Abstract
In recent studies, new species and sections were described in Agaricus subg. Spissicaules. We intended to update this subgenus by including all these recent taxa, some interesting sequences retrieved in GenBank, and two new collections from the Punjab Province, Pakistan. Both morphological and phylogenetic approaches were used. Maximum Likelihood tree based on rDNA ITS sequences revealed that the sequences of the new specimens from Pakistan form a clade with five sequences from India retrieved from GenBank. For the seven samples of this clade, we described the new species Agaricus radiatosquamulosus based on the morphology of the two collections from Pakistan. This new species, which belongs to the recently proposed A. sect. Fulventes was compared to the three other species of this section. Except for the small-sized A. nanofulvus, the other species are difficult to recognize without DNA sequence data. The four species differ from each other at a poly T in ITS2. In addition, each of them is distributed on different continents. Agaricus radiatosquamulosus is the first report of a species of A. subg. Spissicaules in Pakistan. In addition, a sequence from GenBank identified as A. lanatoniger matches with another sample from New Zealand in A. sect. subrutilescentes. In absence of formally published taxonomic treatment, we provisionally named these samples A. cf. lanatoniger.
References
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<p>Bashir, H., Hussain, S., Khalid, A.N., Niazi, A.R., Parra, L.A. & Callac, P. (2018). First report of <em>Agaricus</em> sect. <em>Brunneopicti</em> from Pakistan with descriptions of two new species. <em>Phytotaxa</em> 357 (3): 167–178. https://doi.org/10.11646/phytotaxa.357.3.1</p>
<p>Callac, P. & Chen, J. (2018) Tropical species of Agaricus. <em>In</em>: Sánchez, J.E., Mata, G. & Royse, D.J. (Eds.) <em>Updates on tropical mushrooms</em>. Basic and applied research. San Cristobal de Las Casas, Chiapas, pp. 25–38.</p>
<p>Chen, J., Parra, L.A., Kesel, A.D., Khalid, A.N., Qasim. T., Ashraf, A., Bahkali, A.H., Hyde, K.D., Zhao, R.-L. & Callac, P. (2016) Inter- and intra-specific diversity in <em>Agaricus</em> <em>endoxanthus</em> and allied species reveals a new taxon, <em>A. punjabensis</em>. <em>Phytotaxa</em> 252 (1): 1–16. https://doi.org/10.11646/phytotaxa.252.1.1</p>
<p>Chen, J., Callac, P., Parra, L.A., Karunarathna, S.C., He, M.Q., Moinard, M., De Kesel, A., Raspé, O., Wisitrassameewong, K., Hyde, K.D. & Zhao, R.L. (2017) Study in <em>Agaricus</em> subgenus <em>Minores</em> and allied clades reveals a new American subgenus and contrasting phylogenetic patterns in Europe and Greater Mekong Subregion. <em>Persoonia</em> 38: 170–196. https://doi.org/10.3767/003158517X695521</p>
<p>Dai, R.C., Li, G.J., He, M.Q., Liu, R.L., Ling, Z.L., Wu, J.R. & Zhao, R.L. (2016) Characterization of four species including one new species of Agaricus subgenus Spissicaules from Eastern China. <em>Mycosphere</em> 7: 405–416. https://doi.org/10.5943/mycosphere/7/4/2</p>
<p>Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes, application to the identification of mycorrhizae and rusts. <em>Moleculer Ecology </em>2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x</p>
<p>Guinberteau, J. (2017) On the discovery of a new agaric of section <em>Spissicaules</em> Heinem. Kerrigan: <em>Agaricus bellanniae</em> Guinb., Kerrigan and M. Kuo, with an amphi-Atlantic distribution. <em>Bulletin Semestriel de la Fédération des Associations Mycologiques Méditerranéennes</em> 51: 7–22 .</p>
<p>Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. <em>Nucleic Acids Symposium Series</em> 45: 95–98.</p>
<p>He, M.Q., Hyde, K.D., Wei, S.L., Xi, Y.L., Cheewangkoon, R. & Zhao, R.L. (2018a) Three new species of <em>Agaricus</em> section <em>Minores</em> from China. <em>Mycosphere</em> 9: 189–201. https://doi.org/10.5943/mycosphere/9/2/3</p>
<p>He, M.Q., Chuankid, B., Hyde, K.D., Cheewangkoon, R. & Zhao, R.L. (2018b) A new section and species of <em>Agaricus</em> subgenus <em>Pseudochitonia</em> from Thailand. <em>MycoKeys </em>40: 53–67. https://doi.org/10.3897/mycokeys.40.26918</p>
<p>Heinemann, P. (1956) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II <em>Agaricus</em> Fr ss. <em>Bulletin du Jardin botanique de l’eìtat, Bruxelles</em> 26: 1–127. https://doi.org/10.2307/3667096</p>
<p>Heinemann, P. (1974) Quelques Agaricus de Nouvelle-Zélande. <em>Bulletin du Jardin botanique national de Belgique/Bulletin van de Nationale Plantentuin van Belgie</em>, pp. 355–366. https://doi.org/10.2307/3667677</p>
<p>Heinemann, P. (1978) Essai d’une clé de détermination des genres <em>Agaricus</em> et <em>Micropsalliota</em>. <em>Sydowia</em> 30: 6–37.</p>
<p>Karunarathna, S.C., Chen, J., Mortimer, P.E., Xu, J.C., Zhao, R.L., Callac, P. & Hyde, K.D. (2016) Mycosphere Essay 8: A review of genus <em>Agaricus</em> in tropical and humid subtropical regions of Asia. <em>Mycosphere</em> 7: 417–439. https://doi.org/10.5943/mycosphere/7/4/3</p>
<p>Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. <em>Molecular biology and evolution</em> 30: 772–780. https://doi.org/10.1093/molbev/mst010</p>
<p>Kerrigan, R.W. (1985) Studies in Agaricus II. <em>Agaricus lilaceps</em> reevaluated. <em>Mycologia</em> 77: 137–141. https://doi.org/10.1080/00275514.1985.12025072</p>
<p>Kerrigan, R.W. (2016) <em>Agaricus of North America. Memoirs of the New York Botanical Garden</em>, vol 114. The New York Botanical Garden Press, New York, 574 pp.</p>
<p>Lebel, T. & Syme, A. (2012) Sequestrate species of <em>Agaricus</em> and <em>Macrolepiota</em> from Australia: new species and combinations and their position in a calibrated phylogeny. <em>Mycologia</em> 104: 496–520. https://doi.org/10.3852/11-092</p>
<p>Ling, Z.L., Zhou, J.L., Parra, L.A., DeKesel, A., Callac, P., Cao, B. He, M.-Q. & Zhao, R.-L. (2021) Four new species of <em>Agaricus</em> subgenus <em>Spissicaules</em> from China. <em>Mycologia</em> 113: 476–491. https://doi.org/10.1080/00275514.2020.1852808</p>
<p>Munsell, Color Co. (1975) <em>Munsell Soil Color Charts. Baltimore</em>. MD, Munsell Color Co., USA.</p>
<p>Ortiz-Santana, B., Chen, J., Parra, L.A., Angelini, C., Lodge, D.J. Kerrigan, R.W. & Callac, P. (2021) The genus <em>Agaricus</em> in the Caribbean II. Refined phylogeny of <em>Agaricus</em> subg. <em>Spissicaules</em> with description of two new sections and eight new species. <em>Mycological Progress</em> 20: 381–411. https://doi.org/10.1007/s11557-021-01686-9</p>
<p>Parra, L.A. (2008) <em>Agaricus L., Allopsalliota Nauta & Bas. Fungi Europaei</em> 1. Edizioni Candusso, Alassio, Italy.</p>
<p>Parra, L.A., Angelini, C., Ortiz-Santana, B., Mata, G., Billette, C., Rojo, C., Chen, J. & Callac, P. (2018) The genus <em>Agaricus</em> in the Caribbean. Nine new taxa mostly based on collections from the Dominican Republic. <em>Phytotaxa</em> 345 (3): 219–271. https://doi.org/10.11646/phytotaxa.345.3.2</p>
<p>Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. <em>Bioinformatics</em> 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033</p>
<p>Thongklang, N., Nawaz, R., Khalid, A.N., Chen, J. & Hyde, K.D. (2014) Morphological and molecular characterization of three <em>Agaricus</em> species from tropical Asia (Pakistan, Thailand) reveals a new group in section <em>Xanthodermatei</em>. <em>Mycologia </em>106: 1220–1232. https://doi.org/10.3852/14-076</p>
<p>Vu, D., Groenewald, M., De Vries, M., Gehrmann, T., Stielow, B., Eberhardt, U., Al-Hatmi, A., Groenewald, J.Z., Cardinali, G., Houbraken, J., Boekhout, T., Crous, P.W., Robert, V. & Verkley, G.J.M. (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. <em>Studies in Mycology</em> 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001</p>
<p>White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenies. <em>In</em>: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) <em>PCR protocols: a guide to methods and applications.</em> Academic Press, San Diego, pp. 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1</p>
<p>Zereen, A., Khan, Z.U.D. & Sardar, A.A. (2015) An Assessment and Documentation of Conventional Medico-Botanical Knowledge of Indigenous Communities Around Chichawatni Plantation Reserved Forest. <em>The Pharmaceutical and Chemical Journal</em> 2 (4): 27–35.</p>
<p>Zhao, R.L., Karunarathna, S., Raspé, O., Parra, L.A., Guinberteau, J., Moinard, M., Kesel, A.D., Barroso, G., Courtecuisse, R., Hyde, K.D., Guelly, A.K., Desjardin, D.E. & Callac, P. (2011) Major clades in tropical Agaricus. <em>Fungal Diversity</em> 51: 279–296. https://doi.org/10.1007/s13225-011-0136-7</p>
<p>Zhao, R.L., Zhou, J.L., Chen, J., Margaritescu, S., Sánchez-Ramírez, S., Hyde, K.D., Callac, P., Parra, L.A., Li, G.J. & Moncalvo, J.M. (2016) Towards standardizing taxonomic ranks using divergence times-a case study for reconstruction of the Agaricus taxonomic system. <em>Fungal Diversity</em> 78: 239–292. https://doi.org/10.1007/s13225-016-0357-x</p>
<p>Arya, C.P., Kumar, A.M., Pradeep, C.K. & Parra, L.A. (2022) <em>Agaricus brunneodiscus</em>, a new species of <em>Agaricus</em> section <em>Rarolentes</em> from India<em>. Phytotaxa</em> 533 (4): 181–193. https://doi.org/10.11646/phytotaxa.533.4.1</p>
<p>Baig, S., Qazi, W., Akhtar, A.M., Waqar, M.M., Ammar, A., Gilani, H. & Mehmood, S.A. (2017) Above ground biomass estimation of <em>Dalbergia sissoo</em> forest plantation from dual-polarized ALOS-2 PALSAR data. <em>Canadian Journal of Remote Sensing</em> 43 (3): 297–308. https://doi.org/10.1080/07038992.2017.1330143</p>
<p>Bashir, H., Chen, J., Jabeen, S., Ullah, S., Khan, J., Niazi, A.R., Zhang, M., Khalid, A.N., Parra, L.A. & Callac, P. (2021) An overview of <em>Agaricus</em> section <em>Hondenses</em> and <em>Agaricus </em>section <em>Xanthodermatei </em>with description of eight new species from Pakistan. <em>Scientific Reports</em> 11: 1–35. https://doi.org/10.1038/s41598-021-92261-5</p>
<p>Bashir, H., Hussain, S., Khalid, A.N., Niazi, A.R., Parra, L.A. & Callac, P. (2018). First report of <em>Agaricus</em> sect. <em>Brunneopicti</em> from Pakistan with descriptions of two new species. <em>Phytotaxa</em> 357 (3): 167–178. https://doi.org/10.11646/phytotaxa.357.3.1</p>
<p>Callac, P. & Chen, J. (2018) Tropical species of Agaricus. <em>In</em>: Sánchez, J.E., Mata, G. & Royse, D.J. (Eds.) <em>Updates on tropical mushrooms</em>. Basic and applied research. San Cristobal de Las Casas, Chiapas, pp. 25–38.</p>
<p>Chen, J., Parra, L.A., Kesel, A.D., Khalid, A.N., Qasim. T., Ashraf, A., Bahkali, A.H., Hyde, K.D., Zhao, R.-L. & Callac, P. (2016) Inter- and intra-specific diversity in <em>Agaricus</em> <em>endoxanthus</em> and allied species reveals a new taxon, <em>A. punjabensis</em>. <em>Phytotaxa</em> 252 (1): 1–16. https://doi.org/10.11646/phytotaxa.252.1.1</p>
<p>Chen, J., Callac, P., Parra, L.A., Karunarathna, S.C., He, M.Q., Moinard, M., De Kesel, A., Raspé, O., Wisitrassameewong, K., Hyde, K.D. & Zhao, R.L. (2017) Study in <em>Agaricus</em> subgenus <em>Minores</em> and allied clades reveals a new American subgenus and contrasting phylogenetic patterns in Europe and Greater Mekong Subregion. <em>Persoonia</em> 38: 170–196. https://doi.org/10.3767/003158517X695521</p>
<p>Dai, R.C., Li, G.J., He, M.Q., Liu, R.L., Ling, Z.L., Wu, J.R. & Zhao, R.L. (2016) Characterization of four species including one new species of Agaricus subgenus Spissicaules from Eastern China. <em>Mycosphere</em> 7: 405–416. https://doi.org/10.5943/mycosphere/7/4/2</p>
<p>Gardes, M. & Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes, application to the identification of mycorrhizae and rusts. <em>Moleculer Ecology </em>2: 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x</p>
<p>Guinberteau, J. (2017) On the discovery of a new agaric of section <em>Spissicaules</em> Heinem. Kerrigan: <em>Agaricus bellanniae</em> Guinb., Kerrigan and M. Kuo, with an amphi-Atlantic distribution. <em>Bulletin Semestriel de la Fédération des Associations Mycologiques Méditerranéennes</em> 51: 7–22 .</p>
<p>Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. <em>Nucleic Acids Symposium Series</em> 45: 95–98.</p>
<p>He, M.Q., Hyde, K.D., Wei, S.L., Xi, Y.L., Cheewangkoon, R. & Zhao, R.L. (2018a) Three new species of <em>Agaricus</em> section <em>Minores</em> from China. <em>Mycosphere</em> 9: 189–201. https://doi.org/10.5943/mycosphere/9/2/3</p>
<p>He, M.Q., Chuankid, B., Hyde, K.D., Cheewangkoon, R. & Zhao, R.L. (2018b) A new section and species of <em>Agaricus</em> subgenus <em>Pseudochitonia</em> from Thailand. <em>MycoKeys </em>40: 53–67. https://doi.org/10.3897/mycokeys.40.26918</p>
<p>Heinemann, P. (1956) Champignons récoltés au Congo Belge par Mme M Goossens-Fontana, II <em>Agaricus</em> Fr ss. <em>Bulletin du Jardin botanique de l’eìtat, Bruxelles</em> 26: 1–127. https://doi.org/10.2307/3667096</p>
<p>Heinemann, P. (1974) Quelques Agaricus de Nouvelle-Zélande. <em>Bulletin du Jardin botanique national de Belgique/Bulletin van de Nationale Plantentuin van Belgie</em>, pp. 355–366. https://doi.org/10.2307/3667677</p>
<p>Heinemann, P. (1978) Essai d’une clé de détermination des genres <em>Agaricus</em> et <em>Micropsalliota</em>. <em>Sydowia</em> 30: 6–37.</p>
<p>Karunarathna, S.C., Chen, J., Mortimer, P.E., Xu, J.C., Zhao, R.L., Callac, P. & Hyde, K.D. (2016) Mycosphere Essay 8: A review of genus <em>Agaricus</em> in tropical and humid subtropical regions of Asia. <em>Mycosphere</em> 7: 417–439. https://doi.org/10.5943/mycosphere/7/4/3</p>
<p>Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. <em>Molecular biology and evolution</em> 30: 772–780. https://doi.org/10.1093/molbev/mst010</p>
<p>Kerrigan, R.W. (1985) Studies in Agaricus II. <em>Agaricus lilaceps</em> reevaluated. <em>Mycologia</em> 77: 137–141. https://doi.org/10.1080/00275514.1985.12025072</p>
<p>Kerrigan, R.W. (2016) <em>Agaricus of North America. Memoirs of the New York Botanical Garden</em>, vol 114. The New York Botanical Garden Press, New York, 574 pp.</p>
<p>Lebel, T. & Syme, A. (2012) Sequestrate species of <em>Agaricus</em> and <em>Macrolepiota</em> from Australia: new species and combinations and their position in a calibrated phylogeny. <em>Mycologia</em> 104: 496–520. https://doi.org/10.3852/11-092</p>
<p>Ling, Z.L., Zhou, J.L., Parra, L.A., DeKesel, A., Callac, P., Cao, B. He, M.-Q. & Zhao, R.-L. (2021) Four new species of <em>Agaricus</em> subgenus <em>Spissicaules</em> from China. <em>Mycologia</em> 113: 476–491. https://doi.org/10.1080/00275514.2020.1852808</p>
<p>Munsell, Color Co. (1975) <em>Munsell Soil Color Charts. Baltimore</em>. MD, Munsell Color Co., USA.</p>
<p>Ortiz-Santana, B., Chen, J., Parra, L.A., Angelini, C., Lodge, D.J. Kerrigan, R.W. & Callac, P. (2021) The genus <em>Agaricus</em> in the Caribbean II. Refined phylogeny of <em>Agaricus</em> subg. <em>Spissicaules</em> with description of two new sections and eight new species. <em>Mycological Progress</em> 20: 381–411. https://doi.org/10.1007/s11557-021-01686-9</p>
<p>Parra, L.A. (2008) <em>Agaricus L., Allopsalliota Nauta & Bas. Fungi Europaei</em> 1. Edizioni Candusso, Alassio, Italy.</p>
<p>Parra, L.A., Angelini, C., Ortiz-Santana, B., Mata, G., Billette, C., Rojo, C., Chen, J. & Callac, P. (2018) The genus <em>Agaricus</em> in the Caribbean. Nine new taxa mostly based on collections from the Dominican Republic. <em>Phytotaxa</em> 345 (3): 219–271. https://doi.org/10.11646/phytotaxa.345.3.2</p>
<p>Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. <em>Bioinformatics</em> 30: 1312–1313. https://doi.org/10.1093/bioinformatics/btu033</p>
<p>Thongklang, N., Nawaz, R., Khalid, A.N., Chen, J. & Hyde, K.D. (2014) Morphological and molecular characterization of three <em>Agaricus</em> species from tropical Asia (Pakistan, Thailand) reveals a new group in section <em>Xanthodermatei</em>. <em>Mycologia </em>106: 1220–1232. https://doi.org/10.3852/14-076</p>
<p>Vu, D., Groenewald, M., De Vries, M., Gehrmann, T., Stielow, B., Eberhardt, U., Al-Hatmi, A., Groenewald, J.Z., Cardinali, G., Houbraken, J., Boekhout, T., Crous, P.W., Robert, V. & Verkley, G.J.M. (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. <em>Studies in Mycology</em> 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001</p>
<p>White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenies. <em>In</em>: Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds.) <em>PCR protocols: a guide to methods and applications.</em> Academic Press, San Diego, pp. 315–322. https://doi.org/10.1016/b978-0-12-372180-8.50042-1</p>
<p>Zereen, A., Khan, Z.U.D. & Sardar, A.A. (2015) An Assessment and Documentation of Conventional Medico-Botanical Knowledge of Indigenous Communities Around Chichawatni Plantation Reserved Forest. <em>The Pharmaceutical and Chemical Journal</em> 2 (4): 27–35.</p>
<p>Zhao, R.L., Karunarathna, S., Raspé, O., Parra, L.A., Guinberteau, J., Moinard, M., Kesel, A.D., Barroso, G., Courtecuisse, R., Hyde, K.D., Guelly, A.K., Desjardin, D.E. & Callac, P. (2011) Major clades in tropical Agaricus. <em>Fungal Diversity</em> 51: 279–296. https://doi.org/10.1007/s13225-011-0136-7</p>
<p>Zhao, R.L., Zhou, J.L., Chen, J., Margaritescu, S., Sánchez-Ramírez, S., Hyde, K.D., Callac, P., Parra, L.A., Li, G.J. & Moncalvo, J.M. (2016) Towards standardizing taxonomic ranks using divergence times-a case study for reconstruction of the Agaricus taxonomic system. <em>Fungal Diversity</em> 78: 239–292. https://doi.org/10.1007/s13225-016-0357-x</p>