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Phylogeny of Agaricus subgenus Pseudochitonia with the description of a new section and a new species from Oman

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Abstract

Agaricus is an important mushroom genus with some most common edible and medicinal species, but some members are also poisonous. Taxonomically, the genus is divided into seven subgenera including the subgenus Pseudochitonia. In this study, we analyzed some collections of Agaricus from southern Oman, belonging to A. subgenus Pseudochitonia. Agaricus subg. Pseudochitonia is the largest subgenus in terms of sections, with 13 sections by applying the modern taxonomic system in which supraspecific taxa are ranked according to their divergence times. We applied the same procedure using BEAST (Bayesian evolutionary analysis sampling tree) to evaluate the taxonomic position of our specimens. Our specimens formed a strong monophyletic clade with unclassified Agaricus species (A. lannaensis and A. sp. CA820), based on multigene sequence data (ITS, 28S and TEF1) and ITS alignment. The divergence time is estimated around 20–30 million years for this clade. We proposed a new section Catenulati following the basic principles of modern taxonomic system of Agaricus, which are (i) strong phylogenetic support, (ii) divergence times younger than 30 Ma, and (iii) specific morphological characters where possible. The new section Catenulati is represented by a new species Agaricus arabiensis. Moreover, the new section resolved the pending issue of A. lannaensis, previously as unclassified taxon in A. subg. Pseudochitonia and is now in A. sect. Catenulati. The new section is characterized by a phenolic odor of basidiomata and catenoid cheilocystidia.

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information.

References

  • Al-Kharousi M, Hussain S, Al-Muharabi MA, Al-Shabibi Z, Al-Maqbali D, Al-Balushi AH, Al-Yahya’ei MN, Al-Saady N, Velazhahan R, Al-Sadi AM (2022) The genus Xanthagaricus: an updated global species distribution and phylogeny with the description of two new species from Oman. J Fungi 8(2):173. https://doi.org/10.3390/jof8020173

    Article  CAS  Google Scholar 

  • Bashir H, Chen J, Jabeen S, Ullah S, Khan J, Niazi AR, Zhang M, Khalid AN, Parra LA, Callac P (2021) An overview of Agaricus section Hondenses and Agaricus section Xanthodermatei with description of eight new species from Pakistan. Sci Rep 11(12905). https://doi.org/10.1038/s41598-021-92261-5

  • Belda M, Holtanová E, Halenka T, Kalvová J (2014) Climate classification revisited: from Köppen to Trewartha. Clim Res 59:1–13. https://doi.org/10.3354/cr01204

    Article  Google Scholar 

  • Bookhagen B, Thiede RC, Strecker MR (2005) Abnormal monsoon years and their control on erosion and sediment flux in the high, arid northwest Himalaya. Earth and Planetary Science Letters 231:131–146

    Article  CAS  Google Scholar 

  • Callac P, Chen J (2018) Tropical species of Agaricus. In: Sánchez JE, Mata G, Royse DJ (eds) Updates on tropical mushrooms. Basic and applied research. San Cristobal de Las Casas. Chiapas, Vol, p 1, 227 p

    Google Scholar 

  • Challen MP, Kerrigan RW, Callac P (2003) A phylogenetic reconstruction and emendation of Agaricus section Duploannulatae. Mycologia 95:61–73. https://doi.org/10.1080/15572536.2004.11833132

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Callac P, Parra LA, Karunarathna SC, He MQ, Moinard M, De Kesel A, Raspé O, Wisitrassameewong K, Hyde KD, Zhao RL (2017) Study in Agaricus subgenus Minores and allied clades reveals a new American subgenus and contrasting phylogenetic patterns in Europe and Greater Mekong Subregion. Persoonia 38:170–196. https://doi.org/10.3767/003158517X695521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Zhao R, Parra L, Guelly A, De Kesel A, Rapior S, Hyde K, Chukeatirote E, Callac P (2015) Agaricus section Brunneopicti: a phylogenetic reconstruction with descriptions of four new taxa. Phytotaxa 192(3):145–168. https://doi.org/10.11646/phytotaxa.192.3.2

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and BEAST 1.7. Mol Biol Evol 29:1969–1973

  • El-Sheikh MA (2013) Population structure of woody plants in the arid cloud forests of Dhofar, southern Oman. Acta Botanica Croatica 72(1):97–111

    Article  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. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Guizani N, Rahman MS, Klibi M, Al-Rawahi A, Bornaz S (2013) Thermal characteristics of Agaricus bisporus mushroom: freezing point, glass transition, and maximal-freeze-concentration condition. Int Food Res J 20(4):1945–1952

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98. https://doi.org/10.1021/bk-1999-0734.ch008

    Article  CAS  Google Scholar 

  • He MQ, Chen J, Zhou JL, Cheewangkoon R, Hyde KD, Zhao RL (2017) Tropic origins, a dispersal model for saprotrophic mushrooms in Agaricus section Minores with descriptions of sixteen new species. Sci Rep 7(5122). https://doi.org/10.1038/s41598-017-05203-5

  • He MQ, Chuankid B, Hyde KD, Cheewangkoon R, Zhao RL (2018) A new section and species of Agaricus subgenus Pseudochitonia from Thailand. MycoKeys 40:53–67. https://doi.org/10.3897/mycokeys.40.26918

    Article  Google Scholar 

  • Henderson JC (2015) The development of tourist destinations in the Gulf: Oman and Qatar compared. Tourism Planning & Development 12(3):350–361

    Article  Google Scholar 

  • Hussain S, Sher H (2019) Study in Agaricus section Minores in Pakistan with the description of two new species. Mycol Prog 18:795–204. https://doi.org/10.1007/s11557-019-01493-3

    Article  Google Scholar 

  • Jaichaliaw C, Kumla J, Vadthanarat S, Suwannarach N, Lumyong S (2021) Multigene phylogeny and morphology reveal three novel species and a novel record of Agaricus from northern Thailand. Front Microbiol 12(650513). https://doi.org/10.3389/fmicb.2021.650513

  • Karunarathna SC, Chen J, Mortimer PE, Xu JC, Zhao RL, Callac P, Hyde KD (2016) Mycosphere essay 8: A review of genus Agaricus in tropical and humid subtropical regions of Asia. Mycosphere 7:417–439. https://doi.org/10.5943/mycosphere/7/4/3

    Article  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerrigan RW (2016) Agaricus of North America. New York Botanical Garden

    Google Scholar 

  • Kerrigan RW, Callac P, Parra LA (2008) New and rare taxa in Agaricus section Bivelares (Duploannulati). Mycologia 100:876–892. https://doi.org/10.3852/08-019

    Article  CAS  PubMed  Google Scholar 

  • Kwarteng AY, Dorvlo S, Vijaya GT (2009) Analysis of a 27-year rainfall data (1977–2003) in the Sultanate of Oman. Int J Climatol 29:605–617. https://doi.org/10.1002/joc.1727

    Article  Google Scholar 

  • Lebel T, Syme A (2012) Sequestrate species of Agaricus and Macrolepiota from Australia: new species and combinations and their position in a calibrated phylogeny. Mycologia 104:496–520. https://doi.org/10.3852/11-092

    Article  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 2010. IEEE:1–8.

  • Munsell AH (1975) Munsell soil color charts. Macbeth Division of Kollmorgen Corporation. Baltimore, Maryland

  • Ortiz-Santana B, Chen J, Parra LA, Angelini C, Lodge DJ, Kerrigan RW, Callac P (2021) The genus Agaricus in the Caribbean II. Refined phylogeny of Agaricus subg. Spissicaules with description of two new sections and eight new species. Mycol Prog 20:381–411. https://doi.org/10.1007/s11557-021-01686-9

    Article  Google Scholar 

  • Palmer JM, Lindner DL, Volk TJ (2008) Ectomycorrhizal characterization of an American chestnut (Castanea dentate)-dominated community in western Wisconsin. Mycorrhiza 19:27–36. https://doi.org/10.1007/s00572-008-0200-7

    Article  PubMed  Google Scholar 

  • Parra LA (2013) FungiEuropaei, Agaricus L.: Allopsalliota, Nauta & Bas (Parte II), Candusso Edizioni.

  • Parra LA, Angelini C, Ortiz-Santana B, Mata G, Billette C, Rojo C, Chen J, Callac P (2018) The genus Agaricus in the Caribbean. Nine new taxa mostly based on collections from the Dominican Republic. Phytotaxa 345:219–271. 10.11646/phytotaxa.345.3.2

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Rambaut A, Suchard MA, Xie D, Drummond A (2014) Tracer v1.6. Available from http:// beast.bio.ed.ac.uk/Tracer. .

  • 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

    CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thongklang N, Nawaz R, Khalid AN, Chen J, Hyde KD, Zhao RL, Parra LA, Hanif M, Moinard M, Callac P (2014) Morphological and molecular characterization of three Agaricus species from tropical Asia (Pakistan, Thailand) reveals a new group in section Xanthodermatei. Mycologia 106:1220–1232. https://doi.org/10.3852/14-076

    Article  CAS  PubMed  Google Scholar 

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Zhao R-L, Karunarathna SC, Raspé O, Parra LA, Guinberteau J, Moinard M, De Kesel A, Barroso G, Courtecuisse R, Hyde KD, Guelly AK, Desjardin ED, Callac P (2011) Major clades in tropical Agaricus. Fungal Divers 51:279–296. https://doi.org/10.1007/s13225-011-0136-7

    Article  Google Scholar 

  • Zhao RL, Zhou JL, Chen J, Margaritescu S, Sánchez-Ramírez S, Hyde KD, Callac P, Parra LA, Li GJ, Moncalvo JM (2016) Towards standardizing taxonomic ranks using divergence times–a case study for reconstruction of the Agaricus taxonomic system. Fungal Divers 78:239–292. https://doi.org/10.1007/s13225-016-0357-x

    Article  Google Scholar 

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Acknowledgements

Thanks to Nabil Al Dhanki, Saif Al Salami, Mohammed Al Jahwari, and Ibrahim Al Sabahi (Sultan Qaboos University, Oman) for their help in the collection of mushroom specimens.

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Funding

Financial support to the project came from the Oman Animal and Plant Genetic Resources Centre and Sultan Qaboos University (CR/AGR/CROP/19/01).

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SH, MA, MAA, DA, and ZA performed the experiment and the data analyses and wrote the manuscript. AHA, MNA, NA, RA, RV, and AMA designed the experiments and helped perform the analysis and provided help in writing the reviewing the final manuscript.

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Correspondence to Abdullah M. Al-Sadi.

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Section Editor: Zhu-Liang Yang

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Hussain, S., Al-Kharousi, M., Al-Muharabi, M.A. et al. Phylogeny of Agaricus subgenus Pseudochitonia with the description of a new section and a new species from Oman. Mycol Progress 21, 72 (2022). https://doi.org/10.1007/s11557-022-01819-8

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