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Article

Insight into the Systematics of Microfungi Colonizing Dead Woody Twigs of Dodonaea viscosa in Honghe (China)

by
Dhanushka N. Wanasinghe
1,2,3,
Peter E. Mortimer
1,2,* and
Jianchu Xu
1,2,3,*
1
CAS Key Laboratory for Plant Biodiversity and Biogeography of East Asia (KLPB), Kunming Institute of Botany, Chinese Academy of Science, Kunming 650201, Yunnan, China
2
World Agroforestry, East and Central Asia, 132 Lanhei Road, Kunming 650201, Yunnan, China
3
Honghe Center for Mountain Futures, Kunming Institute of Botany, Honghe County 654400, Yunnan, China
*
Authors to whom correspondence should be addressed.
J. Fungi 2021, 7(3), 180; https://doi.org/10.3390/jof7030180
Submission received: 29 January 2021 / Revised: 26 February 2021 / Accepted: 27 February 2021 / Published: 3 March 2021
(This article belongs to the Special Issue Fungal Biodiversity and Ecology)
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Abstract

:
Members of Dodonaea are broadly distributed across subtropical and tropical areas of southwest and southern China. This host provides multiple substrates that can be richly colonized by numerous undescribed fungal species. There is a severe lack of microfungal studies on Dodonaea in China, and consequently, the diversity, phylogeny and taxonomy of these microorganisms are all largely unknown. This paper presents two new genera and four new species in three orders of Dothideomycetes gathered from dead twigs of Dodonaea viscosa in Honghe, China. All new collections were made within a selected area in Honghe from a single Dodonaea sp. This suggests high fungal diversity in the region and the existence of numerous species awaiting discovery. Multiple gene sequences (non-translated loci and protein-coding regions) were analysed with maximum likelihood and Bayesian analyses. Results from the phylogenetic analyses supported placing Haniomyces dodonaeae gen. et sp. in the Teratosphaeriaceae family. Analysis of Rhytidhysteron sequences resulted in Rhytidhysteron hongheense sp. nov., while analysed Lophiostomataceae sequences revealed Lophiomurispora hongheensis gen. et sp. nov. Finally, phylogeny based on a combined dataset of pyrenochaeta-like sequences demonstrates strong statistical support for placing Quixadomyces hongheensis sp. nov. in Parapyrenochaetaceae. Morphological and updated phylogenetic circumscriptions of the new discoveries are also discussed.

1. Introduction

Fungi are cosmopolitan, featuring a broad geographic distribution and high level of diversity compared to plants and other organisms [1]. 140,000 fungal species have been listed in Kirk [2], and one recent overview of global fungi and fungus-like taxa by Wijayawardene et al. [3] listed approximately 100,000 known taxa. However, both numbers represent less than 5% of global fungal estimates [4,5]. There is a need to bridge the gap between our understanding of these missing fungi and their diversity. Numerous diverse habitats and substrates remain unexplored. It has also been observed that several countries and regions are bountiful repositories of many missing fungi, such as northern Thailand [6]. Despite this, fungi in Asia are relatively understudied [5]. Even though the Greater Mekong Subregion (GMS) hosts a high level of biodiversity and forms an integral part of the Indo-Burma Biodiversity Hotspot, fungi from this region largely remain a mystery. Yunnan Province, China, as part of the GMS, is home to an extremely wide variety of ecosystems. Mycologists working in Yunnan have recently focused their attention on abundant “less-researched habitats” for fungal occurrences, including caves, forests, grasslands, lakes, karst landscapes and mountains; accordingly, there is a rich body of literature documenting novel discoveries across the region [7,8,9,10,11,12,13,14,15,16,17,18,19].
The Honghe Hani and Yi Autonomous Prefecture is in south-eastern Yunnan Province. The region features a mountainous topography, numerous limestone deposits and a south-eastward decreasing elevation gradient. Owing to its abundant precipitation and heat as well as its dramatic altitudinal range and varied flora, this region harbours a rich diversity of plant species [20,21]. Along the altitudinal gradient, vegetation from lower to higher elevations range from tropical and montane rain forests to monsoon evergreen, montane mossy evergreen and summit mossy evergreen broad-leaved forests [22]. This complex topography and climatic diversity are both significant contributors to local biodiversity richness [23]. Among publications documenting fungal encounters across Yunnan Province, ascomycetes are critically neglected when compared to the amount of research on basidiomycetes [24]. Regrettably, studies on microfungi in Honghe are virtually non-existent. Except Marasinghe et al. [25], we could not find a single detailed account of microfungi in Honghe based on both morphological and phylogenetic analyses.
Dodonaea viscosa is a perennial evergreen woody shrub belonging to the family Sapindaceae. It is drought- and pollution-resistant as well as capable of growing on poor soils and rocky sites. The plant can also easily inhabit open areas and secondary forests [26,27]. A fast-growing plant, it typically grows 1 to 3 m in height but on rare occasions can reach up to 8 m [28]. Dodonaea viscosa is believed to have originated from Australia [29], though it grows throughout tropical and subtropical countries, including the African, Asian, Northern American and Southern American continents [30,31,32]. Dodonaea viscosa is effective at performing sand dune fixation and controlling coastal erosion since its roots function as excellent soil binders [33]. It can also be used to reclaim marshes. It is also grown as an ornamental plant owing to its shiny foliage and pink–red winged fruit [33]. Moreover, it is a well-known topic in environmental impact studies to determine the growth and yield of crops based on the presence of D. viscosa [27,34] as well as study its capacity to increase resilience to pollution [35,36] and drought [37]. In traditional medicine systems, plant parts such as the stem, leaves, seeds, roots, bark and aerial parts are used for various treatments [38]. Hossain [39] reported that extract obtained from D. viscosa has shown significant antidiabetic, antimicrobial, insecticidal, antioxidant, cytotoxic, antifertility, anti-inflammatory, analgesic, anti-ulcer, antispasmodic, anti-diarrheal and detoxification properties [27].
This study is the second in a series comprising an exhaustive taxonomic effort to document the microfungi of Yunnan Province [24]. In this study, we collected fresh fungal specimens from dead woody twigs of Dodonaea species at the Centre for Mountain Futures (CMF), an applied research centre jointly managed by World Agroforestry (ICRAF) and the Kunming Institute of Botany, Chinese Academy of Sciences (CAS), in Honghe County of the Honghe Hani and Yi Autonomous Prefecture. Using morphology and multi-gene phylogenetic evidence retrieved from the gathered ascomycetes, we characterized two new genera and four new species in the orders Capnodiales, Hysteriales and Pleosporales from dead twigs of Dodonaea viscosa in Honghe.

2. Materials and Methods

2.1. Herbarium Material and Fungal Strains

Fresh fungal materials were gathered from dead twigs of Dodonaea viscosa at CMF in Honghe County (Yunnan Province, China UTM/WGS84: 48 Q 216849–217075 E, 2592645–2592856 N, 600–750 m above sea level) during the dry season (April 2020). The local environment is characterized by poor eroded soils, steep valleys and a subtropical monsoon climate. Specimens were transported to the laboratory in Ziploc bags. Single spore isolation was conducted in accordance with methods described in Wanasinghe et al. [40]. Germinated spores were individually placed on potato dextrose agar (PDA) plates and grown at 20 °C in daylight. Dry herbarium materials were stored in the herbarium of Cryptogams Kunming Institute of Botany, Academia Sinica (KUN-HKAS). Living cultures were deposited at the Kunming Institute of Botany Culture Collection (KUMCC), Kunming, China and duplicated at China General Microbiological Culture Collection Centre (CGMCC). MycoBank numbers were registered as outlined in MycoBank (http://www.MycoBank.org accessed on 11 November 2020).

2.2. Morphological Observations

The morphology of external and internal macro-/micro-structures were observed as described in Wanasinghe et al. [24]. Images were captured with a Canon EOS 600D digital camera fitted to a Nikon ECLIPSE Ni compound microscope. Measurements were made with the Tarosoft (R) Image Frame Work program, and images used for figures were processed with Adobe Photoshop CS5 Extended version 10.0 software (Adobe Systems, San José, CA, USA).

2.3. DNA Extraction, PCR Amplifications and Sequencing

The extraction of genomic DNA was performed in accordance with the methods of Wanasinghe et al. [24], using the Biospin Fungus Genomic DNA Extraction Kit-BSC14S1 (BioFlux, P.R. China) following the instructions of the manufacturer. The reference DNA for the polymerase chain reaction (PCR) was stored at 4 °C for regular use and duplicated at −20 °C for long-term storage. The primers and protocols used for the amplification are summarized in Table 1. The amplified PCR fragments were then sent to a private company for sequencing (BGI, Ltd. Shenzhen, P.R. China).

2.4. Molecular Phylogenetic Analyses

2.4.1. Sequence Alignment

Sequences featuring a high degree of similarity were determined from a BLAST search to identify the closest matches with taxa in Dothideomycetes and recently published data [49,53,54,55,56]. Initial alignments of the acquired sequence data were first completed using MAFFT v. 7 (http://mafft.cbrc.jp/alignment/server/index.html accessed on 18 January 2021) [57,58] and manually clarified in BioEdit v. 7.0.5.2 when indicated [59].

2.4.2. Phylogenetic Analyses

Single-locus data sets were scanned for topological incongruences between loci for members of the analyses. Conflict-free alignments were concatenated into a multi-locus alignment that underwent maximum-likelihood (ML) and Bayesian (BI) phylogenetic analyses. Evolutionary models for BI and ML were selected independently for every locus using MrModeltest v. 2.3 [60] under the Akaike Information Criterion (AIC) implemented in PAUP v. 4.0b10.
The CIPRES Science Gateway platform [61] was used to perform RAxML and Bayesian analyses. ML analyses were made with RAxML-HPC2 on XSEDE v. 8.2.10 [62] employing the GTR+GAMMA swap model with 1000 bootstrap repetitions.
MrBayes analyses were performed setting GTR+I+GAMMA for 2–5 million generations, sampling every 100 generations and ending the run automatically when standard deviation of split frequencies dropped below 0.01 with a burnin fraction of 0.25. ML bootstrap values equal or greater than 60% and Bayesian posterior probabilities (BYPPs) greater than 0.95 were placed above each node of every tree.
Phylograms were visualized with FigTree v1.4.0 program [63] and reassembled in Microsoft PowerPoint (2007) and Adobe Illustrator® CS5 (Version 15.0.0, Adobe®, San Jose, CA, USA). Finalized alignments and trees were deposited in TreeBASE, submission ID: S27699 (http://purl.org/phylo/treebase/phylows/study/TB2: S27699).

3. Results

3.1. Global Checklist of Fungi on Dodonaea Viscosa

Information for the global checklist (Table 2) was retrieved from the Agriculture Research Service Database generated by the United States Department of Agriculture (USDA) [64], related books and research papers. This checklist includes fungal species associated with Dodonaea viscosa and the countries from which they were recorded.

3.2. Phylogenetic Analyses

Four phylogenetic analyses were performed using the acquired sequences from GenBank (Table 3). The first is a phylogenetic overview of the genera treated in Teratosphaeriaceae (Figure 1), while the remaining three alignments represent the species in Rhytidhysteron (Figure 2), an overview of the phylogeny of the genera treated in Lophiostomataceae (Figure 3) and Parapyrenochaeta, and allied genera in Pleosporineae (Figure 4). Other details related to ML and BI analyses from different datasets are presented in Table 4. The acquired phylogenetic results are discussed where applicable in the notes below.

3.3. Taxonomy of Fungi Colonising Dodonaea Viscosa Twigs

In the current study, two new genera and four novel species were found. These taxa are subsequently described below.
Class Dothideomycetes O.E. Erikss. and Winka, Myconet 1: 5 (1997)
Capnodiales Woron., Annales Mycologici 23: 177 (1925)
Teratosphaeriaceae Crous and U. Braun, Studies in Mycology 58: 8 (2007)
Haniomyces J.C. Xu gen. nov.
MycoBank: MB837991
Etymology: The generic epithet refers to the “Hani” ethnic group in Honghe County, Yunnan Province, China.
It is saprobic on dead twigs and branches in terrestrial habitats. Sexual morph: the ascomata is a scattered, immersed to semi-immersed, subglobose to conical or shaped irregularly, glabrous, brown to dark brown ostiolate. The ostiole is a short papillate, black, smooth periphysate. The peridium comprises cells of textura angularis. The hamathecium comprises numerous, filamentous, branched, septate, pseudoparaphyses. The asci are eight-spored, bitunicate, fissitunicate, clavate, with a pedicel, apically rounded with or without an ocular chamber. The ascospores overlap the biseriate, are ellipsoidal to sub-fusiform, hyaline, one-septate, with small to large guttules in each cell, with the ends remaining rounded, surrounded by a distinct mucilaginous sheath. Asexual morph: Coelomycetous. The conidiomata are sporodochial on PDA, globose, solitary or aggregated, semi-immersed, black, exuding yellow conidial masses. Conidiophores and conidiogenous cells were not observed in vitro. The conidia are solitary, aseptate, globose to ellipsoid, with the hyaline becoming medium to golden brown, and finely verruculose.
Type species: Haniomyces dodonaeae
Haniomyces dodonaeae Wanas. and Mortimer sp. nov. (Figure 5)
MycoBank: MB837997
Etymology: The specific epithet reflects the host genus Dodonaea.
Holotype: HKAS110128
It is saprobic on dead twigs of Dodonaea viscosa Jacq. (Sapindaceae). Sexual morph: the ascomata is a 150–200 μm high, 350–450 μm diam. (M = 165.4 × 390.3 µm, n = 5), scattered, semi-immersed to erumpent, subglobose to conical or shaped irregularly, flattened base, glabrous, brown to dark brown ostiolate, fused with host tissues. The ostiole is a short papillate, black and smooth, with hyaline periphyses (15–25 μm long, 1.5–2 μm wide). The peridium 5–10 µm wide at the base, 10–20 µm wide at sides, comprising 2–4 layers, outer layer pigmented, comprising reddish brown to dark brown, with thin-walled cells of textura angularis, and an inner layer composed of hyaline, loosen, cells of textura angularis. The hamathecium comprises numerous, 2–3 µm wide, filamentous, branched, septate, pseudoparaphyses. The asci are 110–130 × 25–35 µm (M = 118.5 × 31.2 µm, n = 20), eight-spored, bitunicate, fissitunicate, clavate, with a short pedicel (10–15 μm long), apically rounded with an ocular chamber. The ascospores 25–35 × 12–15 µm (M = 32.2 × 14.3 µm, n = 30), overlap the biseriate, are ellipsoidal to sub-fusiform, hyaline, one-septate, with the septum almost median, deeply constricted at the middle septum, with the upper cell wider than the lower cell, and are smooth-walled with small to large guttules in each cell, rounded at both ends and covered by a distinct mucilaginous sheath (30–50 µm, diam.). Asexual morph: Coelomycetous. The conidiomata are up to 250 μm diam., sporodochial on PDA, globose, solitary or aggregated, semi-immersed, black, exuding yellow conidial masses. Conidiophores and conidiogenous cells were not observed in vitro. The conidia are 5.5–7.5 × 4.5–5.5 µm (M = 6.4 × 5.4 µm, n = 30), solitary, aseptate, globose or ellipsoid, with the hyaline becoming medium to golden brown, and finely verruculose.
Culture characteristics: the colonies on PDA reached a 3 cm diameter after 2 weeks at 20 °C. They were circular has a serrate margin, whitish at the beginning, becoming brown at the centre and brownish green towards the margin after 4 weeks. They were slightly raised, and reverse blackish brown. The hyphae septate were branched, hyaline, thin, and smooth-walled.
Known distribution: Yunnan, China, on Dodonaea viscosa.
Material examined: China, Yunnan, Honghe Hani and Yi Autonomous Prefecture, Honghe County, 23.421068 N, 102.229128 E, 735 m, on dead twigs of Dodonaea viscosa, 22 April 2020, D.N. Wanasinghe, Honghe 005 (HKAS110128, holotype), ex-type living culture, KUMCC 20-0220, ibid. 23.419206 N, 102.231375 E, 618 m, Honghe 010 (HKAS110125, paratype), ex-paratype living culture, KUMCC 20-0221.
Hysteriales Lindau, Die Natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten 1 (1): 265 (1897
Hysteriaceae Chevall., Flore Générale des Environs de Paris 1: 432 (1826)
Rhytidhysteron Speg., Anales de la Sociedad Científica Argentina 12 (4): 188 (1881)
Rhytidhysteron hongheenseWanas. sp. nov. (Figure 6)
MycoBank: MB837992
Etymology: The specific epithet is derived from Honghe County, Yunnan Province, China.
Holotype: HKAS110133
It is aaprobic on dead twigs of Dodonaea Mill. (Sapindaceae). Sexual morph: The hystherothecia is 1200–2000 μm long × 350–500 high × 600–1000 µm diam. (M = 1590 × 410 × 840 µm, n = 10), arising singly or in small groups, sessile, and slightly erumpent from the substrate. The receptacle is cupulate, black, flat or slightly concave, with a slightly dentate margin. The excipulum are 70–100 µm wide, with the ectal excipulum narrow layered, deep, and thick-walled, with black cells of textura globulosa to textura angularis; the medullary excipulum is composed of narrow, long, thin-walled, hyaline to brown cells of textura angularis. The hamathecium are 2.5–4 µm wide, numerous, propoloid, pseudoparaphyses, exceeding asci in length, apically swollen, branched and reddish-orange pigmented. The branched apices form a layer on hymenium to develop pseudo-epithecium. The asci are 140–180 × 12–16 µm (M = 163.3 × 13.8 µm, n = 20), eight-spored, long cylindrical, short pedicellate, and is rounded at apex. The ascospores 20–33 × 9–13 µm (M = 28.2 × 11.2 µm, n = 30), overlap the uniseriate, are hyaline to light brown, one-septate, with wrinkled walls when young, becoming dark brown at maturity. They are ellipsoid with conical ends, regularly three-septate, and rarely muriform with one longitudinal septum, smooth walled, guttulate. Asexual morph: Undetermined.
Culture characteristics: Colonies on PDA reached a 4 cm diameter after 2 weeks at 20 °C. The colony was dense, circular, slightly raised, and the surface was smooth, with an undulated edge, with floccose which were greenish grey at the centre and brown towards margin from the top and reverse dark brown. The hyphae septate were branched, hyaline, thin, and smooth-walled.
Known distribution: Yunnan, China, on Dodonaea.
Material examined: China, Yunnan, Honghe Hani and Yi Autonomous Prefecture, Honghe County, 23.421068 N, 102.229128 E, 735 m, on dead twigs of Dodonaea, 22 April 2020, D.N. Wanasinghe, Honghe 006 (HKAS110133, holotype), ex-type culture, KUMCC 20-0222. ibid. on dead twigs of Dodonaea viscosa, 08 December 2020, DWH6-1 (HKAS112348). ibid. 07 December 2020, DWH7-2 (HKAS112349).
Pleosporales Luttr. ex M.E. Barr, Prodromus to class Loculoascomycetes: 67 (1987)
Lophiostomataceae Sacc., Sylloge Fungorum 2: 672 (1883)
Lophiomurispora Wanas. and Mortimer, gen. nov.
MycoBank: MB837993
Etymology: The generic epithet stems from the combined two words ‘‘lophio’’ and ‘‘murispora’’, referring to muriform ascospores in Lophiostomataceae.
It is saprobic on woody substrates in terrestrial habitats. Sexual morph: The ascomata is a solitary or gregarious, semi-immersed, erumpent through the host surface, coriaceous to carbonaceous, dark brown to black, globose to subglobose or conical ostiolate. The ostiole is a slit-like, central papillate, with or without a crest, opening by an apical, lysigenous pore or dehiscence, comprising hyaline periphyses or hyaline to lightly pigmented, pseudoparenchymatous cells. The peridium is broad at the apex and thinner at the base, comprising two strata with several layers of brown or lightly pigmented to hyaline cells of textura angularis to textura prismatica, fusing and indistinguishable from the host tissues. The hamathecium comprises many branched, septate, cellular pseudoparaphyses, located between and above the asci, embedded in a gelatinous matrix. The asci are eight-spored, bitunicate, fissitunicate, cylindric-clavate, pedicellate, and apically rounded, with an ocular chamber. The ascospores are uni- to bi-seriate, partially overlapping, and are hyaline when immature, becoming brown to dark brown when mature. They are ellipsoidal to fusiform, muriform, two-to-eight-transversely septate, with one-to-two-longitudinal septa, constricted at the central septum, with or without a mucilaginous sheath. Asexual morph: Coelomycetous. The conidiomata is pycnidial, phoma-like, solitary, gregarious, dark brown to black, immersed or slightly erumpent, coriaceous to carbonaceous, papillate or apapillate. The conidiomata wall is multi-layered, with three to four outer layers of brown-walled pseudoparenchymatous cells, with the inner most layer being thin and hyaline. The conidiophores are long, septate, and sparsely branched, which are formed from the inner most layer of the pycnidium wall. The conidiogenous cells are phialidic, cylindrical, hyaline, flexuous and smooth, with a short collarette. The conidia are hyaline, aseptate, straight to curved, ellipsoidal with rounded ends, thin-walled, smooth, and numerous.
Type species: Lophiomurispora hongheensis
Lophiomurispora hongheensis Wanas. sp. nov. (Figure 7 and Figure 8)
MycoBank: MB 837998
Etymology: The specific epithet is derived from Honghe County, the region of Yunnan Province in which this species was gathered.
Holotype: HKAS110127
It is saprobic on dead twigs of Dodonaea viscosa Jacq. (Sapindaceae) in terrestrial habitats. Sexual morph: The ascomata is a 280–360 μm high, 200–250 μm diam. (M = 318.6 × 232.7 µm, n = 5), scattered to gregarious, immersed, coriaceous, dark brown to black, globose to subglobose ostiolate. The ostiole is a 70–100 μm long, 40–80 μm diam. (M = 82.1 × 64.8 µm, n = 5), crest-like, central papillate, with a pore-like opening, comprising hyaline periphyses. The peridium is 20–30 μm wide at the base, 30–60 μm wide at the sides, broad at the apex, comprising two strata, with outer stratum composed of small, pale brown to brown, slightly flattened, thick-walled cells of textura angularis, fusing and indistinguishable from the host tissues. The inner stratum is composed of several layers with lightly pigmented to hyaline cells of textura angularis to textura prismatica. The hamathecium comprises 1–2 μm wide, branched, septate, cellular pseudoparaphyses, situated between and above the asci, embedded in a gelatinous matrix. The asci are 120–160 × 17–22 μm (M = 135.2 × 18.5 μm, n = 15), eight-spored, bitunicate, fissitunicate, cylindric-clavate, with a short pedicel, and is rounded at the apex, with an ocular chamber. The ascospores are 25–30 × 11–13 μm (M = 27.8 × 12 µm, n = 30), uni- to bi-seriate, overlapping, and are initially hyaline, turning brown at maturity. They are ellipsoidal to fusiform, muriform, four-to-eight-transversely septate, with one-to-two-longitudinal septa. They are slightly curved, deeply constricted at the central septum, slightly constricted at the remaining septa, conically rounded at the ends, and smooth-walled, with a distinct mucilaginous sheath. Asexual morph: Coelomycetous. The conidiomata is 1–1.5 mm diam. pycnidial, phoma-like, solitary, gregarious, dark brown to black, and immersed, with a sphaerical mass of slimy conidia oozing out at ostiolar apex. The conidiomata wall is multi-layered, with brown-walled pseudoparenchymatous cells, with a hyaline inner most layer. The conidiophores are 10–15 × 1.5–2.5 μm long (M = 12.4 × 2.1 µm, n = 15), septate and sparsely branched, which are formed from the inner most layer of the pycnidium wall. The conidiogenous cells are phialidic, cylindrical, hyaline, flexuous and smooth, with a short collarette. The conidia are 2.5–4 ×1.5–2 μm (M = 3 ×1.7 μm, n = 50), hyaline, aseptate, straight to curved, ellipsoidal with rounded ends, and are thin-walled, smooth-walled, and numerous.
Culture characteristics: the colonies on PDA reached a 4 cm diameter after 2 weeks at 20 °C. They were circular, had a serrate margin, and were whitish at the beginning, becoming greenish-brown 4 weeks later. They were slightly raised, and reverse dark brown. The hyphae septate were branched, hyaline, thin, and smooth-walled.
Known distribution: Yunnan, China, on Dodonaea viscosa.
Material examined: China, Yunnan, Honghe Hani and Yi Autonomous Prefecture, Honghe County, 23.421068 N, 102.229128 E, 735 m, on dead twigs of Dodonaea viscosa, 22 April 2020, D.N. Wanasinghe, Honghe 003 (HKAS110127, holotype), ex-type culture, KUMCC 20-0217, ibid. 23.419206 N, 102.231375 E, 618 m, Honghe 008 (HKAS110129, paratype), ex-paratype living culture, KUMCC 20-0223, ibid. 23 April 2020, ibid. DWHH07-1 (HKAS110130), living culture, KUMCC 20-0224, DWHH01 (HKAS110132), living culture, KUMCC 20-0216, ibid. DWHH04 3 (HKAS110131), living culture, KUMCC 20-0219.
Parapyrenochaetaceae Valenz-Lopez, Crous, Stchigel, Guarro and J.F. Cano, Studies in Mycology 90: 64 (2017)
Quixadomyces Cantillo and Gusmão, Persoonia 40: 317 (2018)
Quixadomyces hongheensis Wanas. sp. nov. (Figure 9)
MycoBank: MB837994
Etymology: The specific epithet is derived from Honghe County, Yunnan Province, China.
Holotype: HKAS110126
It is saprobic on dead twigs of Dodonaea viscosa Jacq. (Sapindaceae) in terrestrial habitats. Sexual morph: Undetermined. Asexual morph: Coelomycetous. The conidiomata is immersed to erumpent, solitary, globose, brown, from 200–300 μm diam, with a central ostiole, exuding a hyaline conidial mass. It has a wall of two to three layers of brown textura angularis. The paraphyses are 20–100 μm long, 2–3 μm wide, cylindrical, hyaline, septate, and smooth. The conidiophores are mostly reduced to conidiogenous cells. The conidiogenous cells are 5–8 × 3.5–5 μm (M = 6.4 × 3.1 µm, n = 15), lining the inner cavity, hyaline, smooth, are ampulliform to subcylindrical, and are phialidic with periclinal thickening. The conidia are 3–4.7 × 1.2–2 (M = 3.7 × 1.7 µm, n = 60) μm, solitary, hyaline, smooth, aseptate, and allantoid with obtuse ends.
Culture characteristics: The colonies on PDA reached a 4 cm diameter after 2 weeks at 20 °C. They were circular, had a serrate margin, and were greenish brown after 4 weeks. They were slightly raised, and reverse dark brown. The hyphae septate were branched, hyaline, thin, and smooth-walled.
Known distribution: Yunnan, China, on Dodonaea viscosa.
Material examined: China, Yunnan, Honghe Hani and Yi Autonomous Prefecture, Honghe County, 23.421068 N, 102.229128 E, 735 m, on dead twigs of Dodonaea viscosa, 22 April 2020, D.N. Wanasinghe, Honghe 01-N (HKAS110126, holotype), ex-type living culture, KUMCC 20-0215. 08 December 2020, HDW4-1 (HKAS112347). ibid. HDW4-3 (HKAS112346).

4. Discussion

Teratosphaeriaceae was introduced by Crous et al. [187]. Given that it is composed of 61 genera, it is regarded as one of the largest families in Dothideomycetes [188]. Members of this family are adapted to a broad range of life modes and can be saprobic, plant and human pathogenic, rock-inhabiting and endophytic; accordingly, they are widely distributed across varied terrain [49,136,139,188,189]. We have included representative sequence data of all available genera listed in Hongsanan et al. [188] for the phylogenetic analyses (except Davisoniella, Pachysacca and Placocrea, which lack DNA-based sequence data). Among them, Aulographina was grouped in Venturiales, and Leptomelanconium was related to Helotiales in the initial analysis. Therefore, they were excluded from the final analysis (Figure 1). In addition, representative taxa for Piedraia were included in the final dataset that were phylogenetically closely related to Teratosphaeriaceae. However, this genus is still considered a member in Piedraiaceae. The phylogeny generated herein (Figure 1) is congruent with those of other published studies to resolve intergeneric relationships in Teratosphaeriaceae [49,188]. In the combined LSU, ITS, rpb2, act, cal and tef1 data analysis, 58 clades are recognized from the ingroup taxa. Two strains from our new collections constitute a distinct monophyletic lineage (subclade 17, Figure 1) within the genera in Teratosphaeriaceae, which we introduce as a new genus.
The phylogeny (Figure 1) reveals a close relationship between two strains of the newly collected fungus (Haniomyces dodonaeae) to Camarosporula persooniae, Lapidomyces hispanicus, Neophaeothecoidea proteae, Teratosphaeriaceae sp. (CCFEE 5569), Xenoconiothyrium catenata and Xenophacidiella pseudocatenata, with 87% ML and 1.00 BYPP support values. Among them, only Camarosporula persooniae is reported from the sexual morph, and despite the high degree of phylogenetic similarity, these two species are morphologically dissimilar [136]. Neophaeothecoidea is more closely related to Haniomyces in the phylogenetic results, but this relationship lacks statistical support. In addition, Neophaeothecoidea is reported as a hyphomycete [188], whereas Haniomyces produces a coelomycetous asexual morph.
Out of the 61 genera listed in Teratosphaeriaceae, only 24 genera are described with sexual morphs. We suggest that the sexual morphs of these genera require further examination with increased collections to verify the accurate treatment of and relationships to remaining species. During asexual stages of Teratosphaeriaceae, most members are pathogenic, whereas they are non-pathogenic during sexual stages. This is an important distinction for identifying opportunistic pathogens, as members of this family can easily spread diseases between locations. The new taxon, Haniomyces dodonaeae, fits morphologically well into Teratosphaeriaceae by its periphysate ostiole and hyaline ascospores with a single septum in each. However, the dimensions of the asci and ascospores are significantly larger than the existing sexual reports of this family. The golden brown, ellipsoidal conidia of Haniomyces dodonaeae are similar to those in Neophaeothecoidea and Readeriella. Phylogenetically, Haniomyces dodonaeae has a close proximity to Neophaeothecoidea proteae. This relationship, however, is not strongly supported in the ML and BI analyses (Figure 1). Neophaeothecoidea proteae was originally isolated as a coelomycete (Phaeothecoidea proteae) based on its yeast-like growth in culture [190]; however, it is currently accounted for in a hyphomycetous genus. Comparison of the 805 base pairs (bp) across the LSU gene region of Haniomyces dodonaeae shows 17 bp (2.1%) differences exist in comparison with Neophaeothecoidea proteae. Similarly, comparison of the 356 bp of the rpb2 gene region shows 56 bp (15.73%) differences in comparison with Neophaeothecoidea proteae.
Rhytidhysteron was introduced by Spegazzini [191] to account for R. brasiliense and R. viride collected from southern Brazil in 1877 and 1880, respectively. Spegazzini [56] did not designate any type; therefore, Clements and Shear [192] designated R. brasiliense as the type species. Subsequently, few species were introduced to this genus based on morphological evidence [193,194,195,196]. In recent studies, more species have been introduced based on both morphology and DNA-based sequence data [55,56,172,177,178,183]. Presently, there are 23 species mentioned in Species Fungorum [197], including saprobic to weakly pathogenic taxa that grow on woody plants in terrestrial habitats [56,181]. Species of Rhytidhysteron are typically involved in wood degradation and occur primarily on the woody parts of a broad range of hosts [64,188].
We introduce a new species into Rhytidhysteron from a dead twig of Dodonaea sp. in Honghe, China, and its relationships with other species are presented based on multigene phylogenetic analyses (Figure 2). Our analysed molecular data generated phylogenies consistent with those of Mapook et al. [55] and Hyde et al. [56]. The novel species, Rhytidhysteron hongheense, is phylogenetically closely related to R. camporesii (KUN-HKAS 104277) and Rhytidhysteron chromolaenae (MFLUCC 17-1516), and these three constitute a strongly supported monophyletic clade. The ascospore and asci characteristics between the three species are similar, but the colour of hysterothecia in R. chromolaenae (green) is different from the other two (black). The pseudo-epithecium of R. camporesii is brown to purple, whereas it is reddish orange in R. hongheense. The significance of these morphological characteristics in species delineation should be further investigated in terms of phylogenetic signals. A pairwise comparison of 521 ITS (+5.8S) sequence data showed 31 (5.95%) bp differences between R. hongheense and R. camporesii as well 28 (5.37%) bp differences between R. hongheense and R. chromolaenae. Currently, there are only two Rhytidhysteron species, viz. Rhytidhysteron magnoliae and Rhytidhysteron thailandicum, reported from China [56,198], making this report the third of its kind from China and first from Honghe Prefecture.
Lophiostomataceae species are usually characterized by a slot-like ostiole on the top of the flattened neck, occurring mainly on twigs, stems or the bark of different woody and herbaceous plants in terrestrial, freshwater and marine environments as saprobes [129,140,188]. Thambugala et al. [129] undertook a comprehensive study of this family and accepted 16 genera. Subsequently, 12 new genera have been introduced by recent publications, and currently the family comprises 28 accepted genera [188]. The most recent multi-locus phylogenetic backbone tree to the family is presented in this study, including a novel genus (Lophiomurispora) found in Honghe County, Yunnan Province, China.
Lophiomurispora morphologically resembles Coelodictyosporium, Platystomum and Sigarispora with its crest-like ostiole and brown, multi-septate ascospores. However, these genera are revealed as phylogenetically distant in multi-gene phylogenetic analysis (Figure 3). Lophiomurispora has a close phylogenetic relationship to Desertiserpentica (Figure 3). However, Desertiserpentica is only known from its hyphomycetous asexual morph [54], whereas Lophiomurispora differs from Desertiserpentica by its coelomycetous asexual morph. Five strains of Lophiomurispora clustered in Lophiostomataceae as a strongly supported monophyletic clade (Figure 3) in both ML and BI of a concatenated SSU, LSU, ITS, tef1 and rpb2 dataset. All specimens were collected from dead twigs of Dodonaea viscosa at the Centre for Mountain Futures (CMF) in Honghe. There was no significant difference between morphological characteristics and DNA-based sequence comparisons between these collections. Therefore, we introduce them as different collections of Lophiomurispora hongheensis.
Parapyrenochaetaceae was proposed by Valenzuela-Lopez et al. [53] to accommodate three isolates which were previously recognized in Pyrenochaeta. They introduced the novel genus Parapyrenochaeta for P. acaciae (Pyrenochaeta acaciae), P. protearum (Pyrenochaeta protearum) and for the strain CBS 137997, formerly misidentified as Pyrenochaeta pinicola (re-identified as Parapyrenochaeta protearum). Later, Crous et al. [131] introduced Quixadomyces as another genus in Parapyrenochaetaceae to accommodate Quixadomyces cearensis. Therefore, there are currently two accepted genera in Parapyrenochaetaceae [3,188].
Crous et al. [131] introduced Quixadomyces for a fungus that was collected from Brazil on decaying bark. However, they did not observe the development of any internal structures. This fungus slightly resembles species in Pleosporales with its setose pycnidia [131,188]. In a multi-gene (concatenated LSU, SSU, ITS, rpb2, tef1 and btub) phylogenetic analysis, the ex-type strain of Quixadomyces cearensis (HUEFS 238438) clustered with two of our new strains as a monophyletic clade with poor bootstrap support (Figure 4). We introduce this isolate as a novel species belonging to this genus, Q. hongheensis. Based on the features of conidiogenous cells and conidia of Quixadomyces hongheensis, no substantial morphological differences exist to warrant two generic ranks. Therefore, this genus could potentially be reclassified as a synonym of Parapyrenochaeta in future studies. Because we did not perform extensive taxonomic reassessment using multiple fresh collections (especially sexual morphs of both genera), we will not attempt to synonymize any extant taxa.
Owing to lack of details on the internal structures of Quixadomyces cearensis, it is difficult to compare morphological characteristics such as conidiogenous cells and conidia between the new collection and this species. Lacking sufficient morphological evidence to perform accurate comparisons, we analysed nucleotide differences between these two strains. Comparing the 544 ITS (+5.8S) nucleotides of the two strains (HUEFS 238438 and KUMCC 20 0215) revealed 32 (5.88%) nucleotide differences. Therefore, it would seem prudent to treat our isolate as a new species in Quixadomyces as Q. hongheensis.
Nearly a century’s worth of taxonomic investigation into Dodonaea viscosa has yielded only 58 fungal records [Table 2]. These are mainly reported as saprobes or pathogens, but very few of these taxa are confirmed by both morphological and phylogenetic evidence. Many of these published records lack illustrations, descriptions or DNA sequence data, resulting in unclear taxonomic relationships. Even though Dodonaea viscosa is widely distributed across southwest and southern China, e.g., Fujian, Guangdong, Guangxi, Hainan, Sichuan and Yunnan [199], there is only one report for the fungus Pseudocercospora mitteriana on this host from China [124]. Previous taxonomic studies have suggested that increased collections might lead to the discovery of many new fungal species, and we, too, believe that Dodonaea is likely teeming with fungal diversity. More Dodonaea collections across different geographic regions are urgently needed, along with accompanying work in culture isolation, morphological description, DNA sequence analyses, phylogenetic relationship investigation, and accurate identification and classification. This study provides a case study for Dodonaea viscosa as a worthwhile host for the further study of microfungal associations and hints that it may potentially host numerous unknown fungal species.

Author Contributions

Conceptualization, D.N.W.; resources, P.E.M. and J.X.; writing—original draft preparation, D.N.W.; writing—review and editing, P.E.M.; supervision, P.E.M. and J.X.; funding acquisition, P.E.M. and J.X. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Research Project, Agroforestry Systems for Restoration and Bio-industry Technology Development (Grant No. 2017YFC0505101), Ministry of Sciences and Technology of China (Grant No. 2017YFC0505100), CAS President’s International Fellowship Initiative (Grant No. 2019PC0008), the 64th batch of China Postdoctoral Science Foundation (Grant No. 2018M643549), Postdoctoral Fund from Human Resources and Social Security Bureau of Yunnan Province, NSFC project codes 41761144055 and 41771063.

Data Availability Statement

The datasets generated for this study can be found in the NCBI GenBank, MycoBank and TreeBASE.

Acknowledgments

Austin G. Smith at World Agroforestry (ICRAF), Kunming Institute of Botany, China, is thanked for English editing. Lu Wen Hua and Li Qin Xian are thanked for their invaluable assistance. We acknowledge Kunming Institute of Botany, Chinese Academy of Sciences for providing the laboratories and instruments for molecular work.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. RAxML tree based on a combined dataset of partial LSU, ITS, rpb2, act, cal and tef1 DNA sequence analysis in Teratosphaeriaceae. The tree is rooted to Staninwardia suttonii (CPC 13055). Bootstrap support values for ML equal to or greater than 60%, Bayesian posterior probabilities (BYPP) equal to or greater than 0.95 are presented as ML/BI above nodes. Known genera are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar presents the expected number of nucleotide substitutions per site.
Figure 1. RAxML tree based on a combined dataset of partial LSU, ITS, rpb2, act, cal and tef1 DNA sequence analysis in Teratosphaeriaceae. The tree is rooted to Staninwardia suttonii (CPC 13055). Bootstrap support values for ML equal to or greater than 60%, Bayesian posterior probabilities (BYPP) equal to or greater than 0.95 are presented as ML/BI above nodes. Known genera are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar presents the expected number of nucleotide substitutions per site.
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Figure 2. RAxML tree based on a combined dataset of partial SSU, LSU, ITS and tef1 DNA sequence analysis in Rhytidhysteron. The tree is rooted to Gloniopsis calami (MFLUCC 15-0739, MFLUCC 10-0927). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known species are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
Figure 2. RAxML tree based on a combined dataset of partial SSU, LSU, ITS and tef1 DNA sequence analysis in Rhytidhysteron. The tree is rooted to Gloniopsis calami (MFLUCC 15-0739, MFLUCC 10-0927). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known species are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
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Figure 3. RAxML tree based on a combined dataset of partial SSU, LSU, ITS, tef1 and rpb2 DNA sequence analysis in Lophiostomataceae. The tree is rooted to Gloniopsis praelonga (CBS 112415) and Hysterium angustatum (MFLUCC 16-0623). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known families and selected genera are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
Figure 3. RAxML tree based on a combined dataset of partial SSU, LSU, ITS, tef1 and rpb2 DNA sequence analysis in Lophiostomataceae. The tree is rooted to Gloniopsis praelonga (CBS 112415) and Hysterium angustatum (MFLUCC 16-0623). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known families and selected genera are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
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Figure 4. RAxML tree based on a combined dataset of partial LSU, SSU, ITS, rpb2, tef1 and btub DNA sequence analysis in Pleosporineae. The tree is rooted to Massarina cisti (CBS 266.62) and M. eburnea (CBS 473.64). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known families and the genus Quixadomyces are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
Figure 4. RAxML tree based on a combined dataset of partial LSU, SSU, ITS, rpb2, tef1 and btub DNA sequence analysis in Pleosporineae. The tree is rooted to Massarina cisti (CBS 266.62) and M. eburnea (CBS 473.64). Bootstrap support values for ML equal to or greater than 60% and BYPP equal to or greater than 0.95 are shown as ML/BI above the nodes. Known families and the genus Quixadomyces are indicated with coloured blocks. Blue represents new isolates. The ex-type strains are indicated in bold. The scale bar represents the expected number of nucleotide substitutions per site.
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Figure 5. The sexual (HKAS110128, holotype) and asexual (KUMCC 20-0220, ex-type) morphs of Haniomyces dodonaeae. (a,b) ascomata on the dead woody twigs of Dodonaea viscosa; (c,d) vertical section of ascoma; (e) periphyses; (f) peridium; (g) pseudoparaphyses; (h–j) asci; (k–p) ascospores (p in Indian Ink); (q,r) colony on potato dextrose agar (PDA) (r from the bottom); (s) squashed pycnidia which were produced on PDA; (t) pycnidia wall; (u–w) conidia. Scale bars, (c,d) 100 µm; (e,h–j,t,u) 20 µm; (f,k–p,v,w) 10 µm; (s) 200 µm.
Figure 5. The sexual (HKAS110128, holotype) and asexual (KUMCC 20-0220, ex-type) morphs of Haniomyces dodonaeae. (a,b) ascomata on the dead woody twigs of Dodonaea viscosa; (c,d) vertical section of ascoma; (e) periphyses; (f) peridium; (g) pseudoparaphyses; (h–j) asci; (k–p) ascospores (p in Indian Ink); (q,r) colony on potato dextrose agar (PDA) (r from the bottom); (s) squashed pycnidia which were produced on PDA; (t) pycnidia wall; (u–w) conidia. Scale bars, (c,d) 100 µm; (e,h–j,t,u) 20 µm; (f,k–p,v,w) 10 µm; (s) 200 µm.
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Figure 6. Rhytidhysteron hongheensis (HKAS110133, holotype). (a,b) Appearance of hysterothecia on the dead woody twigs of Dodonaea viscosa; (c,d) horizontal section of hysteriothecium; (e) vertical section of hysteriothecium; (f) cells of peridium; (g,h) pseudoparaphyses; (i,j) asci; (k–p) ascospores; (q,r) colony on PDA (r from the bottom). Scale bars, (d,e) 200 µm; (f,i,j) 50 µm; (g,h,k–p) 10 µm.
Figure 6. Rhytidhysteron hongheensis (HKAS110133, holotype). (a,b) Appearance of hysterothecia on the dead woody twigs of Dodonaea viscosa; (c,d) horizontal section of hysteriothecium; (e) vertical section of hysteriothecium; (f) cells of peridium; (g,h) pseudoparaphyses; (i,j) asci; (k–p) ascospores; (q,r) colony on PDA (r from the bottom). Scale bars, (d,e) 200 µm; (f,i,j) 50 µm; (g,h,k–p) 10 µm.
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Figure 7. Sexual morph of Lophiomurispora hongheensis (HKAS110127, holotype). (a–c) Ascomata on the dead woody twigs of Dodonaea viscosa; (d) cross section of ascomata; (e) vertical section of ascoma; (f) closeup of ostiole; (g,h) peridium; (i) pseudoparaphyses; (j–l) asci; (m–s) ascospores (s in Indian Ink); Scale bars, (e) 100 µm; (f–h,j–l) 20 µm; (i,m–s) 10 µm.
Figure 7. Sexual morph of Lophiomurispora hongheensis (HKAS110127, holotype). (a–c) Ascomata on the dead woody twigs of Dodonaea viscosa; (d) cross section of ascomata; (e) vertical section of ascoma; (f) closeup of ostiole; (g,h) peridium; (i) pseudoparaphyses; (j–l) asci; (m–s) ascospores (s in Indian Ink); Scale bars, (e) 100 µm; (f–h,j–l) 20 µm; (i,m–s) 10 µm.
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Figure 8. Asexual morph of Lophiomurispora hongheensis (KUMCC 20-0217, ex-type culture). (a,b) colony on PDA (b from the bottom); (c,d) immersed pycnidia in PDA (from the bottom); (e) pycnidia wall; (f–i) conidiophore; (j) conidia. Scale bars, (e–i) 10 µm; (j) 5 µm.
Figure 8. Asexual morph of Lophiomurispora hongheensis (KUMCC 20-0217, ex-type culture). (a,b) colony on PDA (b from the bottom); (c,d) immersed pycnidia in PDA (from the bottom); (e) pycnidia wall; (f–i) conidiophore; (j) conidia. Scale bars, (e–i) 10 µm; (j) 5 µm.
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Figure 9. Quixadomyces hongheensis (KUMCC 20-0215, ex-type culture). (a,b) colony on PDA (b from the bottom); (c) pycnidia on PDA; (d) mycelia; (e) squashed pycnidia; (f) pycnidia wall; (g) paraphyses; (h,i) conidiophore; (j) conidia. Scale bars, (d,f,g) 10 µm; (e) 200 µm; (h–j) 5 µm.
Figure 9. Quixadomyces hongheensis (KUMCC 20-0215, ex-type culture). (a,b) colony on PDA (b from the bottom); (c) pycnidia on PDA; (d) mycelia; (e) squashed pycnidia; (f) pycnidia wall; (g) paraphyses; (h,i) conidiophore; (j) conidia. Scale bars, (d,f,g) 10 µm; (e) 200 µm; (h–j) 5 µm.
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Table
Table 1. Genes/loci used in the study with PCR primers, references and protocols.
Table 1. Genes/loci used in the study with PCR primers, references and protocols.
Locus aPrimers bPCR: Thermal Cycles: c
(Annealing temp. in Bold)		References
actACT-512F
ACT2Rd		(96 °C: 120 s, 52 °C: 60 s, 72 °C: 90 s) × 40 cycles[41,42]
btubTUB2Fw
TUB4Rd		(94 °C: 30 s, 56 °C: 45 s, 72 °C: 60 s) × 35 cycles[43]
calCAL-235F
CAL2Rd		(96 °C: 120 s, 50 °C: 60 s, 72 °C: 90 s) × 40 cycles[42,44]
ITSITS5
ITS4		(95 °C: 30 s, 55 °C:50 s, 72 °C: 90 s) × 35 cycles[45]
LSULR0R
LR5		(95 °C: 30 s, 55 °C:50 s, 72 °C: 90 s) × 35 cycles[46,47]
rpb2fRPB2-5f
fRPB2-7cR		(94 °C: 60 s, 58 °C: 60 s, 72 °C: 90 s) × 40 cycles[48]
fRPB2-414R(96 °C: 120 s, 49 °C: 60 s, 72 °C: 90 s) × 40 cycles[49]
SSUNS1
NS4		(95 °C: 30 s, 55 °C:50 s, 72 °C: 90 s) × 35 cycles[45]
tef1EF1-983F
EF1-2218R		(95 °C: 30 s, 55 °C:50 s, 72 °C: 90 s) × 35 cycles[50,51]
EF1-728F
EF-2		(96 °C: 120 s, 52 °C: 60 s, 72 °C: 90 s) × 40 cycles[41,52]
aact: actin; btub: β-tubulin; cal: calmodulin; ITS: part of rDNA 18S (3’ end), the first internal transcribed spacer (ITS1), the 5.8S rRNA gene, the second ITS region (ITS2), and part of the 28S rRNA (5’ end); LSU: large subunit (28S); rpb2: RNA polymerase II second largest subunit; SSU: small subunit rDNA (18S); tef1: translation elongation factor 1-alpha gene. b fRPB2-5f and fRPB2-414R were used only for Teratosphaeriaceae analysis. c All the PCR thermal cycles include initiation step of 95 °C: 5 min, and final elongation step of 72 °C: 10 min and final hold at 4 °C.
Table
Table 2. Checklist of fungi recorded from Dodonaea viscosa in worldwide.
Table 2. Checklist of fungi recorded from Dodonaea viscosa in worldwide.
Phylum and ClassOrderFamilySpeciesCountryReferences
Ascomycota
DothideomycetesBotryosphaerialesBotryosphaeriaceaeLasiodiplodia iraniensisAustralia[65]
Macrophoma dodonaeaeIndia[66]
Macrophomina phaseolinaArizona[67]
CapnodialesCapnodiaceaeAntennariella californicaFiji[68]
MycosphaerellaceaeCercospora dodonaeaeIndia[69,70,71]
Cercospora sp.Sierra Leone[72]
Pseudocercospora dodonaeaeNew Zealand[73,74,75,76,77,78]
Pseudocercospora mitterianaChina[79]
India[69,71]
Pakistan[71,80]
TeratosphaeriaceaeHaniomyces dodonaeaeChinaThis study
HysterialesHysteriaceaeRhytidhysteron hongheenseChinaThis study
incertae sedisPseudoperisporiaceaeEpisphaerella dodonaeaeDominican Republic[81]
Ecuador[82]
Venezuela[82]
USA[83]
incertae sedisMycothyridium pakistanicumPakistan[80]
Mycothyridium roosselianumPakistan[80]
PatellarialesPatellariaceaeTryblidaria pakistaniPakistan[80]
PleosporalesConiothyriaceaeConiothyrium sp.Venezuela[84]
CorynesporascaceaeCorynespora cassiicolaIndia[85]
DidymosphaeriaceaeDidymosphaeria oblitescensPakistan[80]
LeptosphaeriaceaeLeptosphaeria dodonaeaeEritrea[86]
LophiostomataceaeLophiomurispora hongheensisChinaThis study
ParapyrenochaetaceaeQuixadomyces hongheensisChinaThis study
PleosporaceaePleospora dodonaeaeCyprus[87]
ValsarialesValsariaceaeValsaria rubricosaPakistan[80]
LecanoromycetesOstropalesStictidaceaeStictis marathwadensisIndia[88,89]
LeotiomycetesHelotialesErysiphaceaeOidium sp.Iraq[90]
Israel[90]
South Africa[90]
Zimbabwe[91]
Ovulariopsis erysiphoidesEthiopia[92]
Phyllactiniasp.Ethiopia[90]
Sawadaea bicornisGermany[93]
New Zealand[74,90]
South Africa[90]
Takamatsuella circinataSouth Africa[94]
SordariomycetesDiaporthalesCytosporaceaeCytospora sp.USA[95]
GlomerellalesGlomerellaceaeColletotrichum gloeosporioidesIndia[88]
MeliolalesMeliolaceaeMeliola lyoniHawaii[96,97,98,99]
HypocrealesNectriaceaeCalonectria cylindrosporaUSA[100,101]
Calonectria pauciramosaItaly[102]
Fusarium solaniIran[103]
GlomerellalesPlectosphaerellaceaeVerticillium dahliaeUSA[95]
New Zealand[74]
CoronophoralesScortechiniaceaeTympanopsis lantanaeIndia[104]
AmphisphaerialesSporocadaceaeMonochaetia dodoneaeEthiopia[92]
Pestalotia dodonaeaeEritrea[86]
Sarcostroma kennedyaeNew Zealand[74]
Seimatosporium kennedyaeNew Zealand[73]
TogninialesTogniniaceaePhaeoacremonium alvesiiAustralia[105,106,107,108]
Phaeoacremonium italicumAustralia[109]
Basidiomycota
AgaricomycetesAgaricalesMarasmiaceaeCampanella junghuhniiHawaii[110]
Agaricalesincertae sedisDendrothele incrustansNew Zealand[111]
BartheletiomycetesCantharellalesCeratobasidiaceaeRhizoctonia sp.Italy[112]
HymenochaetalesHymenochaetaceaeArambarria cognataUruguay[113]
Fomitiporia australiensisAustralia[114]
Phellinus melleoporusHawaii[110]
Phellinus robustusUSA[115]
Phellinus sonoraeUSA[116]
SchizoporaceaeHyphodontia alutariaHawaii[110]
Grandinia brevisetaHawaii[110]
PolyporalesHyphodermataceaeHyphoderma sphaeropedunculatumHawaii[110]
PucciniomycetesPuccinialesincertae sedisUredo dodonaeaeIndonesia[117]
Oomycota
PeronosporomycetesPeronosporalesPeronosporaceaePhytophthora drechsleriAustralia[118,119,120]
Phytophthora nicotianaeItaly[121,122,123]
Phytophthora palmivoraItaly[123]
PythiaceaeGlobisporangium debaryanumNew Zealand[73,74]
Globisporangium irregulareNew Zealand[74]
Globisporangium ultimumNew Zealand[73]
Pythium inflatumNew Zealand[73,74]
Pythium sp.New Zealand[73]
USA[75]
Table
Table 3. Taxa used in the phylogenetic analyses and their corresponding GenBank numbers.
Table 3. Taxa used in the phylogenetic analyses and their corresponding GenBank numbers.
SpeciesStrainGenBank Accession NumbersReference
SSULSUactcalITSrpb2tef1btub
Acidiella bohemicaCBS 132720-KF901984---KF902178--[49]
Acidiella parvaCMW 10189-KF901986KF903512KF902537KF901647KF902192KF903097 *-[49]
Acrodontium crateriformeCPC 11509-GU214682GU320413KX289011GU214682KX288404GU384425 *-[124,125]
Acrodontium pigmentosumCBS 111111-KX286963--KX287275KX288412--[125]
Alfoldia vorosiiCBS 145501MK589346MK589354--JN859336-MK599320-[126]
Alpestrisphaeria jonesiiGZCC 16-0021KX687755KX687753--KX687757-KX687759-[14]
Alpestrisphaeria jonesiiGZCC 16-0022KX687756KX687754--KX687758-KX687760-[14]
Alpestrisphaeria monodictyoidesV0216 MH160808--MK503662- -[127]
Alpestrisphaeria terricolaSC-12HJX985749JX985750--JN662930- -[128]
Amorocoelophoma cassiaeMFLUCC 17-2283NG_065775NG_066307--NR_163330MK434894MK360041-[127]
Angustimassarina acerinaMFLUCC 14-0505NG_063573KP888637--NR_138406-KR075168-[129]
Angustimassarina quercicolaMFLUCC 14-0506NG_063574KP888638--KP899133-KR075169-[129]
Angustimassarina rosarumMFLUCC 17-2155MT226662MT214543--MT310590MT394678MT394726-[130]
Apenidiella strumelloideaCBS 114484-KF937229---KF937266--[49]
Araucasphaeria foliorumCPC 33084-MH327829--MH327793---[131]
Astragalicola vasilyevaeMFLUCC 17-0832MG829098MG828986--NR_157504MG829248MG829193-[130]
Austroafricana associataCPC 13119-KF901824KF903526KF902528KF901507KF902177KF903087 *-[49]
Austroafricana sp.CPC 4313-KF901813KF903460KF902527KF901498KF902186KF903086 *-[49]
Austrostigmidium mastodiaeMA 18215-NG_057063------[132]
Austrostigmidium mastodiaeMA 18213-KP282862------[132]
Batcheloromyces alistairiiCPC 12730-KF937220---KF937252--[49]
Batcheloromyces leucadendriCPC 1838-KF937221---KF937253--[49]
Batcheloromyces sedgefieldiiCPC 3026-KF937222---KF937254--[49]
Biappendiculispora japonicaKT 573AB618686AB619005--LC001728-LC001744-[129,133]
Biappendiculispora japonicaKT 686-1AB618687AB619006--LC001729-LC001745-[129,133]
Camarosporidiella caraganicolaMFLUCC 17-0726MF434300MF434212--MF434125-MF434388-[134]
Camarosporidiella elongataAFTOL-ID 1568DQ678009DQ678061---DQ677957DQ677904-[135]
Camarosporidiella eufemianaMFLUCC 17-0207MF434321MF434233--MF434145-MF434408-[134]
Camarosporula persooniaeCPC 3350-JF770460---KF937255--[49,136]
Capulatispora sagittiformisKT 1934AB618693AB369267--AB369268-LC001756-[129,133]
Catenulostroma hermanusenseCPC 18276-KF902089---KF902197--[49]
Catenulostroma protearumCPC 15370-KF902090---KF902198--[49]
Coelodictyosporium pseudodictyosporiumMFLUCC 13-0451-KR025862--KR025858---[137]
Coelodictyosporium rosarumMFLUCC 17-0776NG_063674NG_059056--MG828875-MG829195-[130]
Coniothyrium palmarumCBS 400.71EU754054JX681084--MH860184KT389592-KT389792[138]
Constantinomyces maceransTRN 440-KF310005--NR_164011KF310081--[139]
Constantinomyces minimusCBS 118766-KF310003--NR_144957KF310077--[139]
Crassiclypeus aquaticusKH 91LC312469LC312527--LC312498LC312585LC312556-[140]
Crassiclypeus aquaticusKH 104LC312470LC312528--LC312499LC312586LC312557-[140]
Crassiclypeus aquaticusKH 185LC312471LC312529--LC312500LC312587LC312558-[140]
Crassiclypeus aquaticusKT 970LC312472LC312530--LC312501LC312588LC312559-[140]
Desertiserpentica hydeiSQUCC 15092MW077163MW077156--MW077147MW075773MW077163-[54]
Devriesia agapanthiCPC 19833-JX069859---KJ564346--[49,141]
Devriesia strelitziaeX1037-GU301810--EU436763GU371738GU349049 *-[142]
Dimorphiopsis brachystegiaeCPC 22679-KF777213--KF777160---[143]
Elasticomyces elasticusCCFEE 5313-KJ380894--FJ415474---[49,144]
Elasticomyces elasticusCCFEE 5474-KF309991---KF310046--[139]
Eupenidiella venezuelensisCBS 106.75-KF902163KF903393KF902540KF901802KF902202KF903100 *-[49]
Euteratosphaeria verrucosiafricanaCPC 11167----DQ303056---[139]
Flabellascoma aquaticumKUMCC 15-0258MN304832NG_068307--NR_166305MN328895MN328898-[145]
Flabellascoma cycadicolaKT 2034LC312473LC312531--LC312502LC312589LC312560-[140]
Flabellascoma fusiformeMFLUCC 18-1584-NG_068308--NR_166306-MN328902-[105]
Flabellascoma minimumKT 2013LC312474LC312532--LC312503LC312590LC312561-[140]
Flabellascoma minimumKT 2040LC312475LC312533--LC312504LC312591LC312562-[140]
Forliomyces uniseptataMFLUCC 15-0765NG_061234NG_059659--NR_154006-KU727897-[146]
Friedmanniomyces endolithicusCCFEE 5199-KF310007---KF310093--[139]
Friedmanniomyces endolithicusCCFEE 5283-KF310006---KF310053--[49]
Gloniopsis calamiMFLUCC 15-0739NG_063621NG_059715--NR_164398-KX671965-[147]
Gloniopsis calamiMFLUCC 10-0927MN577426MN577415--MN608546---[148]
Gloniopsis praelongaCBS 112415FJ161134FJ161173---FJ161113FJ161090-[149]
Guttulispora crataegiMFLUCC 13-0442KP899125KP888639--KP899134-KR075161-[129]
Guttulispora crataegiMFLUCC 14-0993KP899126KP888640--KP899135-KR075162-[129]
Haniomyces dodonaeaeKUMCC 20-0220MW264221MW264191MW256802MW256805MW264212MW269527MW256813 *-This study
Haniomyces dodonaeaeKUMCC 20-0221MW264222MW264192MW256803MW256806MW264213MW269528MW256814 *-This study
Hortaea thailandicaCPC 16651-KF902125---KF902206--[49]
Hysterium angustatumMFLUCC 16-0623MH535885MH535893---MH535875FJ161096-[149,150]
Hyweljonesia indicaNFCCI 4146-NG_066398--NR_164021---[151]
Hyweljonesia queenslandicaBRIP 61322b-NG_059766--NR_154095---[152]
Incertomyces perditusCCFEE 5385-KF310008--KF309977KF310083--[139]
Incertomyces vagansCCFEE 5393-KF310009--NR_154064KF310057--[139]
Lapidomyces hispanicusTRN126-KF310016---KF310076--[139]
Lentistoma bipolareHKUCC 10069LC312476LC312534--LC312505LC312592LC312563-[140]
Lentistoma bipolareHKUCC 10110LC312477LC312535--LC312506LC312593LC312564-[140]
Lentistoma bipolareHKUCC 8277LC312478LC312536--LC312507LC312594LC312565-[140]
Lentistoma bipolareKT 2415LC312483LC312541--LC312512LC312599LC312570-[140]
Lentistoma bipolareKT 3056LC312484LC312542--LC312513LC312600LC312571-[140]
Leptoparies palmarumKT 1653LC312485LC312543--LC312514LC312601LC312572-[140]
Leptosphaeria conoideaCBS 616.75JF740099JF740279--JF740201KT389639-KT389804[153]
Leptosphaeria doliolumCBS 505.75NG_062778NG_068574--NR_155309KY064035GU349069JF740144[154]
Lophiohelichrysum helichrysiMFLUCC 15-0701KT333437KT333436--KT333435-KT427535-[155]
Lophiopoacea paramacrostomaMFLUCC 11-0463KP899122KP888636------[129]
Lophiomurispora hongheensisKUMCC 20-0217MW264225MW264195--MW264216MW256808MW256817-This study
Lophiomurispora hongheensisKUMCC 20-0223MW264226MW264196--MW264217MW256809MW256818-This study
Lophiomurispora hongheensisKUMCC 20-0216MW264227MW264197--MW264218MW256810MW256819-This study
Lophiomurispora hongheensisKUMCC 20-0219MW264228MW264198--MW264219MW256811MW256820-This study
Lophiomurispora hongheensisKUMCC 20-0224MW264229MW264199--MW264220MW256812MW256821-This study
Lophiopoacea winteriKT 740AB618699AB619017--JN942969JN993487LC001763-[129,133,156]
Lophiopoacea winteriKT 764AB618700AB619018--JN942968JN993488LC001764-[129,133,156]
Lophiostoma cauliumCBS 623.86GU296163GU301833---GU371791--[152]
Lophiostoma macrostomumKT 635AB521731AB433273--AB433275JN993484LC001752-[129,133]
Lophiostoma multiseptatumJCM 17668AB618684AB619003--LC001726-LC001742-[129,133]
Lophiostoma multiseptatumMAFF 239451AB618685AB619004--LC001727-LC001743-[129,133]
Lophiostoma rosaeTASM 6115NG_065145NG_069558--NR_158531-MG829205-[130]
Lophiostoma semiliberumKT 828AB618696AB619014--JN942970JN993489LC001759-[129,133,156]
Massarina cistiCBS 266.62AB797249AB807539--LC014568FJ795464AB808514-[157,158]
Massarina eburneaCBS 473.64GU296170GU301840--AF383959GU371732GU349040-[143,159]
Meristemomyces frigidumCCFEE 5457-GU250389---KF310066--[49,144]
Meristemomyces frigidumCCFEE 5507-KF310013---KF310067--[139]
Monticola elongataCCFEE 5492-KF309994---KF310065--[139]
Myrtapenidiella corymbiaCPC 14640-KF901838KF903558KF902558KF901517KF902227KF903119 *-[49]
Neocatenulostroma abietisCBS 110038-KF937226---KF937263--[49]
Neocatenulostroma microsporumCPC 1960-KF901814-KF902561KF901499KF902232KF903122 *-[49]
Neocucurbitaria ribicolaCBS 142394MF795840MF795785--MF795785MF795827MF795873MF795911[160]
Neoleptosphaeria jonesiiMFLUCC 16-1442NG_063625KY211870--NR_152375-KY211872-[161]
Neopaucispora rosaecaeMFLUCC 17-0807NG_061293NG_059869--MG828924-MG829217-[130]
Neophaeosphaeria agavesCBS 136429-KF777227--NR_137833---[143]
Neophaeosphaeria filamentosaCBS 102202GQ387516GQ387577--JF740259GU371773--[162]
Neophaeosphaeria phragmiticolaKUMCC 16-0216MG837008MG837009----MG838020-[163]
Neophaeothecoidea proteaeCPC 2831-KF937228---KF937265--[49]
Neopyrenochaeta acicolaCBS 812.95NG_065567GQ387602--NR_160055LT623271-LT623232[164]
Neopyrenochaeta cercidisMFLU 18-2089NG_065769MK347932--MK347718MK434908--[127]
Neopyrenochaeta fragariaeCBS 101634GQ387542GQ387603--LT623217LT623270-LT623231[164]
Neopyrenochaeta inflorescentiaeCBS 119222-EU552153--EU552153LT623272-LT623233[165]
Neopyrenochaeta maesuayensisMFLUCC 14-0043-MT183504--NR_170043-MT454042-[166]
Neopyrenochaeta telephoniCBS 139022-NG_067485--KM516291LT717685-LT717678[154]
Neotrematosphaeria biappendiculataKT 1124GU205256GU205227------[129]
Neotrematosphaeria biappendiculataKT 975GU205254GU205228------[129]
Neotrimmatostroma excentricumCPC 13092-KF901840KF903534KF902562KF901518KF902236KF903123 *-[49]
Neovaginatispora clematidisMFLUCC 17-2149MT226676MT214559--MT310606-MT394738-[167]
Neovaginatispora fuckeliiCBS 101952FJ795496DQ399531---FJ795472--[158]
Neovaginatispora fuckeliiKH 161AB618689AB619008--LC001731-LC001749-[129,133]
Neovaginatispora fuckeliiKT 634AB618690AB619009--LC001732-LC001750-[129,133]
Oleoguttula mirabilisCCFEE 5522-KF310019---KF310070--[139]
Parapaucispora pseudoarmatisporaKT 2237LC100018LC100026--LC100021-LC100030-[168]
Parapenidiella pseudo tasmaniensisCPC 12400-KF901844KF903562KF902589KF901522KF902265KF903152 *-[49]
Parapenidiella tasmaniensisCPC 1555-KF901843KF903451KF902587KF901521KF902263KF903150 *-[49]
Parapyrenochaeta acaciaeCPC 25527-KX228316--NR_155674LT717686-LT717679[53]
Parapyrenochaeta protearumCBS 131315-JQ044453--JQ044434LT717683-LT717677[53]
Paucispora kunmingenseMFLUCC 17-0932MF173430NG_059829--NR_156625MF173436MF173434-[169]
Paucispora quadrisporaKH 448LC001720LC001722--LC001733-LC001754-[129]
Paucispora quadrisporaKT 843AB618692AB619011--LC001734-LC001755-[129,133]
Paucispora versicolorKH 110LC001721AB918732--AB918731-LC001760-[129,133]
Penidiella columbianaCBS 486.80-KF901965KF903587KF902594KF901630KF902272KF903158 *-[49]
Penidiellomyces aggregatusCBS 128772-NG_057905--NR_137772---[170]
Penidiellomyces drakensbergensisCPC 19778-NG_059482--NR_111821---[141]
Penidiellopsis radicularisCBS 131976-KU216314-KU216292KT833148-KU216339 *-[171]
Penidiellopsis ramosusCBMAI 1937-KU216317-KU216295KT833151-KU216342 *-[171]
PhaeoseptumcarolshearerianumNFCCI-4221MK307816MK307813--MK307810MK309877MK309874-[172]
Phaeoseptum hydeiMFLUCC 17-0801MT240624MT240623--MT240622-MT241506-[40]
Phaeoseptum manglicolaNFCCI-4666MK307817MK307814--MK307811MK309878MK309875-[172]
Phaeoseptum terricolaMFLUCC 10-0102MH105780MH105779--MH105778MH105782MH105781-[163]
Phaeothecoidea IntermediaCPC 13711-KF902106KF903564KF902606KF901752KF902286KF903171 *-[49]
Phaeothecoidea MinutisporaCPC 13710-KF902108KF903659KF902607KF901753KF902288KF903172 *-[49]
Piedraia hortae var. hortaeCBS 480.64-KF901943---KF902289--[49]
Piedraia hortae var. paraguayensisCBS 276.32-KF901816------[49]
Piedraia quintanilhaeCBS 327.63-KF901957------[49]
Platystomum actinidiaeKT 521JN941375JN941380--JN942963JN993490LC001747-[129,156]
Platystomum crataegiMFLUCC 14-0925KT026113KT026109--KT026117-KT026121-[129]
Platystomum rosaeMFLU 15-2569KY264750KY264746--KY264742---[173]
Platystomum rosaeMFLUCC 15-0633KT026115KT026111--KT026119---[129]
Platystomum salicicolaMFLUCC 15-0632KT026114KT026110--KT026118---[129]
Pseudolophiostoma cornisporumKH 322LC312486LC312544--LC312515LC312602LC312573-[140]
Pseudolophiostoma obtusisporumKT 2838LC312489LC312547--LC312518LC312605LC312576-[140]
Pseudolophiostoma obtusisporumKT 3119LC312491LC312549--LC312520LC312607LC312578-[140]
Pseudolophiostoma tropicumKH 352LC312492LC312550--LC312521LC312608LC312579-[140]
Pseudolophiostoma tropicumKT 3134LC312493LC312551--LC312522LC312609LC312580-[140]
Pseudopaucispora brunneosporaKH 227LC312494LC312552--LC312523LC312610LC312581-[140]
Pseudoplatystomum scabridisporumBCC 22835GQ925831GQ925844---GU479830GU479857-[174]
Pseudoplatystomum scabridisporumBCC 22836GQ925832GQ925845---GU479829GU479856-[174]
Pseudopyrenochaeta lycopersiciCBS 306.65NG_062728MH870217--NR_103581LT717680-LT717674[154]
Pseudopyrenochaeta terrestrisCBS 282.72-LT623216--LT623228LT623287-LT623246[53]
Pseudoteratosphaeria flexuosaCPC 673-KF902098KF903403KF902653KF901745KF902345KF903228 *-[49]
Pseudoteratosphaeria flexuosaCPC 1109-KF902110KF903421KF902654KF901755KF902346--[49]
Pyrenochaeta nobilisCBS 407.76DQ898287EU754206--NR_103598DQ677991DQ677936MF795916[162]
Pyrenochaeta pinicolaCBS 137997-KJ869209--KJ869152LT717684-KJ869249[175]
Pyrenochaeta sp.DTO 305-C6-KX171361--KX147606---[176]
Pyrenochaetopsis botulisporaCBS 142458-LN907440--LT592945LT593084-LT593014[53]
Pyrenochaetopsis globosaCBS 143034-LN907418--LT592934LT593072-LT593003[53]
Pyrenochaetopsis paucisetosaCBS 142460-LN907336--LT592897LT593035-LT592966[53]
Pyrenochaetopsis setosissimaCBS 119739-GQ387632--LT623227LT623285-LT623245[162]
Queenslandipenidiella kurandaeCPC 13333-KF901860KF903538KF902663KF901538KF902356KF903238 *-[49]
Quixadomyces cearensisHUEFS 238438-NG_066409--NR_160606---[131]
Quixadomyces hongheensisKUMCC 20-0215MW264223MW264193--MW264214MW269529MW256815MW256804This study
Quixadomyces hongheensisHKAS112346MW541833MW541822--MW541826MW556136MW556134-MW556137This study
Quixadomyces hongheensisHKAS112347MW541834MW541823--MW541827-MW556135-MW556138This study
Ramusculicola clematidisMFLUCC 17-2146NG_070667MT214596--MT310640MT394707MT394652-[167]
Readeriella angustiaCPC 13608-KF902114KF903566KF902669KF901759KF902364KF903246 *-[49]
Readeriella deaneiCPC 12715-KF901864KF903583KF902673KF901542KF902368KF903250 *-[49]
Readeriella dimorphosporaCPC 12636-KF901866KF903622KF902675KF901544KF902370KF903252 *-[49]
Readeriella menaiensisCPC 14447-KF901870KF903572KF902678KF901548KF902374KF903256 *-[49]
Recurvomyces mirabilisCCFEE 5264-GU250372---KF310059--[139,144]
Recurvomyces mirabilisCCFEE 5475-KC315876---KF310060--[139,144]
Rhytidhysteron bruguieraeMFLUCC 17-1502MN632464MN632453--MN632458-MN635662-[55]
Rhytidhysteron bruguieraeMFLUCC 17-1515MN632463MN632452--MN632457-MN635661-[55]
Rhytidhysteron bruguieraeMFLUCC 18-0398MN017901MN017833----MN077056-[172]
Rhytidhysteron bruguieraeMFLUCC 17-1511MN632465MN632454--MN632459---[55]
Rhytidhysteron camporesiiHKAS 104277 MN429072--MN429069-MN442087-[148]
Rhytidhysteron chromolaenaeMFLUCC 17-1516NG_070139NG_068675--MN632461-MN635663-[55]
Rhytidhysteron erioiMFLU 16-0584-MN429071--MN429068-MN442086-[148]
Rhytidhysteron hongheenseKUMCC 20-0222MW264224MW264194--MW264215MW256807MW256816-This study
Rhytidhysteron hongheenseHKAS112348MW541831MW541820--MW541824-MW556132-This study
Rhytidhysteron hongheenseHKAS112349MW541832MW541821--MW541825-MW556133-This study
Rhytidhysteron hysterinumEB 0351-GU397350----GU397340-[149]
Rhytidhysteron hysterinumCBS 316.71-MH871912--MH860141---[154]
Rhytidhysteron magnoliaeMFLUCC 18-0719MN989382MN989384--MN989383-MN997309-[177]
Rhytidhysteron mangroveiMFLUCC 18-1113-NG_067868--NR_165548-MK450030-[178]
Rhytidhysteron neorufulumMFLUCC 13-0216KU377571KU377566--KU377561-KU510400-[177]
Rhytidhysteron neorufulumGKM 361AGU296192GQ221893------[179]
Rhytidhysteron neorufulumHUEFS 192194-KF914915------[180]
Rhytidhysteron neorufulumMFLUCC 12-0528KJ418119KJ418117--KJ418118---[181]
Rhytidhysteron neorufulumCBS 306.38AF164375FJ469672----GU349031-[142]
Rhytidhysteron neorufulumMFLUCC 12-0011KJ418110KJ418109--KJ206287---[181]
Rhytidhysteron neorufulumMFLUCC 12-0567KJ546129KJ526126--KJ546124---[181]
Rhytidhysteron neorufulumMFLUCC 12-0569KJ546131KJ526128--KJ546126---[181]
Rhytidhysteron neorufulumMFLUCC 14-0577KU377570KU377565--KU377560-KU510399-[177]
Rhytidhysteron opuntiaeGKM 1190 GQ221892----GU397341-[179]
Rhytidhysteron rufulumEB 0384GU397368GU397354------[182]
Rhytidhysteron rufulumEB 0382GU397367GU397352------[182]
Rhytidhysteron rufulumEB 0383 GU397353------[182]
Rhytidhysteron rufulumMFLUCC 12-0013KJ418113KJ418111--KJ418112---[181]
Rhytidhysteron tectonaeMFLUCC 13-0710KU712457KU764698--KU144936-KU872760-[183]
Rhytidhysteron thailandicumMFLUCC 13-0051 MN509434--MN509433-MN509435-[56]
Rhytidhysteron thailandicumMFLUCC 12-0530KJ546128KJ526125--KJ546123---[172]
Rhytidhysteron thailandicumMFLUCC 14-0503KU377569KU377564--KU377559-KU497490-[177]
Seltsamia ulmiCBS 143002MF795794MF795794--MF795794MF795836MF795882MF795918[160]
Sigarispora arundinisKT 651AB618680AB618999--JN942965JN993486LC001738-[129,133]
Sigarispora caudataMAFF 239453AB618681AB619000--LC001723-LC001739-[129,133]
Sigarispora cauliumMAFF 239450AB618682AB619001--LC001724-LC001740-[129,133]
Sigarispora cauliumJCM 17669AB618683AB619002--LC001725-LC001741-[129,133]
Sigarispora ononidisMFLUCC 15-2667KU243126KU243125--KU243128-KU243127-[169]
Sigarispora rosicolaMFLU 15-1888NG_062116MG829080--MG828968-MG829240-[130]
Simplicidiella nigraCBMAI 1939-KU216313-KU216291KT833147-KU216338 *-[171]
Sparticola junciMFLUCC 15-0030NG_061235KU721765--NR_154428KU727900KU727898-[146]
Staninwardia suttoniiCPC 13055-KF901874KF903517KF902693KF901552KF902392KF903270 *-[49]
Staurosphaeria lyciiMFLUCC 17-0210MF434372MF434284--MF434196-MF434458-[134]
Staurosphaeria lyciiMFLUCC 17-0211MF434373MF434285--MF434197-MF434459-[134]
Stenella araguataFMC 245-KF902168---KF902393--[49]
Suberoteratosphaeria pseudosuberosaCPC 12085-KF902144KF903508-KF901786-KF903275 *-[49]
Suberoteratosphaeria xenosuberosaCPC 13093-KF901879KF903584-KF901557KF902402KF903280 *-[49]
Teichospora mariaeC136-KU601581--KU601581KU601595KU601611-[184]
Teichospora rubriostiolataTR 7-KU601590--KU601590KU601599KU601609-[184]
Teichospora thailandicaMFLUCC 17-2093MT226708MT214597--MT310641MT394708MT394653-[167]
Teichospora trabicolaC 134-KU601591--KU601591KU601600KU601601-[184]
Teratoramularia infinitaCBS 141104-KX287249KX287828KX289125KX287545KX288710KX288107 *-[125]
Teratoramularia rumicicolaCBS 141106-KX287255--KX287550KX288716KX288113 *-[125]
Teratosphaeria aurantiaMUCC 668-KF901884KF903578KF902700KF901561KF902409KF903284 *-[49]
Teratosphaeria blakelyiCPC 12837-KF901888KF903518KF902704KF901565KF902413KF903288 *-[49]
Teratosphaeria destructansCPC 1368-KF901898KF903447KF902716KF901574KF902427KF903301 *-[49]
Teratosphaeria fimbriataCPC 13324-KF901901KF903529KF902720KF901577KF902430KF903306 *-[49]
Teratosphaeria gauchensisCMW 17331-KF902148KF903521KF902729KF901790KF902439KF903315 *-[49]
Teratosphaeria mareebensisCPC 17272-KF901906KF903581KF902734KF901582KF902444KF903320 *-[49]
Teratosphaeria pseudocrypticaCPC 11267-KF902032KF903598KF902760KF901687KF902472KF903348 *-[49]
Teratosphaeriaceae sp.CPC 13680-KF901921KF903657KF902765KF901597KF902477KF903353 *-[49]
Teratosphaeriaceae sp.CCFEE 5569-KF310015---KF310071--[139]
Teratosphaericola pseudoafricanaCPC 1231-KF902045KF903435KF902782KF901699KF902499KF903370 *-[49]
Teratosphaericola pseudoafricanaCPC 1230-KF902084KF903473KF902783KF901737KF902500KF903371 *-[49]
Teratosphaeriopsis pseudoafricanaCPC 1261-KF902085KF903436KF902784KF901738KF902501KF903372 *-[49]
Vaginatispora amygdaliKT 2248LC312495LC312553--LC312524LC312611LC312582-[140]
Vaginatispora appendiculataMFLUCC 16-0314KU743219KU743218--KU743217-KU743220-[185]
Vaginatispora armatisporaMFLUCC 18-0247MK085058MK085060--MK085056MK087669MK087658-[146]
Vaginatispora nypaeMFLUCC 18-1543NG_065779NG_066313--NR_163340MK434877MK360091-[127]
Vaginatispora scabrisporaKT 2443LC312496LC312554--LC312525LC312612LC312583-[140]
Westerdykella ornataCBS 379.55GU296208GU301880--AY943045-GU349021-[142]
Xenopenidiella inflataCBMAI 1945-KU216337-KU216312KT833171-KU216359 *-[171]
Xenopenidiella tardaCBMAI 1940-KU216326-KU216303KT833160-KU216351 *-[171]
Xenophacidiella pseudocatenataCPC 18472-KF902092---KF902508--[49]
Xenopyrenochaetopsis pratorumCBS 445.81NG_062792NG_057858--NR_111623KT389671-KT389846[186]
GenBank accession numbers with * are resulting from EF1-728F and EF-2 primers and – means missing data or not used in the phylogenetic analyses. The newly generated sequences are indicated in bold.
Table
Table 4. Maximum-likelihood (ML) and Bayesian (BI) analyses results for each sequenced dataset.
Table 4. Maximum-likelihood (ML) and Bayesian (BI) analyses results for each sequenced dataset.
AnalysesTeratosphaeriaceaeRhytidhysteronLophiostomataceaeParapyrenochaeta
Number of Taxa1063410637
Gene regionsLSU, ITS, rpb2, act, cal and tef1SSU, LSU, ITS and tef1SSU, LSU, ITS, tef1 and rpb2LSU, SSU, ITS, rpb2, tef1 and btub
Number of character positions (including gaps)3517366746495510
ML optimization likelihood value−50604.86449−10388.988691−42280.12689−27947.901235
Distinct alignment patterns in the matrix197373920821710
Number of undetermined characters or gaps (%)48.76%30.69%27.07%38.18%
Estimated base frequenciesA0.236930.2413880.248930.245506
C0.268130.2443260.247320.244909
G0.2837330.2778590.2679170.265204
T0.2112070.2364270.2358330.244381
Substitution ratesAC1.4988331.5332681.5494061.619926
AG2.7843662.5077744.373874.391077
AT1.6628351.3406211.4623921.995039
CG1.1299051.0291211.4536741.225921
CT6.2101756.5296128.8082748.980921
GT1.01.01.01.0
Proportion of invariable sites (I)0.4169890.6108230.4535450.55191
Gamma distribution shape parameter (α)0.6266120.4759110.514540.443538
Number of generated trees in BI2986134519001951
Number of trees sampled in BI after 25% were discarded as burn-in2239625896751714
Final split frequency0.0099990.0092610.0099770.007923
The total of unique site patterns197474020841711
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Wanasinghe, D.N.; Mortimer, P.E.; Xu, J. Insight into the Systematics of Microfungi Colonizing Dead Woody Twigs of Dodonaea viscosa in Honghe (China). J. Fungi 2021, 7, 180. https://doi.org/10.3390/jof7030180

AMA Style

Wanasinghe DN, Mortimer PE, Xu J. Insight into the Systematics of Microfungi Colonizing Dead Woody Twigs of Dodonaea viscosa in Honghe (China). Journal of Fungi. 2021; 7(3):180. https://doi.org/10.3390/jof7030180

Chicago/Turabian Style

Wanasinghe, Dhanushka N., Peter E. Mortimer, and Jianchu Xu. 2021. "Insight into the Systematics of Microfungi Colonizing Dead Woody Twigs of Dodonaea viscosa in Honghe (China)" Journal of Fungi 7, no. 3: 180. https://doi.org/10.3390/jof7030180

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