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Research Article
Striatiguttulaceae, a new pleosporalean family to accommodate Longicorpus and Striatiguttula gen. nov. from palms
expand article infoSheng-Nan Zhang‡§|, Kevin D. Hyde, E.B. Gareth Jones#, Rajesh Jeewon¤, Ratchadawan Cheewangkoon|, Jian-Kui Liu«§
‡ University of Electronic Science and Technology of China, Chengdu, Thailand
§ Guizhou Key Laboratory of Agricultural Biotechnology, Guizhou Academy of Agricultural Science, Guiyang, China
| Chiang Mai University, Chiang Mai, Thailand
¶ Mae Fah Luang University, Chiang Rai, Thailand
# Unaffiliated, Hants, United Kingdom
¤ University of Mauritius, Mauritius, Mauritius
« University of Electronic Science and Technology of China, Chengdu, China

Corresponding author: Jian-Kui Liu ( ljiankui@gmail.com )

Academic editor: George Mugambi
© 2019 Sheng-Nan Zhang, Kevin D. Hyde, E.B. Gareth Jones, Rajesh Jeewon, Ratchadawan Cheewangkoon, Jian-Kui Liu.
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: Zhang S-N, Hyde KD, Jones EBG, Jeewon R, Cheewangkoon R, Liu J-K (2019) Striatiguttulaceae, a new pleosporalean family to accommodate Longicorpus and Striatiguttula gen. nov. from palms. MycoKeys 49: 99-129. https://doi.org/10.3897/mycokeys.49.30886
Open Access

Abstract

Palms represent the most morphological diverse monocotyledonous plants and support a vast array of fungi. Recent examinations of palmicolous fungi in Thailand led to the discovery of a group of morphologically similar and interesting taxa. A polyphasic approach based on morphology, multi-gene phylogenetic analyses and divergence time estimates supports the establishment of a novel pleosporalean family Striatiguttulaceae, which diversified approximately 39 (20–63) MYA (crown age) and 60 (35–91) MYA (stem age). Striatiguttulaceae is characterized by stromata or ascomata with a short to long neck, trabeculate pseudoparaphyses and fusiform to ellipsoidal, 1–3-septate ascospores, with longitudinal striations and paler end cells, surrounded by a mucilaginous sheath. Multi-gene phylogenetic analysis showed that taxa of Striatiguttulaceae form a well-supported and distinct monophyletic clade in Pleosporales, and related to Ligninsphaeriaceae and Pseudoastrosphaeriellaceae. However, these families can be morphologically demarcated by the slit-like ascomata and extremely large ascospores in Ligninsphaeriaceae and the rather narrow fusiform ascospores in Pseudoastrosphaeriellaceae. Eight strains of Striatiguttulaceae formed two monophyletic sub-clades, which can be recognized as Longicorpus gen. nov. and Striatiguttula gen. nov. Morphologically, the genus Longicorpus can be differentiated from Striatiguttula by its elongated immersed ascomata and fusiform ascospores with relatively larger middle cells and paler end cells. Two new species Striatiguttula nypae and S. phoenicis, and one new combination, Longicorpus striataspora are introduced with morphological details, and phylogenetic relationships are discussed based on DNA sequence data.

Keywords

6 new taxa, divergence times, Dothideomycetes, epitype, sexual morphs

Introduction

Fungi associated with palms have been intensively investigated by Hyde and his co-workers (Goh and Hyde 1996, Fröhlich and Hyde 2000, Hyde and Alias 2000, Hyde et al. 2000, Yanna et al. 2001a,b,c, Taylor and Hyde 2003, Hyde et al. 2007), and provided a significant contribution to their diversity and taxonomy. There have been a number of interesting studies on palm fungi. For example, Fröhlich and Hyde (1999) reviewed the biodiversity of palm fungi in the tropics, and proposed the ratio of host specific fungi to palm species as 33 to 1 rather than the general ratio of 6 to 1 for all plants proposed by Hawksworth (1991). Taylor et al. (2000) investigated biogeographical distribution of microfungi from temperate and tropical palms, and found different fungal assemblages from these two regions, and also revealed that the difference was more related to climatic influences than hosts sampled. Subsequently, Yanna et al. (2001b, 2002) studied fungal communities and succession of palms, and pointed out that fungal species compositions were distinct on different hosts and at different sites, and even differed from different palm tissues. In addition, some studies were dedicated to endophytic palmicolous fungi (Rodrigues and Samuels 1990, Taylor et al. 1999, Fröhlich et al. 2000, Hyde and Soytong 2008, Pinruan et al. 2010a, Mahmoud et al. 2017) and pathogens (Fröhlich et al. 1997, Hyde and Cannon 1999, Elliott et al. 2010, Mohammadi 2014). Other studies have focused on fungi on peat swamp palms (Pinruan et al. 2002, 2007, 2008, 2010b, 2014, Pinnoi et al. 2003) and from mangrove palms (Suetrong et al. 2009, Loilong et al. 2012, Zhang et al. 2018). All these examples indicate that species are diverse and palms harbour numerous undescribed microfungi.

Ascomycetes from palms are a very diverse assemblage and the best represented family is Xylariaceae (Xylariales, Sordariomycetes), with three commonly recorded genera Anthostomella (Xylariaceae), Linocarpon (Linocarpaceae) and Oxydothis (Oxydothidaceae) (Taylor and Hyde 2003, Hidayat et al. 2006, Konta et al. 2016b, 2017). In recent years, a series of Dothideomycetes from palms were described as new on the basis of morphology and phylogenetic analyses, such as astrosphaeriella-like species (recognized as three groups: Astrosphaeriellopsis, Astrosphaeriellaceae and Pseudoastrosphaeriellaceae) and species of Botryosphaeria (Botryosphaeriaceae), Fissuroma (Aigialaceae), Neodeightonia (Botryosphaeriaceae) and Roussoella (Roussoellaceae) (Liu et al. 2010, 2011a,b, 2012, 2014, Phookamsak et al. 2015, Konta et al. 2016a,c, Wanasinghe et al. 2018). The diversity of palmicolous ascomycetes recovered can in part be due to the wide range of hosts and habitats sampled, the latter including terrestrial, freshwater, and marine or mangrove ecosystems. There are four palm species encountered as mangrove associates in Asia (Tomlinson 1986): Calamus erinaceus (Becc.) J.Dransf., Nypa fruticans Wurmb., Oncosperma tigillarium (Jack) Ridl. and Phoenix paludosa Roxb. Loilong et al. (2012) documented the greatest biodiversity of fungi on N. fruticans listing 135 taxa (90 Ascomycota, three Basidiomycota and 42 asexual taxa), of which 97 taxa were described (Hyde 1992a,b, Hyde et al. 1999, Hyde and Alias 2000, Pilantanapak et al. 2005, Hyde and Sarma 2006) with support from DNA sequence data (Suetrong et al. 2015). Nevertheless, few studies have focused on fungi growing on Phoenix paludosa, where Lignincola conchicola, Kirschsteiniothelia phoenicis and Acuminatispora palmarum were recently reported (Liu et al. 2011a, Hyde et al. 2018, Zhang et al. 2018).

Nypa fruticans is an ancient palm that grows in brackish water, while Phoenix paludosa is found in the upper parts of mangroves and tolerates salt water, with both occurring in Thailand mangrove sites. In an ongoing study on the taxonomy of fungi occurring on palms, we collected fungi colonizing these two palm hosts from different mangrove sites in Thailand. Interestingly, a group of ascomycetes recovered appears to be new to science based on morphology and multi-gene phylogenetic evidence. The aim of this study was to characterize the novel taxa and investigate their phylogenetic relationships in the order Pleosporales, as well as apply the divergence times as additional evidence, especially in higher taxa ranking, for the establishment of new family Striatiguttulaceae.

Materials and methods

Specimen collection, examination and single spore isolation

Decayed rachides or petioles of Nypa fruticans and Phoenix paludosa were collected from Chanthaburi, Krabi and Ranong provinces in Thailand. The collected specimens were washed under running water and examined via laboratory procedures as outlined by Jones and Hyde (1988). Morphological characters were observed using a Carl Zeiss stereo microscope fitted with an AxioCam ERC 5S camera and photographed by a Nikon ECLIPSE 80i compound microscope fitted with a Canon EOS 600D digital camera. Free hand sections of fruiting bodies were made into slides within water mounts and observed under Motic SMZ 168 stereo microscope. Measurements were taken by Tarosoft Image Frame Work program v. 0.9.7 and images used for figures processed with Adobe Photoshop CS6 Extended v. 13.0 software. Isolations were obtained from single spores as described in Choi et al. (1999). New taxa were established based on recommendations outlined by Jeewon and Hyde (2016). The strains isolated in this study were deposited in Mae Fah Luang University Culture Collection (MFLUCC) and Guizhou Culture Collection (GZCC). Herbarium specimens were deposited at the herbaria of Mae Fah Luang University (MFLU), Chiang Rai, Thailand and Kunming Institute of Botany Academia Sinica (HKAS), Kunming, China. MycoBank numbers (Crous et al. 2004) and Facesoffungi numbers (Jayasiri et al. 2015) are provided.

DNA extraction, PCR amplification and sequencing

Fungal genomic DNA was extracted from fresh mycelia scraped from the margin of a colony on PDA that was incubated at 25 °C–28 °C for 30 days, followed by the Ezup Column Fungi Genomic DNA Purification Kit (Sangon Biotech (Shanghai) Co., Ltd, China) following the manufacturer’s instructions. Two partial rDNA genes and two protein coding genes were used in this study: the large subunit of the nuclear ribosomal RNA genes (LSU), the small subunit of the nuclear ribosomal RNA (SSU), the translation elongation factor 1-alpha (TEF1α) and the second largest subunit of RNA polymerase II (RPB2). The primers used were LR0R and LR5 for LSU (Vilgalys and Hester 1990), NS1/NS4 for SSU (White et al. 1990), EF1-983F/EF1-2218R for TEF1α (Rehner and Buckley 2005) and fRPB2-5F/fRPB2-7cR for RPB2 (Liu et al. 1999). The amplification reactions were performed in 25μL of PCR mixtures containing 9.5μL ddH2O, 12.5μL 2× PCR MasterMix (TIANGEN Co., China), 1μL DNA temple and 1μL of each primer. The PCR thermal cycle program for LSU, SSU and TEF1α amplification were as follows: initial denaturing step of 94 °C for 3 min, followed by 40 cycles of denaturation at 94 °C for 45 seconds, annealing at 56 °C for 50 seconds, elongation at 72 °C for 1 min, and final extension at 72 °C for 10 min. The PCR thermal cycle program for the partial RNA polymerase second largest subunit (RPB2) was followed as initially 95 °C for 5 min, followed by 40 cycles of denaturation at 95 °C for 1 min, annealing at 52 °C for 2 min, elongation at 72 °C for 90 seconds, and final extension at 72 °C for 10 min. Purification and sequencing of PCR products were carried out with primers mentioned above at Sangon Biotech (Shanghai) Co., Ltd, China.

Sequence alignment and phylogeny analyses

A concatenated data set of LSU, SSU, TEF1α and RPB2 sequences was used for phylogenetic analyses with the inclusion of reference taxa from GenBank (Table 1). Sequences were aligned using MAFFT v.7 (http://mafft.cbrc.jp/alignment/server/) (Katoh and Standley 2013) and then checked visually and manually optimized using BioEdit v.7.0.9 (Hall 1999). Representative families in Pleosporales and several major groups in Dothideomycetes were included in our analyses, and taxa in Arthoniomycetes were selected as outgroup. A maximum likelihood (ML) analysis was performed at the CIPRES web portal (Miller et al. 2010) using RAxML v.7.2.8 as part of the “RAxML-HPC Blackbox (8.2.10)” tool (Stamatakis 2006, Stamatakis et al. 2008). A general time-reversible model (GTR) was applied with a discrete GAMMA distribution and four rate classes. Fifty thorough ML tree searches were carried out in RAxML v.7.2.7 under the same model. One thousand non-parametric bootstrap iterations were run with the GTR model and a discrete gamma distribution. The resulting replicates were plotted on to the best scoring tree obtained previously.

Table 1.
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Taxa used in this study and their GenBank accession numbers. The type species of each genus are marked with superscript T and ex-type strains are in bold.

Taxa Strain / Culture GenBank Accession numbers
LSU SSU TEF1α RPB2
Acrocordiopsis patilii BCC28167 GU479773 GU479737 – GU479812
Acrocordiopsis patilii T BCC28166 GU479772 GU479736 – GU479811
Acuminatispora palmarum MFLUCC 18-0460 MH390438 MH390402 MH399249 MH399252
Acuminatispora palmarum T MFLUCC 18-0264 MH390437 MH390401 MH399248 –
Aigialus grandis T BCC18419 GU479774 GU479738 GU479838 GU479813
Aigialus mangrovei BCC33563 GU479776 GU479741 GU479840 GU479815
Aigialus parvus BCC 18403 GU479778 GU479744 GU479842 GU479817
Aigialus rhizophorae BCC 33572 GU479780 GU479745 GU479844 GU479819
Alternaria alternata CBS 916.96 DQ678082 DQ678031 DQ677927 DQ677980
Amniculicola lignicola T Ying01 EF493861 EF493863 – EF493862
Anteaglonium abbreviatum T ANM 925a GQ221877 – GQ221924 –
Anteaglonium globosum ANM 925.2 GQ221879 – GQ221925 –
Antealophiotrema brunneosporum T CBS 123095 LC194340 – LC194382 LC194419
Aquasubmersa japonica KT 2862 LC061587 LC061582 – LC194421
Aquasubmersa mircensis T MFLUCC 11-0401 JX276955 JX276956 – –
Arthonia dispersa UPSC2583 AY571381 AY571379 – –
Ascocratera manglicola T BCC 09270 GU479782 GU479747 GU479846 GU479821
Astrosphaeriella fusispora T MFLUCC 10-0555 KT955462 – – KT955413
Astrosphaeriella neofusispora MFLUCC 11-0161 KT955463 KT955444 – KT955418
Astrosphaeriella stellata KT998 AB524592 AB524451 – –
Astrosphaeriellopsis bakeriana MFLUCC 11-0027 JN846730 – – –
Astrosphaeriellopsis bakeriana T CBS 115556 GU301801 – GU349015 –
Bimuria novae-zelandiae T CBS 107.79 AY016356 AY016338 DQ471087 DQ470917
Botryosphaeria dothidea CMW 8000 KF766319 KF766233 – –
Byssothecium circinans T CBS 675.92 AY016357 – GU349061 DQ767646
Capnodium coffeae CBS 147.52 DQ247800 DQ247808 DQ471089 DQ247788
Caryospora minima – EU196550 EU196551 – –
Caryospora aquatica MFLUCC 11-0008 MH057847 MH057850 – –
Cladosporium herbarum CBS 399.80 DQ678074 DQ678022 DQ677918 DQ677971
Cryptocoryneum condensatum CBS 122629 LC194351 LC194309 LC096139 LC194433
Cryptocoryneum pseudorilstonei CBS 113641 LC194364 LC194322 LC096152 LC194446
Delitschia chaetomioides SMH 3253.2 GU390656 – – –
Delitschia didyma UME 31411 DQ384090 AF242264 – –
Delitschia winteri CBS 225.62 DQ678077 – – DQ677975
Dendrographa decolorans Ertz 5003 (BR) NG_027622 AY548809 – –
Didymella exigua T CBS 183.55 EU754155 EU754056 – –
Didymosphaeria rubi-ulmifolii MFLUCC 14-0023 KJ436586 KJ436588 – –
Dissoconium aciculare CBS 204.89 GU214419 GU214523 – –
Dothidotthia aspera CPC 12933 EU673276 EU673228 – –
Dothidotthia symphoricarpi T CPC 12929 EU673273 EU673224 – –
Extremus antarcticus CCFEE 5312 KF310020 – – KF310086
Fissuroma bambusae MFLUCC 11-0160 KT955468 KT955448 KT955430 KT955417
Halotthia posidoniae T BBH 22481 GU479786 – – –
Hermatomyces iriomotensis MAFF 245730 LC194367 – LC194394 LC194449
Hypsostroma caimitalense GKM 1165 GU385180 – – –
Hypsostroma saxicola T SMH 5005 GU385181 – – –
Hysterium angustatum CBS 236.34 FJ161180 GU397359 FJ161096 –
Hysterobrevium smilacis CBS 114601 FJ161174 FJ161135 FJ161091 –
Latorua caligans T CBS 576.65 KR873266 – – –
Latorua grootfonteinensis CBS 369.72 KR873267 – – –
Lecanactis abietina Ertz 5068 (BR) AY548812 AY548805 – –
Longicorpus striataspora T MFLUCC 18-0267 MK035988 MK035973 MK034428 MK034436
Longicorpus striataspora MFLUCC 18-0268 MK035989 MK035974 MK034429 MK034437
Longicorpus striataspora MFLUCC 17-2515 MK035990 MK035975 MK034430 MK034438
Longicorpus striataspora MFLUCC 17-2516 MK035991 MK035976 MK034431 MK034439
Lepidosphaeria nicotiae CBS 101341 DQ678067 – – DQ677963
Leptosphaeria doliolum T CBS 505.75 GU301827 GU296159 GU349069 –
Leptoxyphium fumago CBS 123.26 GU301831 GU214535 GU349051 GU371741
Ligninsphaeria jonesii GZCC 15-0080 KU221038 – – –
Ligninsphaeria jonesii T MFLUCC 15-0641 KU221037 – – –
Lindgomyces cinctosporae R56-1 AB522431 AB522430 – –
Lindgomyces ingoldianus T ATCC 200398 AB521736 AB521719 – –
Lindgomyces rotundatus KT1096 AB521740 AB521723 – –
Lophiostoma macrostomoides GKM1033 GU385190 – – –
‘Lophiotrema’ boreale CBS 114422 LC194375 – LC194402 LC194457
Lophiotrema lignicola CBS 122364 GU301836 GU296166 GU349072 –
Lophiotrema nucula T CBS 627.86 GU301837 GU296167 GU349073 GU371792
Macrodiplodiopsis desmazieri T CPC 24971 KR873272 – – –
Massaria anomia CBS 591.78 GU301839 GU296169 – GU371769
Massaria gigantispora M26 HQ599397 HQ599447 HQ599337 –
Massaria inquinans T M19 HQ599402 HQ599444 HQ599342 HQ599460
Massarina eburnea T CBS 473.64 GU301840 GU296170 GU349040 GU371732
Mauritiana rhizophorae T BCC 28866 GU371824 – GU371817 GU371796
Melanomma pulvis-pyrius T CBS 124080 GU456323 GU456302 GU456265 GU456350
Murispora rubicunda T IFRD 2017 FJ795507 GU456308 – –
Mycosphaerella graminicola CBS 292.38 DQ678084 DQ678033 – DQ677982
Neoastrosphaeriella krabiensis T MFLUCC 11-0025 JN846729 JN846739 – –
Neodeightonia palmicola MFLUCC10-0822 HQ199222 HQ199223 – –
Neotestudina rosatii CBS 690.82 DQ384107 DQ384069 – –
Nigrograna mackinnonii T CBS 674.75 GQ387613 – – KF015703
Nigrograna marina CY 1228 GQ925848 – – GU479823
Phaeosphaeria oryzae T CBS 110110 GQ387591 GQ387530 – KF252193
Phoma herbarum T CBS 276.37 DQ678066 DQ678014 DQ677909 DQ677962
Piedraia hortae var. hortae CBS 480.64 GU214466 AY016349 – DQ677990
Pleomassaria siparia T CBS 279.74 DQ678078 DQ678027 – DQ677976
Pleospora herbarum T CBS 191.86 DQ247804 DQ247812 DQ471090 DQ247794
Polyplosphaeria fusca T KT 1616 AB524604 AB524463 – –
Preussia funiculata T CBS 659.74 GU301864 – – –
Prosthemium orientale KT1669 AB553748 AB553641 – –
Pseudoastrosphaeriella africana MFLUCC 11-0176 KT955474 KT955454 KT955436 KT955421
Pseudoastrosphaeriella bambusae MFLUCC 11-0205 KT955475 – KT955437 KT955414
Pseudoastrosphaeriella longicolla MFLUCC 11-0171 KT955476 – KT955438 KT955420
Pseudoastrosphaeriella thailandensis T MFLUCC 11-0144 KT955478 KT955457 KT955440 KT955416
Pseudotetraploa curviappendiculata T HC 4930 AB524608 AB524467 – –
Quadricrura septentrionalis T HC 4984 AB524616 AB524475 – –
Racodium rupestre L346 EU048583 EU048575 – –
Roccella fuciformis Tehler 8171 FJ638979 – – –
Roussoella nitidula T MFLUCC 11-0182 KJ474843 – KJ474852 KJ474859
Roussoellopsis macrospora MFLUCC 12-0005 KJ474847 – KJ474855 KJ474862
Salsuginea ramicola KT2597.2 GU479801 GU479768 GU479862 GU479834
Salsuginea ramicola T KT 2597.1 GU479800 GU479767 GU479861 GU479833
Striatiguttula nypae T MFLUCC 18-0265 MK035992 MK035977 MK034432 MK034440
Striatiguttula nypae MFLUCC 17-2517 MK035993 MK035978 MK034433 MK034441
Striatiguttula nypae MFLUCC 17-2518 MK035994 MK035979 MK034434 –
Striatiguttula phoenicis T MFLUCC 18-0266 MK035995 MK035980 MK034435 MK034442
Tetraplosphaeria sasicola T KT563 AB524631 AB524490 –
Trematosphaeria pertusa T CBS 122371 FJ201992 – – GU371801
Triplosphaeria maxima T KT 870 AB524637 AB524496 – –
Ulospora bilgramii T CBS 101364 DQ678076 DQ678025 DQ677921 DQ677974
Verruculina enalia T BCC 18401 GU479802 – GU479863 GU479835
Wicklowia aquatica AF289-1 GU045446 – – –
Wicklowia aquatica T F76-2 GU045445 GU266232 – –
Zopfia rhizophila T CBS 207.26 DQ384104 – – –

Abbreviations:

ATCC: American Type Culture Collection, Virginia, USA;

BBH: Biotec Bangkok Herbarium, Thailand;

BCC: BIOTEC Culture Collection, Bangkok, Thailand;

CBS: Centraal bureau voor Schimmel cultures, Utrecht, The Netherlands;

CPC: Collection of Pedro Crous housed at CBS;

DAOM: Plant Research Institute, Department of Agriculture (Mycology), Ottawa, Canada;

GZCC: Guizhou Culture Collection;

IFRDCC: Culture Collection, International Fungal Research & Development Centre, Chinese Academy of Forestry, Kunming, China;

JCM: the Japan Collection of Microorganisms, Japan;

MAFF: Ministry of Agriculture, Forestry and Fisheries, Japan;

MFLU: Mae Fah Luang University Herbarium Collection;

MFLUCC: Mae Fah Luang University Culture Collection, Chiang Rai, Thailand.

ANM: A.N. Miller;

GKM: G.K. Mugambi;

JK: J. Kohlmeyer;

KT: K. Tanaka;

SMH: S.M. Huhndorf.

Maximum parsimony (MP) analyses were performed using the heuristic search option with 1000 random taxa additions and tree bisection and reconnection (TBR) as the branch-swapping algorithm. All characters were unordered and of equally weight; gaps were treated as missing data. Maxtrees setting was 1000, and zero-length branches were collapsed, and all parsimonious trees were saved. Clade stability was assessed using a bootstrap (BT) analysis with 1000 replicates, each with 10 replicates of random stepwise addition of taxa (Hillis and Bull 1993). Tree length [TL], Consistency index [CI], Retention index [RI], Rescaled consistency index [RC], Homoplasy index [HI] were calculated.

The Bayesian analysis was performed using PAUP v.4.0b10 (Swofford 2002) and MrBayes v.3.1.2 (Ronquist and Huelsenbeck 2003). The best model for different genes partition in the concatenated data set was determined by MrModeltest 2.3 (Nylander 2004). Posterior probabilities (Rannala and Yang 1996) were determined by Markov Chain Monte Carlo sampling (MCMC) (Larget and Simon 1999) in MrBayes v.3.1.2. Four simultaneous Markov chains were run for 10 million generations and trees were sampled every 1000th generation, thus 10,000 trees were obtained. The suitable burn-in phases were determined by inspecting likelihoods and parameters in Tracer version 1.6 (Rambaut et al. 2013). Based on the tracer analysis, the first 1,000 trees representing 10% were discarded as the burn-in phase in the analysis. The remaining trees were used to calculate posterior probabilities in the majority rule consensus tree (critical value for the topological convergence diagnostic set to 0.01). Phylogenetic tree was visualized by FigTree v.1.4.2 (Rambaut 2014), and the alignment is deposited in TreeBASE under the accession number TB2: S23392 (http://purl.org/phylo/treebase/phylows/study/TB2:S23392).

Divergence times estimates

One secondary data and two fungal fossil calibrations were used in this study. The split between Arthoniomycetes and Dothideomycetes was selected as a secondary calibration point referring to previous evolutionary molecular studies (Gueidan et al. 2011, Prieto and Wedin 2013, Beimforde et al. 2014, Pérez-Ortega et al. 2016, Phukhamsakda et al. 2016), with a mean of 300 MYA and standard deviation (SD) of 50 MYA in a normal posterior distribution. Simultaneously, one ascomycete fossil Metacapnodiaceae (Schmidt et al. 2014), was used as the common ancestor of Capnodiales, with constraint of mean 100 MYA and SD 150 MYA in a normal posterior distribution (Pérez-Ortega et al. 2016, Hongsanan et al. 2016, Phukhamsakda et al. 2016, Liu et al. 2017). Whereas the fossil Margaretbarromyces dictyosporus (Mindell et al. 2007, Berbee and Taylor 2010, Taylor et al. 2015) was used to calibrate the Aigialus (Aigialaceae) crown, with an offset of 35 MYA in a gamma distribution (Phukhamsakda et al. 2016). Divergence time estimates were carried out by BEAST v 1.8.0 (Drummond et al. 2012). Aligned sequence data were partitioned separately for LSU, SSU, TEF1α and RPB2 data set, and loaded to prepare an XML file constructed with BEAUti v1.8.0. The substitution models, clock models and the tree prior parameters were set to be linked. The nucleotide substitution model was set to GTR (Generalized Time Reversible) + Gamma + Invariant sites, with estimated base frequencies, four gamma categories and without partitions. An uncorrelated relaxed clock model (Drummond et al. 2007) with a lognormal distribution of rates for each gene estimate was used for the analyses. We used a Yule tree prior, which assumes a constant speciation rate per lineage, and a randomly generated starting tree. The analysis was run for 100 million generations and parameters were sampled every 10,000 generations. Tracer v.1.6 (Rambaut et al. 2013) was used to analyze the trace files, and the acceptable effective sample sizes (ESS) values were greater than 200. Maximum clade creditability (MCC) trees were annotated using TreeAnnotator v1.8.0 and then visualized in FigTree v.1.4.2 (Rambaut 2014).

Results

Phylogenetic results

The multi-gene dataset comprised 113 taxa and 4113 characters after alignment (LSU: 919 bp; SSU: 1245 bp; TEF1α: 929 bp; RPB2: 1020 bp) including gaps. RAxML, MP and Bayesian analyses were conducted and resulted in generally congruent topologies, and the familial assignments are similar to previous work (Hashimoto et al. 2017, Liu et al. 2017). Maximum parsimony analyses indicated that 2,302 characters were constant, 355 variable characters parsimony uninformative and 1,456 characters are parsimony-informative. A heuristic search yield four equally most parsimonious trees (TL = 10905, CI = 0.278, RI = 0.561, RC = 0.156, HI = 0.722). The combined dataset provided higher confidence values for the familial level than those of the individual gene trees (data not shown), and RAxML analysis based on LSU, SSU, TEF1α and RPB2 yielded a best sorting tree (Figure 1) with a final optimization likelihood value of -52455.532059.

Figure 1. 

RAxML tree of Pleosporales based on analysis of combined LSU, SSU, TEF1α and RPB2 sequence data. Bootstrap values for ML and MP equal to or greater than 75% are placed above and below the branches respectively. Branches with Bayesian posterior probabilities (PP) from MCMC analysis equal or greater than 0.95 are in bold. Newly generated sequences are indicated in red.

The eight newly generated strains clustered together and positioned outside the two suborders (Massarineae and Pleosporineae) of Pleosporales, and formed a well-supported monophyletic clade and represented as a new linage of Pleosporales. The phylogeny also revealed that this clade is close to Ligninsphaeriaceae, Pseudoastrosphaeriellaceae, Testudinaceae and Tetraplosphaeriaceae, and can be recognized as a novel family (Striatiguttulaceae). Furthermore, the eight strains formed two well-supported monophyletic sub-clades, which can be identified as two new genera (Longicorpus and Striatiguttula) with three species (Longicorpus striataspora, Striatiguttula nypae and S. phoenicis).

Divergence time estimates

The maximum clade credibility (MCC) tree with divergence estimates (Figure 2) obtained through BEAST was topologically identical to those recovered by Bayesian and ML procedures with regards to the placement Pleosporales and several major lineages within Dothideomycetes. The mean dates of Pleosporales crown corroborate reported estimates (Phukhamsakda et al. 2016, Liu et al. 2017, 2018) are provided in Table 2. The results showed that the new family Striatiguttulaceae diverged approximately 60 (35–91) MYA, which is line with recommendations for ranking families proposed in related studies (Hyde et al. 2017, Liu et al. 2017).

Figure 2. 

Maximum clade credibility (MCC) tree with divergence times estimates for Pleosporales and selected groups in Dothideomycetes, obtained from a Bayesian approach (BEAST) using one secondary and two fossil calibrations. Numbers at nodes indicate posterior probabilities (pp) for node support; bars correspond to the 95% highest posterior density (HPD) intervals. Numbers inside green circles indicate nodes used for calibrations: 1) the split of Arthoniomycetes and Dothideomycetes; 2) Metacapnodiaceae; 3) Margaretbarromyces dictyosporus.

Table 2.
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Divergence time estimates of Pleosporales and selected lineages of Dothideomycetes obtained from a Bayesian approach (BEAST) on basis of three calibrations. For each divergence, the median and the 95% highest posterior density (HPD) are provided. Divergence times are provided in millions of years (MYA).

Nodes Crown group Divergence times
This study Phukhamsakda et al. (2016) Liu et al. (2017) Liu et al. (2018)
Crown age Stem age Crown age
1 Arthoniomycetes-Dothideomycetes 312 (220–413) – 317 – 310~320
2 Capnodiales 195 (131–266) 269 (196–347) 147 216/ (151–283) ~120
3 Aigialus 41 (35–56) 64 (44–91) 39 – ~50
4 Dothideomycetes 286 (210–369) 312 (220–413) 293 ~(210–370) 341 (257–425) 255 (166–344)
5 Pleosporales 206 (148–274) 221 (158–292) 211 ~(140–270) 204 (148–260) 195 (124–271)
6 Striatiguttulaceae 39 20–63) 60 (35–91) – – –

Taxonomy

Striatiguttulaceae S.N.Zhang, K.D.Hyde & J.K.Liu, fam. nov.

MycoBank No: MB828272
Facesoffungi: FoF 05032

Etymology

Name refers to the name of the type genus.

Description

Saprobic on palms distributed in mangrove habitats. Sexual morph: Stromata black, scattered to gregarious, immersed beneath host epidermis, and erumpent to superficial, with a papilla or a short to long neck, ampulliform, subglobose or conical, uni-loculate or bi-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate, clypeate or not clear, glabrous or somewhat interwoven pale brown hyphae or setae. Peridium composed of several brown to hyaline cell layers. Hamathecium of trabeculate pseudoparaphyses. Asci 8-spored, bitunicate, cylindric-clavate, pedicellate. Ascospores hyaline to brown, uniseriate to biseriate or triseriate, fusiform or ellipsoidal, 1–3-septate, striate, guttulate, with paler end cells and surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Type genus

Striatiguttula S.N.Zhang, K.D.Hyde & J.K.Liu.

Notes

The family Striatiguttulaceae is introduced to accommodate two new genera Longicorpus and Striatiguttula, characterized by the immersed, and erumpent to superficial stromata, with a papilla or a short to long neck, trabeculate pseudoparaphyses, bitunicate asci, and hyaline to brown, fusiform to ellipsoidal, striate, guttulate, 1–3-septate ascospores, with paler end cells and surrounded by a mucilaginous sheath. Members of Striatiguttulaceae are morphologically similar to the genera Leptosphaeria and Trematosphaeria, but they are phylogenetically distinct and also differ in ascospores characteristics and the latter two have coriaceous, heavily pigmented thick-walled peridium. Multi-gene phylogenetic analyses revealed a close relationship of Striatiguttulaceae to Ligninsphaeriaceae and Pseudoastrosphaeriellaceae. However, Striatiguttulaceae differs from Pseudoastrosphaeriellaceae as the latter has 1–3-septate or 2–5-septate ascospores, which are narrowly fusiform with acute ends and all cells are concolorous. The slit-like ascomata and broad fusiform, 1-septate, rather large ascospores (79–121 × 14–23 µm) in Ligninsphaeriaceae (Zhang et al. 2016) are distinct from those found in Striatiguttulaceae. Additionally, a divergence time estimate analysis indicated that the crown age 39 (20–63) MYA and stem age 60 (35–91) MYA of Striatiguttulaceae, match with the recommendations of using divergence times to recognize families in Liu et al. (2017). Attempts were made to culture the asexual morph in order to build comprehensive familial concept for Striatiguttulaceae, but it was not successful. Further morphological investigations together with more molecular data are needed.

Striatiguttula S.N.Zhang, K.D.Hyde & J.K.Liu, gen. nov.

MycoBank No: MB828273
Facesoffungi: FoF 05033

Etymology

Name refers to the striate and guttulate ascospores.

Description

Saprobic on palms which are distributed in mangrove habitats. Sexual morph: Stromata black, scattered to gregarious, immersed beneath host epidermis, and erumpent to superficial, with a papilla or a short to long neck, ampulliform, subglobose or conical, uni-loculate or bi-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate, clypeate or not, glabrous or somewhat interwoven pale brown hyphae or setae, lying at apex of the neck. Peridium thin, composed of several pale brown to hyaline angular cells. Wall of the neck having elongated angular cells. Hamathecium filament thin, trabeculate pseudoparaphyses, septate, branched, anastomosing, embedded in a gelatinous matrix. Asci 8-spored, bitunicate, cylindric-clavate, pedicellate, apically rounded, with an ocular chamber. Ascospores hyaline to brown, uniseriate to biseriate or triseriate, fusiform to ellipsoidal, 1–3-septate, constrict, the middle cells slightly swollen towards the central septa, striate, guttulate, end cells slightly paler or not, surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Type species

Striatiguttula nypae S.N.Zhang, K.D.Hyde & J.K.Liu.

Striatiguttula nypae S.N.Zhang, K.D.Hyde & J.K.Liu, sp. nov.

MycoBank No: MycoBank number: MB828274
Facesoffungi number: FoF 05034
Figure 3

Etymology

The epithet reflects the genus name of the host plant Nypa fruticans, from which the specimens were collected.

Type

THAILAND. Ranong: Ranong, on decayed rachis of Nypa fruticans Wurmb (Arecaceae), 3 December 2016, S.N.Zhang, SNT44 (holotype: MFLU 18–1576; isotype: HKAS 97480; ex-type living culture MFLUCC 18–0265 = GZCC 18–0005).

Description

Saprobic on mangrove palm Nypa fruticans. Sexual morph: Stromata in vertical section 240–380 µm high, 195–385 µm diameter, (x̄ = 318.2 × 289.0 µm, n = 15), black, scattered, gregarious, immersed beneath host epidermis, and erumpent to superficial, with a papilla or short to long neck up to 550 µm, subglobose or conical, uni-loculate or bi-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate and clypeate, glabrous or somewhat interwoven pale brown hyphae or with setae, lying at apex of the neck. Peridium 9–16 µm thin, composed of several pale brown to hyaline angular cells, compressed and pallid inwardly. Wall of the clypeus composed of brown cells of textura epidermoidea and dark brown host tissue. Wall of the neck with thicker and elongated angular cells. Hamathecium 1–2 µm wide, trabeculate pseudoparaphyses, septate, branched, filamentous, anastomosing, embedded in a gelatinous matrix. Asci 64–145 × 8–17 µm, (x̄= 106.3 × 13.8 µm, n = 30), 8-spored, bitunicate, fissitunicate, cylindric-clavate, pedicellate, apically rounded, with an ocular chamber. Ascospores 18–26 × 4–6 µm, (x̄ = 22.2 × 5.3 µm, n = 50), hyaline to brown, uniseriate to biseriate or triseriate, fusiform, 1–3-septate, constricted at the central septum, the upper middle cell slightly swollen towards the central septum, straight or slightly curved, striate, guttulate, end cells slightly paler, surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Figure 3. 

Striatiguttula nypae (holotype MFLU 18–1576, paratype MFLU 18–1578). a–c Appearance of stromata on host surface d–f vertical section through a stroma g structure of peridium h structure of clypeus near the ostiole, composed of epidermoidea cells and host tissue i ostiole with periphyses j pseudoparaphyses k apex of the neck, with somewhat interwoven pale brown hyphae or setae l–o ascus p–s ascospores t ascospore in India ink and presenting a clear mucilaginous sheath u germinating ascospore v colony on PDA. Scale bars: 500 μm (a), 200 μm (b, c), 100 μm (d–f), 10 μm (g, p–s, u), 20 μm (h, i, l–o, t), 50 μm (k).

Culture characteristics

Colonies on PDA attaining 15 mm diam. within 21 days at 25 °C under natural light, velvety, centrally raised, greenish grey or greyish olivaceous, reverse dull green or grey olivaceous, with a margin of translucent, milky white to hyaline mycelia.

Additional specimens examined

Thailand. Krabi: near Pali, Mueang Krabi District, on submerged decaying rachis of Nypa fruticans Wurmb (Arecaceae), 30 August 2017, S.N.Zhang, SNT207 (paratype: MFLU 18–1577; living culture MFLUCC 17–2517 = GZCC 18–0006); Thailand. Krabi: near Pali, Mueang Krabi District, on submerged decaying rachis of Nypa fruticans Wurmb (Arecaceae), 30 August 2017, S.N.Zhang, SNT208 (paratype: MFLU 18–1578; living culture MFLUCC 17–2518 = GZCC 18–0007).

Habitat and distribution

Inhabiting Thai mangrove forests, Andaman sea (west) coastline, Thailand.

Notes

Striatiguttula nypae varies in ascomatal appearance, mostly immersed beneath the plant surface, sometimes visible as a papilla or dome-shaped area on the plant surface, and becomes erumpent to superficial, with a papilla or a short to long neck. The typical morphological characters of S. nypae are the appearance of stromata, with interwoven pale brown hyphae or setae at the apex of the neck, and the hyaline to brown, 1–3-septate, fusiform ascospores, striate, guttulate, with slightly paler end cells and a mucilaginous sheath. We have compared Striatiguttula nypae to previously encountered species on Nypa fruticans, and several morphologically similar mangrove fungal species. However, the striation of ascospores can be a reliable morphological character to distinguish Striatiguttula nypae from Astrosphaeriella nipicola (Hyde and Fröhlich 1998), A. nypae (Hyde 1992a) and Leptosphaeria spp. (Spegazzini 1881, Cribb and Cribb 1955, Hyde et al. 1999, Pang et al. 2011), which are characterized by one or three septa and hyaline or brown ascospores. The presence of erumpent to superficial stromata, the number of septa and size of ascospores in S. nypae are also different from Trematosphaeria spp. (Table 3), despite being quite similar in ascospore morphology. In addition, the phylogenetic analysis showed that the three isolates of Striatiguttula nypae clustered together and were distinct from S. phoenicis.

Table 3.
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Morphological comparison of three new species to Trematosphaeria lineolatispora, T. mangrovis and T. striataspora.

Taxa Ascomata Peridium (µm) Pseudoparaphyses (µm) Asci (µm) Ascospores References
Ascomata morphology (high × diam. μm) Ascospores morphology Ascospores size (µm)
Longicorpus striataspora Immersed, erumpent, ampulliform, subglobose or conical, CA 300–500 × 230–560 11–15 1.5 85–160 × 10–17 Fusiform, 1–3-septate, CC 24–45 × 7–8.8 This study
Striatiguttula nypae Immersed and erumpent to superficial, subglobose or conical, uni-loculate or bi-loculate, CA 240–380 × 195–385 9–16 1–2 64–145 × 8–17 Fusiform, 1–3-septate, CC 18–26 × 4–6 This study
Striatiguttula phoenicis Immersed, erumpent, ampulliform, subglobose, uni-loculate, CB 195–580 × 135–390 10–24 1–2 89–141 × 12–18 Fusiform to ellipsoidal, 1–3-septate, CC but nearly concolorous 20–29 × 6–10 This study
Trematosphaeria lineolatispora K.D. Hyde Immersed with a flattened base, conical to subglobose, clypeate, ostiolate, papillate 90–180 × 216–360 up to 25 2–4 120–204 × 14–18 Fusiform, mostly 5-septate; CC 34–48 × 7–10 Hyde 1992b
Trematosphaeria mangrovis Kohlm. Semi-immersed, conical or subglobose, papillate 380–750 × 450–800 64–88 1.6–2.2 190–220 × 20–22 Broad fusiform or ellipsoidal, 3-septate, CC but no striations 30–35.6–41 × 10–11.8–13 (–16.5) Kohlmeyer 1968
Trematosphaeria striataspora K.D. Hyde Developing amongst the host cortical cells beneath the host epidermis, ampulliform, subglobose or conical, CA 176–355 × 352–528 42–57 (clypeus), thin-walled 0.8–2.1 99–173 × 11–23 Fusiform, 3(–6)- septate, CC 31–38 × 6–9 Hyde 1988

CA: (Characteristics A) clypeate, ostiolate, periphysate, papillate;

CB: (Characteristics B) ostiolate, periphysate, papillate;

CC: (Characteristics C) central cells larger, brown, end cells smaller and paler, ascospore wall covered in distinct longitudinal striations, and surrounded by a sheath.

Striatiguttula phoenicis S.N.Zhang, K.D.Hyde & J.K.Liu, sp. nov.

MycoBank No: MB828275
Facesoffungi: FoF 05035
Figure 4

Etymology

The epithet referring to the host on which the fungus was collected.

Type

THAILAND. Ranong: Amphoe Mueang Ranong, Tambon Ngao, on decayed rachis of Phoenix paludosa Roxb. (Arecaceae), 6 December 2016, S.N.Zhang, SNT51 (holotype: MFLU 18–1579; isotype: HKAS 97481; ex-type culture MFLUCC 18–0266 = GZCC 18–0008).

Description

Saprobic on mangrove date palm Phoenix paludosa. Sexual morph: Ascomata in vertical section 195–580 µm high, 135–390 µm diameter, (x̄ = 396.0 × 230.3 µm, n = 15), black, scattered, rarely gregarious, immersed, and erumpent through host epidermis by a papilla or a short neck, ampulliform, subglobose, uni-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate, glabrous or somewhat interwoven pale brown hyphae or setae, lying around apex of the neck. Peridium 10–24 µm thin, composed of several pale brown to hyaline cells of textura angularis, compressed and pallid inwardly. Wall of the neck composed thick and elongated angular pale brown to brown cells with hyaline inner layers. Hamathecium of 1–2 µm wide, septate, branched, filamentous, anastomosing, trabeculate pseudoparaphyses, embedded in a gelatinous matrix. Asci 89–141 × 12–18 µm, (x̄ = 120.5 × 15.4 µm, n = 20), 8-spored, bitunicate, fissitunicate, cylindric-clavate, pedicellate, apically rounded, with an ocular chamber. Ascospores 20–29 × 6–10 µm, (x̄ = 24.5 × 7.8 µm, n = 40), hyaline to brown (all cells nearly concolorous), uniseriate to biseriate, fusiform to ellipsoidal, 1–3-septate, constricted at the central septum, the upper middle cell slightly swollen and larger, straight or slightly curved, striate, guttulate, surrounded by an irregular mucilaginous sheath. Asexual morph: Undetermined.

Figure 4. 

Striatiguttula phoenicis (holotype MFLU 18–1579). a–c Appearance of ascoma on host surface d, e vertical section through an ascoma f ostiole g apex of the neck, with somewhat interwoven pale brown hyphae or setae h structure of peridium i, j pseudoparaphyses k–n asci o–t ascospores u ascospore in India ink and presenting a clear mucilaginous sheath v germinating ascospore w colony on PDA. Scale bars: 500 μm (a), 100 μm (b, c), 200 μm (d, e), 50 μm (f, g), 20 μm (h, k–n), 10 μm (i, j, o–v).

Culture characteristics

Colonies on PDA attaining 14 mm diam within 21 days at 25 °C under natural light, velvety, centrally raised, greenish grey or greyish olivaceous, reverse dull olivaceous or grey, with a margin of translucent, milky white to hyaline mycelium.

Habitat and distribution

Inhabiting Thai mangrove forests, Andaman sea (west) coastline, Thailand.

Notes

The fusiform to ellipsoidal, 1–3-septate ascospores of Striatiguttula phoenicis is similar to those of Trematosphaeria mangrovis, associated with submerged roots of mangrove trees. However, Striatiguttula phoenicis differs from T. mangrovis (Kohlmeyer 1968) as the latter has larger ascospores and lacks striations (Table 3). Striatiguttula phoenicis is morphologically different from S. nypae as it has ellipsoidal ascospores which are broader in width. Currently, the erumpent to superficial stromata have not been found in S. phoenicis. The phylogenetic analysis also confirms that they are distinct species. There are 26 noticeable nucleotide differences across the 474 nucleotides (Suppl. material 1) of ribosomal ITS sequence data (strains: MFLUCC 18–0266 vs. MFLUCC 18–0265, MFLUCC 17–2517 and MFLUCC 17–2518).

Longicorpus S.N.Zhang, K.D.Hyde & J.K.Liu, gen. nov.

MycoBank No: MB828276
Facesoffungi: FoF 05036

Etymology

Name refers to the elongated ascomata and ascospores.

Description

Saprobic on mangrove palms. Sexual morph: Ascomata black, scattered to gregarious, immersed, and erumpent through host epidermis by a papilla or a short to long neck, sometimes visible as a slightly raised, dome-shaped area, with a clypeus comprises host tissue and fungal hyphae, ampulliform, subglobose or conical, uni-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate, glabrous or somewhat interwoven pale brown hyphae or setae. Peridium composing of pale brown or brown angular cells. Hamathecium of septate, branched, thin, anastomosing trabeculate pseudoparaphyses, embedded in a gelatinous matrix. Asci 8-spored, bitunicate, cylindric-clavate, pedicellate, apically rounded, with an ocular chamber. Ascospores uniseriate to biseriate, hyaline to brown, fusiform, 1–3-septate, the upper middle cell slightly swollen towards the central septum, and the end cells paler and smaller, striate, guttulate, surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Type species

Longicorpus striataspora (K.D.Hyde) S.N.Zhang, K.D.Hyde & J.K.Liu.

Notes

Longicorpus differs from Striatiguttula in having elongate, fusiform ascospores with relatively larger middle cells and paler end cells (Figures 3–5). Multi-gene phylogeny also strongly supports the establishment of two genera. Longicorpus is sister to Striatiguttula but forms a distinct phylogenetic sub-clade (Figure 1). There are noticeable differences (nucleotide substitutions) at specific positions in the large subunit nuclear ribosomal DNA: 51, 428, 436, 465 (T substituted by C); 53, 55, 102, 153, 163, 166, 251, 367, 369, 427, 435, 440, 446, 448, 466, 504, 550, 654 (C substituted by T); 130 (G substituted by A); 362, 406 (G substituted by T); 370 (C substituted by A); 547 (A substituted by C).

Longicorpus striataspora (K.D.Hyde) S.N.Zhang, K.D.Hyde & J.K.Liu, comb. nov.

MycoBank No: MB828277
Facesoffungi: FoF 05037
Figure 5

Trematosphaeria striataspora K.D.Hyde, Botanical Journal of the Linnean Society 98(2): 142. 1988.

Astrosphaeriella striataspora (K.D.Hyde) K.D.Hyde, Botanical Journal of the Linnean Society 110(2): 97. 1992. Type: North Sumatra. K.D.Hyde (holotype: IMI 312390).

Epitype

THAILAND. Ranong: Ranong, on decayed rachis of Nypa fruticans Wurmb (Arecaceae), 6 December 2016, S.N. Zhang, SNT93 (epitype designated here: MFLU 18–1580; epi-isotype designated here: HKAS 97479; ex-epitype living culture MFLUCC 18–0267 = GZCC 18–0009).

Description

Saprobic on mangrove palms. Sexual morph: Ascomata in vertical section (including short papilla) 300–500 µm high, 230–560 µm diameter, (x̄ = 405.3 × 376.6 µm, n = 15), long neck up to 1285 µm, black, scattered to gregarious, immersed, and erumpent through host epidermis by a papilla or a short to long neck, sometimes visible as a slightly raised, dome-shaped area, with a clypeus comprises host tissue and fungal hyphae, ampulliform, subglobose or conical, uni-loculate, coriaceous to carbonaceous, ostiolate, periphysate, papillate, glabrous or somewhat interwoven pale brown hyphae or setae, lying at apex of the neck. Peridium 11–15 µm wide, composing of brown to pale brown angular cells, thicker at the rim towards the apex. Hamathecium comprising up to 1.5 µm wide, septate, branched, filamentous, trabeculate, anastomosing pseudoparaphyses, embedded in a gelatinous matrix. Asci 85–160 × 10–17 µm (x̄ = 122.7 × 13.7 µm, n = 22), 8-spored, bitunicate, cylindric-clavate, pedicellate, apically rounded, with an ocular chamber. Ascospores 24–45 × 7–8.8 µm, (x̄ = 34.2 × 7 µm, n = 40), uniseriate to biseriate, hyaline to brown, fusiform, 1–3-septate, the upper middle cell slightly swollen towards the central septate, middle cells larger and longer, end cells paler and smaller, straight or slightly curved, striate, guttulate, surrounded by a mucilaginous sheath. Asexual morph: Undetermined.

Figure 5. 

Longicorpus striataspora (epitype MFLU 18–1580, epi-paratype MFLU 18–1582). a, b Appearance of ascoma on host surface c–e vertical section through an ascoma, with a clypeus near the ostiole f ostiole with periphyses g apex of the neck, with somewhat interwoven pale brown hyphae or setae h–k ascus l peridium in vertical section m vertical section of the neck, with thicker angular cells n pseudoparaphyses o–r ascospores s ascospore in India ink and presenting a clear mucilaginous sheath t germinating ascospore u, v Colony on PDA. Scale bars: 500 μm (a), 200 μm (b), 100 μm (c–e), 10 μm (f, l, n–t), 50 μm (g), 20 μm (h–k, m).

Culture characteristics

Colonies on PDA attaining 12 mm diameter within 21 days at 25 °C under natural light, velvety, centrally raised, irregular to circular in shape, greenish grey and mixed with milky white mycelium at the edge of a colony, the reverse dull green or grey olivaceous.

Additional specimens examined

Thailand. Chanthaburi, 12°26'43"N, 102°15'47"E, on rachis of Phoenix paludosa Roxb. (Arecaceae), immersed mangrove mud and water, 25 April 2017, S.N.Zhang, SNT130 (epi-paratype MFLU 18–1581; living culture MFLUCC 18–0268 = GZCC 18–0010); Thailand. Krabi, near Pali, on decayed rachis of Nypa fruticans Wurmb (Arecaceae), immersed mangrove mud and water, 30 August 2017, S.N.Zhang, SNT195 (epi-paratype MFLU 18–1582; living culture MFLUCC 17–2515 = GZCC 18–0011; MFLUCC 17–2516 = GZCC 18–0012).

Habitat and distribution

Inhabiting in Thai mangrove forests, the Andaman sea (west) coastline and the Gulf of Thailand (east).

Notes

Longicorpus striataspora was found on two mangrove palm species, Nypa fruticans and Phoenix paludosa. The typical characteristics of L. striataspora are the deeply immersed, carbonaceous ascomata with a long neck, and the striate, guttulate, fusiform, 1–3-septate ascospores, with larger middle cells and relatively smaller and paler end cells, surrounded by a mucilaginous sheath. However, such characteristics are similar to Trematosphaeria spp. (Table 3), and match with Trematosphaeria striataspora (Hyde 1988), the holotype collected from intertidal wood of Nypa fruticans in North Sumatra. Trematosphaeria striataspora was later accommodated in Astrosphaeriella Syd. & P. Syd. (Hyde 1992a) with proposals for recollection and further phylogenetic studies (Liu et al. 2011b, Phookamsak et al. 2015). We have compared the fresh collections of Longicorpus striataspora with the type material of Trematosphaeria striataspora, and concluded that the two are identical in morphology. On the other hand, the genus Trematosphaeria Fuckel has been assigned to the family Trematosphaeriaceae K.D. Hyde, Y. Zhang ter, Suetrong & E.B.G. Jones, based on molecular data of its type species T. pertusa Fuckel. Therefore, we follow Ariyawansa et al. (2014) and designate an epitype for Longicorpus striataspora in this study.

Discussion

A novel pleosporalean family, Striatiguttulaceae is introduced herein, which has been compared to several morphologically similar genera and species recovered from mangroves. This study introduces three novel species including an epitypification. The use of divergence times as an additional evidence for ranking taxa (especially in higher taxa ranking) has become possible and several studies have been carried out across different fungal groups (Phukhamsakda et al. 2016, Samarakoon et al. 2016, Divakar et al. 2017, Hongsanan et al. 2017, Hyde et al. 2017, Liu et al. 2017, Zhao et al. 2017). To better understand the placement of Striatiguttulaceae, divergence time was also estimated and this study supports taxonomic schemes proposed earlier. The recent study of ranking a family with divergence time estimates is Liu et al. (2018), who introduced Lentimurisporaceae, a new pleosporalean family. We have recovered essentially similar phylogenetic topology, and in an extensive dataset that included berkleasmium-like taxa (referred to Liu et al. 2018), phylogenies generated were also topologically identical to those recovered herein (Figure 1). The monotypic family Ligninsphaeriaceae is sister to Striatiguttulaceae, and berkleasmium-like taxa are close to Aquasubmersaceae, Hermatomycetaceae and Salsuginaceae respectively. In this study, the ages of most families in Pleosporales, especially those positioned outside the two suborders were estimated in our divergence time analysis, and the results are comparable to other studies. However, Ligninsphaeriaceae, Pseudoastrosphaeriellaceae and Testudinaceae have relatively younger stem ages than that in Liu et al. (2017), presumably due to different taxa sampling in our phylogeny.

The nature of the pseudoparaphyses (sensu Liew et al. 2000) is worth considering here and may provide evidence for separate lineages. The family Striatiguttulaceae, currently with three species, have trabeculate pseudoparaphyses, but also appearing septate. Phylogenetically closely related families of Ligninsphaeriaceae and Pseudoastrosphaeriellaceae are characterized by cellular pseudoparaphyses and trabeculate pseudoparaphyses respectively.

Considering the ecology of these Striatiguttulaceae species in relation to the mangrove ecosystem, salinity may be an important contributor to their presence. Loilong et al. (2012) have compared fungal community from Nypa fruticans at different salinities, and found freshwater species in lower salinity and marine species at higher salinity. Although no salinity was measured during our collections, Longicorpus striataspora, Striatiguttula nypae and S. phoenicis can be considered as manglicolous, because they are found from decayed rachides/petioles of palms, which are perennials submerged in soft mangrove mud and salty water, and well adapted to the varying salinity in mangroves by tidal water. On the other hand, their ascospores have mucilaginous sheaths and lack elaborate appendages, which are also typical characteristics of most mangrove fungi (Jones 2000).

Acknowledgements

We are grateful to the grant the Thailand Research Fund for supporting collection and research facilities (Grant No. RSA5980068). Jian-Kui Liu thanks the National Natural Science Foundation of China (NSFC 31600032) and Science and Technology Foundation of Guizhou Province (LH [2015]7061). Kevin D. Hyde would like to thank the Thailand Research Grants (No. RDG6130001 and No. 60201000201). The authors would like to thank the staff of Ngao Mangrove Forest Research Center for their assistance in the sample’s collection. We are also grateful to Dr. Shaun Pennycook (Manaaki Whenua Landcare Research, New Zealand) for advising on fungal nomenclature. Ning-Guo Liu is acknowledged for assisting in molecular experiments. We also thank the University of Mauritius for its support.

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Supplementary material

Supplementary material 1 

Phylogenetic analysis

Sheng-Nan Zhang, Kevin D. Hyde, E.B. Gareth Jones, Rajesh Jeewon, Ratchadawan Cheewangkoon, Jian-Kui Liu
This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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