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Research Article
New species and records of Botryosphaeriales (Dothideomycetes) associated with tree dieback in Beijing, China
expand article infoYingying Wu‡, Cheng Peng‡, Rong Yuan‡, Mingwei Zhang‡, Yang Hu§, Chengming Tian‡
‡ Beijing Forestry University, Beijing, China
§ The Forestry Protection Station of Tonghzou Strict in Beijing, Beijing, China

Corresponding author: Chengming Tian ( chengmt@bjfu.edu.cn )

Academic editor: Ning Jiang
© 2024 Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu, Chengming Tian.
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: Wu Y, Peng C, Yuan R, Zhang M, Hu Y, Tian C (2024) New species and records of Botryosphaeriales (Dothideomycetes) associated with tree dieback in Beijing, China. MycoKeys 106: 225-250. https://doi.org/10.3897/mycokeys.106.122890
Open Access

Abstract

Botryosphaeriales species are important pathogens that have worldwide distribution. In this study, 23 Botryosphaeriales strains were isolated from 13 host species during a dieback disease survey in Beijing, China. Based on morphological and phylogenetic analyses, six Botryosphaeriales species were identified, including two new species named Dothiorella hortiarborum sp. nov. and Phaeobotryon fraxini sp. nov., and four new host records: Aplosporella ginkgonis from Cotinus coggygria var. cinereus, A. javeedii from Acer miyabei, Acer truncatum, Forsythia suspensa, Lagerstroemia indica, Sambucus williamsii, Syringa vulgaris, Ulmus pumila, Xanthoceras sorbifolium, A. yanqingensis from Acer truncatum, and Do. acericola from Forsythia suspensa, Ginkgo biloba, and Syringa oblata. This study enriches the species diversity associated with tree dieback in Beijing, China, and contributes to the further study of the taxonomy of this order.

Key words

Dothiorella, morphology, Phaeobotryon, phylogeny, taxonomy

Introduction

Botryosphaeriales species are important plant pathogens commonly found on the trunks and branches of woody plants (Phillips et al. 2013; Lawrence et al. 2017; Zhu et al. 2018; Zhang et al. 2021). They are associated with branch canker, dieback, decline, and death, with consequences for the ecological and economic value of the forest (Slippers and Wingfield 2007; Phillips et al. 2013; Mohali-Castillo 2023). Botryosphaeriales species occur on a wide range of hosts, in the form of endophytes on woody plants and herbs, lichens, and even seaweed leaves in marine environments, suggesting that they have great potential for research value (Yang et al. 2017; Akinsanmi et al. 2019; Zhang et al. 2021; Mohali-Castillo 2023; Rathnayaka et al. 2023).

Phylogenetic analyses of DNA sequence data have an enormous influence on the systematics and taxonomy of the order Botryosphaeriales, including redefining families and genera and identifying new species (Phillips et al. 2019; Mohali-Castillo 2023). Schoch et al. (2006) combined SSU, LSU, tef1-α, and rpb2 to first propose the order Botryosphaeriales, which contains only a single family of Botryosphaeriaceae. Minnis et al. (2012) supplemented the DNA sequence data of Planistromellaceae with phylogenetic analyses combining SSU, ITS, LSU, and rpb1, which introduced the family into the Botryosphaeriales. Wikee et al. (2013) reintroduced the Phyllostictaceae, grouped under Botryosphaeriales, to accommodate Phyllosticta using intronic genes (ITS, act, and tef1-α) and highly conserved coding regions of genes (LSU and GPDH). Slippers et al. (2013) added three new families, Aplosporellaceae (Aplosporella and Bagnisiella), Melanopsaceae (Melanops), and Saccharataceae (Saccharata), to Botryosphaeriales based on DNA sequence data of six loci (SSU, LSU, ITS, tef1-α, tub2, and mtSSU). Wyka and Broders (2016) introduced Septorioideaceae based on morphological and molecular evidence. Yang et al. (2017) mentioned that the LSU-rpb2 combination could effectively classify taxa at the family and genus levels, and rpb2 in combination with ITS, tef1-α, and tub2 added additional resolution for species delimitation. For this reason, they combined the five fragments ITS, tef1-α, tub2, LSU, and rpb2 to propose two new families, Endomelanconiopsisaceae and Pseudofusicoccumaceae. Therefore, Botryosphaeriales contained a total of nine families. However, Phillips et al. (2019) reassessed the families of Botryosphaeriales in terms of morphology of the sexual morphs and phylogenetic relationships of ITS and LSU sequence data, ultimately concluding that the order contained only six families (Aplosporellaceae, Botryosphaeriaceae, Melanopsaceae, Phyllostictaceae, Planistromellaceae, and Saccharataceae), with Endomelanconiopsisaceae, Pseudofusicoccumaceae, and Septorioideaceae as synonyms of existing families. Up to date, six families and 32 genera are accepted in Botryosphaeriales (https://www.outlineoffungi.org/). Of these, Botryosphaeriaceae is rich in species diversity, high in pathogenicity, and widely distributed.

Botryosphaeriaceae was first established by Theissen and Sydow (1918), containing three genera: Botryosphaeria, Dibotryon, and Phaeobotryon. Morphologically, Botryosphaericeae species are distinctive from other families in Botryosphaeriales by their large, ovoid to oblong, usually hyaline, aseptate ascospores (Phillips et al. 2013). Liu et al. (2012) assumed that ascospores could become pigmented and septate with age. Conidia in the asexual state of Botryosphaericeae are diverse in morphological characteristics (Phillips et al. 2005). Phylogenetically, however, there is a random distribution of hyaline or colored conidia or ascospores in the phylogenetic tree of Botryosphaericeae (Slippers et al. 2013). Therefore, accurate identification of species in the family by a single circumscription is not suitable. Currently, 22 genera and more than 200 species are contained within the family (https://www.outlineoffungi.org/). Recently, many new species have been introduced in the Botryosphaeriaceae, especially in the genera Dothiorella and Phaeobotryon (Jia et al. 2023; Li et al. 2023; Lin et al. 2023a; Wu et al. 2023).

Saccardo (1880) first established Dothiorella and designated Do. pyrenophora as the type species. Up to now, some scholars have made systematic revisions of Dothiorella to establish a more stable phylogenetic relationship (Dissanayake et al. 2016; Dissanayake et al. 2020; Zhang et al. 2021). The distinctive features of the genera are that the conidia are colored in the early stages of development, and with 1-septate, the sexual form of ascospores is brown and septate (Senanayake et al. 2023). The type species of the genus Phaeobotryon is P. cercidis, which is characterized by 2-septate brown ascospores with conical apiculate-elliptic to oblong or obovoid shapes at both ends and hyaline or brown conidia (Phillips et al. 2013; Fan et al. 2015b; Zhu et al. 2018; Pan et al. 2019).

In recent years, multiple studies have revealed that new species of Botryosphaeriales infest branches and trunks. Pan et al. (2019) found that Phaeobotryon rhois and Diplodia quercicola were detrimental to Rhus typhina and Quercus variabilis separately in Yudu Mountain, Beijing. Aplosporella yanqingensis and Dothiorella baihuashan are mainly recorded on Pinaceae or Cupressaceae (Lin et al. 2023a). Lasiodiplodia regiae caused the canker and dieback of apple trees (Wang et al. 2023). These studies suggest that Botryosphaeriales is rich in species diversity and has the potential to continue to be explored for new species. During the investigation of plant pathogens in Beijing, a higher number of diseased plant branches caused by Botryosphaeriales fungi were found. This study used phylogenetic analysis and morphological comparisons to describe new species and new host records, enriching the fungal taxa within Botryosphaeriales.

Materials and method

Sample collection and fungal isolation

A survey on dieback diseases was conducted from March to November 2023 in the Tongzhou District of Beijing, China. A total of thirteen tree species were examined, namely Acer miyabei, A. truncatum, Cotinus coggygria var. cinereus, Forsythia suspensa, Fraxinus chinensis, Ginkgo biloba, Lagerstroemia indica, Sambucus williamsii, Styphnolobium japonicum, Syringa oblata, Syringa vulgaris, Ulmus pumila, and Xanthoceras sorbifolium. Twenty specimens showing typical dieback symptoms (Fig. 1) with typical conidiomata and/or ascomata were collected. All samples were placed in paper bags and transported to the laboratory. Specimens with typical conidiomata pycnidial were selected for isolation. Removing the spore mass from conidiomata and generating single spore colonies or plating superficially sterilized diseased tissue on potato dextrose agar plates (PDA; containing 200 g potatoes, 20 g dextrose, and 20 g agar per liter) and incubating Petri dishes at 25 °C in the dark for 2–3 d. When colonies just formed, they transferred to fresh PDA Petri dishes (Crous et al. 2019). All specimens were deposited at the Museum of Beijing Forestry University (BJFC), and all cultures were preserved at the China Forestry Culture Collection Center (CFCC).

Figure 1. 

Disease symptoms associated with Botryosphaeriales species collected from Tongzhou District, Beijing, China A Xanthoceras sorbifolium B Fraxinus chinensis C Lagerstroemia indica D Sambucus williamsii E Styphnolobium japonicum F Forsythia suspensa.

Morphological observation

Cultures were incubated on PDA at 25 °C in a 12-h day/night regime (Crous et al. 2019). After 14 days, the colonies were measured, and characteristics based on the color, shape, and sparseness of the aerial mycelium of the pathogen colonies were observed and recorded. Conidiomata were manually sectioned with a double-edged razor blade. Observations were conducted using a Leica DM 2,500 dissecting microscope (Wetzlar, Germany) and a Nikon Eclipse 80i compound microscope, equipped with differential interference contrast (DIC) illumination. Images were captured using a Nis DS-Ri2 camera with the Nikon Nis-Elements F4.30.01 software. Conidial length was measured from the base of the basal cell to the base of the apical appendage, while conidial width was measured at its widest point. A randomized selection of conidia was used for measurement (n = 50).

DNA extraction, PCR amplification, and sequencing

Genetic DNA was extracted using the cetyltrime-thylammonium bromide (CTAB) method when the mycelium was well spread on the PDA. DNA samples were stored at -20 °C. The PCR reaction primers (forward and reverse) and amplification conditions are detailed in Table 1. Polymerase chain reaction (PCR) amplification was run on a PTC-200 Thermal Cycler amplifier from Bio-Rad, USA. The PCR amplification systems were all 20 μL, including 10 μL of Mix (Promega), 7 μL of double deionized water, 1 μL each of pre- and post-primers, and 1 μL of DNA template. PCR products were assayed by electrophoresis on 2% agarose gels. Amplified PCR products were sent to a commercial sequencing provider (Tsingke Biotechnology Co. Ltd., Beijing, China).

Table 1.
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Genes used in this study with PCR primers.

Locus PCR primers PCR: thermal cycles: (Annealing temp. in bold) References
ITS ITS1/ITS4 (95 °C: 30 s, 51 °C: 30 s, 72 °C: 1 min) × 35 cycles White et al. 1990
LSU LROR/LR5 (95 °C: 45 s, 55 °C: 30 s, 72 °C: 1 min) × 35 cycles Vilgalys and Hester 1990
tef1-α EF1-728F/EF1-986R (95 °C: 15 s, 55 °C: 30 s, 72 °C: 1 min) × 35 cycles Carbone and Kohn 1999
tub2 Bt2a/Bt2b (95 °C: 30 s, 55 °C: 30 s, 72 °C: 1 min) × 35 cycles Glass and Donaldson 1995

Phylogenetic analyses

The sequences obtained were assembled using SeqMan v. 7.1.0 software, and reference sequences from related publications (Phillips et al. 2019; Li et al. 2023; Lin et al. 2023a; Wu et al. 2023) were retrieved from the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov). All sequences generated in this study were submitted to GenBank (Table 2). Sequences were aligned in MAFFT v. 7 at the web server (https://mafft.cbrc.jp/alignment/server/) (Katoh and Standley 2013; Katoh et al. 2019) and further adjustments and editing of the sequences were made with MEGA v. 6 (Tamura et al. 2013). Maximum parsimony (MP), maximum likelihood (ML), and Bayesian inference (BI) were selected to construct phylogenetic trees using PAUP v. 4.0b10, PhyML 3.0, and MrBayes V3.1.2 (Huelsenbeck and Ronquist 2001; Swofford 2003; Silvestro and Michalak 2012). Phylograms were visualized with FigTree v. 1.4.0 (http://tree.bio.ed.ac.uk/software/figtree/) and additional edited with Adobe Illustrator CS v. 5 (Adobe Systems Inc., USA). Maximum-parsimony bootstrap values (MPBP) and maximum-likelihood bootstrap values (MLBP) ≥ 50% and Bayesian posterior probabilities (BYPP) ≥ 0.90 are shown for each tree.

Table 2.
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Isolates of Aplosporella, Dothiorella, and Phaeobotryon used in the molecular analyses in this study. Notes: NA: not applicable, Strains in this study are marked in bold, T: ex-type strains.

Species Strain Host Origin GenBank accession numbers
ITS tef1-α tub2 LSU
Aplosporella africana CBS 121777T Acacia mellifera Namibia KF766196 EU101360 NA NA
A. africana CBS 1217778T Acacia mellifera Namibia EU101316 EU101361 NA NA
A. artocarpi CPC 22791T Artocarpus heterophyllus Thailand KM006450 KM006481 NA NA
A. ginkgonis CFCC 52442T Rhus typhina China MH133916 MH133950 NA NA
A. ginkgonis CFCC 89661T Rhus typhina China KM030583 KM030597 NA NA
A. ginkgonis CFCC 70746 Cotinus coggygria var. cinereus China PP188498 PP541796 NA NA
A. hesperidica CBS 732.79T Citrus aurantium Buenos Aires KX464083 NA NA NA
A. hesperidica CBS 208.37 Citrus sinensis Zimbabwe JX681069 NA NA NA
A. javeedii CFCC 50054T Juniperus chinensis China KP208840 KP208846 NA NA
A. javeedii CFCC 50052 Gleditsia sinensis China KP208838 KP208844 NA NA
A. javeedii CFCC 58330 Populus canadensis China OQ651161 OQ692921 NA NA
A. javeedii CFCC 58329 Populus beijingensis China OQ651162 OQ692922 NA NA
A. javeedii CFCC 58412 Populus alba var. pyramidalis China OQ651163 OQ692923 NA NA
A. javeedii CFCC 70733 Styphnolobium japonicum China PP188499 PP541797 NA NA
A. javeedii CFCC 70734 Forsythia suspensa China PP188500 PP541798 NA NA
A. javeedii CFCC 70735 Forsythia suspensa China PP188501 PP541799 NA NA
A. javeedii CFCC 70736 Ulmus pumila China PP188502 PP541800 NA NA
A. javeedii CFCC 70737 Acer truncatum China PP188503 PP541801 NA NA
A. javeedii CFCC 70739 Sambucus williamsii China PP188504 PP541802 NA NA
A. javeedii CFCC 70740 Acer miyabei China PP188505 PP541803 NA NA
A. javeedii CFCC 70741 Lagerstroemia indica China PP188506 PP541804 NA NA
A. javeedii CFCC 70742 Xanthoceras sorbifolium China PP188507 PP541805 NA NA
A. javeedii CFCC 70744 Syringa vulgaris China PP188508 PP541806 NA NA
A. javeedii CFCC 70745 Ulmus pumila China PP188509 PP541807 NA NA
A. macropycnidia CGMCC 3.17725T Cerasus yedoensis China KT343648 KX011176 NA NA
A. macropycnidia CGMCC 3.17726 Cerasus yedoensis China KT343649 KX011177 NA NA
A. papillata CBS 121780T Acacia tortillas South Africa EU101328 EU101373 NA NA
A. papillata CBS 121781 Acacia tortillas South Africa EU101329 EU101374 NA NA
A. prunicola CBS 121167T Prunus persica var. nucipersica South Africa KF766147 NA NA NA
A. prunicola STE-U 6326 Prunus persica var. nucipersica South Africa EF564375 NA NA NA
A. sophorae CPC 29688T Sophora microphylla New Zealand North KY173388 NA NA NA
A. thailandica MFLU 16-0615T Dead stems Thailand KX423536 KX423537 NA NA
A. yalgorensis MUCC511T Acacia cochlearis Australia EF591926 EF591977 NA NA
A. yalgorensis MUCC512 Eucalyptus gomphocephala Australia EF591927 EF591978 NA NA
A. yanqingensis CFCC 58791T Platycladus orientalis China OQ651164 OQ692924 NA NA
A. yanqingensis CFCC 58792T Platycladus orientalis China OQ651165 OQ692925 NA NA
A. yanqingensis CFCC 70743 Acer truncatum China PP188510 PP541808 NA NA
A. yanqingensis CFCC 70738 Acer truncatum China PP188511 PP541809 NA NA
Alanomyces indica CBS 134264T Soil India HF563622 AB872219 NA NA
Dothiorella alpina CGMCC 3-18001T Platycladus orientalis China KX499645 KX499651 NA NA
Do. acacicola CBS 141295T Acacia mearnsii Réunion KX228269 KX228376 NA NA
Do. acericola KUMCC 18-0137T Acer palmatum China MK359449 MK361182 NA NA
Do. acericola CFCC 70755 Forsythia suspensa China PP188520 PP766251 PP566659 NA
Do. acericola CFCC 70760 Ginkgo biloba China PP188521 PP766252 PP566660 NA
Do. acericola CFCC 70761 Syringa oblata China PP188522 PP766253 PP566661 NA
Do. albiziae MFLUCC 22-0057T Albizia lebbeck Thailand ON751762 ON799588 ON799590 NA
Do. alpina CFCC 58299T Populus szechuanica China OQ651166 OQ692932 OQ692926 NA
Do. americana CBS 128309T Vitis species and Vitis vinifera USA: Missouri HQ288218 HQ288262 HQ288297 NA
Do. baihuashanensis CFCC 58549T Juniperus chinensis China OQ651167 OQ692933 OQ692927 NA
Do. baihuashanensis CFCC 58788T Juniperus chinensis China OQ651168 OQ692934 OQ692928 NA
Do. brevicollis CBS 130411 = CMW 36463T Acacia karroo South Africa JQ239403 JQ239390 JQ239371 NA
Do. californica CBS 119635 Laurus nobilis Turkey MT587396 MT592108 MT592579 NA
Do. californica CBS 141587T Umbellularia californica USA KX357188 KX357211 KX357165 NA
Do. camelliae CMGCC 3.24158T Camellia oleifera China OQ190531 OQ241464 OQ275064 NA
Do. capri-amissi CBS 121763 = CMW 25403 = CAMS 1158T Acacia erioloba South Africa EU101323 EU101368 KX464850 NA
Do. capri-amissi CBS 121878 = CMW 25404 = CAMS 1159T Acacia erioloba South Africa EU101324 EU101369 KX464851 NA
Do. casuarinae CBS 120688 = CMW 4855T Casuarina sp. Australia DQ846773 DQ875331 DQ875340 NA
Do. casuarinae CBS 120689 = CMW 4856 Casuarina sp. Australia DQ846772 DQ875332 DQ875339 NA
Do. casuarinae CBS 120690 = CMW 4857 Casuarina sp. Australia DQ846774 DQ875333 DQ875341 NA
Do. citricola CBS 124728 = ICMP 16827 Citrus sinensis New Zealand EU673322 EU673289 KX464852 NA
Do. citricola CBS 124729 = ICMP 16828T Citrus sinensis New Zealand EU673323 EU673290 KX464853 NA
Do. citrimurotticola BE5 = CGMCC3.20392T Citrus unshiu China MW880663 MW884166 MW884195 NA
Do. citrimurotticola BE8 = CGMCC3.20394 Citrus reticulatachen × C. sinensis China MW880661 MW884164 MW884193 NA
Do. diospyricola CBS 145972 Diospyros mespiliformis South Africa MT587398 MT592110 MT592581 NA
Do. dulcispinae CBS 121764 = CMW 25406 = CAMS 1159 Acacia mellifera Namibia EU101299 EU101344 KX464854 NA
Do. dulcispinae CBS 130413 = CMW 36460T Acacia karroo South Africa JQ239400 JQ239387 JQ239373 NA
Do. eriobotryae CBS 140852T Eriobotrya japonica Spain KT240287 KT240262 MT592582 NA
Do. franceschinii CBS 147722 Rhamnus alaternus Italy OP999677 OQ067247 NA NA
Do. guttulata MFLUCC 17-0242 Alnus glutinosa Italy KY797637 NA NA NA
Do. heterophyllae CMW 46458T Acacia heterophylla Réunion MN103794 MH548348 MH548324 NA
Do. hortiarborum CFCC 70756T Fraxinus chinensis China PP188523 PP723042 PP566662 NA
Do. hortiarborum CFCC 70757 Fraxinus chinensis China PP188524 PP723043 PP566663 NA
Do. hortiarborum CFCC 70758 Lagerstroemia indica China PP188525 PP723044 PP566664 NA
Do. hortiarborum CFCC 70759 Lagerstroemia indica China PP188526 PP723045 PP566665 NA
Do. iberica CBS 113188 = DA-1 Quercus suber Spain AY573198 EU673278 EU673097 NA
Do. iberica CBS 113189 = DE-14 Quercus ilex Spain AY573199 AY573230 KX464855 NA
Do. iberica CBS 115041 = CAP 145T Quercus ilex Spain AY573202 AY573222 EU673096 NA
Do. irannica CBS 124722 = CJA 153 = IRAN 1587CT Olea europaea Iran, Golestan KC898231 KC898214 KX464856 NA
Do. koae CMW 48017T Acacia koa Hawaiian Is. MH447652 MH548338 MH548327 NA
Do. lampangensis MFLUCC 18-0232T Rutaceae Thailand MK347758 MK340869 MK412874 NA
Do. longicollis CBS 122066 = CMW 26164 Terminalia sp. Australia EU144052 EU144067 KX464857 NA
Do. longicollis CBS 122067 = CMW 26165 Lysiphyllum cunninghamii Australia EU144053 EU144068 KX464858 NA
Do. longicollis CBS 122068 = CMW 26166T Lysiphyllum cunninghamii Australia EU144054 EU144069 KF766130 NA
Do. magnoliae CFCC51563T Magnolia grandiflora China KY111247 KY213686 NA NA
Do. mangifericola CBS 124727T Mangifera indica Iran KC898221 KX464614 NA NA
Do. mangifericola IRAN 1584C Mangifera indica Iran MT587407 MT592119 NA NA
Do. moneti WAC 13154 = MUCC 505T Acacia rostellifera Australia EF591920 EF591971 EF591954 NA
Do. neclivorem DAR 80992T Vitis vinifera Australia KJ573643 KJ573640 KJ577551 NA
Do. oblonga CBS 121765 = CMW 25407 = CAMS 1162T Acacia mellifera South Africa EU101300 EU101345 KX464862 NA
Do. oblonga CBS 121766 = CMW 25408 = CAMS 1163 Acacia mellifera South Africa EU101301 EU101346 KX464863 NA
Do. obovata MFLUCC22-0058T Pavonia odorata Thailand ON751763 ON799589 ON799591 NA
Do. omnivora CBS 124717 = CJA 214 = IRAN 1570C Juglans regia Iran KC898233 KC898216 KX464865 NA
Do. omnivora CBS 392.80 – France KX464133 KX464626 KX464897 NA
Do. omnivora CBS 124716 = CJA 241 = IRAN 1573C Juglans regia Iran KC898232 KC898215 KX464864 NA
Do. omnivora CBS 242.51 – Italy EU673317 EU673284 EU673105 NA
Do. omnivora CBS 188.87 Juglans regia France EU673316 EU673283 EU673119 NA
Do. parva CBS 124720 = CJA 27 = IRAN 1579CT Corylus sp. Iran KC898234 KC898217 KX464866 NA
Do. parva CBS 124721 = CJA 35 Corylus sp. Iran KX464123 KX464615 KX464867 NA
Do. parva CBS 125580 Corylus avellana Austria KX464124 KX464616 KX464868 NA
Do. plurivora CBS 124724 = CJA 254 = IRAN 1557CT Citrus sp. Iran KC898225 KC898208 KX464874 NA
Do. pretoriensis CBS 130404 = CMW 36480T Acacia karroo South Africa JQ239405 JQ239392 JQ239376 NA
Do. prunicola CBS 124723 = CAP 187 = IRAN 1541CT Prunus dulcis Portugal EU673313 EU673280 EU673100 NA
Do. rhamni MFLUCC 14-0902T Rhamnus cathartica South European Russia MF398893 MF398945 NA NA
Do. rosulata CBS 121760 = CMW 25389 = CAMS 1444T Acacia karroo Namibia KF766227 EU101335 KX464877 NA
Do. rosulata CBS 121761 = CMW 25392 = CAMS 1147 Acacia mellifera South Africa EU101293 EU101338 KX464878 NA
Do. rosulata CBS 121762 = CMW 25395 = CAMS 1150 Acacia mellifera South Africa EU101319 EU101364 KX464879 NA
Do. rosulata CBS 500.72 Medicago sativa South Africa EU673318 EU673285 EU673118 NA
Do. santali WAC 13155 = MUCC 509T Santalum acuminatum Australia EF591924 EF591975 EF591958 NA
Do. saprophytica MFLUCC 23-0210 – Thailand OR527239 OR532455 OR532454 NA
Do. sarmentorum IMI 63581b Ulmus sp. UK: England AY573212 AY573235 EU673102 NA
Do. sempervirentis IRAN 1581C = CBS 124719 Cupressus sempervirens Iran KC898237 KC898220 KX464885 NA
Do. sempervirentis IRAN 1583C = CBS 124718 = CJA 264T Cupressus sempervirens Iran KC898236 KC898219 KX464884 NA
Do. sp. CBS 121783 = CMW 25432 = CAMS 1187 Acacia mearnsii South Africa EU101333 EU101378 KX464859 NA
Do. sp. CBS 121784 = CMW 25430 = CAMS 1185 Acacia mearnsii South Africa EU101331 EU101376 KX464860 NA
Do. sp. CBS 121785 = CMW 25433 = CAMS 1188 Acacia mearnsii South Africa EU101334 EU101379 KX464861 NA
Do. striata CBS 124730 = ICMP 16819 Citrus sinensis New Zealand EU673320 EU673287 EU673142 NA
Do. striata CBS 124731 = ICMP 16824T Citrus sinensis New Zealand EU673321 EU673288 EU673143 NA
Do. styphnolobii Cr01T Styphnolobium japonicum Crym MH880849 MK069594 NA NA
Do. symphoricarpicola CPC 33923T Symphoricarpos Italy MT587414 MT592126 MT592606 NA
Do. tectonae MFLUCC18-0232T Tectona grandis Thailand KM396899 KM409637 KM510357 NA
Do. thailandica CBS 133991 = CPC 21557 = MFLUCC 11-0438 Dead bamboo culm Thailand JX646796 JX646861 JX646844 NA
Do. thripsita CBS 125445 = BRIP 51876aT Acacia harpophylla Australia KJ573642 KJ573639 KJ577550 NA
Do. ulmacea CBS 141414T Ulmus laevis Germany MT587415 MT592127 MT592608 NA
Do. uruguayensis CBS 124908 = CMW 26763T Hexachlamis edulis Uruguay EU080923 EU863180 KX464886 NA
Do. vidmadera CBS 621.74 Pyrus communis Switzerland KX464129 KX464621 KX464887 NA
Do. vidmadera CBS 725.79T Pyrus malus Switzerland KX464130 KX464622 KX464888 NA
Do. vinea-gemmae DAR 81012T Vitis vinifera Australia KJ573644 KJ573641 KJ577552 NA
Do. viticola CBS 117009T Vitis vinifera Spain AY905554 AY905559 EU673104 NA
Do. westralis WA10NO01T Vitis vinifera Australia HM009376 HM800511 NA NA
Do. yunnana CGMCC 3-17999T Camellia sp. China KX499643 KX499649 NA NA
Do. yunnana CGMCC 3-18000 Camellia sp. China KX499644 KX499650 NA NA
Do. zanthoxyli CMGCC 3.24159T Zanthoxylum bungeanum Sichuan OQ190536 OQ241468 OQ275069 NA
Neofusicoccum luteum CBS 562.92T Actinidia deliciosa New Zealand MH862376 KX464690 KX464968 NA
Neofusicoccum parvum CMW 9081T Populus nigra New Zealand AY236943 AY236888 AY236917 NA
Phaeobotryon aplosporum CFCC 53774 Syzygium aromaticum China MN215836 MN205996 NA MN215871
P. aplosporum CFCC 53775T Rhus typhina China MN215837 NA NA MN215872
P. aplosporum CFCC 53776 Rhus typhina China MN215838 MN205997 NA MN215873
P. aplosporum CFCC 58596 Juglans mandshurica China OQ651169 NA NA OQ652540
P. aplosporum CFCC 58784 Juglans mandshurica China OQ651170 NA NA OQ652541
P. cupressi CBS 124700 = IRAN 1455CT Cupressus sempervirens Iran FJ919672 FJ919661 NA KX464538
P. cupressi CBS 124701 = IRAN 1458C Cupressus sempervirens Iran FJ919671 FJ919660 NA KX464539
P. fraxini CFCC 70762T Fraxinus chinensis China PP188527 PP505782 NA PP177348
P. fraxini CFCC 70763 Fraxinus chinensis China PP188528 PP505783 NA PP177349
P. juniperi JU001 T Juniperus formosana China OP941637 OP948218 NA OP941644
P. juniperi JU005 Juniperus formosana China OP941638 OP948219 NA OP941645
P. mali XJAU 2930T Malus pumila China MW326854 MW509519 NA MW367101
P. mali XJAU 2772 Juglans regia China MW326853 MW509520 NA MW367094
P. mali XJAU 2782 Malus ‘Royalty’ China MW326852 MW509516 NA MW367092
P. mali XJAU 3094 Elaeagnus angustifolia China MW326858 MW509517 NA MW367100
P. mali XJAU 3100 Rhus typhina China MW326878 MW509518 NA MW367093
P. mamane CBS 122980 = CPC 12440T Sophora chrysophylla USA EU673332 EU673298 NA EU673248
P. mamane CPC 12442 Sophora chrysophylla USA EU673333 EU673299 NA DQ377899
P. negundinis CAA 797 Acer negundo Russia KX061513 KX061507 NA NA
P. negundinis CAA 798 Ligustrum vulgare Russia KX061514 KX061508 NA NA
P. negundinis CAA 799 Forsythia intermedia Russia KX061515 KX061509 NA NA
P. negundinis CPC 33384 Acer nugundo Ukraine MT587542 MT592276 NA MT587323
P. negundinis CPC 33388 Dead stem Ukraine MT587543 MT592277 NA MT587324
P. negundinis CPC 34752 Acer negundo Ukraine MT587544 MT592278 NA MT587325
P. negundinis MFLUCC 15-0436T Acer negundo Russia KU820970 KU853997 NA NA
P. platycladi CFCC 58799T Platycladus orientalis China OQ651172 OQ692930 NA OQ652543
P. platycladi CFCC 58800 Platycladus orientalis China OQ651173 OQ692931 NA OQ652544
P. rhoinum CFCC 52449 Rhus typhina China MH133923 MH133957 NA MH133940
P. rhoinum CFCC 52450T Rhus typhina China MH133924 MH133958 NA MH133941
P. rhois CFCC 89662 = CCTCC AF2014017T Rhus typhina China KM030584 KM030598 NA KM030591
P. rhois CFCC 89663 = CCTCC AF2014016 Rhus typhina China KM030585 KM030599 NA KM030592
P. rhois CFCC 58679T Populus alba var. pyramidalis China OQ651171 OQ692929 NA OQ652542
P. spiraeae CFCC 53925T Spiraea salicifolia China OM049420 NA NA OM0049432
P. spiraeae CFCC 53926 Spiraea salicifolia China OM049421 NA NA OM0049433
P. spiraeae CFCC 53927 Spiraea salicifolia China OM049422 NA NA OM0049434
P. ulmi 94-13 Ulmus pumila USA AF243398 NA NA NA
P. ulmi CBS 114123 = UPSC 2552 Ulmus glabra Sweden MT587539 MT592273 NA MT587320
P. ulmi CBS 138854 = CPC 24264T Ulmus laevis Germany MT587540 MT592274 NA MT587321
P. ulmi CBS 123.30 = ATCC 24443 Ulmus sp. USA KX464232 KX464766 NA DQ377861
P. ulmi CBS 174.63 Ulmus glabra Finland MT587541 MT592275 NA MT587322
P. ulmi CMH 299 House dust USA KF800390 NA NA NA
P. ulmi PB_11f Ulmus glabra Poland MK134682 NA NA NA
Alanphillipsia aloeicola CBS 138896 = CPC 23674T Aloe sp. South Africa KP004444 MT592027 NA KP004472

Maximum parsimony analysis was performed using the tree bisection and reconnection (TBR) branch swapping algorithm with a heuristic search option of 1000 random-addition sequences (Swofford 2003). Max trees were set to 5000 branches of zero length, and all parsimonious trees were saved. Other measures calculated were tree length (TL), consistency index (CI), retention index (RI), and rescaled consistency (RC) (Swofford 2003). Maximum likelihood analysis was performed with the GTR GAMMA model of site substitution, including estimation of gamma-distributed rate heterogeneity and a proportion of invariant sites (Guindon et al. 2010). The branch support from MP and ML analysis was evaluated with a bootstrapping (BS) method of 1 000 replicates (Hillis and Bull 1993). The Bayesian inference analysis employing a Markov chain Monte Carlo (MCMC) algorithm was performed with Bayesian posterior probabilities (Rannala and Yang 1996). The model of nucleotide substitution was estimated by MrModeltest v.2.3 (Posada and Crandall 1998), and a weighted Bayesian analysis was considered. Two MCMC chains were run starting from random trees for 1,000,000 generations and stopped when the average standard deviation of split frequencies fell below 0.01; the trees were sampled every 100th generation. The first 25% of trees were discarded as the burn-in phase of each analysis, and the Bayesian posterior probabilities (BPP) were calculated using the remaining 7,500 trees.

Result

Phylogenetic analysis

The BLAST results indicated that the 23 isolates resided in Aplosporella, Dothiorella, and Phaeobotryon (14 for Aplosporella, 7 for Dothiorella, and 2 for Phaeobotryon). Separate phylogenetic trees for each of the three genera were constructed in this study.

In Aplosporella, the combined ITS and tef1-α dataset consists of 944 characters, including alignment gaps (508 for ITS and 436 for tef1-α), of which 794 are constant and 60 are variable parsimony uninformative characters. MP analysis with the remaining 90 parsimony-informative characters resulted in one equally parsimonious tree: tree length (TL) = 230; consistency index (CI) = 0.817; retention index (RI) = 0.896; and rescaled consistency index (RC) = 0.732. In ML analysis based on the combined gene dataset, the matrix had 193 distinct alignment patterns. Estimated base frequencies are as follows: A = 0.217607, C = 0.264598, G = 0.259539, T = 0.258256, AC = 2.784746, AG = 2.845183, AT = 1.353935, CG = 1.848853, CT = 4.935430, GT = 1.000000, gamma distribution shape parameter: α = 0.157110, and likelihood value of ln: -2 499.855852. The maximum likelihood (ML) and Bayesian methods (BI) for phylogenetic analyses have the same topology and terminal clades. Fourteen isolates were distributed in Aplosporella, aggregated with three known species, A. javeedii, A. yanqingensis, and A. ginkgonis, separately (Fig. 2). The single gene tree for ITS and tef1-α of Aplosporella is shown in Suppl. material 1.

Figure 2. 

Phylogram generated from RAxML analysis based on ITS with tef1-α sequence data of Aplosporella isolates. The tree was rooted in Alanomyces indica (CBS 134264). The MP, ML (≥ 50%), and BI (≥ 0.9) bootstrap supports are given near the nodes, respectively. Isolates from this study are marked in blue, and ex-type strains are marked in bold.

In Dothiorella, sequences of the combined ITS, tef1-α, and tub2 were aligned; the dataset consists of 1,319 characters, including alignment gaps (534 for ITS, 369 for tef1-α, and 416 for tub2), of which 905 are constant and 107 are variable parsimony uninformative characters. MP analysis with the remaining 307 parsimony-informative characters resulted in one equally parsimonious tree: tree length (TL) = 1,282; consistency index (CI) = 0.477; retention index (RI) = 0.824; and rescaled consistency index (RC) = 0.394. In ML analysis based on the combined gene dataset, the matrix had 601 distinct alignment patterns. Estimated base frequencies are as follows: A = 0.206208, C = 0.312741, G = 0.250328, T = 0.230723, AC = 0.833804, AG = 2.174710, AT = 1.041501, CG = 0.791470, CT = 3.735830, GT = 1.000000, gamma distribution shape parameter: α = 0.215045, and likelihood value of ln: -8 567.497788. Three of the seven isolates were of the known species Dothiorella acericola, and the other four isolates formed a separate clade for designation as new species based on phylogenetic analysis (Fig. 3). The single gene tree for ITS, tef1-α, and tub2 of Dothiorella is shown in Suppl. material 2.

Figure 3. 

Phylogram generated from RAxML analysis based on ITS, tef1-α, and tub2 sequence data of Dothiorella isolates. The tree was rooted in Neofusicoccum luteum (CBS 562.92) and Neofusicoccum parvum (CMW9081). The MP, ML (≥ 50%), and BI (≥ 0.9) bootstrap supports are given near the nodes, respectively. Isolates from this study are marked in blue, and ex-type strains are marked in bold.

In Phaeobotryon, the combined ITS, LSU, and tef1-α dataset consists of 1,394 characters, including alignment gaps (494 for ITS, 333 for LSU, and 567 for tef1-α), of which 1,218 are constant and 56 are variable parsimony uninformative characters. MP analysis with the remaining 120 parsimony-informative characters resulted in one equally parsimonious tree: tree length (TL) = 259; consistency index (CI) = 0.799; retention index (RI) = 0.913; and rescaled consistency index (RC) = 0.730. In ML analysis based on the combined gene dataset, the matrix had 239 distinct alignment patterns. Estimated base frequencies are as follows: A = 0.224820, C = 0.266099, G = 0.277247, T = 0.231833, AC = 0.602998, AG = 2.181745, AT = 0.500445, CG = 0.607508, CT = 4.549533, GT = 1.000000, gamma distribution shape parameter: α = 0.020014, and likelihood value of ln: -3 357.887099. Eight isolates were assigned to Phaeobotryon, one isolate aggregated with P. mali, and two isolates stood alone, not branching off from known species, representing a new species (Fig. 4). The single gene tree for ITS, LSU, and tef1-α of Phaeobotryon is shown in Suppl. material 3.

Figure 4. 

Phylogram generated from RAxML analysis based on ITS, LSU, and tef1-α sequence data of Phaeobotryon isolates. The tree was rooted in Alanphillipsia aloeicola (CBS 138896). The MP, ML (≥ 50%), and BI (≥ 0.9) bootstrap supports are given near the nodes, respectively. Isolates from this study are marked in blue, and ex-type strains are marked in bold.

Taxonomy

Aplosporella ginkgonis C.M. Tian, Z. Du & K.D. Hyde, Mycosphere 8(2): 1249 (2017)

Description

See Du et al. 2017.

Material examined

China, Beijing City, Tongzhou District, Majuqiao Wetland Park, 39°46'12"N, 116°37'12"E, on the disease branches of Cotinus coggygria var. cinereus, 2 May 2023, Y.Y. Wu, BJFC-S1931, living culture CFCC 70746.

Notes

Aplosporella ginkgonis was first reported in Gansu Province, China, causing canker and dieback disease in Ginkgo biloba and Morus alba (Du et al. 2017). Zhu et al. (2018) and Li et al. (2023) discovered the species on Rhus typhina and Zanthoxylum bungeanum, respectively, extending its host range. In the present study, one isolate (CFCC 70746) was identified as A. ginkgonis based on the phylogenetically highly supported clade with 99% MP, 95% ML, and 0.94 BYPP values (Fig. 2) and morphological characteristics. This is the first report of A. ginkgonis on Cotinus coggygria var. cinereus.

Aplosporella javeedii Jami, Gryzenh., Slippers & M.J. Wingf., Fungal Biology 118(2): 174 (2013)

Description

See Fan et al. 2015.

Material examined

China, Beijing City, Tongzhou District, Hougezhuang Plain Forest, 29°50'24"N, 116°54'00"E, on the dead branches of Styphnolobium japonicum, 8 April 2023, C.M. Tian, S.J. Li & Y.Y. Wu, BJFC-S1932, living culture CFCC 70733; ibid. on the dead branches of Forsythia suspensa, BJFC-S1933, living culture CFCC 70734; ibid. on the dead branches of Forsythia suspensa, BJFC-S1934, living culture CFCC 70735; ibid. on the dead branches of Ulmus pumila, BJFC-S1935, living culture CFCC 70736; China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, from branches of Acer truncatum, 12 April 2023, C.M. Tian, Y.M. Liang, C. Peng, Y. Hu & Y.Y. Wu, BJFC-S1936, living culture CFCC 70737; China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Sambucus williamsii, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu, BJFC-S1937, living culture CFCC 70739; ibid. on the dead branches of Acer miyabei, BJFC-S1938, living culture CFCC 70740; ibid. on the dead branches of Lagerstroemia indica, BJFC-S1939, living culture CFCC 70741; ibid. on the dead branches of Xanthoceras sorbifolium, BJFC-S1940, living culture CFCC 70742; China, Beijing City, Tongzhou District, Majuqiao Wetland Park, 39°46'12"N, 116°37'12"E, from branches of Syringa vulgaris, 2 May 2023, Y.Y. Wu, BJFC-S1941, living culture CFCC 70744, ibid. on the dead branches of Ulmus pumila, BJFC-S1942, living culture CFCC 70745.

Notes

Aplosporella javeedii was initially reported on Celtis africana and Searsia lancea in South Africa (Jami et al. 2014). Fan et al. (2015a) recorded this species in China for the first time, associating it with the canker or dieback disease of five hosts: Albizia julibrissin, Broussonetia papyrifera, Gleditsia sinensis, Juniperus chinensis, and Styphnolobium japonicum. Aplosporella javeedii is widespread on host plants of more than 10 families (Fan et al. 2015a; Zhu et al. 2018; Pan et al. 2019; Lin et al. 2023a). In this study, we report new host records for this species, including Acer miyabei, Acer truncatum, Forsythia suspensa, Lagerstroemia indica, Sambucus williamsii, Syringa vulgaris, Ulmus pumila, and Xanthoceras sorbifolium.

Aplosporella yanqingensis L. Lin & X.L. Fan, MycoKeys 97: 9 (2023)

Description

See Lin et al. 2023a.

Material examined

China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Acer truncatum, 12 April 2023, C.M. Tian, Y.M. Liang, C. Peng, Y. Hu & Y.Y. Wu, BJFC-S1943, living culture CFCC 70743; ibid. BJFC-S1944, living culture CFCC 70738.

Notes

Aplosporella yanqingensis was first discovered on the branches of Platycladus orientalis in Beijing (Lin et al. 2023a). In this study, the two isolates (CFCC 70738 and CFCC 70743) from Acer truncatum formed a clade with 100% MP, 100% ML, and 1.00 BYPP values in the multi-locus phylogenetic tree with A. yanqingensis (Fig. 2). Compared with the description of Lin et al. (2023a), this study has shorter conidia and thinner conidiogenous cells (11.0–16.5 × 6.0–9.0 µm vs. 16.0–21.5 × 6.0–9.5 µm and 5.0–20.5 × 1.0–2.0 µm vs. 6.0–13.5 × 2.0–3.0 µm). Thus, these isolates were identified as A. yanqingensis, and herewith we are providing a new host record for A. yanqingensis, Acer truncatum.

Dothiorella acericola Phookamsak, Tennakoon & K.D. Hyde, Fungal Diversity 95: 78 (2019)

Description

See Pan et al. 2021.

Material examined

China, Beijing City, Tongzhou District, Hougezhuang Plain Forest, 29°50'24"N, 116°54'00"E, on the dead branches of Forsythia suspensa, 8 April 2023, C.M. Tian, S.J. Li & Y.Y. Wu, BJFC-S1948, living culture CFCC 70755; China, Beijing City, Tongzhou District, Majuqiao Wetland Park, 39°46'12"N, 116°37'12"E, on the dead branches of Ginkgo biloba, 2 May 2023, Y.Y. Wu, BJFC-S1949, living culture CFCC 70760; ibid. on the dead branches of Syringa oblata, BJFC-S1950, living culture CFCC 70761.

Notes

Based on phylogenetic analyses (Fig. 3), three isolates in this study clustered with Dothiorella acericola and formed a clade with 99% MP, 100% ML, and 1.00 BYPP values. Dothiorella acericola is reported to be associated with the canker disease of Acer palmatum in China (Phookamsak et al. 2019). Pan et al. (2021, 2023) found that Do. acericola infests Ziziphus jujuba and Koelreuteria paniculata branches. The fungus was also recorded on dead branches of Euonymus japonicus (Lin et al. 2023b). This is the first discovery of this fungus in the host families Oleaceae and Ginkgoaceae.

Dothiorella hortiarborum Y.Y. Wu & C.M. Tian, sp. nov.

MycoBank No: 851826
Fig. 5

Etymology

“Hort” means “garden,” and “arbor” means “tree” in Latin. Collected from Fraxinus chinensis and Lagerstroemia indica, both of which are landscaping and greening trees.

Holotype

China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Fraxinus chinensis, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu (holotype BJFC-S1951, ex-type cultures CFCC 70756).

Description

Sexual morph : Not observed. Asexual morph: Conidiomata pycnidial, scattered to aggregated, immersed to semi-immersed in bark, globose to subglobose, dark gray to black, unilocular, 260–450 μm diam. Disc black, ovoid, 310–330 μm diam. Ostioles single, light gray, circular, central, papillate, 30–45 μm diam. Locules single, black, oval, 100–380 μm, Conidiophores reduced to conidiogenous cells. Conidiogenous cells: hyaline, smooth, thin-walled, holoblastic, cylindrical to subcylindrical, 4.5–11.0 × 2.0–4.0 μm (av. ± S.D.= 6.8 ± 1.3 × 2.9 ± 0.5 µm). Conidia initially hyaline, then producing light yellow pigmentation, uneven surface, thick-walled, dark brown when matrues, 1-septate, constricted at the septum, smooth, ovoid with a broadly rounded apex, truncate base. 10.0–19.0 × 6.0–11.0 μm (av. ± S.D.= 14.9 ± 2.6 × 8.1 ± 1.0 µm).

Figure 5. 

Dothiorella hortiarborum (BJFC-S1951) A, B habit of conidiomata on branch C transverse section of conidioma D longitudinal section through conidioma E, F conidiogenous cells and conidia G top (left) and bottom (right) sides of colonies on potato dextrose agar (PDA) H, I conidia. Scale bars: 1000 μm (A); 200 μm (B–D); 10 μm (E–F, H–I).

Culture characters

Colonies on PDA with aerial mycelium gray-green, thick and dense, fluffly, margin with undulate and irregular, reverse with inky blue pigment accumulation, reaching 60 mm diam in 7 days at 25 °C.

Other material examined

China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Fraxinus chinensis, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu, BJFC-S2366, living culture CFCC 70757; China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Lagerstroemia indica, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu, BJFC-S1952, living culture CFCC 70758; ibid. BJFC-S2367, living culture CFCC 70759.

Notes

Dothiorella hortiarborum formed an independent clade with 87% MP, 97% ML, and 0.99 BYPP values and is distinct from Do. acericola and Do. plurivora in the multi-locus analyses (Fig. 3). Morphologically, Do. hortiarborum can be distinguished from Do. acericola by shorter conidia (Phookamsak et al. 2019) and Do. plurivora by smaller conidia (10.0–19.0 × 6.0–11.0 μm vs. 22.3–22.7 × 10.8–11.2 μm) (Abdollahzadeh et al. 2014). Additionally, Do. hortiarborum differs from Do. acericola in tef1-α (five bp difference from 170 characters, with 97.1% similarity, including no gaps) sequences, and Do. plurivora in tef1-α (one bp difference from 254 characters, with 99.6% similarity, including one gap), tub2 (three bp difference from 370 characters, with 99.2% similarity, including one gap) sequences.

Phaeobotryon fraxini Y.Y. Wu & C.M. Tian, sp. nov.

MycoBank No: 851827
Fig. 6

Etymology

Named after the host, Fraxinus chinensis.

Holotype

China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Fraxinus chinensis, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu (holotype BJFC-S1953, ex-type cultures CFCC 70762).

Description

Sexual morph : Not observed. Asexual morph: Conidiomata pycnidial, scattered, occasionally aggregated, superficial or immersed, globose, dark brown to black, unilocular, 200–360 μm diam. Disc inconspicuous. Ostioles single, brown or black, circular, central, papillate, 40–85 μm diam. Locules single, globose, 100–170 μm, Conidiophores reduced to conidiogenous cells. Conidiogenous cells hyaline, smooth, thin-walled, holoblastic, cylindrical, formed from the cells lining the inner walls of the locules, 7.0–14.0 × 1.0–5.0 μm (av. ± S.D.= 10.6 ± 2.0 × 3.1 ± 0.8 µm). Conidia initially hyaline, smooth, thin-walled, then gradually producing light yellow pigment, becoming yellow or light brown, occasionally with bubbles, mature with 1-septate, brownish yellow to dark brown, oblong, obtuse, rounded at both ends, 13.0–20.0 × 7.0–10.0 μm (av. ± S.D.= 17.6 ± 1.3 × 8.7 ± 0.7 µm).

Figure 6. 

Phaeobotryon fraxini (BJFC-S1953) A habit of conidiomata on branch B transverse section of conidioma C longitudinal section through conidioma D, E conidiogenous cells and conidia F top (left) and bottom (right) sides of colonies on potato dextrose agar (PDA) G-L conidia. Scale bars: 500 μm (A); 200 μm (B, C); 10 μm (D, E, G–L).

Culture characters

Colonies on PDA with aerial gray-white mycelium, thick and dark black at the edge, thin and paler in color in the center, fluffly, entire margin, reverse with black pigment accumulation, reaching 60 mm diam in 7 days at 25 °C.

Other material examined

China, Beijing City, Tongzhou District, Central Green Forest Park, 39°52'16"N, 116°42'04"E, on the dead branches of Fraxinus chinensis, 19 April 2023, C.M. Tian, C. Peng, R. Yuan, M.W. Zhang & Y.Y. Wu, BJFC-S2368, living culture CFCC 70763.

Notes

Based on multi-locus phylogenetic analysis, the two isolates cluster separately in a high-supported clade with 100% MP, 100% ML, and 1.00 BYPP value (Fig. 4). In the phylogenetic analysis, Phaeobotryon fraxini showed a close relationship to P. mali and P. rhois. These three species could be distinguished based on ITS, tef1-α, and LSU loci from P. mali by nineteen bp (6/465 in ITS; 10/184 in tef1-α; 3/559 in LSU) and P. rhois by twenty-two bp (7/465 in ITS; 12/184 in tef1-α; 3/559 in LSU). Moreover, P. fraxini differs from P. mali and P. rhois in having smaller conidia (13.0–20.0 × 7.0–10.0 µm vs. 22.0–31.5 × 12–16.5 µm for P. mali and 20–25 × 10–12 µm for P. rhois) (Fan et al. 2015b; Jia et al. 2023) (Table 3). Therefore, P. fraxini is introduced as a novel species.

Table 3.
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Comparison of species in Phaeobotryon.

Species Host Location Conidial size Septation Reference
Phaeobotryon aplosporum Rhus typhina China 17–19 × 5.5–7 aseptate Pan et al. 2019
P. mali Malus pumila China 22.0–31.5 × 12–16.5 1-septate Jia et al. 2023
P. cupressi Cupressus sempervirens Iran 24.1–25 × 12.2–12.5 1(–2)-septate Abdollahzadeh et al. 2009
P. fraxini Fraxinus chinensis China 13–20 × 7–10 1-septate This study
P. juniperi Juniperus formosana China 24.5–27.5 × 12.0–13.5 1-septate Peng et al. 2023
P. mamane Sophora chrysophylla USA 35–38 × 14–15 1(–2)-septate Phillips et al. 2008
P. negundinis Acer negundo Russia 16–24.5 × 7.9–11.5 aseptate Daranagama et al. 2016
P. platycladi Platycladus orientalis China 23.0–31.0 × 9.5–12.5 aseptate or 1-septate Lin et al. 2023a
P. rhoinum Rhus typhina China 19–21 × 7.5–9 1-septate Zhu et al. 2018
P. rhois Rhus typhina China 20–25 × 10–12 1-septate Fan et al. 2015b
P. spiraeae Spiraea salicifolia China 23.5–28.5 × 8.5–13.5 aseptate Jin and Karunarathna 2021
P. ulmi Ulmus laevis Germany 28.5–32.5 × 16.5–18.5 aseptate or 1-septate Zhang et al. 2021

Discussion

In this paper, 23 Botryosphaeriales isolates were identified as six species based on multi-locus phylogenetic analyses. These species included two new species, namely Dothiorella hortiarborum and Phaeobotryon fraxini, and four new hosts: Aplosporella ginkgonis on Cotinus coggygria var. cinereus; A. javeedii on Acer miyabei; Acer truncatum; Forsythia suspensa; Lagerstroemia indica; Sambucus williamsii; Syringa vulgaris; Ulmus pumila; Xanthoceras sorbifolium; A. yanqingensis on Acer truncatum; and Do. acericola on Forsythia suspensa; Ginkgo biloba; and Syringa oblata. The six fungal species identified in this study involve a total of 13 different hosts, which elucidates the wide range of hosts of Botryospaeriales.

Aplosporella is the type genus of Aplosporellaceae (Slippers et al. 2013). The distinctive morphological feature of Aplosporella species is that both ascospores and conidia are aseptately hyaline to pigmented (Slippers et al. 2013; Phillips et al. 2019). In this study, a total of three new host record species of the genus were identified, including A. ginkgonis, A. javeedii, and A. yanqingensis. Aplosporella javeedii has the highest isolation rate and the widest host range, involving five orders of host plants, including Dipsacales, Fabales, Lamiales, Myrtales, and Rosales. Currently, this species is mainly found in warm temperate and tropical regions (Fan et al. 2015a; Zhu et al. 2018), and further exploration is needed to determine whether the geographic range of A. javeedii is related to climate.

Dothiorella was considered a synonym of Diplodia based on a broad morphological concept (Crous and Palm 1999). Phillips et al. (2005) compared the morphological characteristics again and found that the conidia of Dothiorella were brown, with 1-septate in early development, and the conidia still adhered to the conidiogenous cells. In contrast, the conidia of Diplodia become black and septate after being excreted from the conidiomata. Crous et al. (2006) confirmed these morphological differences. Therefore, Dothiorella is regarded as an independent genus in the Botryosphaeriaceae. In this study, the conidia of Do. hortiarborum are transparent and aseptate when attached to conidiogenous cells. After being released by the conidiomata, the conidia bear yellowish pigment or become brown with a 1-septate. In recent years, many new species of Dothiorella have been published with conidial morphology similar to Do. hortiarborum (Li et al. 2023; Lin et al. 2023a; Wu et al. 2023). These suggest that the morphological characteristics of Dothiorella are not always stable. Thus, it is not accurate to rely solely on the morphology of conidia for Dothiorella; combining phylogenetic analysis and the size of conidia of neighboring species is necessary. Dothiorella species have been reported on more than 20 host plants in China (https://fungi.ars.usda.gov/). This study has expanded its host range in Oleaceae plants (Do. acericola in Forsythia suspensa, Ginkgo biloba and S. oblata, and Do. hortiarborum in Fraxinus chinensis).

Currently, many Dothiorella species have been recorded from Fraxinus, distributed mainly in regions such as Europe and North America (Table 4). In this study, a new species, Do. hortiarborum, from F. chinensis, was introduced in China. However, based on morphological and DNA sequence data, Do. hortiarborum shows significant differences from other species in Fraxinus. Phylogenetic analysis showed that Do. hortiarborum belongs to a different lineage from Do. omnivora, Do. sp., and Do. vidmadera (Fig. 3), while distinguishing them based on the size of conidia and the number of septates (Table 4). Do. concaviuscula, Do. fraxini, and Do. fraxinicola were not available for sequence information due to their earlier publication; however, Do. hortiarborum can also be easily distinguished from them based on their documented conidia size. In addition, Do. lagerstroemiae and Do. hortiarborum were both isolated from Lagersiroemia alba, but its conidia were significantly smaller than Do. hortiarborum (8.3–10 × 3.5–4 µm vs. 10.0–19.0 × 6.0–11.0 μm).

Table 4.
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Comparison of species from Fraxinus in Dothiorella.

Specise Host Location Conidial size Septation Reference
Dothiorella concaviuscula Fraxinus viridis USA 4–6 × 2.5–3 no description Jepson 1896
Do. fraxini Fraxinus sp. Belgium 26–30 × 12 1-septate Saccardo 1892
Do. fraxinicola Fraxinus sp. USA 18–30 × 6–7 no description Ellis and Everhart 1895
Do. hortiarborum Fraxinus chinensis China 10.0–19.0 × 6.0–11.0 1-septate This study
Do. omnivora Fraxinus excelsior Bosnia 19.3–25.5 × 7.5–10.6 1-septate Linaldeddu et al. 2016
Do. sp. Fraxinus excelsior Bosnia, Herzegovina 11–14 × 6–8 2–4-septate Zlatković et al. 2016
Do. vidmadera Fraxinus ornus Australia 21.2–21.9 × 9.6–9.8 1-septate Pitt et al. 2013

Phaeobotryon species have more overlapping morphological characters, with 1(–2) septate or aseptate conidia and similar pigmentation variations. For example, P. cupressi and P. juniperi have overlapping sizes of conidia (24.1–25 × 12.2–12.5 μm vs. 24.5–27.5 × 12.0–13.5 μm), P. rhoinum and P. rhois are derived from the same host and geographic origin, and the conidia have 1-septate (Table 3). So, morphology combined with phylogenetics to further clarify the affinities between species is essential. Furthermore, Phaeobotryon species were reported on a variety of hosts and considered to be potential or opportunistic pathogens (Weiland et al. 2016; Zhu et al. 2020; Ilyukhin and Ellouze 2023; Jia et al. 2023). In this study, P. fraxini was isolated only from dead Fraxinus chinensis; more extensive specimen collection was needed to confirm its distribution characteristics and pathogenicity.

Although Botryosphaeriales recorded many fungi on Index Fungorum (https://www.indexfungorum.org/), only some species are now recognized. Mainly due to the early records of many species, the lack of model specimens, or the low quality of specimens, it is difficult to obtain strains and DNA data. Therefore, more detailed sampling is needed to revise the classification system of related taxa in Botryosphaeriales.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study is financed by National Natural Science Foundation of China (Project No.: 32371887), Survey of Insect and Pathogen Diversity in Beijing Municipal Administrative Center.

Author contributions

Conceptualization, Yingying Wu and Chengming Tian; data curation, Yingying Wu; funding acquisition, Chengming Tian; investigation, Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu; project administration, Chengming Tian; resources, Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu; supervision, Chengming Tian; writing-original draft, Yingying Wu; writing-review and editing, Yingying Wu, Cheng Peng, and Chengming Tian. All authors have read and agreed to the published version of the manuscript.

Author ORCIDs

Yingying Wu https://orcid.org/0009-0007-5095-2738

Rong Yuan https://orcid.org/0009-0006-5597-7531

Chengming Tian https://orcid.org/0000-0002-3352-7664

Data availability

All of the data that support the findings of this study are available in the main text or Supplementary Information.

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Supplementary materials

Supplementary material 1 

Aplosporella

Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu, Chengming Tian

Data type: pdf

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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Supplementary material 2 

Dothiorella

Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu, Chengming Tian

Data type: pdf

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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Supplementary material 3 

Phaeobotryon

Yingying Wu, Cheng Peng, Rong Yuan, Mingwei Zhang, Yang Hu, Chengming Tian

Data type: pdf

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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