloma species from the Prismorsky Territory, Russian Far East. Mycotaxon 112: 231–255.
Noordeloos, M.E. & Gates, G.M. (2012) The Entolomataceae of Tasmania. Fungal diversity research series, vol 22. Springer, London.
Noordeloos, M.E., Weholt, Ø., Bendiksen, E., Brandrud, T.E., Eidissen, S.E., Lorås, J., Morozova, O. & Dima, B. (2018) Entoloma aurorae-borealis sp. nov. and three rare Entoloma species in the Sinuatum clade (subg. Entoloma) from northern Europe. Sydowia 70: 199–210.
Noordeloos, M.E., Lorås, J.A., Eidissen, S.E., Brandrud, T.E., Bendiksen, E., Morozova, O., Jordal, J.B., Weholt, Ø., Jansen, G.M., Larsson, E. & Bálint, D. (2021) Three new Entoloma species of the Cyanula clade from (sub)alpine habitats in Northern Norway and Sweden. Sydowia 73: 185–196. https://doi.org/10.12905/0380.sydowia73-2020-0185
Pegler, D.N. (1977) Entolomataceae (Agaricales) from India & Sri Lanka. Kew Bull 32: 189–220. 
Rajpar, M.N., Ozturk, M., Altay, V., Ullah, S., Ullah, A., Martin, C.O., Gücel, S., Zakaria, M. (2020) Species composition of dry-temperate forest as an important habitat for wildlife fauna species. Journal of Environmental Biology 41: 328–336. 
Reschke, K., Noordeloos, M.E., Manz, C., Hofmann, T.A., Rodríguez-Cedeño, J., Dima, B. & Pipenbring, M. (2022) Fungal diversity in the tropics: Entoloma spp. in Panama. Mycological Progress 21: 93–145.
Ridgway, R. (1912) Color standards and color nomenclature. Ridgway, Washington, DC.
Singer, R. (1936) Das System der Agaricales. Annales Mycologici 34 (6): 1–428.
Singer, R. (1986) The Agaricales in modern taxonomy, 4th edition. Koeltz Scientific Books, Koenigstein. 
Smith, M.E., Amses, K.R., Elliott, T.F., Obase, K., Aime, M.C. & Henkel, T.W. (2015) New sequestrate fungi from Guyana: Jimtrappea guyanensis gen. sp. nov., Castellanea pakaraimophila gen. sp. nov., and Costatisporus cyanescens gen. sp. nov. (Boletaceae, Boletales). IMA fungus 6: 297–317.
Sulzbacher, M.A., Orihara, T., Grebenc, T., Wartchow, F., Smith, M.E., Martín, M.P., Giachini, A.J. & Baseia, I.G. (2020) Longistriata flava (Boletaceae, Basidiomycota) – a new monotypic sequestrate genus and species from Brazilian Atlantic Forest. MycoKeys 62: 53–73. https://doi.org/10.3897/mycokeys.62.39699
Sultana, K., Rauf, C.A., Riaz, A., Naz, F., Irshad, G. & Haque, M.I. (2011) Checklist of Agarics of Kaghan Valley-1. Pakistan Journal of Botany 43: 1777–1787.
Wang, J.R. & Bau, T. (2013) A new species and a new record of the genus Entoloma from China. Mycotaxon 124: 165–171. 
Weholt, Ø., Lorås, J. & Eidissen, S.E. (2014) One new and one rare species of Entoloma from the Norwegian nature reserve Holmvassdalen. Österr Z Pilzk 23: 55–60.
White, T.J., Bruns, T.D. & Taylor, L.J. (1990) Amplification direct sequencing of fungal ribosomal RNA genes for Phylogenetics. In: Innis, M.A., Gelf, D.H., Sninsky, J.J. & White, T.J. (Eds.) PCR protocols: A guide to methods applications. Academic Press, New York, pp. 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1