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. 2022 Jul 20;10:1–18. doi: 10.3114/fuse.2022.10.01

Four new nodulose-spored species of Inocybe (Agaricales) from West Africa

HL Aïgnon 1,*, S Jabeen 2, A Verbeken 3, PB Matheny 4, NS Yorou 1, M Ryberg 5
PMCID: PMC9903347  PMID: 36789280

Abstract

We describe four new nodulose-spored species of Inocybe from tropical regions of Africa: I. beninensis, I. flavipes, I. fuscobrunnea and I. pallidiangulata. The new species are recognised based on morphological data and phylogenetic analyses of ITS, 28S and RPB2 sequences. Phylogenetic analyses indicated that I. flavipes and I. beninensis are part of a subclade leading to the I. calida group. Inocybe fuscobrunnea appears sister to the I. asterospora group. Inocybe pallidiangulata is nested within a clade of mainly tropical species from South Asia, Africa, and South America, close to the subclade of I. lilacinosquamosa and I. ayangannae from Guyana. Complete descriptions and illustrations, including photographs and line drawings, and a key to nodulose-spored taxa of tropical African species of Inocybe are provided.

Citation: Aïgnon HL, Jabeen S, Verbeken A, Matheny PB, Yorou NS, Ryberg M (2022). Four new nodulose-spored species of Inocybe (Agaricales) from West Africa. Fungal Systematics and Evolution 10: 1–18. doi: 10.3114/fuse.2022.10.01

Keywords: Agaricomycetes, ectomycorrhizal fungi, Inocybaceae, molecular phylogeny, new taxa, systematics, taxonomy

INTRODUCTION

Inocybe is the most diverse genus in the Inocybaceae with 850 species described worldwide (Matheny et al. 2020), but this number has increased as more areas are intensively studied and new species described (Matheny & Bougher 2017, Matheny & Kudzma 2019, Bandini & Oertel 2020, Caiafa et al. 2021). While competing infrageneric classification systems are available based on morphological analyses (Kuyper et al. 1986, Singer 1986, Bon 1997, 1998), these classifications are a poor representation of the phylogenetic relations within the group. For example, nodulose-spored species of the genus do not form a monophyletic group (Matheny et al. 2002, Matheny 2005, Kropp et al. 2010, Ryberg et al. 2010, Esteve-Raventós et al. 2016).

Anatomically, species of Inocybe are distinguished from those belonging to other genera of the family by possession of pleurocystidia and/or angular, nodulose, or spinose basidiospores, often with a distinct apiculus (Matheny et al. 2020). Some subgroups of Inocybe lack caulocystidia, whereas others possess them near the apex or along the entire length of the stipe correlated with the presence/absence of a partial veil (Kuyper 1986).

Despite progress to assess the diversity of Inocybe in many parts of the world, African regions remain poorly explored (Aïgnon et al. 2021a). To date, only four nodulose-spored species of Inocybe have been recorded from Africa. Hennings (1902) described I. cyaneovirescens, from what used to be called “German East Africa”, which today encompasses the nations of Burundi, Rwanda and continental region of Tanzania. Pegler (1969) described I. ghanaensis from West Africa (Ghana). Lastly, Buyck & Eyssartier (1999) described two species I. conspicuospora and I. glaucodisca from Zambia. In addition to these, two studies published sequence data from several undescribed species from Zambia (Matheny et al. 2009, Tedersoo et al. 2011). In recent years, eight Inocybe species were recorded from Morocco (Ouabbou et al. 2014, Akil et al. 2015). Recently, Aïgnon et al. (2021b) estimated that approximately 62 species of Inocybe occur in Africa.

According to Matheny et al. (2020), certain regions such as Mediterranean types of habitats in North America and Australia are predominantly rich in species of Inocybe with smooth spores (Nishida 1989, Matheny & Bougher 2017), but tropical regions have accumulated a diverse assemblage of species with angular-nodulose spores (Matheny et al. 2003, Horak et al. 2015). This seems indeed to be the case in tropical Africa where we discovered four new species of Inocybe, all with angular-nodulose spores. Detailed descriptions and illustrations, as well as comparisons with closely related species, are provided. A key to nodulose-spored species of Inocybe from tropical Africa is also provided.

MATERIAL AND METHODS

Study area and specimen sampling

Specimens were collected between 2013 and 2018 in Benin, Burkina Faso, Ivory Coast and Togo. Collections were made in woodlands, with more than 10 % woody cover, including shrublands with a canopy only 2 m high, and that were dominated by ectomycorrhizal trees of Euphorbiaceae, Fabaceae and Phyllanthaceae. Colour codes of fresh specimens were recorded with the Online Auction Colour chart (2004). After labelling and recording morphological data, specimens were preserved by drying using an electric dryer (type Stöckli Dörrex) for 24 h at 45 °C. All studied materials, including the holotypes were deposited at the Mycological Herbarium of Parakou University, Benin Republic (UNIPAR).

Morphological and anatomical analyses

Fine sections from the dried basidiomata were rehydrated and examined in 3 % KOH and Congo Red for microscopic investigation. Drawings of microscopic characters were made with the aid of a drawing tube attached to a Leica DM2700 light microscope. Microscopic characters were drawn at 1000× magnification. For each species, spore measurements were made from 40 spores. We measured length (L) and width (W) of the basidiospores and calculated the ratio Q = L/W. Measurements of basidiospores and basidia excluded the apiculus and sterigmata, and spore dimensions included nodules. Spore measurements are given as (a–)b–c(–d), where (a) = extreme minimum value, range b–c contains minimum of 90 % of the calculated values and (d) = extreme maximum value following Aïgnon et al. (2021a, c).

Molecular analyses

DNA extraction, PCR and sequencing: Genomic DNA was extracted from dried specimens by a QIAGEN® plant mini kit. The ITS, parts of 28S, and RPB2 were amplified. For the ITS region, we produced amplicons using primers pairs ITS1F and ITS4 (White et al. 1990, Gardes & Bruns 1993). For the 28S region, we used the LR0R, LR7, LR5 and LR3R primers (Vilgalys & Hester 1990, Cubeta et al. 1991, Rehner & Samuels 1995) and for the RPB2 region, primer pairs b6F and b7.1R (Matheny 2005) were used. PCR products were purified and sequenced at Macrogen Inc. (Netherlands) using the same primers as those used for PCR. We refer to Aignon et al. (2021a, c) for detailed methods of the DNA extraction and amplification.

Sequence alignment and phylogenetic analyses: New sequences derived in this study were compared with closely related Inocybe sequences that were retrieved from GenBank (Benson et al. 2010). Species of different groups, clades and sections of Inocybe such as I. praetervisa group, I. mixtilis group, I. napipes group, I. xanthomelas group, I. diabolica group, I. lacera group, I. lanuginosa group, I. giacomi group, Smooth-spored temperate boreal clade, Smooth-spored temperate boreal clade and Sect. Inocybe were selected on the basis of a literature survey (Ryberg et al. 2008, Horak et al. 2015, Matheny & Bougher 2017, Matheny et al. 2017, Latha & Manimohan 2017, Esteve-Raventós et al. 2018, Bandini et al. 2019, Cripps et al. 2019, Matheny et al. 2020). Sequences of the different regions (ITS, 28S and RPB2) were aligned separately using MAFFT v. 7.464 (Katoh et al. 2019), and a final concatenated data set of ITS, 28S and RPB2 was generated using Geneious v. 7.0.2 software (Biometer, Auckland, New Zealand). The dataset was partitioned into ITS + 28S, RPB2 codon position 1 + RPB2 codon position 2 and RPB2 codon position 3 + the intron in RPB2 separately. For phylogenetic analyses, the substitution models and the best partitioning schemes were determined for both Maximum Likelihood (ML) and Bayesian Inference (BI). The substitution models for each locus were determined based on the AICc model selection criterion as implemented in PartitionFinder (Lanfear et al. 2016).

Maximum Likelihood analyses were performed with IQ-TREE v. 1.6.12 (Nguyen et al. 2015). Ultrafast bootstrapping (UFBoot) was done with 1 000 replicates (Hoang et al. 2017). BI analyses were performed in MrBayes v. 3.2.7a (Ronquist et al. 2012) using a GTR+I+G model at the Cipres Science Gateway (Miller et al. 2010). Two independent Markov Chain Monte Carlo (MCMC) were run in parallel, each with four chains for 20 M generations. Posterior probabilities (BPP) were calculated after discard the first 25 % samples from the cold chain by default. Sequences of Nothocybe distincta were used for rooting purposes based on Matheny et al. (2020). Nodes that received bootstrap proportions, ≥ 80 % of SHaLRT support, ≥ 95 % of UFBoot support and > 0.95 of BPP support were considered strongly supported, and nodes that met the criteria for strong support for at least one, but not all three of the methods, were considered moderately supported. Phylogenetic reconstructions for gene regions (ITS+28S, RPB2) was also performed separately with IQ-TREE v. 1.6.12.

RESULTS

Phylogenetic analysis

This study generated 17 new sequences submitted to GenBank (Table 1). The new species named Inocybe beninensis failed to yield any RPB2 amplicons. In the dataset, the ITS partition included 150 taxa and 925 sites, the 28S partition included 163 taxa and 1 529 sites and RPB2 included 85 taxa and 782 sites. Individual gene tree phylogenies (ITS+28S and RPB2) are shown in Supplementary Figs S1, S2. No strongly supported conflict was observed. Phylogenetic analyses of ITS, 28S and RPB2 sequences data supported the distinction of four novel nodulose-spored Inocybe from tropical regions of Africa described below as I. beninensis sp. nov., I. flavipes sp. nov., I. fuscobrunnea sp. nov. and I. pallidiangulata sp. nov. All four new species were well-separated from sister species, and separate collections of the same species formed well supported clades with short internal branches in ML and BI analyses (Fig. 1).

Table 1.

List of taxa used in the molecular analyses along with vouchers, GenBank accession numbers and geographic origin. The new species and their accession numbers are in bold.

Species Voucher Country GenBank accession no.
References
ITS 28S RPB2
Inocybe acanthosperma Matheny & Bougher PBM3773 Australia KJ729861 KJ729889 KJ729923 Matheny et al. (2017)
I. acuta Boud TURA:5066 Finland KP171102 KM197208 n/a Unpublished
I. aff. asterospora Quél PBM2453, PBM-2014 USA DQ404390 AY702015 n/a Kuo & Matheny (2015)
I. aff. diabolica Vauras PBM2976 USA n/a KP170948 KM246001 Horak et al. (2015)
I. aff. xanthomelas Boursier & Kühner PAM06060405, TENN063834 France HQ586867 HQ641109 n/a Horak et al. (2015)
I. alpinomarginata C.L. Cripps, E. Larss.& Vauras CLC1303 USA MK153644 MK153644 n/a Cripps et al. (2019)
I. ambigua Romagn BJ910730 Sweden AM882800 AM882800 n/a Ryberg et al. (2008)
I. angustifolia (Corner & E. Horak) Garrido DED8139 Thailand GQ892988 GQ892942 MH577422 Horak et al. (2015)
I. antoniniana E. Sesli, Bandini & Krisai Fungi 4064 Turkey MN988712 n/a n/a Bandini et al. (2020b)
I. appendiculata Kühner SAT0026155 USA n/a JN974946 MH577432 Ryberg & Matheny (2012)
I. arctica E. Larss., Vauras & C.L. Cripps JV2238 Norway KY033843 KY033843 n/a Larsson et al. (2017)
I. argenteolutea Vauras EL9906 Sweden FN550889 FN550889 n/a Ryberg et al. (2010)
I. asterospora Quél EL100-14 Sweden MN296110 MN296110 n/a Cripps et al. (2019)
I. ayangannae Matheny, Aime & T.W. Henkel MCA 1232 Guyana n/a AY239018 AY337364 Matheny et al. (2009)
I. babruka K.P.D. Latha & Manim. CAL 1344 India KY440086 KY549116 KY553237 Latha & Manimohan (2017)
I. baltica Vauras & E. Larss. EL50-09 Svalbard KY033838 KY033838 n/a Larsson et al. (2017)
I. beninensis Aïgnon, Yorou & Ryberg HLA0390 Benin MN096196 MN097888 n/a This study
HLA0467 Benin MT994602 n/a n/a
I. bombina Bandini & B. Oertel KR-M-0043212 Germany MK929261 n/a n/a Bandini et al. (2019)
I. botaurina Bandini & B. Oertel DB1-6-12-1 Germany MK929259 n/a n/a Bandini et al. (2019)
I. brevisquamulosa E. Horak, Matheny & Desjardin ZT10102 Thailand NR_153123 GQ892974 n/a Horak et al. (2015)
I. brunneolipes Grund & D.E. Stuntz DG1863 Canada KY923032 NG_057289 n/a Unpublished
I. cacaocolor Matheny & Bougher PBM3790 Australia KJ778845 KJ756464 KJ756422 Matheny et al. (2017)
I. calida Valen TAA185175 Estonia AM882760 AM882760 n/a Ryberg et al. (2008)
I. calocephala Matheny & Bougher PBM3600 Australia n/a NG 057234 KJ756413 Matheny & Bougher (2017)
I. calospora f. pectinata Guinb PAM10082903 France KP171112 KP170900 n/a Unpublished
I. calospora Quél PAM08092808 France n/a KP170899 n/a Unpublished
I. calospora Quél PAM99082905 France HQ586871 HQ641114 n/a Unpublished
I. calospora Quél PAM10092501 France KP171113 KP170901 n/a Matheny et al. (2017)
I. calospora Quél PAM00073102 France HQ586853 HQ641093 n/a Unpublished
I. calospora Quél PAM03082401 France HQ586852 Q641094 n/a Unpublished
I. calospora Quél EL9505 Finland AM882759 AM882759 n/a Ryberg et al. (2008)
I. candidipes Kropp & Matheny BK 24-July-99-7 USA n/a AY239019 AY337366 Kropp & Matheny (2004)
I. caprimulgi Vauras & E. Larss. JV5808 Finland KT958924 KT958924 n/a Vauras & Larsson (2016)
I. cerasphora Singer BSI 01/184 Chile n/a AY380370 AY337367 Matheny (2005)
I. ceskae Bandini PBM 1315 USA n/a AY380387 AY337395 Matheny (2005)
I. cf. intricata Peck TENN:063834 France n/a KP170914 KM245990 Matheny & Bougher (2017)
I. cf. xanthomelas Boursier & Kühner EL3505 Norway AM882989 AM882989 n/a Ryberg et al. (2008)
I. chalcoceps Matheny & Bougher TENN:068946 Australia n/a NG 057228 n/a Matheny & Bougher (2017)
I. chondroderma D.E. Stuntz ex Matheny, Norvell & E.C. Giles PBM1776 USA GU949579 JN974967 MH249789 Matheny et al. (2013)
I. conspicuospora Buyck & Eyssart. PC 96042 Zambia n/a EU555471 EU555470 Matheny et al. (2009)
I. corydalina Quél TURA6488/AM10687 Belgium/Russia AY038314 AY337370 n/a Matheny et al. (2002)
I. curvipes P. Karst PBM 2401 USA n/a AY239022 AY337414 Matheny (2005)
I. diabolica Vauras EL9006 Sweden FN550896 FN550896 n/a Ryberg et al. (2010)
I. dunensis P.D. Orton EL22906 France FN550888 FN550888 n/a Unpublished
I. epidendron Matheny, Aime & T.W. Henkel MCA 1880, TH9186 Guyana JN168725 EU569840 n/a Matheny et al. (2009)
I. eriocaulis Matheny & Bougher PBM2132 Australia KJ778853 EU569843 EU569842 Matheny et al. (2009)
I. favrei Bon JV30673 Norway KY033798 KY033798 n/a Larsson et al. (2017)
I. fibrosa (sowerby) Gillet EL2599 Estonia AM882846 AM882846 n/a Ryberg et al. (2008)
I. flavipes Aïgnon, Yorou & Ryberg MR00383 Togo MN096197 MN097889 MW080915 This study
HLA0363 Benin MT994601 n/a n/a
L4512_Inoc_Zam05 Zambia FR731552 n/a n/a Tedersoo et al. (2011)
I. flavoalbida Matheny & Bougher PBM3768 Australia KJ729873 KJ729901 KJ729932 Matheny & Bougher (2017)
I. flavobrunnescens Esteve-Rav., G. Moreno & Bizio EL484-13 Spain MK153642 MK153642 n/a Esteve-Raventós et al. (2015)
I. flavosquamulosa C.K. Pradeep & Matheny CAL 1353 India KY440087 KY549117 KY553238 Latha & Manimohan (2017)
I. flavosquamulosa C.K. Pradeep & Matheny CAL 1355 India KY440088 KY549118 n/a Latha & Manimohan (2017)
I. floccosistipitata K.P.D. Latha & Manim. CAL 1256 India KY440089 KY549119 KY553239 Latha & Manimohan (2017)
I. fuligineoatra Huijsman PBM 2662 USA EU523589 EU307831 EU307833 Matheny et al. (2009)
I. fuscata Singer MES544 Chile KP171120 KP170909 KM245986 Horak et al. (2015)
I. fuscicothurnata Grund & D.E. Stuntz PBM3980 USA MF487844 KY990485 MF416408 Larsson et al. (2014)
I. fuscobrunnea Aïgnon, Yorou & Ryberg MR00378 Burkina Faso MN096201 MN097893 MW21933 This study
HLA0567 Ivory Coast MT994603 n/a n/a
I. giacomi J. Favre JV21543 Finland MK153656 MK153656 n/a Cripps et al. (2019)
I. glaucodisca Buyck & Eyssart. PC 96081 Zambia n/a EU569853 n/a Matheny et al. (2009)
I. godeyi Gillet JV 14914F Italy n/a AY038316 AY337378 Matheny et al. (2002)
I. gracilior E. Horak PDD:72707 New Zealand KY827277 KY827242 n/a Horak (2018)
I. griseovelata Kühner PBM2442 USA KC305453 JN974938 KC305420 Ryberg & Matheny (2012), Braaten et al. (2014)
I. hirculus Vauras JV30693 Finland MK153643 MK153643 n/a Cripps et al. (2019)
I. horakomyces Garrido PDD:72491 New Zealand KY827286 KY827251 n/a Horak (2018)
I. humidicola Matheny & Bougher PBM3719 Australia KP171126 KJ801181 KJ811575 Matheny & Bougher (2017)
I. hydrocybiformis (Corner & E. Horak) Garrido CAL 1376 India KY440090 KY549120 KY553240 Latha & Manimohan (2017)
I. hystrix (Fr.) P. Karst. SJ020824 Sweden AM882810 AM882810 n/a Ryberg et al. (2008)
I. impexa (Lasch) Kuyper TAA172127 Finland AM882821 AM882821 n/a Ryberg et al. (2008)
I. insulana K.P.D. Latha & Manim. CAL 1258 India KY440092 KY549122 KY553241 Latha & Manimohan (2017)
I. iringolkavensis K.P.D. Latha & Manim. K(M) 191731 India KM924524 KM924519 KY553242 Latha & Manimohan (2017)
I. johannis-stanglii Bandini, Esteve-Rav. & G. Moreno BAN959 KR M 0043321 Germany KX290793 n/a MH496019 Esteve-Raventós et al. (2018)
I. kapila K.P.D. Latha & Manim. CAL 1346 India KY440093 KY549123 n/a Latha & Manimohan (2017)
I. kohistanensis Jabeen, I. Ahmad & Khalid LAH 35001 Pakistan NR_153155 n/a n/a Jabeen et al. (2015)
I. krieglsteineri Fern. Sas. RFS031213-03 France KT958914 KT958914 n/a Kropp et al. (2010)
I. kurkuriya K.P.D. Latha & Manim. CAL 1352 India KY440095 KY549125 KY553245 Latha & Manimohan (2017)
I. kuruvensis K.P.D. Latha & Manim. K(M) 191734 India KM924522 KM924517 KY553246 Latha & Manimohan (2017)
I. lacera (Fr.) P. Kumm. PBM2541 USA KP171144 JN974993 KM245991 Ryberg & Matheny (2012)
I. lacunarum Vauras & E. Larss. JV12244 Finland KT958908 KT958908 n/a Vauras & Larsson (2015)
I. lanuginosa (Bull.) P. Kumm PBM3023/PBM3719 USA KP171126 KP170923 KM245992 Matheny et al. (2020)
I. lasseri Dennis MCA 1971 Guyana n/a EU569857 EU569856 Matheny et al. (2009)
I. lasseroides (E. Horak) Garrido PBM3749 Australia KP171145 KP170924 KM245993 Horak et al. (2015)
I. leptospermi (E. Horak) Garrido PBM3628 New Zealand KP308758 KP170935 KJ811592 Matheny & Bougher (2017)
I. lilacinosquamosa Matheny, Aime & T.W. Henkel MCA 1464 Guyana n/a AY380386 AY337389 Matheny et al. (2009)
I. lineata E. Horak, Matheny & Desjardin DED8048 Thailand n/a GQ892958 KM245999 Horak et al. (2015)
I. luteifolia A.H. Sm., PBM2642 USA n/a EU307814 EU307816 Kropp et al. (2010)
I. luteo-olivacea Matheny, Bougher & Halling NY:01491109 Australia KP308772 KP170946 KJ811603 Matheny & Bougher (2017)
I. melanopoda D.E. Stuntz 1954 PBM3975 USA n/a MH220276 MH249807 Matheny et al. (2020)
I. mendica E. Horak PDD:97864 New Zealand KP308780 KP170951 KM406193 Horak et al. (2015)
I. mixtilis (Britzelm.) Sacc. ARAN-Fungi 4711 Spain MH500842 MH500842 MH496022 Esteve-Raventós et al. (2018)
I. murina E. Larss., C.L. Cripps & Vauras CLC1226 USA MK153679 MK153679 n/a Cripps et al. (2019)
I. muthangensis K.P.D. Latha & Manim. K(M) 191735 India KM924521 KM924516 KY553247 Latha & Manimohan (2017)
I. napipes J.E. Lange PBM 2376 Norway n/a AY239024 AY337390 Matheny (2005)
I. nothomixtilis Esteve-Rav., Bandini & V. González AH 46558, MC0003 Spain, Italy MT384015 n/a MH496025 Kropp & Matheny (2004)
I. oblectabilis (Britzelm.) Sacc. BJ920908 Sweden AM882831 AM882831 n/a Ryberg et al. (2008)
I. obtusiuscula Kühner PAM02081710 France HQ586869 HQ641112 n/a Matheny & Bougher (2017)
I. occulta Esteve-Rav., Bandini, B. Oertel & G. Moreno AH 36443 Spain NR_160564 n/a MH496017 Esteve-Raventós et al. (2018)
I. ohenojae Vauras & E. Larss. ohenojae02081975 Canada KJ399955 KJ399955 n/a Larsson et al. (2014)
I. olivaceohinnulea Matheny & Bougher PBM3624 Australia KP308797 KP170965 KM406205 Matheny & Bougher (2017)
I. pallidiangulata Aïgnon, Yorou & Ryberg HLA0563 Burkina Faso MZ605435 n/a n/a This study
MR00377 Burkina Faso MN096202 MN097894 MW21932
MR00379 Burkina Faso MZ605434 n/a n/a
MR00384 Burkina Faso MZ605433 n/a n/a
I. pallidicremea Grund & D.E. Stuntz PBM2448 USA HQ201357 HQ201357 MF416425 Matheny et al. (2020)
I. papilliformis C.K. Pradeep & Matheny CAL 1372 India KY440096 KY549126 n/a Latha & Manimohan (2017)
I. paragiacomi E. Larss., C.L. Cripps & Vauras EL64-11 Sweden MK153670 MK153670 n/a Cripps et al. (2019)
I. parvibulbosa E. Horak, Matheny & Desjardin SFSU:DED8021 Thailand GQ892999 GQ892954 KM555134 Horak et al. (2015)
I. persicinipes Matheny & Bougher PBM2197/E7044 Australia KF977215 EU600837 EU600836 Matheny et al. (2009), Matheny & Bougher (2017)
I. phaeocystidiosa Esteve-Rav., G. Moreno & Bon, CLC1133 USA MK153630 MK153630 n/a Cripps et al. (2019)
I. phaeoleuca Kühner EL297-08 Hungary KJ399958 KJ399958 n/a Seress et al. (2016)
I. phaeosticta Furrer-Ziogas PAM05091310 France HQ586859 HQ641102 MH577435 Unpublished
I. pileosulcata E. Horak, Matheny & Desjardin CAL 1362 India KY440098 KY549128 n/a Latha & Manimohan (2017)
I. pileosulcata E. Horak, Matheny & Desjardin CAL 1368 India KY440099 KY549129 n/a Latha & Manimohan (2017)
I. pingala K.P.D. Latha & Manim. CAL 1345 India KY440100 KY549130 KY553248 Latha & Manimohan (2017)
I. pluppiana Bandini, B. Oertel & U. Eberh. SMNS-STU-F-0901254 Netherlands MN512327 MN512327 n/a Bandini et al. (2020a)
I. pluvialis Matheny, Bougher & G.M. Gates PBM3228 Australia KF871777 KF853401 KF891954 Matheny & Bougher (2017)
I. populea Takah. Kobay. & Courtec. TAKK15655 Japan KT958911 n/a n/a Kobayashi & Courtecuisse (2000)
Inocybe praetervisa Quél AH44415 Spain KT203793 KT203793 n/a Esteve-Raventós et al. (2015)
SF229598 Italy KT203792 n/a n/a
UBC:F19322 Canada HQ604397 HQ604397 n/a
UBC:F19334 Canada HQ604401 HQ604401 n/a
I. pseudodestricta Stangl & J. Veselský JV061030 Italy FN550908 FN550908 n/a Unpublished
I. pulchella Matheny, Aime & T.W. Henkel MCA 1122 Guyana n/a EU600842 n/a Matheny et al. (2009)
I. purpureobadia Esteve-Rav. & A. Caball. CLC 1205 USA MK153689 MK153689 n/a Cripps et al. (2019)
I. purpureoflavida K.B. Vrinda & C.K. Pradeep CAL 1379 India KY440101 KY549131 n/a Latha & Manimohan (2017)
I. rekhankitha K.P.D. Latha & Manim. CAL 1356 India KY440102 KY549132 n/a Latha & Manimohan (2017)
I. relicina (Fr.) Quél. JV 10258 Finland n/a AY038324 AY333778 Matheny et al. (2002)
I. rivularis Jacobsson & Vauras Weholt120818 Norway KY033811 KY033811 n/a Unpublished
I. roseifolia Murrill CO5576 USA n/a MK421968 MH577441 Matheny et al. (2020)
I. rufobadia Matheny & Bougher NLB885 Australia KF977213 KF915290 KF991385 Matheny & Bougher (2017)
I. sambucina (Fr.) Quél. SJ01002 Sweden AM882757 AM882757 n/a Ryberg et al. (2008)
I. scissa (E. Horak) Garrido PDD:82757 New Zealand KY827287 KY827239 n/a Horak (2018)
I. sejuncta Matheny, Bougher & M.D. Barrett PBM3752 Australia n/a KP171002 KM555103 Matheny & Bougher (2017)
I. serrata Cleland PBM3235 Australia KP636810 KP171012 KM555111 Matheny & Bougher (2017)
I. silvana K.P.D. Latha & Manim. CAL 1259 India KY440104 KY549134 n/a Latha & Manimohan (2017)
I. snigdha K.P.D. Latha & Manim. CAL 1350 India KY440105 KY549135 KY553250 Latha & Manimohan (2017)
I. soluta Velen. EL2904 Sweden AM882755 AM882755 n/a Ryberg et al. (2008)
Inocybe sp. PC 96039 Zambia n/a EU555474 EU555473 Matheny et al. (2009)
Inocybe sp. PC 96095 Zambia n/a EU569860 n/a Matheny et al. (2009)
Inocybe sp. PC 96111 Zambia EU600875 EU600875 n/a Matheny et al. (2009)
Inocybe sp. MR00219 Australia KF830031 KF808343 KF830049 Matheny & Bougher (2017)
Inocybe sp. PERTH:08383235 Australia KP636839 KP171043 KM555138 Matheny & Bougher (2017)
Inocybe sp. 3243F7 USA KF618024 KF618024 n/a Unpublished
Inocybe sp. DPL12128 USA MH578022 MT241843 MH618233 Unpublished
Inocybe sp. D25 (WTU) Argentina n/a AY380363 AY337361 Matheny (2005)
Inocybe sp. L4517e_Inoc_Zam11 Zambia FR731548 n/a n/a Tedersoo et al. (2011)
Inocybe sp. 96083 (PC) Zambia n/a EU600884 n/a Matheny et al. (2009)
Inocybe sp. ZT10031 (SFSU) Thailand GQ893020 GQ892976 n/a Horak et al. (2015)
I. spadicea Matheny & Bougher PBM2203 Australia KP636866 EU600865 n/a Matheny et al. (2009), Matheny & Bougher (2017)
I. spiniformis Matheny & Bougher PBM3748 Australia KP636868 KP171064 KM656103 Matheny & Bougher (2017)
I. splendens R. Heim EL313-12 France KJ399959 KJ399959 n/a Larsson et al. (2014)
I. stellata E. Horak, Matheny & Desjardin CAL 1369 India KY440106 KY549136 KY553251 Latha & Manimohan (2017)
I. strickeriana Bandini, Anja Schneid. & M. Scholler KR:KR-M-0044749 Germany MG012477 MG551670 n/a Bandini et al. (2018)
I. subcarpta Kühner & Boursier EL8905 Finland AM882754 AM882754 n/a Ryberg et al. (2008)
I. subexilis (Peck) Sacc. PBM2620/ACAD:11680 USA/Canada MH578001 EU307845 EU307847 Esteve-Raventós et al. (2018)
I. subferruginea Matheny & Bougher E7066 (PERTH) Australia n/a EU600894 n/a Matheny et al. (2009)
I. subfibrosoides Singer FLAS:MES543 Chile KP636879 KP171073 KM656117 Matheny & Bougher (2017)
I. subfulva Peck PBM1482 USA KP641623 JN974989 n/a Ryberg & Matheny (2012), Matheny & Bougher (2017)
I. subgiacomi C.L. Cripps, Vauras & E. Larss JV29938 Sweden MK153665 MK153665 n/a Cripps et al. (2019)
I. subporospora Kuyper RP950618 Sweden AM882931 AM882931 n/a Ryberg et al. (2008)
I. substellata Kühner EL52-13 France KT958927 KT958927 n/a Vauras & Larsson (2016)
I. subtrivialis Esteve-Rav., M. Villarreal & Heykoop AH26789 Spain KX354977 n/a MH496024 Esteve-Raventós et al. (2018)
I. sylvicola Matheny, Bougher & G.M. Gates TENN:065735 Australia NR_153163 NG 057199 KM656126 Horak et al. (2015)
I. taxocystis (J. Favre & E. Horak) Senn-Irlet Voucher358 Italy JF908095 n/a n/a Osmundson et al. (2013)
I. tertia Matheny & Bougher PBM3730, TENN:066951 Australia KP641633 KP171086 KM656128 Matheny & Bougher (2017)
I. thailandica E. Horak, Matheny & Desjardin DED8049 Thailand GQ893013 GQ892968 KM656129 Matheny et al. (2009), Horak et al. (2015)
I. torresiae Matheny, Bougher & M.D. Barrett PBM2157/E6978 Australia KP641635 EU600874 EU600873 Matheny et al. (2009), Horak et al. (2015)
I. tubarioides G.F. Atk. PBM 2570 USA n/a AY732210 n/a Matheny & Moreau (2009)
I. tumidula Matheny & Bougher PBM3770 Australia KP641638 KP171090 KM656134 Horak et al. (2015), Matheny & Bougher (2017)
I. turbata E. Horak PDD:82818 New Zealand KY827281 KY827245 n/a Horak (2018)
I. umbrosa E. Horak PDD:106098 New Zealand MN047364 MN047420 n/a Unpublished
I. undinea Bandini, P.-A. Moreau, B. Oertel FR-0246019 Germany MK929265 n/a n/a Bandini et al. (2020b)
I. villosa Bandini, B. Oertel & U. Eberh. BAN1420 Germany MG012478 n/a n/a Esteve-Raventós et al. (2018)
I. viraktha K.P.D. Latha & Manim. CAL 1357 India KY440107 KY549137 KY553252 Latha & Manimohan (2017)
I. vulpinella Bruyl. NI250904 Canada n/a EU307834 n/a Matheny et al. (2009)
I. wayanadensis K.P.D. Latha & Manim. K(M) 191737 India KM924520 KM924515 KY553254 Latha & Manimohan (2017)
I. xanthomelas Boursier & Kühner PAM08082901 France HQ586856 HQ641097 n/a Esteve-Raventós et al. (2015)
I. xerophytica Pegler GUA242 British Virgin Islands n/a EU600880 n/a Matheny et al. (2009)
Nothocybe distincta (K.P.D. Latha & Manim.) Matheny & K.P.D. Latha, CAL 1310 India KX171343 NG_057278 KX171345 Matheny et al. (2009), Latha et al. (2016)
ZT 9250 India n/a EU604546 EU600904
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Fig. 1.

Fig. 1.

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ML tree of ITS, 28S and RPB2 sequences showing the placement of four new species described from tropical regions of Africa: Inocybe beninensis, I. flavipes I. fuscobrunnea and I. pallidiangulata. Filled circles indicate internodes that are strongly supported (bootstrap proportions SHaLRT support ≥ 80 % / ultrafast bootstrap support ≥ 95 % / Bayesian posterior probabilities > 0.95). Empty circles indicate internodes with moderate support where at least one, but not all, support statistics meet the criteria for strong support). The geographic origin of each tip is given after the species name.

Inocybe beninensis and I. flavipes were part of a subclade leading to the I. calida group, together with the specimen Inocybe sp. L4517e_Inoc_Zam11 from Zambia (belonging to what seems to be an undescribed species). Inocybe beninensis in turn was weakly supported (60 % SH-aLRT values, 75 % ML ultrafast bootstrap, 0.8 BPP) as sister to the common clade that they formed. The low sequence divergences (1.9 %) between the sequences of ITS of the collections MR00383, HLA0363, investigated here, and the sequence of the collection L4512_Inoc_Zam05 from Zambia, indicated that they may very well be conspecific, suggesting a wide distribution for I. flavipes.

Inocybe fuscobrunnea was moderately supported (88 % SH-aLRT values, 50 % ML ultrafast bootstrap, 0.6 BPP) as sister to the I. asterospora group including the European species I. fibrosa and I. asterospora, and Asian species I. rekhankitha, I. silvana and I. pileosulcata.

Inocybe pallidiangulata was weakly supported (54 % SH-aLRT values, 60 % ML ultrafast bootstrap, 0.7 BPP) as member of an inclusive clade with a major tropical component; including many species from India, Zambia, and Guyana.

Taxonomy

Inocybe beninensis Aïgnon, Yorou & Ryberg, sp. nov. MycoBank MB 837971. Figs 2, 3, 10A, B.

Fig. 2.

Fig. 2.

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Micromorphology of Inocybe beninensis (HLA0390). A. Basidio-spores. B. Basidia. C. Cheilocystidia. D. Pleurocystidia. E. Caulocystidia. F. Pileipellis. G. Stipitipellis. Scale bars: A = 3 μm, B = 5 μm; C–G = 10 μm.

Fig. 3.

Fig. 3.

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Inocybe beninensis (HLA0390), microscopical characters in KOH. A. Basidiospores. B. Cheilocystidia. C. Pleurocystidia. D. Caulocystidia. Scale bars = 20 μm.

Fig. 10.

Fig. 10.

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Macro-morphology. A, B. Inocybe beninensis (A = HLA0390, B = HLA0462). C. Inocybe flavipes (MR00383). D. Inocybe fuscobrunnea (MR00378). E, F. Inocybe pallidiangulata (E = MR00377, F = HLA0565). Bar = 1 cm.

Etymology: beninensis (L.), referring to the type locality of Benin.

Diagnosis: Inocybe beninensis is morphologically similar to I. flavipes from Benin and Togo but differs from it by the larger basidiospores on average (10.4 × 8.8 μm vs. 8.6 × 5.3 μm) and whitish yellow stipe.

Typus: Benin, Collines region, Toui-Kilibo forest reserve, 8.545722N, 2.67375E, on soil in woodlands dominated by Isoberlinia doka and I. tomentosa, 22 Jun. 2017, leg. H.L. Aïgnon (holotype HLA0390, deposited at UNIPAR). GenBank accessions: ITS (MN096196) and 28S (MN097888).

Description: Pileus 7–20 mm wide, conical to plane, sometimes umbonate, fibrillose to tomentose, yellowish (oac715) to orange-brown (oac719); margin dentate. Flesh white, 2 mm thick at umbo, wider towards the edges, margin smooth. Lamellae 2–4 mm deep, regular, adnexed to adnate, moderately close, white when young becoming yellowish orange (oac768) with age, edge slightly crisped. Lamellulae multi-tiered. Stipe 18–20 × 1.5–3 mm, hollow, flocculose, yellowish white (oac717), central, cylindrical, straight or curved, pruinose, surface slightly fibrillose at the base, veil present. Odour and taste not distinctive. Basidiospores (8.0–)8.7–12.0(–12.1) × (6.0–)6.6–10.9(–11.0) μm, avl × avw = 10.4 × 8.8 μm, Q = (1–)0.9–1.4(–1.5), avQ = 1.1, globose, distinctly nodulose with mostly 4–6 conic nodules, brown in KOH under the microscope. Basidia 27–40 × 9–12 μm, 4–spored, clavate to cylindric. Cheilocystidia 24–55 × 11–18 μm, subclavate, sometimes thin-walled, with apex sometimes crystalliferous. Pleurocystidia 32–44 × 10–15 μm, utriform, thick-walled. Caulocystidia 42–45 × 11–25 μm, pyriform to clavate, thin-walled, observed only at the apex of the stipe. Pileipellis a trichoderm of filamentous hyphae; subpellis of compact hyphae 3–8 μm wide, thin-walled. Stipitipellis a cutis of subcylindrical hyphae 5–20 μm wide, hyaline, thick-walled, with differentiated terminal cells.

Habit: Solitary or in groups, scattered on soil.

Habitat: In woodland dominated by Isoberlinia doka and I. tomentosa. Occurring June to September.

Geographical distribution: Hitherto known from Benin only.

Additional specimen examined: Benin, Borgou Province, N’dali forest reserve, 9.74279N, 2.6929277E, on soil in woodlands dominated by Isoberlinia doka and I. tomentosa, 1 Sep. 2017, leg. H.L. Aïgnon, Specimen voucher (HLA0467). GenBank accession: ITS (MT994602).

Inocybe flavipes Aïgnon, Yorou & Ryberg, sp. nov. MycoBank MB 837975. Figs 4, 5, 10C.

Fig. 4.

Fig. 4.

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Micromorphology of Inocybe flavipes (MR00383). A. Basidio-spores. B. Basidia. C. Cheilocystidia. D. Pleurocystidia. E. Caulocystidia. F. Pileipellis. G. Stipitipellis. Scale bars: A = 3 μm; B = 5 μm; C–G = 10 μm.

Fig. 5.

Fig. 5.

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Inocybe flavipes (MR00383), microscopical characters in KOH. A. Basidiospores. B. Cheilocystidia. C. Pleurocystidia. D. Caulocystidia. Scale bars: A–D = 20 μm.

Etymology: flavipes (L.), referring to the yellow stipe.

Diagnosis: Inocybe flavipes is most similar to I. beninensis from Benin but differs from it by the absence of a veil on the stipe, stipe light yellow to light orange, and smaller basidiospores on average (8.6 × 5.3 μm vs. 10.4 × 8.8 μm).

Typus: Togo, Central region, prefecture of Assoli, Aledjo forest reserve, 9.340278N, 1.251944E, on soil in gallery forest dominated by Isoberlinia tomentosa, 17 Jul. 2013, leg. M. Ryberg (holotype MR00383, deposited at UNIPAR). GenBank accessions: ITS (MN096201), 28S (MN097893) and RPB2 (MW080915).

Description: Pileus 6–13 mm wide, hemispherical, conical to conical with broad umbo, surface fibrillose to minutely scaly, yellow brown (oac734) to orange-brown (oac755). Flesh white, 1mm thick at umbo, margin smooth. Lamellae 2.5 mm deep, adnexed, lamellulae in tiers, brown (oac734). Stipe 14–24 × 1–1.5 mm, surface fibrillose, pruinose in the upper part, more or less equal but with a basal rounded bulb, whitish remnants of a velipellis in lower parts, light yellow (oac716) to light orange (oac718). Odour and taste not distinctive. Basidiospores (6–) 6.3–10(–10.9) × (3.7–)4–10(–10.4) μm, avl × avw = 8.6 × 5.3 μm, Q = (1–)1.1–2.2(2.5) μm, avQ = 1.6, elongate, with 3–5, obtuse nodules, prominent and distinct. Basidia 20–32 × 6–10 μm, generally 4–spored, sometimes 2 or 3-spored. Cheilocystidia 32–51 × 11–22 μm, obovoid, apex sometimes crystalliferous, thick-walled. Pleurocystidia 35–60 × 12–22 μm, utriform, sometimes obovoid, with short pedicel, sometimes with rounded or truncate base, thick-walled, apex usually crystalliferous. Caulocystidia 23–45 × 10–22 μm, sometimes crystalliferous, in upper part of the stipe only, pale brown apex usually. Pileipellis a cutis made up of subparallel hyphae 3–12 μm wide. Stipitipellis a trichoderm of dense, compact hyphae 4–12 μm wide and thick-walled.

Habit: Solitary, in pairs or in small groups, scattered on soil.

Habitat: In gallery forest dominated by Isoberlinia tomentosa or Isoberlina doka. Occurring in June to July.

Geographical distribution: Until now known from West Africa: Benin and Togo.

Additional specimen examined: Benin, Borgou Province, Commune of Tchaourou, 9.2446277 N, 2.7262333E, on soil in Okpara forests dominated by Isoberlina doka, 10 Jun. 2017, leg. H.L. Aïgnon, Specimen voucher (HLA0363), GenBank accession: ITS (MT994601).

Inocybe fuscobrunnea Aïgnon, Yorou & Ryberg, sp. nov. MycoBank MB 837976. Figs 6, 7, 10D.

Fig. 6.

Fig. 6.

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Micromorphology of Inocybe fuscobrunnea (MR00378). A. Basidiospores. B. Basidia. C. Cheilocystidia. D. Pleurocystidia. E. Caulocystidia. F. Pileipellis. G. Stipitipellis. Scale bars: A = 3 μm, B = 4 μm, C–G = 10 μm.

Fig. 7.

Fig. 7.

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Inocybe fuscobrunnea (MR00378), microscopical characters in KOH. A. Basidiospores. B. Cheilocystidia. C. Pleurocystidia. D. Caulocystidia. Scale bars: A–D = 20 μm.

Etymology: fuscobrunnea (L.), referring to the dark brown pileus.

Diagnosis: Inocybe fuscobrunnea has a dark brown, slightly rimose pileus, nodulose spores measuring 7–12 × 6–10.4 μm, similar to I. pallidiangulata in size, but differs from it by the dark reddish brown pileus and larger basidiospores (9.5 × 8.3 μm vs. 7.0 × 5.2 μm).

Typus: Burkina Faso, Bobo-Dioulasso region, forest reserve of Kou, 11.188027N, 4.440556W, on soil in gallery forests dominated by Berlinia grandiflora, 13 Jul. 2013, leg. M. Ryberg (holotype MR00378, deposited at UNIPAR). GenBank accessions: ITS (MN096201), 28S (MN097893) and RPB2 (MW21933).

Description: Pileus 19–40 mm wide, wide conical to plane with obtuse umbo, surface flocculose/tomentose to smooth rimose, brown (oac646) to dark reddish brown (oac836-838), margin smooth, slightly rimose. Flesh white, 2 mm thick under the disc, thinner towards edges, margin rimose. Lamellae 3–5 mm deep, adnexed, pale grey (oac809) turning brown with age (oac807), 34 reaching stipe. Lamellae alternate with lamellulae, multi-tiered. Stipe 32–72 × 2.5–4 mm, subclavate, mostly silky greyish yellowish white (oac857), smooth to longitudinally substriate, pruinose in the upper 1/3 part. Odour and taste not distinctive. Basidiospores (7–)7.6–11.4(–12) × (6–)6.2–10(–10.4) μm, avl × avw = 9.5 × 8.3 μm, Q = 0.9–1.4 μm, avQ = 1.1, globose, with 3–6 obtuse nodules. Basidia 25–38 × 9–14 μm, ventricose, 4-spored. Cheilocystidia 30–47 × 12–20 μm, utriform sometimes obovoid, hyaline crystals on the top, often short pedicels, thin-walled. Pleurocystidia 35–52 × 11–27 μm, utriform, apex sometimes crystalliferous, rounded or truncate base, thin-walled. Caulocystidia 38–51 × 12–17 μm, thin-walled, sometimes crystalliferous, observed only near of the stipe’s apex. Pileipellis a cutis composed of parallel hyphae 4–31 μm wide. Stipitipellis a cutis of subparallel hyphae 6–17 μm wide, hyaline and thick-walled.

Habit: Solitary or in small groups, scattered on soil.

Habitat: In gallery forest dominated by Berlinia grandiflora. Occurring in July.

Geographical distribution: Known from West Africa: Burkina Faso and Ivory Coast.

Additional specimen examined: Ivory Coast, Koudianikro, gbeke region, Bouake, 7.629444N, 4.746667W, on soil in woodland dominated by Berlinia grandiflora, 11 Jul. 2018, leg. L.H. Aïgnon, Specimen voucher (HLA0567), deposited at UNIPAR. GenBank accession: ITS (MT994603).

Inocybe pallidiangulata Aïgnon, Yorou & Ryberg, sp. nov. MycoBank MB 837977. Figs 8, 9, 10E, F.

Fig. 8.

Fig. 8.

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Fig. 8. Micromorphology of Inocybe pallidiangulata (MR00377). A. Basidiospores. B. Basidia. C. Cheilocystidia. D. Pleurocystidia. E. Caulocystidia. F. Pileipellis. G. Stipitipellis. Scale bars: A = 3 μm, B = 5 μm; C–G = 10 μm.

Fig. 9.

Fig. 9.

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Inocybe pallidiangulata (MR00377), microscopical characters in KOH. A. Basidiospores. B. Cheilocystidia. C. Pleurocystidia. D. Caulocystidia. Scale bars: A–D = 20 μm.

Etymology: pallidiangulata (L.), referring to the pale pileus and angular spores.

Diagnosis: Inocybe pallidiangulata is characterised by a pale brown to honey-yellow pileus, nodulose spores measuring 6–9 × 3–6.4 μm, caulocystidia only at the apex of the stipe, and apparent ectomycorrhizal association with tropical Fabaceae and/or Phyllanthaceae. It is superficially similar to I. fuscobrunea by being rimose pileus, similar in size, and occurring in the same habitat but differs from it by the paler pileus and smaller basidiospores with very inconspicuously protruding nodules.

Typus: Burkina Faso, Bobo Dioulasso, forest reserve of Kou, 11.186861N, 4.4415277W, on soil in gallery forest dominated by Berlinia grandiflora. 17 Jul. 2013, leg. M. Ryberg (holotype MR00377, deposited at UNIPAR). GenBank accession: ITS (MN096202), 28S (MN097894) and RPB2 (MW21932).

Description: Pileus 11–29 mm wide, oval, obtuse, conical when young, becoming plane with age, umbo wide, surface fibrillose, fibrils, pale brown (oac825), almost honey-yellow (oac826). Flesh white to greyish white (oac847), 5 mm thick at centre, thinner at edges, margins serrate and slightly rimose. Lamellae 3 mm deep, adnexed, 36 reaching stipe, grey white (oac816). Lamellulae multi-tiered. Stipe 14–45 × 4.5–6 mm, equal to slightly wider at the centre, base bulbous having marginate bulb in young specimens, not obvious in old specimens, stipe surface longitudinally striated, white when young becoming yellow (oac858) with age, possible remnants of veil. Odour and taste not distinctive. Basidiospores (6–)5.6 –8.5(–9) × (3–) 4–6(–6.4) μm, avl × avw = 7.0 × 5.2 μm, Q = (1–)1.1–1.7(–1.8) μm, avQ = 1.4, ellipsoid with 2–3, very inconspicuously protruding nodules. Basidia 20–35 × 7–12 μm, generally 4–spored, seldom 2–spored, clavate. Cheilocystidia 25–52 × 11–25 μm, utriform, truncate base or sometimes rounded, apex usually crystalliferous. Pleurocystidia 33–63 × 12–22 μm, obovoid sometimes utriform with long pedicel truncate base, apex usually crystalliferous wall thickness. Caulocystidia 35–40 × 16–27 μm obovoid, present at stipe apex only, pale brown apex sometimes crystalliferous. Pileipellis a cutis made up of compact hyphae, subparallel 4–12 μm wide. Stipitipellis a cutis often disrupted, composed of parallel hyphae 6–15 μm wide, thick-walled, encrusted, brownish pigment.

Habit: Solitary on soil.

Habitat: In gallery forest dominated by Berlinia grandiflora. Occurring in July.

Geographical distribution: West Africa: Burkina Faso, Ivory Coast and Togo.

Additional specimens examined: Burkina Faso, Bobo-Dioulasso region, forest reserve of Kou, 11.18694N, 4.441667W, on soil in gallery forest dominated by Berlinia grandiflora, 13 Jul. 2013, leg. M. Ryberg, specimen voucher (MR00379), deposited at UNIPAR. Ivory Coast, Kekrekouakoukro, Gbeke, Bouake region, 7.675388N, 4.908111W, on soil in woodland dominated by Berlinia grandfifolia 11 Jul. 2018, leg. H.L. Aïgnon, specimen voucher (HLA0565). Togo, Central region, prefecture of Assoli, forest reserve of Aledjo, 9.276944N, 1.225556E, on soil in gallery forest dominated by Berlinia grandiflora and Uapaca guineensis, 17 Jul. 2013, leg. M. Ryberg, specimen voucher (MR00384).

Taxonomic key to nodulose-spored Inocybe species from tropical Africa

1a. Basidiomata blackish blue and becoming green with a stipe slightly thickened at the base, basidiospores subglobose-quandrangular, 10–13 × 9–12 um, from Tanzania ......................................................................................................... Inocybe cyaneovirescens

1b. Basidiomata not blackish blue and not turning green, stipe base bulbous or not, basidiospores smaller than above if similar in size then basidiomata not turning green .......................................................................................................................................... 2

2a. Stipe pruinose along entire length .................................................................................................................................................... 3

2b. Stipe pruinose over the upper part or apex only ............................................................................................................................. 4

3a. Stipe robust with a marginate bulb, pale brown to subconcolourous with the pileipellis ........................................... I. glaucodisca

3b. Stipe remarkably slender, base not bulbous, dark brown but paler and more or less honey-brown in the upper part, with some reddish-brown tinges towards the base .......................................................................................................... I. conspicuospora

4a. Pileus margin rimose, straight, stipe surface longitudinally silky-striate, lacking smell when fresh .............................. I. ghanaensis

4b. Pileus margin not rimose, stipe surface not silky-striate, smell present when fresh ........................................................................ 5

5a. Pileus margin dentate or serrate ....................................................................................................................................................... 6

5b. Pileus margin smooth ........................................................................................................................................................................ 7

6a. Pileus fibrillose to tomentose, margins dentate, stipe hollow, flocculose, yellowish white, surface slightly fibrillose at the base, caulocystidia pyriform to clavate ............................................................................................................................. I. beninensis

6b. Pileus conical to conical with broad umbo, surface fibrillose to minutely scaly, stipe surface fibrillose, more or less equal but with a bulb, light yellow to light orange, caulocystidia crystalliferous .................................................................................... I. flavipes

7a. Stipe wider, white to yellow, base bulbous having marginate bulb in young specimens ........................................ I. pallidiangulata

7b. Stipe slender, mostly silky greyish yellowish white, base not bulbous ....................................................................... I. fuscobrunnea

DISCUSSION

Four species with nodulose-spores; Inocybe conspicuospora, I. cyaneovirescens, I. ghanaensis and I. glaucodisca have been described from tropical Africa before this study (Hennings 1902, Pegler 1969, Buyck & Eyssartier 1999), but many undescribed species with nodulose-spores are known from Zambia (Matheny et al. 2009, Tedersoo et al. 2011). Most of these species have a restricted distribution and so that what is found in tropical Africa is not likely to be the same species as something from other parts of the world (Buyck & Eyssartier 1999). Here we describe four additional new species of Inocybe; I. beninensis, I. flavipes, I. fuscobrunnea and I. pallidiangulata from tropical African regions. Our phylogenetic analyses show that I. conspicuospora and I. glaucodisca are distinct from the species described here by their distinct positions in the phylogenetic tree. Inocybe cyaneovirescens is distinguished by its colour and I. ghanaensis differs from the others by the presence of a marginate bulb. In the phylogenetic tree, as none of the new describe species belong in the I. praetervisa group, I. mixtilis group, I. napipes group, I. oblectabilis group, I. xanthomelas group, I. diabolica group, I. calospora group, I. lacera group, I. giacomi group, Smooth-spored temperate boreal clade and Smooth-spored temperate Austral clade, these groups or clades have been reduced without violating the result (Fig. 1). While all the species of these groups used in the phylogenetic analyses are shown in Supplementary Fig. S3. The new species described here emerge as sister to other groups, either by themselves or together with undescribed species from Zambia, or as even more isolated in the phylogeny (Fig.1).

The autonomy of the new species is supported by morphological and molecular data. The new species are currently known from Benin, Burkina Faso, Ivory Coast, Togo and/or Zambia and are associated with Isoberlinia doka, I. tomentosa, Berlinia grandiflora and/or Uapaca guineensis in West Africa and associated with the species of the family Phyllanthaceae and/or Fabaceae in miombo woodlands. All species described here have pleurocystidia with crystals and nodulose basidiospores, typical characteristics that support their placement in Inocybe (Matheny et al. 2020).

This study doubles the described diversity of the nodulose-spored species from tropical Africa, but we expect the actual number of species of Inocybe from Africa to be higher given the extent and diversity of ectomycorrhizal habitats, ectomycorrhizal tree species, and paucity of previous studies in this group.

ACKNOWLEDGEMENTS

We are grateful to our colleagues Kassim Tchan and Evans Codjia (Research Unit Tropical Mycology and Plant-Soil Fungi Interactions, University of Parakou) for their assistance during fieldwork and Anneli Svanholm, Bobby Sulistyo with Brandan Furneaux (Systematic Biology program, Department of Organismal Biology, Uppsala University) for their assistance during DNA extraction. Financial support for fieldwork was received from the National Geographic Society (grant n° CP 126R-17). The molecular analysis was supported by the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (grant n° 226-2014-1109). We are also indebted to the Deutscher Akademischer Austauschdienst (DAAD, grant n° PKZ 300499) for granting the university of Parakou with a Leica DM5700 microscope that enabled us to perform microscopic investigations. Matheny was supported by a U.S. National Science Foundation grant (DEB-2030779). Yorou NS is grateful to the Federal Ministry for Education and Research (BMBF, Germany, grant No. 01D20015).

Footnotes

Conflict of interest: The authors declare that there is no conflict of interest.

Supplementary Material: http://fuse-journal.org/

Fig. S1.

ML tree of ITS+28S sequences showing the placement of Inocybe beninensis, I. flavipes I. fuscobrunnea and I. pallidiangulata. For each node, the ML ultrafast bootstrap support ≥ 95 % is presented above or in front of the branch leading to that node.

fuse-2022-10-1-SF1.jpg (494.3KB, jpg)
Fig. S2.

ML tree of RPB2 sequences showing the placement of Inocybe flavipes, I. fuscobrunnea and I. pallidiangulata. For each node, the ML ultrafast bootstrap support ≥ 95 % is presented above or in front of the branch leading to that node.

fuse-2022-10-1-SF2.jpg (715.2KB, jpg)
Fig. S3.

ML tree showing the placement of four new species described from tropical regions of Africa: Inocybe beninensis, I. flavipes I. fuscobrunnea and I. pallidiangulata based on phylogenetic analyses of ITS, 28S and RPB2 data set.

fuse-2022-10-1-SF3.jpg (568.6KB, jpg)

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Fig. S1.

ML tree of ITS+28S sequences showing the placement of Inocybe beninensis, I. flavipes I. fuscobrunnea and I. pallidiangulata. For each node, the ML ultrafast bootstrap support ≥ 95 % is presented above or in front of the branch leading to that node.

fuse-2022-10-1-SF1.jpg (494.3KB, jpg)
Fig. S2.

ML tree of RPB2 sequences showing the placement of Inocybe flavipes, I. fuscobrunnea and I. pallidiangulata. For each node, the ML ultrafast bootstrap support ≥ 95 % is presented above or in front of the branch leading to that node.

fuse-2022-10-1-SF2.jpg (715.2KB, jpg)
Fig. S3.

ML tree showing the placement of four new species described from tropical regions of Africa: Inocybe beninensis, I. flavipes I. fuscobrunnea and I. pallidiangulata based on phylogenetic analyses of ITS, 28S and RPB2 data set.

fuse-2022-10-1-SF3.jpg (568.6KB, jpg)

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