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Research Article
New species and records of Neomassaria, Oxydothis and Roussoella (Pezizomycotina, Ascomycota) associated with palm and bamboo from China
expand article infoHong Min Hu‡, Li Li Liu‡, Xu Zhang‡, Yan Lin‡, Xiang Chun Shen‡, Si Han Long‡, Ji Chuan Kang§, Nalin N. Wijayawardene|‡, Qi Rui Li‡, Qing De Long‡
‡ Guizhou Medical University, Guiyang, China
§ Guizhou University, Guizhou, China
| Qujing Normal University, Qujing, China
¶ Section of Genetics, Institute for Research and Development in Health and Social Care, Battaramulla, Sri Lanka

Corresponding author: Qi Rui Li ( lqrnd2008@163.com )

Corresponding author: Qing De Long ( longqingde@gmc.edu.cn )

Academic editor: Chitrabhanu Bhunjun
© 2022 Hong Min Hu, Li Li Liu, Xu Zhang, Yan Lin, Xiang Chun Shen, Si Han Long, Ji Chuan Kang, Nalin N. Wijayawardene, Qi Rui Li, Qing De Long.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Hu HM, Liu LL, Zhang X, Lin Y, Shen XC, Long SH, Kang JC, Wijayawardene NN, Li QR, Long QD (2022) New species and records of Neomassaria, Oxydothis and Roussoella (Pezizomycotina, Ascomycota) associated with palm and bamboo from China. MycoKeys 93: 165-191. https://doi.org/10.3897/mycokeys.93.89888
Open Access

Abstract

Several micro fungi were gathered from bamboo and palm in Guizhou Province, China. In morphology, these taxa resemble Neomassaria, Roussoella and Oxydothis. Multi-gene phylogenetic analyses based on combined ITS, LSU, SSU, rpb2 and tef1 loci confirmed that two are new geographical records for China, (viz. Roussoella siamensis, Neomassaria fabacearum), while two of them are new to science (viz. Oxydothis fortunei sp. nov. and Roussoella bambusarum sp. nov.). The stromata of Roussoella bambusarum are similar to those of R. thailandica, but its ascospores are larger. In addition, multi-gene phylogenetic analyses show that Oxydothis fortunei is closely related to O. inaequalis, but the J- ascus subapical ring as well as the ascospores of O. inaequalis are smaller. Morphological descriptions and illustrations of all species are provided.

Keywords

2 new taxa, bambusicolous and palm fungi, phylogeny, Pleosporales, taxonomy, Xylariales

Introduction

Ascomycetous taxa on bamboo and palm are commonly observed with immersed ascomata (Dai et al. 2017). Oxydothis Penz. & Sacc. and Roussoella Sacc. are well-documented on bamboo and palms in different localities in Asia (Liu et al. 2014; Konta et al. 2016; Dai et al. 2017).

The family Oxydothidaceae S. Konta & K.D. Hyde was erected to accommodate a single genus (Oxydothis) by Konta et al. (2016). Species of Oxydothis are characterized by the cylindrical asci with a J+ (rarely J-) subapical apparatus and filiform to fusiform, hyaline,1-septate ascospores with spine-like or rounded ends (Konta et al. 2016). Anamorph is Selenosporella sp. (descriptions from Samuels and Rossman 1987). Eighty-five epithets of Oxydothis have been listed in Index Fungorum (accession date: 1 May 2022). Oxydothis species (such as O. oraniopsidis Fröhlich & Hyde, O. cyrtostachicola Hidayat, To-Anun & K.D. Hyde, O. garethjonesii Konta & Hyde) are the initial colonizers of dead palm material (Hyde 1993; Fröhlich and Hyde 1994; Hidayat et al. 2006; Konta et al. 2016).

Liu et al. (2014) introduced Roussoellaceae Jian K. Liu et al. to accommodate three genera, i.e. Neoroussoella Jian K. Liu et al., Roussoella Sacc. and Roussoellopsis I. Hino & Katum (Liu et al. 2014). Later, Appendispora K.D. Hyde, Cytoplea Bizz. & Sacc., Elongatopedicellata Jin F. Zhang et al., Immotthia M.E. Barr and, Pararoussoella Wanas et al., were added to this family (Hyde 1994; Hyde et al. 1996; Ariyawansa et al. 2015; Hyde et al. 2017; Phookamsak et al. 2019; Wijayawardene et al. 2020). Most species of Roussoellaceae were reported as saprophytic taxa on the terrestrial plants including bamboo, palms and mangroves (Liu et al. 2014; Jiang et al. 2019; Poli et al. 2020). The members of this family have 4–8 spored, and bitunicate asci with aseptate, brown to dark brown ascosporic, melanconiopsis-like or neomelanconium-like asexual morphs (Liu et al. 2014).

Hyde et al. (2016) introduced the monotypic genus Neomassaria Mapook et al. to accommodate N. fabacearum Mapooket et al. in Neomassariaceae. The Neomassaria is characterized by globose to subglobose ascomata with fusoid, hyaline, 1-septate ascospores, with or without a sheath but the asexual morph is undetermined (Hyde et al. 2016; Ariyawansa et al. 2018; Yang et al. 2022). Currently, only three species have been reported, viz., Neomassaria fabacearum from the branch of Hippocrepis emerus (L.) Lassen (Hyde et al. 2016), N. formosana H.A. Ariyaw. et al. on a dead stem of Rhododendron sp. (Ariyawansa et al. 2018), and N. hongheensis E.F. Yang & Tibpromma on a decayed branch of Mangifera indica L. (Yang et al. 2022).

In this study, several specimens of bamboo and palm were collected from Guizhou Province. Based on their morphology and phylogeny, two new species and two new records from China are herein reported. Full descriptions, photo plates of macro-and micro-morphological characteristics and a phylogenetic tree to show the phylogenetic placement of the new records and the new species are provided.

Materials and methods

Fungi collections, isolations and morphology

From 2021 to 2022, fresh materials were collected from bamboo and palms in forests and nature reserves of Guizhou Province, China, and returned to the lab in paper or plastic bags. Samples were treated and examined with the method described by Taylor and Hyde (2003). Morphological characteristics were examined using a Nikon SMZ 745 series stereomicroscope and photographed using a Canon 700D digital camera. Melzer’s iodine reagent was used for testing the amyloid reaction of the apical apparatus structures. Micro-morphological structures were photographed using a Nikon digital camera (Canon 700D) fitted to a light microscope (Nikon Ni). At least 30 ascospores and asci of each specimen were measured using the Tarosoft image framework (v. 0.9.0.7). Photo plates were arranged and improved using Adobe Photoshop CS6 software. Specimens were kept in the Herbarium of Guizhou Medical University (GMB) and Herbarium of Kunming Institute of Botany, Chinese Academy of Sciences (KUN-HKAS).

Isolations were made by single spore isolation (Long et al. 2019) and germinated spores were transferred onto potato dextrose agar (PDA) medium for purification. The colonies grown on PDA at 25 °C were transferred to three 1.5 mL microcentrifuge tubes filled with sterile water and stored with 10% glycerol at –20 °C. Living cultures were deposited at Guizhou Medical University Culture Collection (GMBC).

DNA extraction, Polymerase chain reaction (PCR) amplification and sequencing

The OMEGA E.Z.N.A. Fungal Genomic DNA Extraction Kit (D3390, Guangzhou Feiyang Bioengineering Co., Ltd, China) was used to extract genomic DNA from fresh fungal mycelium, according to the manufacturer’s instructions. The extracted DNA was stored at –20 °C.

ITS5/ITS4 (White et al. 1990), LR0R/LR5 (Vilgalys and Hester 1990) and NS1/NS4 primers (White et al. 1990) were used for the amplification of ITS, LSU and SSU. Translation elongation factor 1-α gene region (tef1) and RNA polymerase II second largest subunit (rpb2) genes were amplified using EF1-983F and EF 1-2218R (Rehner 2001), rpb2-5f and rpb2-7cr primers (Liu et al. 1999) respectively.

PCR was carried out in a volume of 25 μL containing 9.5 μL of ddH2O, 12.5 μL of 2× Tap PCR Master Mix (2× Tap Master Mix with dye, TIANGEN, China), 1 μL of DNA extracts and 1 μL of forward and reverse primers in each reaction. The PCR thermal cycle of ITS, LSU, SSU and tef1 amplification is as follows: initially 95 °C for 5 minutes, followed by 35 cycles of denaturation at 94 °C for 1 minute, annealing at 52 °C for 1 minute, elongation at 72 °C for 1.5 minutes, and final extension at 72 °C for 10 minutes. The PCR thermal cycle program for the partial rpb2 was followed as initially 95 °C for 5 minutes, followed by 35 cycles of denaturation at 95 °C for 1 minute, annealing at 54 °C for 2 minutes, elongation at 72 °C for 1.5 minutes, and final extension at 72 °C for 10 minutes. The amplified PCR fragments were sent to Sangon Biotech (Shanghai) Co., China, for sequencing. Generated new sequences of ITS, LSU, SSU, rpb2 and tef1 regions were deposited in GenBank (Table 1).

Table 1.
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Taxa of Neomassaria, Roussoella, Oxydothis and related genera used for phylogenetic analyses.

Species Strain number GenBank Accession number References
ITS LSU SSU rpb2 tef1
Acrocordiella occulta RS10 KT949894 NA NA NA NA Jaklitsch et al. (2016)
Acrocordiella occulta RS9 KT949893 NA NA NA NA Jaklitsch et al. (2016)
Aigialus grandis JK 5244A NA GU301793 GU296131 GU371762 NA Schoch et al. (2009)
Albertiniella polyporicola CBS 457.88 NA AF096185 AF096170 NA NA Suh et al. (1999)
Amniculicola lignicola CBS 123094 (HT) NA EF493861 EF493863 EF493862 GU456278 Zhang et al. (2009)
Amphibambusa bambusicola MFLUCC 11-0617 KP744433 KP744474 NA NA NA Liu et al. (2015)
Amphisphaeria sorbi MFLUCC 13 C0721 NA KP744475 NA NA NA Liu et al. (2015)
Amphisphaeria umbrina AFTOL-ID 1229 (ET) NA FJ176863 FJ176809 NA NA Unpublished
Apiospora bambusae ICMP 6889 NA DQ368630 DQ368662 NA NA Tang et al. (2007)
Apiospora hydei CBS 114990 KF144890 KF144936 NA NA NA Crous et al. (2013)
Apiospora montagnei AFTOL-ID 951 NA DQ471018 NA NA NA Spatafora et al. (2006)
Arecophila bambusae HKUCC 4794 NA AF452038 AY083802 NA NA Jeewon et al. (2003)
Arthopyrenia saltuensis CBS 368.94 KF443410 AY538339 NA KF443397 KF443404 Lumbsch et al. (2005)
Arthrinium phaeospermum HKUCC 3395 NA AY083832 AY083816 NA NA Unpublished
Astrosphaeriella aggregata MAFF 239486 (HT) NA AB524591 AB524450 AB539092 AB539105 Tanaka et al. (2009)
Bartalinia robillardoides CBS 122705 (ET) KJ710460 KJ710438 NA NA NA Crous et al. (2014)
Beltrania pseudorhombica CBS138003 KJ869158 KJ869215 NA NA NA Crous et al. (2014)
Beltraniella endiandrae CBS137976 KJ869128 KJ869185 NA NA NA Crous et al. (2014)
Broomella vitalbae MFLUCC 15-0023 KP757755 KP757751 KP757759 NA NA Liu et al. (2015)
Cainia graminis CBS 136.62 (ET) NA AF431949 AF431948 NA NA Lumbsch et al. (2002)
Cephalotheca foveolata UAMH11631 (ET) KC408422 KC408398 NA NA NA Unpublished
Clypeosphaeria uniseptata HKUCC6349 (ET) NA DQ810219 DQ810255 NA NA Unpublished
Colletotrichum gloeosporioides LC0555 JN943090 JN940412 JN940356 NA NA Schoch et al. (2012)
Coniocessia anandra Co108 GU553338 GU553349 NA NA NA Asgari et al. (2011)
Coniocessia maxima Co117 GU553332 GU553344 NA NA NA Asgari et al. (2011)
Coniocessia nodulisporioides Co126 (ET) GU553333 GU553352 NA NA NA Asgari et al. (2011)
Cordana abramovii PE 0063-1a NA KF83336 NA NA NA Zelski et al. (2014)
Cordana inaequalis CBS 508.83 HE672146 HE672157 NA NA NA Unpublished
Cordana pauciseptata CBS 121804 (ET) HE672149 HE672160 NA NA NA Unpublished
Creosphaeria sassafras CM AT-018 NA DQ840056 NA NA NA Unpublished
Cryptendoxyla hypophloia WM10.89 NA HQ014708 NA NA NA Unpublished
Cycasicola goaensis MFLU 17-0581 (HT) NR_157510 NG_059057 NA NA NA Wanasinghe et al. (2018)
Delitschia didyma UME 31411 NA DQ384090 AF242264 NA NA Kruys et al. (2006)
Delitschia winteri AFTOL-ID 1599 NA DQ678077 DQ678026 DQ677975 DQ677922 Schoch et al. (2006)
Diatrype disciformis AFTOL-ID 927 NA DQ470964 DQ471012 NA NA Spatafora et al. (2006)
Diatrype palmicola MFLUCC 11-0020 KP744438 KP744482 KP753950 NA NA Liu et al. (2015)
Diatrype whitmanensis ATCC MYA-4417 FJ746656 NA NA NA NA Unpublished
Didymella exigua CBS 183.55 (HT) NA NA GU296147 GU371764 NA Schoch et al. (2009)
Eutypa lata CBS 208.87 DQ006927 NA NA NA NA Rolshausen et al. (2006)
Herpotrichia juniperi AFTOL-ID 1608 NA DQ678080 DQ678029 DQ677978 DQ677925 Schoch et al. (2006)
Hyalotiella spartii MFLUCC 13-0397 KP757756 KP757752 KP757760 NA NA Liu et al. (2015)
Hyponectria buxi UME 31430 NA AY083834 AF130976 NA NA Unpublished
Immersidiscosia eucalypti HHUF 29920 AB594793 AB593722 AB593703 NA NA Tanaka et al. (2011)
Iodosphaeria tongrenensis MFLU15-0393 KR095282 KR095283 KR095284 NA NA Li et al. (2015)
Lepteutypa cupressi IMI 052255 NA AF382379 AY083813 NA NA Jeewon et al. (2002)
Leptosphaerulina australis CBS 317.83 NA GU301830 GU296160 GU371790 GU349070 Schoch et al. (2009)
Lopadostoma turgidum LT2 KC774618 NA NA NA NA Voglmayr et al. (2017)
Lophiostoma arundinis AFTOL-ID 1606 NA DQ782384 DQ782383 DQ782386 DQ782387 Schoch et al. (2006)
Lophiostoma macrostomoides CBS 123097 NA FJ795439 FJ795482 FJ795458 GU456277 Zhang et al. (2009)
Massaria anomia WU 30509 NA HQ599378 HQ599453 NA HQ599318 Voglmayr et al. (2011)
Massaria ariae WU 30510 (HT) NA HQ599381 HQ599458 NA HQ599321 Voglmayr et al. (2011)
Massaria aucupariae WU 30512 NA HQ599384 HQ599455 NA HQ599324 Voglmayr et al. (2011)
Massaria campestris WU 30610 NA HQ599386 NA NA HQ599326 Voglmayr et al. (2011)
Massaria conspurcata WU 30519 NA HQ599393 HQ599441 NA HQ599333 Voglmayr et al. (2011)
Massaria gigantispora WU 30521 NA HQ599397 HQ599447 NA HQ599337 Voglmayr et al. (2011)
Massaria inquinans WU 30527 NA HQ599402 HQ599444 HQ599460 HQ599342 Voglmayr et al. (2011)
Massaria lantanae WU 30533 (HT) NA HQ599406 HQ599443 NA HQ599346 Voglmayr et al. (2011)
Massaria macra WU 30535 (HT) NA HQ599408 HQ599450 NA HQ599348 Voglmayr et al. (2011)
Massaria mediterranea WU 30547 (HT) NA HQ599414 NA NA HQ599354 Voglmayr et al. (2011)
Massaria parva WU 30553 NA HQ599418 HQ599467 NA NA Voglmayr et al. (2011)
Massaria platanoidea WU 30556 NA HQ599423 NA NA HQ599362 Voglmayr et al. (2011)
Massaria pyri WU 30562 (HT) NA HQ599424 HQ599445 NA HQ599363 Voglmayr et al. (2011)
Massaria ulmi WU 30565 NA HQ599427 NA NA HQ599366 Voglmayr et al. (2011)
Massaria vindobonensis WU 30602 NA HQ599432 NA NA HQ599371 Voglmayr et al. (2011)
Massaria vomitoria WU 30606 NA HQ599437 HQ599440 HQ599466 HQ599375 Voglmayr et al. (2011)
Massaria zanthoxyli WU 30620 NA HQ599439 HQ599454 NA HQ599377 Voglmayr et al. (2011)
Massarina eburnea CBS 473.64 NA GU301840 GU296170 GU371732 GU349040 Schoch et al. (2009)
Massariosphaeria grandispora CBS 613.86 NA GU301842 GU296172 GU371725 GU349036 Schoch et al. (2009)
Melogramma campylosporum MBU (ET) JF440978 NA NA NA NA Jaklitsch et al. (2016)
Microdochium phragmitis CBS 423.78 (ET) MH861162 KP858948 NA NA NA Vu et al. (2018)
Microdochium trichocladiopsis CBS 623.77 KP858998 KP858934 NA NA NA Hernandez et al. (2016)
Monosporascus cannonballus FMR6682 NA NA AF340016 NA NA Collado et al. (2002)
Neomassaria fabacearum MFLUCC 16-1875 (HT) NA KX524145 KX524147 NA NA Mapook et al. (2016)
Neomassaria fabacearum GMB0314 NA ON4611373 ON461375 NA ON505016 This study
Neomassaria fabacearum GMB0388 NA ON505052 ON505050 NA ON505019 This study
Neomassaria formosana NTUCC 17-007 NA MH714756 MH714759 NA NA Ariyaw et al. (2018)
Neomassaria hongheensis KUMCC 21-0344 (HT) NA OL423113 OL423115 NA NA Yang et al. (2022)
Neoroussoella bambusae MFLUCC 11-0124 KJ474827 KJ474839 NA KJ474856 KJ474848 Liu et al. (2014)
Neoroussoella heveae MFLUCC 17-1983 MH590693 MH590689 NA NA NA Senwanna et al. (2018)
Neoroussoella solani CPC 26331 KX228261 KX228312 NA NA NA Crous et al. (2013)
Neottiosporina paspali CBS 331.37 NA EU754172 EU754073 GU371779 GU349079 Gruyter et al. (2009)
Oxydothis calamicola MFLUCC 14-1165 (ET) NA KY206761 KY206767 NA NA Konta et al. (2016)
Oxydothis cyrtostachicola FIH 151 DQ660334 DQ660337 NA NA NA Hidayat et al. (2006)
Oxydothis fortunei GMB0315 (HT) ON479893 ON479894 NA NA NA This study
Oxydothis fortunei GMB0389 ON510944 ON510945 NA NA NA This study
Oxydothis inaequalis FIH 018 DQ660336 DQ660339 NA NA NA Hidayat et al. (2006)
Oxydothis metroxylonicola MFLUCC 15-0281 (ET) KY206774 KY206763 KY206769 NA NA Konta et al. (2016)
Oxydothis palmicola MFLUCC 15-0806 (ET) KY206776 KY206765 KY206771 NA NA Konta et al. (2016)
Oxydothis phoenicis MFLUCC 18-0270 (ET) MK088066 MK088062 NA NA NA Unpublished
Oxydothis rhapidicola MFLUCC 14-0616 (ET) NA KY206766 KY206772 NA NA Konta et al. (2016)
Paramassaria samaneae HKAS 102338 NA NG068281 NG067686 NA MK105748 Samarak and Hyde (2019)
Pararoussoella mangrovei MFLU 17-1542 (HT) MH025951 MH023318 NA MH028250 MH028246 Wanasinghe et al. (2018)
Pararoussoella mukdahanensis MFLU 11-0237 (HT) NR155722 NA NA NA NA Dai et al.(2016)
Pararoussoella rosarum MFLU 0654 (HT) NR_157529 NG_059872 NA NA NA Wanasinghe et al. (2018)
Parathyridaria percutanea CBS 868.95 KF322118 KF366449 NA KF366452 KF407987 Ahmed et al. (2014)
Parathyridaria ramulicola CBS 141479 (HT) NR_147657 NA NG_061254 KX650584 KX650536 Jaklitsch et al. (2016)
Parathyridaria robiniae MFLUCC 14-1119 (HT) KY511142 KY511141 NA NA KY549682 Unpublished
Pestalotiopsis theae SAJ-0021 (ET) JN943623 JN940838 JN940785 NA NA Unpublished
Phialemonium atrogriseum CBS 604.67 HE599384 HQ231981 NA NA NA Summerbell et al. (2011)
Pseudomassaria chondrospora It 1200 KR092790 KR092779 NA NA NA Senanayake et al. (2015)
Pseudomassaria chondrospora PC1 (ET) JF440982 NA NA NA NA Jaklitsch et al. (2016)
Pseudoneoconiothyrium euonymi CBS:143426 (HT) MH107915 MH107961 NA MH108007 NA Crous et al. (2018)
Pseudoneoconiothyrium rosae MFLU 18-0117 (HT) NR_157523 NG_059868 NA NA NA Wanasinghe et al. (2018)
Pseudoroussoella elaeicola MFLUCC 15-15-0276a MH742329 MH742326 NA – – Unpublished
Requienella aquatic MFLUCC 18-1040 (HT) NR_171975 NG_073797 NA NA NA Unpublished
Requienella chiangraina MFLUCC 10-0556 (HT) NR_155712 NG_059510 NA NA NA Liu et al. (2014)
Requienella doimaesalongensis MFLUCC 14-0584 (HT) NR_165856 NG_068241 NA KY678394 KY651249 Thambugala et al. (2017)
Requienella guttulata MFLUCC 20-0102 (HT) NR_172428 NG_075383 NA NA NA Zhang et al. (2020)
Requienella hysterioides MAFF 239636 NA AB524621 AB524480 AB539101 AB539114 Schoch et al. (2009)
Requienella hysterioides CBS 546.94 MH862484 MH874129 NA KF443392 KF443399 Vu et al. (2018)
Requienella intermedia CBS 170.96 KF443407 KF443382 NA KF443394 KF443398 Ahmed et al. (2014)
Requienella japanensis MAFF 239636 (HT) NR_155713 NA NA NA NA Liu et al. (2014)
Requienella kunmingensis HKAS 101773 (HT) MH453491 MH453487 NA MH453484 MH453480 Unpublished
Requienella magnatum MFLUCC 15-0185 (HT) NA KT281980 NA NA NA Unpublished
Requienella margidorensis MUT 5329 (HT) NR169906 MN556322 NA MN605917 MN605897 Poli et al. (2020)
Requienella mediterranea MUT5369 (HT) KU314947 MN556324 NA MN605919 MN605899 Poli et al. (2020)
Requienella mexicana CPC 25355 (HT) KT950848 KT950862 NA NA NA Crous et al. (2014)
Requienella bambusarum GMB0316 (HT) ON479891 ON479892 NA ON505011 ON505015 This study
Requienella bambusarum GMB0390 ON505055 ON505051 NA ON505012 ON505017 This study
Requienella neopustulans MFLUCC 11-0609 (HT) KJ474833 KJ474841 NA NA KJ474850 Liu et al. (2014)
Requienella nitidula MFLUCC 11-0634 KJ474834 KJ474842 NA KJ474858 KJ474851 Liu et al. (2014)
Requienella padinae MUT 5503 (HT) NA MN556327 NA MN605922 MN605902 Poli et al. (2020)
Requienella pseudohysterioides GMBC0009 (HT) MW881445 MW881451 NA MW883345 NA Unpublished
Requienella pustulans KT 1709 NA AB524623 NA AB539103 AB539116 Tanaka et al. (2009)
Requienella seminuda RS12 KT949912 NA NA NA NA Jaklitsch et al. (2016)
Requienella seminuda RS13 KT949913 NA NA NA NA Jaklitsch et al. (2016)
Requienella siamensis MFLUCC 0149 (HT) KJ474837 KJ474845 NA KJ474861 KJ474854 Liu et al. (2014)
Requienella siamensis GMB0317 ON4617749 ON461896 NA ON505010 ON505014 This study
Requienella siamensis GMB0391 ON505054 ON505053 NA ON505013 ON505018 This study
Requienella thailandica MFLUCC 0621 (HT) KJ474838 KJ474846 NA NA NA Liu et al. (2014)
Requienella tosaensis KT 1659 NA AB524625 NA AB539104 AB539117 Tanaka et al. (2009)
Requienella tuberculata MFLUCC 0854 (HT) KU940132 KU863121 NA NA KU940199 Dai et al. (2016)
Requienella verrucispora CBS 125434 (HT) KJ474832 NA NA NA NA Liu et al. (2014)
Requienella yunnanensis HKAS 101762 MH453492 MH453488 NA NA MH453481 Unpublished
Robillarda sessilis CBS 114312 (ET) KR873256 KR873284 NA NA NA Crous et al. (2014)
Robillarda terrae CBS 587.71 KJ710484 KJ710459 NA NA NA Crous et al. (2014)
Roussoella scabrispora MFLUCC 14-0582 KY026583 KY000660 NA NA NA Unpublished
Roussoellopsis macrospora MFLUCC 12-0005 NA KJ474847 NA KJ474862 KJ474855 Liu et al. (2014)
Seiridium phylicae CPC 19962 KC005785 KC005807 NA NA NA Crous et al. (2012)
Seynesia erumpens SMH 1291 NA AF279410 AF279409 NA NA Bhattacharya et al. (2000)
Subramaniomyces fusisaprophyticus CBS 418.95 EU040241 NA NA NA NA Crous et al. (2007)
Thyridaria acaciae CBS:138873 KP004469 KP004497 NA NA NA Crous et al. (2014)
Thyridaria broussonetiae CBS 121895 KX650567 NA NA KX650585 KX650538 Jaklitsch et al. (2016)
Thyridariella mahakoshae NFCCl 4215 MG020435 MG020438 NA MG020446 MG023140 Devadatha et al. (2018)
Thyridariella mangrovei NFCCl 4213 MG020434 MG020437 NA MG020445 MG020443 Devadatha et al. (2018)
Torula herbarum CBS 111855 KF443409 KF443386 NA KF443396 KF443403 Ahmed et al. (2014)
Trematosphaeria pertusa CBS 122371 NA GU301876 GU348999 GU371801 GU349085 Schoch et al. (2009)
Vialaea mangiferae MFLUCC 12-0808 KF724974 KF724975 NA NA NA Senanayake et al. (2014)
Vialaea minutella BRIP 56959 (ET) KC181926 KC181924 NA NA NA McTaggart et al. (2013)
Xylaria hypoxylon CBS 122620 (ET) AM993141 NA NA NA NA Persoh et al. (2009)
Xylaria polymorpha MUCL: 49904 FN689809 NA NA NA NA Fournier et al. (2011)
Zopfia rhizophila CBS 207.26 NA DQ384104 L76622 NA NA LoBuglio et al. (1996)

Notes: Type specimens are marked with HT (holotype), ET (epitype); NA: No sequence is available in GenBank; newly generated sequences are indicated in bold.

Phylogenetic analysis

All sequences used for phylogenetic analysis were downloaded from the GenBank, based on published literature and the highest hit rate of ITS in the GenBank database. Sequence data for the construction of the phylogenetic trees are listed in Table 1. Single gene sequence alignments were generated with MAFFT v.7.110 (http://mafft.cbrc.jp/alignment/server/index.html, Katoh and Standley 2013) and multiple sequence alignments were edited manually when necessary in BioEdit v.7.0 (Hall 1999). ALTER (http://www.sing-group.org/ALTER/) was used to convert the file format (Alignment Transformation Envi-Ronment). The maximum likelihood analysis was carried out with GTR+G+I model of site substitution by using RAxML 8.2.12 BlackBox. Bayesian Inference (BI) analysis was performed with MrBayes v.3.2.7a (Huelsenbeck 2012). The branch support was evaluated with 1000 bootstrap replicates (Silvestro and Michalak 2012). Posterior probabilities (PP) were determined by Markov Chain Monte Carlo sampling (MCMC) in MrBayes v. 3.2.7a (Ronquist et al. 2012). Trees were visualized by FigTree v. 1.4.4, and additionally, layouts were done with Photoshop CS6. The alignments and respective phylogenetic trees were uploaded in TreeBASE (http://www.treebase.org. submission number: ID 29735; ID 29736; ID 29737).

Abbreviations

AFTOL-ID: Assembling the Fungal Tree of Life; ATCC: American Type Culture Collection; CBS: Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands; CMW: Tree Pathology Co-operative Program, Forestry and Agricultural Biotechnology Institute, University of Pretoria, South Africa; CPC: Culture collection of Pedro Crous, housed at the Westerdijk Fungal Biodiversity Institute; GMB: herbarium of Guizhou Medical University; HKAS: herbarium of Cryptogams Kunming Institute of Botany Academia Sinica, Chinese Academy of Sciences, Kunming, China; HKUCC: Hong Kong University Culture Collection; ICMP: International Collection of Microorganisms from Plants; IMI: CABI Bioscience UK Centre; JK: J. Kohlmeyer; KT: K. Tanaka; KUMCC: Kunming Institute of Botany Culture Collection, Chinese Science Academy, Kunming, China; MAFF: Ministry of Agriculture, Forestry and Fisheries, Japan; MFLU: Mae Fah Luang University Herbarium, Chiang Rai, Thailand; MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand; MUCL: University Catholique de Louvain; NFCCI: National Fungal Culture Collection of India; SMH: Sabine M. Huhndorf; WU: Fungarium of the Department of Botany and Biodiversity Research, University of Vienna; Others: information not available.

Results

Phylogenetic analyses

Three phylogenetic trees for each genus and their related genera were provided.

The dataset for Fig. 1 consists of 40 taxa for representative strains of species in Neomassariaceae, which has 1989 characters including gaps (SSU: 1–515, tef1:516–1192, LSU: 1193–1989). The best scoring likelihood tree was selected with a final ML optimization likelihood value of -23512.21. Paramassaria samaneae Samarak & K.D. Hyde (HKAS 102338) was selected as the outgroup taxon. Strain GMB0314 gathered with N. fabacearum with high statistical support (100% ML, 1.00 BYPP, Fig. 1).

Figure 1. 

RAxML tree of Neomassaria and related genera obtained from the concatenated DNA sequence data of LSU, SSU and tef1 genes. Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are given above the nodes. The new collections are in red bold and type strains are in bold.

The dataset for Fig. 2 consists of 46 taxa for representative strains of species in Roussoellaceae with 2330 characters, including gaps (ITS: 1–375, tef1: 376–1063, LSU: 1064–1592, rpb2: 1593–2330). The final ML optimization likelihood value of the best scoring likelihood was -16254.35. Torula herbarum Link (CBS 111855) was selected as the outgroup taxon. Strains of the R. bambusarum formed a clade with R. doimaesalongensis Thambug. & K.D. Hyde with statistical support (26% ML, 0.97 BYPP). Strain GMB0317 gathered with R. siamensis Phook., Jian K. Liu & K.D. Hyde with high statistical support (100% ML, 1.00 BYPP, Fig. 2).

Figure 2. 

RAxML tree of Roussoella and related genera based on a combined ITS, LSU, rpb2 and tef1 sequences dataset. Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are given above the nodes. The new collections are in red bold, type strains are in bold.

The alignment for Fig. 3 consists of 66 taxa for representative strains of species in Oxydothidaceae including outgroup taxa with 1630 characters (ITS: 1–307, LSU: 308–1089, SSU: 1090–1630). The best scoring likelihood tree was selected with a final ML optimization likelihood value of -19975.73. Cordana pauciseptata Preuss (CBS 121804) was selected as the outgroup taxon. Our strains of the new species O. fortunei are from a distinct clade with O. inaequalis Hidayat et al. (98% ML, 1 BYPP, Fig. 3).

Figure 3. 

RAxML tree of Oxydothis and related genera based on a combined ITS, LSU and SSU sequences dataset. Bootstrap support values for ML equal to, or greater than, 60% and BYPP equal to or greater than 0.95 are given above the nodes. The new collections are in red bold and ex-type strains are in bold.

Taxonomy

The four species in this study were Neomassaria fabacearum, Roussoella bambusarum, Roussoella siamensis, Oxydothis fortunei. Neomassaria and Roussoella is a genus of ascomycete fungi in the order Pleosporales. Oxydothis is a genus of ascomycete fungi in the order Xylariales.

Neomassaria fabacearum Mapook, Camporesi & K.D. Hyde, Fungal Diversity 80: 77 (2016)

MycoBank No: 552274
Fig. 4

Descriptions

see Hyde et al. (2016).

Specimens examined

China, Guizhou Province, the campus of Guizhou Medical University (26°24'34.02"N, 106°45'16.22"E), on bamboo, 12 December 2021. Altitude: 1145 m, H.M. Hu, 2021GYHS23 (GMB0314; KUN-HKAS 123429; living culture GMBC0314).

Figure 4. 

Neomassaria fabacearum (GMB0314) A stromata on host substrate B, C appearance of ascomata on substrate D cross section of ascomata E pseudoparaphyses F, H asci I longitudinal section of an ascoma J peridium K–N ascospores O apical apparatus (stained in Melzer’s Reagent). Scale bars: 0.5 mm (C–D); 10 μm (E–H, K–O); 50 μm (I, J).

Other material examined

China, Guizhou Province, the campus of Guizhou Medical University (26°24'34.01"N, 106°45'09.24"E), on bamboo, 12 December 2021. Altitude: 1135 m, H.M. Hu, 2021GYHS28 (GMB0388, living culture GMBC0388).

Notes

There are three Neomassaria species documented in Index Fungorum (accession date: May 1, 2022). Type species of N. fabacearum was originally described from Italy (Hyde et al. 2016). Subsequently, N. formosana, and N. hongheensis were introduced from Taiwan and Yunnan in China, respectively (Ariyawansa et al. 2018; Yang et al. 2022). The ascospore dimension of N. fabacearum is between those of N. formosana (20–30 × 3–7 μm) and N. hongheensis (14–17 × 4–8 μm) (Hyde et al. 2016; Ariyawansa et al. 2018; Yang et al. 2022). Phylogenetic analyses of the combined SSU, LSU and tef1 sequences dataset shows that new collections gather with N. fabacearum (MFLU 16–1875), the type specimen, with the high support (100% ML, 1 BYPP; Fig. 1). Morphologically, the features of GMB0314 are consistent with those of N. fabacearum (Hyde et al. 2016). Neomassaria fabacearum was first introduced to the China.

Roussoella bambusarum H. M. Hu & Q. R. Li, sp. nov.

MycoBank No: 844142
Fig. 5

Holotype

GMB0316.

Etymology

In reference to the host, Bambusa bambusarum (Lour.) Raeusch. ex Schult. ‘Fernleaf’ R. A. Young

Description

Saprobic on decaying culms of B. bambusarum. Sexual morp: Ascostromata 111–146 μm high, 460–560 μm diam., (x̄ = 123 × 539 μm, n = 30), immersed under a clypeus, solitary or scattered, raised hemispherical or dome-shaped on host epidermis, black, coriaceous, glabrous, uni-loculate. Locules 335–414 μm diam., 128–212 μm high, immersed within ascostromata, black, globose to subglobose. Ostioles with minute papillate. Peridium 19–34 μm thick, composed of dark brown thin-walled cells of textura angularis. Hamathecium comprised of 1–2 μm wide, numerous, septate, branched, anastomosing, filiform, hyaline, pseudoparaphyses. Asci 120–143 × 8–12 μm (x̄ = 134 × 10 μm, n = 30), 8-spored, bitunicate, cylindrical, curved, short pedicellate with knob-like pedicel, apically rounded with an indistinct ocular chamber. Ascospores 14–20 × 6–7 μm (x̄ = 17.6 × 6.7 μm, n = 30), dark brown to brown, 1-seriate, sometimes overlapping, 2-celled, constricted at the septum, ellipsoidal to fusiform, straight, rough-walled, guttulate, conically rounded ends, with longitudinal striations. Asexual morph: Undetermined.

Figure 5. 

Roussoella bambusarum (Holotype, GMB0316) A stromata on host substrate B ascostromata on bamboo culm C cross-section of ascostromata D–F asci G longitudinal section of ascostromata H peridium I pseudoparaphyses J apical apparatus (stained in Melzer’s Reagent) K–N ascospores. Scale bars: 0.5 mm (B–C); 10 μm (D–F, H–N); 50 μm (G).

Culture characters

Ascospores germinated on PDA within 24 hours at 25 °C, colonies are reaching 5 cm diam. The colony on the surface is white, grey, circular, flocculent, dense, cottony mycelium, colony reverse is white and gray, white in the middle. Not sporulating on OA nor on PDA.

Specimens examined

China, Guizhou Province, Guiyang Huaxi National Urban Wetland Park (26°2'2.34"N, 106°34'16.22"E), on decaying culms of B. bambusarum, 12 October 2021. Altitude: 1130 m, Y.P Wu and H.M Hu, 2021 HXGY01 (GMB0316, holotype; KUN-HKAS 123431, isotype; GMBC0316, ex-type living culture).

Other examined material

China, Guizhou Province, Guiyang Huaxi National Urban Wetland Park (26°10'44.13"N, 106°43'13.12"E), on decaying culms of B. bambusarum, 15 October 2021. Altitude: 1201 m, Y.P Wu and H.M Hu, 2021 HXGY55 (GMB0390; GMBC0390, living culture).

Notes

Morphologically, Roussoella bambusarum is similar to R. thailandica D.Q. Dai et al., but differs from the latter by having larger ascospores (17.6 × 6.7 μm vs. 14.5 × 5.5 μm), larger upper cells, occasionally curve, narrowly at both ends, with irregular longitudinal striations. (Liu et al. 2014). Phylogenetic analysis showed that R. bambusarum and R. doimaesalongensis Thambug. & K.D. Hyde were clustered together (26% ML, 0.97 BYPP; Fig. 2) (Thambugala et al. 2017).

Roussoella siamensis Phook., Jian K. Liu & K.D. Hyde, Phytotaxa 181(1): 18 (2014)

MycoBank No: 550665
Fig. 6

Descriptions

see Liu et al. (2014).

Specimens examined

China, Guizhou Province, Guiyang Huaxi National Urban Wetland Park (26°2'23.04"N, 106°34'16.22"E) on decaying culms of B. bambusarum, 12 October 2021. Altitude: 1130 m, Y.P. Wu and H.M. Hu, 2021 HXGY03 (GMB0317; living culture GMBC0317).

Figure 6. 

Roussoella siamensis (GMB0317) A stromata on host substrate B, C ascostromata on bamboo culm D cross-section of ascostromata E Longitudinal section of ascostromata F peridium G–I asci J pseudoparaphyses K–L culture on PDA M–P ascospores Scale bars: 0.5 mm (C–D); 50 μm (E); 10 μm (F–J, M–P).

Other material examined

China, Guizhou Province, Guiyang Huaxi National Urban Wetland Park (26°2'10.10"N, 106°34'16.10"E) on decaying culms of B. bambusarum, 15 October 2021. Altitude: 1145 m, Y.P. Wu and H.M. Hu, 2021 HXGY70 (GMB0391; living culture GMBC0391).

Notes

Phylogenetic analyses of the alignment combining ITS, LSU, rpb2 and tef1 show that GMB0317 cluster with R. siamensis (MFLU 13-0639) with the high support value (100% ML, 1 BYPP; Fig. 2). Characteristics of GMB0317 are consistent with those of R. siamensis, which was originally introduced from decaying bamboo culms in Thailand (Liu et al. 2014) This species was first found in China.

Oxydothis fortunei H. M. Hu & Q. R. Li, sp. nov.

MycoBank No: 844141
Fig. 7

Holotype

GMB0315.

Etymology

In reference to the host, Trachycarpus fortunei (Hook.) H. Wendl.

Description

Saprobic on surface of culms of T. fortunei. Sexual morph: Ascomata 205–317 μm diam. (x̄ = 261 μm, n = 30), solitary or aggregated in groups, immersed, forming slightly raised as blistering areas on the host surface, long axis horizontal to that of the host, 18–41 μm high × 155–207 μm broad, in transverse section, ellipsoid, ostiolate, coriaceous, black, flat. Peridium 24–27 μm thick, composed of 2–3 several layers of flattened, light-brown cells. Asci 108–121× 9–14 μm (x̄ = 114 × 12 μm, n = 20), 8-spored, unitunicate, cylindrical, mostly straight, pedicellate, with a J-, subapical apparatus, 4.2–4.9 μm high, 5.5–6.8 μm diam. Ascospores 56–72 μm × 3–4 μm (x̄ = 66 × 3.3 μm, n = 30), fusiform, hyaline, obliquely 1–2-seriate, tapering gradually from the center to the ends, with multi-guttules in each cell, pointed processes. Asexual morph: Undetermined.

Figure 7. 

Oxydothis fortunei (Holotype, GMB0315) A stromata on host substrate B close-up of ascomata C cross-section of the ascomata D longitudinal section of an ascoma E peridium F–H asci I apical apparatus (stained in Melzer’s Reagent) J, K ascospores. Scale bars: 0.5 mm (B–C); 10 μm (D–K).

Culture characteristics

Ascospores germinated on PDA within 24 hours at 25 °C, colonies are reaching 4.5 cm diam. circular, transparent, thin, colony reverse is same. Not sporulating on OA nor on PDA.

Specimen examined

China Guizhou Province, Long gong scenic spot (26°04'35.02"N, 105°52'15.04"E), on surface of culms of T. fortunei, 5 December 2021. Altitude: 1120m, Q.R. Li and X. Xu, 2021 LG9 (GMB0315, holotype; KUN-HKAS 123430, isotype; ex-type living culture GMBC0315).

Other examined material

China, Guizhou Province, Long gong scenic spot (26°04'47.41"N, 105°31'10.34"E), on surface of culms of palm, 7 December 2021. Altitude: 1095m, Q.R. Li and X. Xu, 2021 LG15 (GMB0389; living culture GMBC0389).

Notes

Oxydothis fortunei is morphologically similar to O. nonamyloidea K.D. Hyde and O. rhapidicola S. Konta & K.D. Hyde in the shape of ascospores (Hyde 1994; Hidayat et al. 2006; Konta et al. 2016). However, the ascospores of O. fortunei (56–72 × 3–4 μm) are shorter than those of O. nonamyloidea (94–115 × 3.5–4.5 μm) and O. rhapidicola (47–50 × 3–5 μm). Moreover, it is distinguished from O. rhapidicola since the latter has a blue slit-like ascus subapical apparatus in Melzer’s reagent (Konta et al. 2016). Oxydothis fortunei showed the close kinship to O. inaequalis (100% ML, 1 BYPP; Fig. 3). However, O. fortunei differs from O. inaequalis by its shape of the ascospores, and the J- ascus subapical apparatus as well as the smaller ascospores (56–72 × 2.9–3.9 μm vs. 78–100 × 5–6 μm) (Hidayat et al. 2006).

Discussion

In this study, two new species and two new records associated with bamboo and palm were introduced based on phylogenetic relationships of combined ITS, LSU, SSU, rpb2 and tef1 sequences and morphological evidences.

There are a large number of fungi associated with bamboo and palm in China (Hyde et al. 2002; Phukhamsakda et al. 2022). Studies on the diversity of bamboo and palm fungi can be of economic significance and of academic value (Arnold and Lewis 2005). According to statistics, there are nearly 500 bamboo species distributed in 37 genera in China, which play an important role in human life, such as in the fields of architecture, production tools, artwork, and landscaping, etc. (Zhao and Wei 2018). In China, palms are mainly used for ornamental purposes in landscape gardens (Fetouh et al. 2018). About 2,450 species of palm plants were documented in the world, belonging to 183 genera (Qureshimatva et al. 2018). The rich and diverse ecosystems composed of these bamboo and palm resources provide good habitats for fungi to survive, creating the diversity of fungal species (Cheek et al. 2020). There are 75 genera and 189 fungal species on bamboo that have been reported in mainland China, and 79 species and 58 genera of bamboo fungi that have been reported in Hong Kong (Yong et al. 2009; Shukla et al. 2016). Many species of Roussoella have been introduced from the bamboo (Liu et al. 2014). New collections of Roussoella also were saprophyte on bamboo. Most species of Oxydothis were discovered on palm including O. fortunei (Konta et al. 2016). This is the first introduction of Neomassaria species associated on bamboo (Ariyawansa et al. 2018; Yang et al. 2022). In this study, four microfungi were introduced, which enriches the diversity of fungi on bamboo and palm in China. Meanwhile, all those four species are saprophyte on and accelerates the decay of bamboo or palm. As an ideal growth substrate for fungi, bamboo fungi are rich in species, and there are a large number of fungi to be discovered.

Acknowledgements

This research was supported by the National Natural Science Foundation of China (31960005 and 32000009); the Fund of the Science and Technology Foundation of Guizhou Province ([2020]1Y059); Guizhou Province Ordinary Colleges and Universities Youth Science and Technology Talent Growth Project [2021]154.

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