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. 2024 Aug 23;65(5):244–252. doi: 10.47371/mycosci.2024.07.002

Leucoagaricus karjaticus (Agaricaceae), a new species from Maharashtra, India

Prashant B Patil a, Nitinkumar P Patil b, Sunita Chahar c, Satish Maurya d,*
PMCID: PMC11669478  PMID: 39722751

Abstract

A new species, Leucoagaricus karjaticus, was described from the tropical region of the Western Ghats of Maharashtra, India based on morphological characteristics and molecular phylogenetic analysis. Leucoagaricus karjaticus is characterised by its yellowish brown to reddish brown granular scales on the pileus, stipe apex exudes colourless drops, broadly ellipsoid to ellipsoid to ovoid basidiospores, clavate to cylindrical, catenulate cheilocystidia with subglobose to cylindrical ante-terminal elements. Further, the molecular markers nrITS and nrLSU sequence data analyses of Leucoagaricus karjaticus with their sister taxa revealed the distinct phylogenetic position of the new species.

Keywords: Lepiotoid fungi, phylogeny, taxonomy

Marcel V. Locquin classified Leucoagaricus as a subgenus of Leucocoprinus Pat. among the lepiotoid fungi (Locquin, 1943a, 1943b). Singer (1948) later elevated Leucoagaricus to the genus level. The small to medium-sized, slender, fragile to sturdy basidiomata with non-plicate pileus margins, free lamellae, presence of annulus, smooth or ornamented basidiospores with or without germ pore, dextrinoid and metachromatic in cresyl blue, hymenium without pseudoparaphyses, presence of cheilocystidia, and hyphae without clamp connections were the defining characteristics of the genus Leucoagaricus Locq. ex Singer. Morphologically, Leucocoprinus differs from Leucoagaricus in that the pileus has striations and pseudoparaphyses around the basidia. However, Leucoagaricus is polyphyletic, and species of Leucoagaricus are intermixed with those of Leucocoprinus, and Micropsalliota Hohn in the phylogenetic analyses (Dutta et al., 2021; Ma et al., 2022; Vellinga, 2004b; Vellinga et al., 2011).

Vellinga (2004a) stated that Leucoagaricus species are more common and diverse in the tropics, and numerous recent macrofungal studies have identified Leucoagaricus species from tropical locations (Ashraf et al., 2023; Dutta et al., 2021; Ge, 2010; Ge et al., 2015; Hussain et al., 2018; Justo et al., 2021; Khalil et al., 2023; Khan et al., 2023; Kumar & Manimohan, 2009; Latha et al., 2020; Liang et al., 2010; Ma et al., 2022; Qasim et al., 2015; Sysouphanthong et al., 2018; Sysouphanthong & Thongklang, 2022; Ullah et al., 2019; Yuan et al., 2014). In India, so far 29 species of Leucoagaricus with five varieties have been reported (Dutta, et al., 2021; Farook et al., 2013; Kumar & Manimohan, 2009; Kumari & Atri, 2013; Latha, et al., 2020; Manjula, 1983; Natarajan et al., 2005; Rajput et al., 2015; Sathe & Daniel, 1980; Senthilarasu, 2014).

During the mycofloristic survey in monsoon seasons from 2017 to 2021 in the different locations of Matheran Hills (one of the hotspots in Western Ghats, Maharashtra, India), we found an interesting fungus collected from the vicinity of termite mounds belonging to the Lepiotaceous group. In our current study, we followed the broad generic concept in the sense of Vellinga (2001) for Leucoagaricus & Leucocoprinus, and described the new species, Leucoagaricus karjaticus on the basis of morphological characteristics and molecular phylogenetic analyses.

Basidiomata were photographed in the habitat using a Canon EOS 700D Camera (Canon Inc., Japan), and their macroscopic characteristics were studied from fresh specimens in the laboratory. Colour notations of fresh mushrooms were recorded from the ‘Methuen Handbook of Colour’ (Kornerup & Wanscher, 1978). After being examined, the mushrooms were dried in a hot air oven for 24 h at 45-50 °C temperature (Hu et al., 2022). The dried holotype samples were then placed in the Ajrekar Mycological Herbarium (AMH), Pune, India, while the paratypes were kept in the Botany department of Smt. Chandibai Himathmal Mansukhani College, Thane, India. The microscopic characteristics were studied from thin hand-cut sections of dried material, then rehydrated in 5% (w/v) KOH, stained with 1% (w/v) phloxin and 0.5% (w/v) Congo red in distilled water with assistance of a compound microscope MLX-B (Olympus, Tokyo, Japan) connected with Magnus Magcam DC-5 camera (Magnus Opto Systems India Pvt. Ltd., New Delhi, India). Melzer's reagent was used to check the amyloidity of basidiospores, whereas cresyl blue and cotton blue were used to detect the metachromatic and cyanophilic reactions of basidiospores respectively. The abbreviation [50/1/3] means 50 basidiospores were measured from 1 basidiocarp of 3 collections. At least 20 each of basidia, cheilocystidia, pileal, and stipe elements were measured. The following notations were used for describing basidiospores: Xm for arithmetic mean of length by width of basidiospores (± standard deviation), Q for quotient of length divided by width of individual basidiospores and Qm stands for the mean of Q values (± standard deviation). The abbreviation La is used for Leucoagaricus, Lc for Leucocoprinus and L for Lepiota.

The CTAB (Doyle & Doyle, 1987) approach was used to extract the whole genomic DNA. Furthermore, the DNA markers nrITS and nrLSU were chosen for the molecular phylogenetic investigations based on the findings of earlier studies (Dutta et al., 2021; Ge et al., 2015; Hussain et al., 2018; Justo et al., 2021; Ma et al., 2022; Vellinga et al., 2011). For the chosen markers, the Polymerase Chain Reaction (PCR) amplification was done at Genematrix LLP (Pune, India). ITS1/ITS4 primers (White et al., 1990) were used to amplify the nrITS, whereas LROR/LR5 primers (Moncalvo et al., 2000; Vilgalys & Hester, 1990) were used to amplify the nrLSU region. Following the markers' successful amplification, the PCR products were purified and sent to Apical Scientific Sdn Bhd (Seri Kembangan, Selangor, Malaysia) for Sanger sequencing. Using Chromas (Technelisium Pvt. Ltd, Australia) software, the acquired sequences were examined for quality and then further curated using BioEdit v 7.2.5 (Hall, 1999). Both forward and reverse sequences were used to create the consensus sequences, which were then uploaded to GenBank (Table 1).

Table 1 Fungal taxa, voucher specimen numbers, localities and GenBank accession numbers for nrITS and nrLSU sequences used for the present phylogenetic analyses. “-” means information not available from GenBank database. Sequences newly generated in the present study were shown in bold.

Taxon Voucher number/strain Locality GenBank accession numbers References
nrITS nrLSU
Cystolepiota pseudoseminuda KUN-HKAS 92275 China MN810149 MN810101 Hou & Ge, 2020
Cystolepiota pseudoseminuda KUN-HKAS 73969 China MN810144 MN810100 Hou & Ge, 2020
Cystolepiota seminuda 4-X-1989 H.A. Huijser s.n. Netherlands AY176350 AY176351 Vellinga, 2004b
Lepiota aff. furfuraceipes E.C. Vellinga 3646 Thailand MN582751 - GenBank
Lepiota aff. furfuraceipes E.C. Vellinga 3621 Thailand - HM488778 Vellinga et al., 2011
Leucoagaricus adelphicus 15-XI-2001, E.C. Vellinga 2669 (UC) USA AY243622 - GenBank
Lepiota cf. atrodisca E.C. Vellinga 3164 USA GU903304 - Vellinga & Balsley, 2010
Lepiota cf. atrodisca E.C. Vellinga 3415 USA GU903305 - Vellinga & Balsley, 2010
Lepiota cf. phaeosticta TN51705 USA GU903307 - Vellinga & Balsley, 2010
Lepiota flammeotincta Duke JJ97 Costa Rica U85331 U85296 Johnson & Vilgalys, 1998
Lepiota sp. BAB-5053 India KR155098 - GenBank
Lepiotaceae sp. PA635 PA635 Panama EF527366 - Vo et al., 2009
Lepiotaceae sp. PA624 PA624 Panama EF527358 - Vo et al., 2009
Lepiotaceae sp. PA617 PA617 Panama EF527352 - Vo et al., 2009
Lepiotaceae sp. PA652 PA652 Panama EF527378 - Vo et al., 2009
Lepiotaceae sp. PA634 PA634 Panama EF527365 - Vo et al., 2009
Lepiotaceae sp. PA639 PA639 Panama EF527368 - Vo et al., 2009
Lepiotaceae sp. PA530 PA530 Panama EF527339 - Vo et al., 2009
Leucoagaricus albosquamosus CFSZ20662 China OM976879 OM976865 Ma et al., 2022
Leucoagaricus albosquamosus CFSZ22880 China OM976878 OM976866 Ma et al., 2022
Leucoagaricus amanitoides E.C. Vellinga 3331 (UC) USA EF080869 EF080873 Vellinga & Davis, 2007
Leucoagaricus americanus 6-VIII-2000, E.C. Vellinga 2454 (UCB) USA AY176407 AF482891 Vellinga, 2004b
Leucoagaricus americanus NYBG:0005 USA KY350857 KY350858 GenBank
Leucoagaricus asiaticus LAH10012012 Pakistan KP164971 - Ge et al., 2015
Leucoagaricus atroviridis SYAU-073 China OM976852 Ma et al., 2022
Leucoagaricus atroviridis SYAU-074 China OM976853 OM976869 Ma et al., 2022
Leucoagaricus atroazureus HKAS 48450 China EU416299 EU416300 Liang et al., 2010
Leucoagaricus aurantioruber CFSZ18372 China OM976874 OM976862 Ma et al., 2022
Leucoagaricus aurantioruber CFSZ19756 China OM976875 OM976863 Ma et al., 2022
Leucoagaricus badhamii MCVE:3047 Italy GQ329056 - GenBank
Leucoagaricus barssii AFTOL-ID 1899, ECV 3126 USA DQ911600 DQ911601 GenBank
Leucoagaricus bresadolae Bas7981 (L) USA AF295929 - Vellinga, 2000
Leucoagaricus brunneocanus Z.L. Yang 3972 China KP096238 - Ge et al., 2015
Leucoagaricus brunneodiscus CUH AM708 India MT943754 MT940572 Dutta et al., 2021
Leucoagaricus brunneodiscus CUH AM709 India MT940574 MT940575 Dutta et al., 2021
Leucoagaricus brunnescens R. Balsley (UC) USA GQ203804 - Vellinga et al., 2010
Leucoagaricus bulbiger ANGE 197 Dominican Republic MN483028 - Justo et al., 2021
Leucoagaricus bulbiger ANGE 197B Dominican Republic MN483029 - Justo et al., 2021
Leucoagaricus callainitinctus CAL 1799 India MT108797 MT108798 Latha et al., 2020
Leucoagaricus candidus CFSZ 11287 China OM976876 OM976861 Ma et al., 2022
Leucoagaricus candidus CFSZ 20964 China OM976877 OM976864 Ma et al., 2022
Leucoagaricus centricastaneus SYAU-075 China OM976854 OM976870 Ma et al., 2022
Leucoagaricus centricastaneus SYAU-076 China OM976855 OM976871 Ma et al., 2022
Leucoagaricus cinerascens 28-XII-199, P.B. Matheny 1831 (WTU) USA AY176410 - Vellinga, 2004b
Leucoagaricus croceovelutinus E.C. Vellinga 3131 (UC) USA EU166351 - GenBank
Leucoagaricus croceovelutinus 19-IX-1998, E.C. Vellinga 2243 (L) Netherlands AF482862 - Vellinga et al., 2003
Leucoagaricus crystallifer 3-IX-1998, H.A. Huijser Germany AF482863 AY176412 Vellinga et al., 2003
Leucoagaricus cupresseus E.C. Vellinga 2841 (UC) USA GU136193 - Vellinga et al., 2010
Leucoagaricus dacrytus TENN: 074972 USA MT196954 - GenBank
Leucoagaricus dyscritus E.C. Vellinga 3956 (UC) USA GU13680 HM488777 Vellinga et al., 2010
Leucoagaricus flammeotinctoides E.C. Vellinga 3304 (UC) USA GQ258475 - Vellinga et al., 2010
Leucoagaricus flavovirens HKAS 50024 China EU416295 EU416296 Liang et al., 2010
Leucoagaricus georginae 19-IX-1998, E.C. Vellinga 2238 (L) Netherlands AY176413 AY176414 Vellinga, 2004b
Leucoagaricus guatopoensis ANGE 419 Dominican Republic MN483031 - Justo et al., 2021
Leucoagaricus guatopoensis ANGE 199 Dominican Republic MN483030 - Justo et al., 2021
Leucoagaricus hesperius E.C. Vellinga 3515 (UC) USA GU139788 - Vellinga et al., 2010
Leucoagaricus irinellus 21-VIII-1997, R. Chalange 97082101 France AY243648 - GenBank
Leucoagaricus jubilaei 9-X-1999, J. & A. Guinberteau 99101101 France AY243635 - GenBank
Leucoagaricus karjaticus AMH 10515 India OR775576 OR775580 In this study
Leucoagaricus karjaticus MMH 1311 India OR775578 - In this study
Leucoagaricus lacrymans P. Zhang 599 China KY039574 - Yang & Ge, 2017
Leucoagaricus lahorensis LAH 10042012 Pakistan KJ701794 - Qasim et al., 2015
Leucoagaricus leucothites HMAS 88854 China JN944083 JN940293 GenBank
Leucoagaricus littoralis MCVE:702 Italy GQ329041 - GenBank
Leucoagaricus majusculus MFLU 09-0164 Thailand HM488764 - Vellinga et al., 2011
Leucoagaricus margaritifer ANGE 254 Dominican Republic MN482998 - Justo et al., 2021
Leucoagaricus margaritifer ANGE 509 Dominican Republic MN482997 - Justo et al., 2021
Leucoagaricus melanotrichus 23-IX-1998, E.C. Vellinga 2262 (L) Netherlands AY176417 AY176418 Vellinga, 2004b
Leucoagaricus melanotrichus var. fuligineobrunneus H.A. Huijser Netherlands GU903306 - Vellinga & Balsley, 2010
Leucoagaricus meleagris 30-VII-1996, E.C. Vellinga 1990 (L) Netherlands - AF482890 Vellinga et al., 2003
Leucoagaricus meleagris 18 & 19-VIII-1997, E.C. Vellinga 2095 (L) Netherlands AF482867 - Vellinga et al., 2003
Leucoagaricus naucinus CBS 387.66 Argentina MH858835 MH870472 Vu et al., 2019
Leucoagaricus nivalis MYR 414 China OM974308 OM967225 Ma et al., 2022
Leucoagaricus nivalis Yang 5792 China KY039573 KY039578 Yang & Ge, 2017
Leucoagaricus nympharum HMAS 99343 China EU416310 EU681805 Liang et al., 2010
Leucoagaricus orientiflavus HKAS 54260 China GU084262 JN940290 Ge, 2010
Leucoagaricus orientiflavus HKAS 54265 China GU084261 JN940291 Ge, 2010
Leucoagaricus pardalotus E.C. Vellinga 3313 (UC) USA GQ258479 - Vellinga et al., 2010
Leucoagaricus pegleri CA 20 Dominican Republic MN483002 - Justo et al., 2021
Leucoagaricus pegleri ANGE 192 Dominican Republic MN483003 - Justo et al., 2021
Leucoagaricus pilatianus 16-X-1999, J. & A. Guinberteau 99101608 France AY243626 - GenBank
Leucoagaricus proximus LE 262861 Russia JX133172 - Malysheva et al., 2013
Leucoagaricus proximus LE 262855 Russia JX133171 - Malysheva et al., 2013
Leucoagaricus purpureolilacinus 6-XI-1998, E.C. Vellinga 2291(L) Netherlands AF482869 - Vellinga et al., 2003
Leucoagaricus pyrrhulus E.C. Vellinga 3306 (UC) USA GQ258474 - Vellinga et al., 2010
Leucoagaricus roseovertens ANGE 196 Dominican Republic MN483005 - Justo et al., 2021
Leucoagaricus roseovertens CA 19 Dominican Republic KM983716 - Justo et al., 2021
Leucoagaricus rubrobrunneus LE 262863 Russia NR120166 - Malysheva et al., 2013
Leucoagaricus rubrotinctus HKAS 54240 China JN944081 JN940295 GenBank
Leucoagaricus sabinae ANGE 182 Dominican Republic MN483007 - Justo et al., 2021
Leucoagaricus sabinae ANGE 305 Dominican Republic KM983666 - Justo et al., 2021
Leucoagaricus serenus 11-IX-1995, E.C. Vellinga 1930 (L) Belgium AF482871 AY176421 Vellinga et al., 2003
Leucoagaricus sericifer 1-X-1997, E.C. Vellinga 2116 (L) Netherlands AY176426 AY176427 Vellinga, 2004b
Leucoagaricus silvestris ANGE 251 Dominican Republic MN482994 - Justo et al., 2021
Leucoagaricus silvestris ANGE 489 Dominican Republic MN482995 - Justo et al., 2021
Leucoagaricus sinicus HKAS 60647 China DQ182505 DQ457653 GenBank
Leucoagaricus sp. ECV-2010c R.B. Balsley photo 938 (UC) USA GU903308 - Vellinga et al., 2010
Leucoagaricus sp. ecv2484 E.C. Vellinga 2484 (UC) USA GU136182 - Vellinga et al., 2010
Leucoagaricus sp. Vellinga 2561 E.C. Vellinga 2561 (UCB) USA AY176430 AY176431 Vellinga, 2004b
Leucoagaricus sublittoralis 19-IX-1998, E.C. Vellinga 2235 (L) Netherlands AY176442 AY176443 Vellinga, 2004b
Leucoagaricus subpurpureolilacinus HKAS 123027 China OM974314 OM967227 Ma et al., 2022
Leucoagaricus stillatus ANGE 252 Dominican Republic MN483000 - Justo et al., 2021
Leucoagaricus stillatus ANGE 256 Dominican Republic MN483001 - Justo et al., 2021
Leucoagaricus tangerinus HKAS 50036 China NR155314 - Yuan et al., 2014
Leucoagaricus tener 23-X-1998, E.C. Vellinga 2261 (L) Netherlands AY176444 AY176445 Vellinga, 2004b
Leucoagaricus tener MCVE:751 Italy GQ329043 - GenBank
Leucoagaricus tropicus CUH AM699 India MT669365 MT669370 Dutta et al., 2021
Leucoagaricus tropicus CUH AM707 India MT669367 MT669371 Dutta et al., 2021
Leucoagaricus truncatus Z.W. Ge 793 China KP096235 - Ge et al., 2015
Leucoagaricus truncatus HKAS 49288 China NR155319 - Ge et al., 2015
Leucoagaricus turgipes ANGE 583 Dominican Republic MN483017 - Justo et al., 2021
Leucoagaricus turgipes ANGE 511 Dominican Republic MN483019 - Justo et al., 2021
Leucoagaricus umbonatus SHL 1 Pakistan KU647739 KU900521 Hussain et al., 2018
Leucoagaricus variicolor AH 40328 Spain NR120314 - Muñoz et al., 2012
Leucoagaricus virens CFSZ 19869 China OM976881 - Ma et al., 2022
Leucoagaricus virens CFSZ 19794 China OM976880 OM976867 Ma et al., 2022
Leucoagaricus viridiflavus INM-2-87722 Japan KR259170 KR259171 GenBank
Leucoagaricus viriditinctus HKAS 50033 China EU419375 EU419376 Liang et al., 2010
Leucoagaricus wychanskyi IX/X-1987 H.A. Huijser (L) Netherlands AF482874 - Vellinga et al., 2003
Leucocoprinus aff. heinemannii ANGE 357 Dominican Republic MN483013 - Justo et al., 2021
Leucocoprinus aff. heinemannii AJ 490 USA MN483012 - GenBank
Leucocoprinus antillarum ANGE 500 Dominican Republic MN482992 - Justo et al., 2021
Leucocoprinus antillarum ANGE 255 Dominican Republic MN482991 - Justo et al., 2021
Leucocoprinus birnbaumii CBS 323.80 Japan MH861267 MH873036 Vu et al., 2019
Leucocoprinus brebissonii 13-X-1991, E.C. Vellinga 1784 (L) France AF482859 AY176446 Vellinga et al., 2003
Leucocoprinus cepaestipes NY-EFM548 UK U85338 U85286 GenBank
Leucocoprinus cf. fragilissimus PA250 Panama AF079738 AF079656 Mueller et al., 1998
Leucocoprinus cf. zamurensis PA415 Panama AF079753 AF079671 Mueller et al., 1998
Leucocoprinus cretaceus 9-II-1999, T. Lassee & J. Omar TL6171 Malaysia AY176447 - Vellinga, 2004b
Leucocoprinus fuligineopunctatus ANGE 463 Dominican Republic MN482982 - Justo et al., 2021
Leucocoprinus fuligineopunctatus ANGE 421 Dominican Republic MN482983 - Justo et al., 2021
Leucocoprinus griseofloccosus GE17001 (PC) France MH257568 -
Leucocoprinus microlepis CA 31 Dominican Republic MN482987 - Justo et al., 2021
Leucocoprinus microlepis ANGE 190 Dominican Republic MN482988 - Justo et al., 2021
Leucocoprinus scissus ANGE 257 Dominican Republic MN482986 - Justo et al., 2021
Leucocoprinus scissus ANGE 154 Dominican Republic MN482985 - Justo et al., 2021
Leucocoprinus sp. ANGE 418 Dominican Republic MN483016 - Justo et al., 2021
Micropsalliota geesterani LAPAG 520 UK KM922965 KM923966 Parra et al., 2016
Micropsalliota geesterani 23-IX-1998 E.C. Vellinga 2263 (L) Netherlands AF482857 AF482888 Vellinga et al., 2003
Micropsalliota pseudoglobocystis GX20172236 China MT671234 MT671246 Li et al., 2021
Micropsalliota pseudoglobocystis GX20172228 China MT671245 MT671233 Li et al., 2021
Micropsalliota rubrobrunescens ZRL3048 Thailand HM436627 HM436586 Zhao et al., 2010
Termiticola sp. HKAS 122480 China ON794316 - GenBank
Termiticola sp. rlc-381 China MW374173 - GenBank
Termiticola sp. WML-08 China OK584457 - GenBank
Termiticola sp. 2-II-1999, TL6106 Malaysia AY176352 AY176353 Vellinga, 2004b
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Following the earlier studies, the ingroups and outgroups (Cystolepiota seminuda (Lasch) Bon and Cystolepiota aff. seminuda as outgroups) were retrieved from NCBI database to construct the phylogenetic Accessions (Dutta et al., 2021; Ge et al., 2015; Hussain et al., 2018; Justo et al., 2021; Ma et al., 2022; Vellinga et al., 2011). The newly generated sequences were aligned along with NCBI data using the MSA-Muscle tool available with MEGA v 7.0 (Kumar et al., 2016). Initially, the nrITS and nrLSU trees were constructed individually to check their topology. Both the trees depicted exactly same tree topology. Further, to construct the combined tree, both the markers were analysed to understand their congruence using Partition Homogeneity Test (ILD) in PAUP v 4.0b10 (Swofford & Sullivan, 2003). Based on the ILD test, both the matrix was concatenated using TaxonDNA v 1.7.8 (Vaidya et al., 2010). The combined dataset consists of 144 nrITS and 62 nrLSU sequences (including three newly generated sequences during the present study).

In order to estimate the phylogenetic position and relationship, two methods were used: Maximum Likelihood (ML) and Bayesian inference (BI). For ML analysis, IQTree v1.6.8 (Nguyen et al., 2014) was used, and the best fit evolutionary model (GTR+F+R5) was selected using ModelFinder (an inbuilt tool of IQTree; Kalyaanamoorthy et al., 2017). MrBayes v 3.2.6 (Ronquist et al., 2012) was used to generate the Bayesian tree, and the following parameters were used: the MCMCMC algorithm was run with two parallel chains for four million generations, the standard deviation of split frequency was obtained less than 0.01, and the effective sample size (ESS) for each parameter was ensured exceeding 200. However, using jModeltest, the most appropriate evolutionary model was determined to be GTR+I+G (Darriba et al., 2012). Moreover, FigTree v 1.4.2 displayed the consensus trees (Rambaut, 2014). The phylogram's statistical supports were calculated using posterior probabilities (PP) and bootstrap values (BS).

Taxonomy

Leucoagaricus karjaticus P.B. Patil, N.P. Patil, S. Chahar & S. Maurya, sp. nov.　Figs. 1, 2.

MycoBank no.: MB 850864.

Fig. 1 - Leucoagaricus karjaticus (AMH 10515, holotype). A, B: Basidiomata in the natural habitat, found close to forest termite mounds. C: Basidiomata with scale bar. D, E: Basidiomata showing lamellae with colourless drops on stipe surface. F: Pileal surface. Bars: D-F 1 cm.

Fig. 1 - Leucoagaricus karjaticus (AMH 10515, holotype). A, B: Basidiomata in the natural habitat, found close to forest termite mounds. C: Basidiomata with scale bar. D, E: Basidiomata showing lamellae with colourless drops on stipe surface. F: Pileal surface. Bars: D-F 1 cm.

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Fig. 2 - Leucoagaricus karjaticus (AMH 10515, holotype). A, B: Basidiospores, some exceptionally large basidiospores as mentioned in the text. C-E: Basidia. F-H: Cheilocystidia. I, J: Pileipellis hyphae. K: Annulus hyphae from context. Bars: A, B 5 μm; C-H 10 μm; I-K 20 μm.

Fig. 2 - Leucoagaricus karjaticus (AMH 10515, holotype). A, B: Basidiospores, some exceptionally large basidiospores as mentioned in the text. C-E: Basidia. F-H: Cheilocystidia. I, J: Pileipellis hyphae. K: Annulus hyphae from context. Bars: A, B 5 μm; C-H 10 μm; I-K 20 μm.

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Diagnosis: Differs from La. tangerinus by its white, fugacious annulus, larger basidiospores and basidia, and longer, narrowly clavate to subfusiform cheilocystidia.

Type: INDIA, Maharashtra, Raigad District, Matheran Hills (18°58’48.00”N, 73°16’12.00”E, 800 m a.s.l.), collected by P. B. Patil on 22 Jul 2018. (AMH 10515, Holotype).

DNA sequence ex-Holotype (preserved holotype as per ICN rule art 8.4 and recommendation 8B.2): OR775576 (nrITS) and Paratype (OR775578).

Etymology: The species epithet “karjaticus” refers to the place “Karjat” where the holotype was collected.

Basidiomata medium to large. Pileus 45-80 mm, ovate to campanulate when young, becoming convex to applanate at maturity, dry, with or without obtusely umbonate, umbo reddish brown (8E4) to dark brown (8F4), sometimes cracks at maturity, surface covered with yellowish brown (5D5) to reddish brown (8E8) granular scales, gradually paler and sparser towards the margin, on a creamy white background, margin striate, with white floccose remnants, exceeding the lamellae, context 3-5 mm thick on disc, white, no change in colour upon bruising, lamellae free, creamy white, 2-4 mm broad, straight to slightly ventricose, moderately crowded, remote from the stipe, lamellulae of 6 different lengths, edges entire. Stipe 70-100 × 6-10 mm, central, cylindrical, fistulose, mostly curved, slightly attenuated towards apex, stipe apex often exudes colourless drops, creamy white to light brown above annulus, yellowish brown below annulus, slightly granular-scaly towards base, scales concolorous with those of pileus, basal mycelia white. Annulus superior, membranous, ascending, white on upper side, granular-scaly (similar to the pileus surface) below.

Basidiospores [50/1/3] (4)4.5-6(7) × 3-4.5(5) µm, Q = 1.22-1.68(1.75), [Xm = 5.1 ± 0.7 × 3.6 ± 0.45 µm, Qm = 1.4 ± 0.12] (some basidiospores exceptionally large up to 7.5-9 × 5-5.5 µm), broadly ellipsoid to ellipsoid to ovoid in side view, ovoid in front view, with rounded apex, smooth, no germ pore, slightly thick walled (0.5 µm thick), hyaline, dextrinoid, metachromatic in cresyl blue, with one to two guttules when observed in KOH. Basidia 14-18.3 × 6-8 µm, clavate, thin walled, hyaline, 4-spored, rarely 2-spored, sterigmata 1.7-2.5 µm long. Basidioles 12-15 × 5.8-6.5 µm, clavate, thin walled, hyaline. Pleurocystidia absent. Cheilocystidia numerous and crowded at lamella edge, 17-35 × 6.5-14 µm, broadly clavate to cylindrical to capitate-stipitate, regularly catenulate by 3-5 elements with subglobose to cylindrical ante-terminal elements, hyaline, thin walled. Hymenophoral trama regular, hyphae interwoven, hyaline, thin walled. Pileipellis a trichoderm, composed of radially arranged cylindrical hyphae, constricted at the septa, 3.5-8 µm broad, often branched, terminal elements 15-40 × 6-8 µm, oblong to cylindrical with slightly rounded apex. Annulus hyphae cylindrical, thin walled, 3-7 µm broad, interwoven, often branched. Stipitipellis consist of parallel hyphae, 8-13 µm wide. Clamp connections are absent in all tissues.

Habitat and distribution: All sample collections were free-living, found close to forest termite mounds, solitary to scattered in semi-evergreen forests dominated by tree species like Memecylon umbellatum Burm.F., Garcinia talbotii Raizada ex Santapau., Olea dioica Roxb., Xantolis tomentosa (Roxb). Raf. So far known only from Matheran Hills, Maharashtra, India.

Additional specimens (paratypes) examined: INDIA, Maharashtra, Raigad District, Matheran Hills (18°58’48.00”N, 73°16’12.00”E), 5 Aug 2019 (MMH 1311, OR775578 for nrITS and OR053821 for nrLSU), 8 Sep 2019 (MMH 1312), 14 Aug 2022 (MMH 1313), Prashant B. Patil.

Based on the overall appearance of basidiomata, phylogenetic placement and the other Leucoagaricus taxa that exude droplets at stipe, La. karjaticus appears close to La. tangerinus Y. Yuan & J.F. Liang, La. margaritifer Justo, Bizzi & Angelini, La. stillatus Justo, Bizzi & Angelini, La. brunneodiscus A.K. Dutta & K. Acharya, La. tener (P.D. Orton) Bon, La. dacrytus Vellinga and Lepiota furfuraceipes Han C. Wang & Zhu L. Yang. However, the Chinese species, La. tangerinus differs by having white, fugacious annulus, larger basidiospores (6.5-7 × 4-4.5 µm) and basidia (16-26 × 7-10 µm), and longer, narrowly clavate to subfusiform cheilocystidia (25-60 × 8-15 µm) (Yuan et al., 2014). The taxon described from Dominican Republic, La. margaritifer is distinguishable from La. karjaticus by its whitish annulus, larger and less broad, ovoid, ellipsoid to oblong basidiospores (5.5-7.5 × 3.5-4.5 µm), larger (24-74 × 8-30 µm), clavate, ventricose, mostly mucronate, lageniform or bifurcated cheilocystidia (Justo et al., 2021). Another Dominican Republic species, La. stillatus has a jagged margin, white annulus, larger basidiospores (6-8 × 4-4.5 µm) and larger clavate, ventricose cheilocystidia (22-58 × 7-20 µm; Justo et al., 2021). The Indian taxon, La. brunneodiscus differs from La. karjaticus by its larger basidiospores (7.1-7.8 × 4.3-4.8 µm) and basidia (19-24 × 7-8 µm; Dutta et al., 2021). Leucoagaricus tener has a smaller size basidiomata, turns orange when touched and larger, narrowly clavate to slightly fusiform cheilocystidia measuring 19-75 × 6.5-13 µm (Vellinga, 2001). Leucoagaricus dacrytus has smaller basidiomata (pileus 10-33 mm; stipe 20-50 × 1.5-3.5 mm), pileus surface with cobwebby patches and less broad, oblong-ellipsoid basidiospores measuring 5.9-7.4 × 2.9-4.1 µm (Vellinga & Balsley, 2010). Lepiota furfuraceipes is distinctly differs from La. karjaticus in the presence of densely covered furfuraceous to punctate squamules on the pileus and stipe surface, non-metachromatic, larger basidiospores (6-8 × 4-5 µm), longer, subfusiform, narrowly clavate cheilocystidia (17-72 × 5-18.5 µm) and much longer terminal elements of pileipellis (17-105 × 5-13 µm; Wang & Yang, 2005). Leucocoprinus lacrymans T.K.A. Kumar & Manim. and Lc. cepistipes (Sowerby) Pat. also exude droplets but differs from La. karjaticus in the basidiospores having germ pore and basidia surrounded by pseudoparaphyses (Kumar & Manimohan, 2004; Vellinga, 2001). Leucoagaricus silvestris Justo, Bizzi & Angelini (not exude drops) is morphologically related to La. karjaticus but markedly differs by having larger basidiospores (7-9 × 5-6 µm) and basidia (18-29 × 8-12 µm), and longer polymorphic cheilocystidia (18.5-50 × 9-23 µm; Justo et al., 2021). Leucoagaricus karjaticus is also morphologically close to the monotypic genus, Termiticola E. Horak comprising the single species T. rubescens, described from Papua New Guinea by E. Horak in 1979. They shared common characteristics such as growing near termite mounds, granular-scaly pileus surface, margin striate with white floccose remnants, superior, membranous annulus, clavate to subfusoid, catenulate cheilocystidia. However, T. rubescens is distinguishable from La. karjaticus in having larger basidiospores (6-7 × 3.5-4 µm) and basidia (20-28 × 5-8 µm), chained hyphae forming palisade-like pileus covering.

The combined dataset alignment contained 1491 characters, which includes the aligned sequence dataset composed of 788 bp from nrITS, and 703 bp from nrLSU for the analyses. The partition homogeneity test revealed the strong congruence between two markers with a significance value of 1.0 and suggests that the dataset can be combined for further analysis. Based on combined analysis using ML and Bayesian methods we obtained similar tree topologies.

In phylogenetic analyses, Leucoagaricus karjaticus appears as a sister to an undescribed species with three sequences from the China (Termiticola sp. HKAS 122480, rlc 381, WML-08) and one from Malaysia (Termiticola sp. TL6106) by strong statistical support values (100% MLBS, 1 PP) (Fig. 3). All three sequences were roughly indicated as Termiticola spp. In addition, the Chinese taxon, La. tangerinus, and an unknown species from Thailand (L. aff. furfuraceipes) are also sister to La. karjaticus. (Fig. 3). The Malaysian taxon (Termiticola sp. TL6106) was found growing close to termite mounds with brown spores; Vellinga (2004b) tentatively assigned it to the genus Termiticola. Furthermore, Vellinga (2004b) 's phylogenetic analysis placed this taxon in the clade of the Leucoagaricus/Leucocoprinus. In fact, the majority of ant-cultivated fungi and its closely related species belong to Leucoagaricus/Leucocoprinus clade (Heisecke et al., 2021; Mueller et al., 1998; Mueller, 2002; Vo et al., 2009). In phylogenetic analyses of Vo et al. (2009), the ITS r-DNA gene sequences of two free living Leucocoprinaceous taxa were closely related to ant-cultivated fungi, suggesting that these cultivated fungi were brought recently into the symbiosis or that the free-living counterparts recently escaped the symbiosis as hypothesized by Mueller et al. (1998). This discovery of free-living counterparts suggested that ant-cultivated fungi might have close links to free-living Leucocoprinaceous fungi (Vo et al., 2009). Our present studied species is free-living but growing near termite mounds; so, it might left symbiosis recently and completed its life cycle as free-living, but we cannot rule out the possibility of the presence of hyphal connections between fruiting bodies and termite mounds. Moreover, we cannot overlook the report of polyphyly of the genera Leucoagaricus/Leucocoprinus by the various researchers, but the lack of molecular dataset from this group continued this uncertainty (Dutta et al., 2021; Johnson, 1999; Johnson & Vilgalys, 1998; Vellinga, 2004b; Vellinga et al., 2011). Following the previous studies and a conservative approach, currently, we describe the new species under the genus Leucoagaricus.

Fig. 3 - Maximum likelihood phylogram generated from the combined dataset of two nuclear genes (nrITS and nrLSU). Bootstrap values (BS/ right side) ≥ 70 and Bayesian posterior probability (PP/ left side) ≥ 0.8 are given at the internodes. Cystolepiota seminuda and Cystolepiota pseudoseminuda are selected as outgroups. The highlighted taxa represents the basidiomata exude drops. The scale bar represents a phylogenetic distance of 0.07 nucleotide substitutions per site.

Fig. 3 - Maximum likelihood phylogram generated from the combined dataset of two nuclear genes (nrITS and nrLSU). Bootstrap values (BS/ right side) ≥ 70 and Bayesian posterior probability (PP/ left side) ≥ 0.8 are given at the internodes. Cystolepiota seminuda and Cystolepiota pseudoseminuda are selected as outgroups. The highlighted taxa represents the basidiomata exude drops. The scale bar represents a phylogenetic distance of 0.07 nucleotide substitutions per site.

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Disclosure

The authors declare no conflicts of interest.

Acknowledgements

We greatly acknowledge the Principal, Smt. C.H.M. College, Ulhasnagar, Maharashtra, India for providing the laboratory facilities. We also thank the Principal, Bajaj College of Science, Wardha, for providing laboratory facilities for us to work in, as well as the DST-Fist (grant number-SR/FST/COLLEGE-/2022/1205, dated 19th December, 2022) for funding support to the Bajaj College of Science, Wardha, in order to enhance the laboratory facilities.

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