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Research Article
Morphology and phylogeny of Cytospora (Cytosporaceae, Diaporthales) species associated with plant cankers in Tibet, China
expand article infoJiangrong Li‡§, Jieting Li‡§, Ning Jiang|
‡ Tibet Agricultual & Animal Husbandry University, Nyingchi, China
§ National Key Station of Field Scientific Observation & Experiment, Nyingchi, China
| Key Laboratory of Biodiversity Conservation of National Forestry and Grassland Administration, Ecology and Nature Conservation Institute, Chinese Academy of Forestry, Beijing, China

Corresponding author: Ning Jiang ( n.jiang@caf.ac.cn )

Academic editor: Xinlei Fan
© 2024 Jiangrong Li, Jieting Li, Ning Jiang.
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: Li J, Li J, Jiang N (2024) Morphology and phylogeny of Cytospora (Cytosporaceae, Diaporthales) species associated with plant cankers in Tibet, China. In: Wijayawardene N, Karunarathna S, Fan X-L, Li Q-R (Eds) Taxonomy and secondary metabolites of wood-associated fungi. MycoKeys 104: 51-70. https://doi.org/10.3897/mycokeys.104.113567
Open Access

Abstract

During our biodiversity investigations in Tibet, China, typical Cytospora canker symptoms were observed on branches of hosts Myricaria paniculate, Prunus cerasifera and Sibiraea angustata. Samples were studied, based on morphological features coupled with multigene phylogenetic analyses of ITS, act, rpb2, tef1 and tub2 sequence data, which revealed two new species (Cytospora myricicola sp. nov. and C. sibiraeicola sp. nov.) and a known species (C. populina). In addition, Cytospora populina is newly discovered on the host Prunus cerasifera and in Tibet.

Key words

Ascomycota, molecular phylogeny, novel taxa, Sordariomycetes, taxonomy

Introduction

The genus Cytospora (Cytosporaceae, Diaporthales, Sordariomycetes, Ascomycota) was proposed by Ehrenberg (1818) and C. chrysosperma was selected as the lectotype later (Donk 1964). Cytospora has priority over Leucocytospora, Leucostoma, Valsa, Valsella and Valseutypella based on the dual-nomenclature criterion (Adams et al. 2005; Rossman et al. 2015). Members of Cytospora are characterised by the single or labyrinthine, loculate stromata, filamentous conidiophores or asci and allantoid hyaline conidia or ascospores (Spielman 1985; Adams et al. 2005; Norphanphoun et al. 2017, 2018; Fan et al. 2020; Shang et al. 2020). Species identification in Cytospora was previously largely based on the host affiliation and morphological descriptions; however, molecular phylogeny combined with morphology and host affiliation have became the main approaches recently (Fan et al. 2020; Shang et al. 2020; Zhu et al. 2020). Currently, over 690 species epithets of Cytospora have been listed in Index Fungorum (http://www.indexfungorum.org/; 2023). However, most of these were regarded as synonyms and most descriptions were unable to identify them accurately (Adams et al. 2005; Fan et al. 2020; Pan et al. 2020).

Cytospora is distributed worldwide and often known to be associated with plant diseases (Monkai et al. 2021; Pan et al. 2021; Lin et al. 2022; Travadon et al. 2022). For example, C. chrysosperma is the main canker disease pathogen of polar and willow trees in China (Fan et al. 2014; Wang et al. 2015; Lin et al. 2023); C. kuanchengensis and additional five species are associated with Chinese chestnut cankers (Jiang et al. 2020); Fifteen Cytospora species were identified from destructive canker and dieback pathogens of woody hosts in the USA (Lawrence et al. 2018).

The Tibet Tibetan Autonomous Region is located on the Qinghai-Tibet Plateau, which is known as the third pole of the earth. During our biodiversity investigations in Tibet, typical fruiting bodies of Cytospora were discovered from Myricaria paniculate (Tamaricaceae), Prunus cerasifera (Rosaceae) and Sibiraea angustata (Rosaceae). The aim of the present study was to identify Cytospora species from the three hosts based on morphological features and molecular phylogeny of combined sequence data.

Materials and methods

Sample collection, morphology and isolation

Our biodiversity investigations were conducted in Lhasa and Shigatse cities in Tibet Tibetan Autonomous Region, China during 2022 and 2023. Diseased branches of Myricaria paniculate, Prunus cerasifera and Sibiraea angustata were observed and collected, packed in paper bags and returned to the laboratory for morphological study and fungal isolation.

Observation and description of Cytospora species was based on fruiting bodies naturally formed on the host barks. Ascostromata and conidiomata from tree barks were sectioned by hand using a double-edged blade and structures were observed under a dissecting microscope. At least 10 conidiomata/ascostromata, 10 asci and 50 conidia/ascospores were measured to calculate the mean size and standard deviation. Measurements are reported as maximum and minimum in parentheses and the range representing the mean plus and minus the standard deviation of the number of measurements is given in parentheses. Microscopy photographs were captured with a Nikon Eclipse 80i compound microscope, equipped with a Nikon digital sight DS-Ri2 high definition colour camera, using differential interference contrast illumination.

Isolates of Cytospora were obtained by removing the spore masses from the fruiting bodies on to clean PDA plates and incubating at 25 °C until spores germinated. Single germinated spores were then transferred to the new PDA plates and incubated at 25 °C in the dark. The cultures were deposited in the China Forestry Culture Collection Center (CFCC, http://cfcc.caf.ac.cn/) and the specimens in the Herbarium of the Chinese Academy of Forestry (CAF, http://museum.caf.ac.cn/).

DNA extraction, PCR amplification and sequencing

Genomic DNA was extracted from fresh fungal mycelia following the method described by Doyle and Doyle (1990). Polymerase chain reactions (PCR) were conducted to amplify the internal transcribed spacer region rDNA (ITS), the partial actin (act) region, RNA polymerase II second largest subunit (rpb2), translation elongation factor 1-alpha (tef1) and the partial beta-tubulin (tub2) gene using primers and conditions listed in Table 1. The PCR products were assayed via electrophoresis in 2% agarose gels. DNA sequencing was performed using an ABI PRISM 3730XL DNA Analyser with a BigDye Terminator Kit v.3.1 (Invitrogen, Waltham, MA, USA) at the Shanghai Invitrogen Biological Technology Company Limited (Beijing, China).

Table 1.
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Primers and PCR protocols.

Gene Regions Primers PCR conditions References
ITS ITS5/ITS4 95 °C for 4 min, 35 cycles of 94 °C for 45 s, 48 °C for 1 min, and 72 °C for 2 min , 72 °C for 10 min White et al. (1990)
act ACT512F/ACT783R 95 °C for 4 min, 35 cycles of 94 °C for 45 s, 55 °C for 1 min, and 72 °C for 2 min , 72 °C for 10 min Carbone and Kohn (1999)
rpb2 fRPB2-5f/fRPB2-7cR 95 °C for 5 min, 35 cycles of 95 °C for 1 min, 55 °C, 1.25 min, and 72 °C for 2 min , 72 °C for 10 min Liu et al. (1999)
tef1 983F/2218R 94 °C for 3 min, 35 cycles of 94 °C for 30 s, 54 °C for 50 s, and 72 °C for 2 min, 72 °C for 10 min Rehner (2001)
tub2 Bt2a/Bt2b 95 °C for 4 min, 35 cycles of 94 °C for 45 s, 54 °C for 1 min, and 72 °C for 2 min , 72 °C for 10 min Glass and Donaldson (1995)

Sequence alignment and phylogenetic analyses

The obtained sequences of ITS, act, rpb2, tef1 and tub2 were assembled using SeqMan software version 7.1.0 (DNASTAR Inc., WI) and subjected to BLASTn search against the GenBank nucleotide database at National Center for Biotechnology Information (NCBI) to identify closely-related sequences. Sequences data of related taxa were obtained from previous publications (Fan et al. 2020; Lin et al. 2023) and downloaded from the GenBank database (Table 2). The sequences were aligned using MAFFT v.7 online web server (http://mafft.cbrc.jp/alignment/server/index.html, Katoh et al. 2019) under default settings. The Maximum Likelihood (ML) phylogenic analysis was run in the CIPRES Science Gateway platform (Miller et al. 2010), using RAxMLHPC2 on the XSEDE (v. 8.2.10) tool under the GTR substitution model and 1000 non-parametric bootstrap replicates. Bayesian analysis was performed using MrBayes v. 3.2.6 on XSEDE at the CIPRES Science Gateway with four simultaneous Markov Chain runs for 1,000.000 generations. The resulting trees were visualised in FigTree v. 1.4.0 (Rambaut 2012).

Results

Phylogenetic analyses

The combined ITS, act, rpb2, tef1 and tub2 dataset consisted of 199 strains, with Diaporthe vaccinii (CBS 160.32) as the outgroup taxon (Table 2). The final alignment comprised 3,166 characters (ITS: 567, act: 323, rpb2: 741, tef1: 727, tub2: 808), including gaps. The final ML optimisation likelihood value of the best RAxML tree was -60353.67 and the matrix had 2069 distinct alignment patterns, with 40.24% undetermined characters or gaps. Estimated base frequencies were as follows: A = 0. 244507, C = 0. 288246, G = 0. 237262, T = 0. 229984; substitution rates AC = 1.372283, AG = 2.995828, AT = 1.353835, CG = 0.976452, CT = 5.021434, GT = 1.0; gamma distribution shape parameter α = 0.372885. The RAxML and Bayesian analyses yielded a similar tree topology. The topology of our phylogenetic tree is nearly identical to previous publications. Six isolates from the present study formed two new clades distinct from previously-known species named Cytospora myricicola sp. nov. and C. sibiraeicola sp. nov. and a known clade named C. populina (Fig. 1).

Table 2.
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GenBank accession numbers used in the phylogenetic analyses.

Species Strain Host Origin GenBank accession numbers
ITS act rpb2 tef1 tub2
Cytospora ailanthicola CFCC 89970 Ailanthus altissima China MH933618 MH933526 MH933592 MH933494 MH933565
Cytospora albodisca CFCC 53161 Platycladus orientalis China MW418406 MW422899 MW422909 MW422921 MW422933
Cytospora albodisca CFCC 54373 Platycladus orientalis China MW418407 MW422900 MW422910 MW422922 MW422934
Cytospora alba CFCC 55462T Salix matsudana China NR182387 OK303457 OK303516 OK303577 OK303644
Cytospora alba CFCC 55463 Salix matsudana China MZ702596 OK303458 OK303517 OK303578 OK303645
Cytospora ampulliformis MFLUCC 16-0583T Sorbus intermedia Russia KY417726 KY417692 KY417794 NA NA
Cytospora ampulliformis MFLUCC 16-0629 Acer platanoides Russia KY417727 KY417693 KY417795 NA NA
Cytospora amygdali CBS 144233T Prunus dulcis USA MG971853 MG972002 NA MG971659 NA
Cytospora atrocirrhata CFCC 89615 Juglans regia China KR045618 KF498673 KU710946 KP310858 KR045659
Cytospora atrocirrhata CFCC 89616 Juglans regia China KR045619 KF498674 KU710947 KP310859 KR045660
Cytospora beilinensis CFCC 50493T Pinus armandii China MH933619 MH933527 NA MH933495 MH933561
Cytospora beilinensis CFCC 50494 Pinus armandii China MH933620 MH933528 NA MH933496 MH933562
Cytospora berberidis CFCC 89927T Berberis dasystachya China KR045620 KU710990 KU710948 KU710913 KR045661
Cytospora berberidis CFCC 89933 Berberis dasystachya China KR045621 KU710991 KU710949 KU710914 KR045662
Cytospora bungeana CFCC 50495T Pinus bungeana China MH933621 MH933529 MH933593 MH933497 MH933563
Cytospora bungeana CFCC 50496 Pinus bungeana China MH933622 MH933530 MH933594 MH933498 MH933564
Cytospora californica CBS 144234T Juglans regia USA MG971935 MG972083 NA MG971645 NA
Cytospora carbonacea CFCC 89947 Ulmus pumila China KR045622 KP310842 KU710950 KP310855 KP310825
Cytospora carpobroti CMW48981T Carpobrotus edulis South Africa MH382812 NA NA MH411212 MH411207
Cytospora celtidicola CFCC 50497T Celtis sinensis China MH933623 MH933531 MH933595 MH933499 MH933566
Cytospora celtidicola CFCC 50498 Celtis sinensis Anhui, China MH933624 MH933532 MH933596 MH933500 MH933567
Cytospora centrivillosa MFLUCC 16-1206T Sorbus domestica Italy MF190122 NA MF377600 NA NA
Cytospora centrivillosa MFLUCC 17-1660 Sorbus domestica Italy MF190123 NA MF377601 NA NA
Cytospora ceratosperma CFCC 89624 Juglans regia China KR045645 NA KU710976 KP310860 KR045686
Cytospora ceratosperma CFCC 89625 Juglans regia China KR045646 NA KU710977 KP310861 KR045687
Cytospora ceratospermopsis CFCC 89626T Juglans regia China KR045647 KU711011 KU710978 KU710934 KR045688
Cytospora ceratospermopsis CFCC 89627 Juglans regia China KR045648 KU711012 KU710979 KU710935 KR045689
Cytospora chrysosperma CFCC 89629 Salix psammophila China KF765673 NA KF765705 NA NA
Cytospora chrysosperma CFCC 89981 Populus alba China MH933625 MH933533 MH933597 MH933501 MH933568
Cytospora chrysosperma CFCC 89982 Ulmus pumila China KP281261 KP310835 NA KP310848 KP310818
Cytospora cinnamomea CFCC 53178T Prunus armeniaca China MK673054 MK673024 NA NA MK672970
Cytospora coryli CFCC 53162T Corylus mandshurica China MN854450 NA MN850751 MN850758 MN861120
Cytospora corylina CFCC 54684T Corylus heterophylla China MW839861 MW815937 MW815951 MW815886 MW883969
Cytospora corylina CFCC 54685 Corylus heterophylla China MW839862 MW815938 MW815952 MW815887 MW883970
Cytospora cotini MFLUCC 14-1050T Cotinus coggygria Russia KX430142 NA KX430144 NA NA
Cytospora cotoneastricola CF 20197027 Cotoneaster sp. China MK673072 MK673042 MK673012 MK672958 MK672988
Cytospora cotoneastricola CF 20197028 Cotoneaster sp. China MK673073 MK673043 MK673013 MK672959 MK672989
Cytospora curvata MFLUCC 15-0865T Salix alba Russia KY417728 KY417694 NA NA NA
Cytospora curvispora CFCC 54000T Corylus heterophylla China MW839851 MW815931 MW815945 MW815880 MW883963
Cytospora curvispora CFCC 54001 Corylus heterophylla China MW839853 MW815932 MW815946 MW815881 MW883964
Cytospora davidiana CXY 1350T Populus davidiana China KM034870 NA NA NA NA
Cytospora diopuiensis CFCC 55479 Euonymus japonicus China OQ344753 OQ410625 OQ398735 OQ398762 OQ398791
Cytospora diopuiensis CFCC 55527 Euonymus japonicus China OQ344754 OQ410626 OQ398736 OQ398763 OQ398792
Cytospora discotoma CFCC 53137 T Platycladus orientalis China MW418404 MW422897 MW422907 MW422919 MW422931
Cytospora discotoma CFCC 54368 Platycladus orientalis China MW418405 MW422898 MW422908 MW422920 MW422932
Cytospora donetzica MFLUCC 15-0864 Crataegus monogyna Russia KY417729 KY417695 KY417797 NA NA
Cytospora donetzica MFLUCC 16-0574T Crataegus monogyna Russia KY417731 KY417697 KY417799 NA NA
Cytospora donglingensis CFCC 53159 T Platycladus orientalis China MW418412 MW422903 MW422915 MW422927 MW422939
Cytospora donglingensis CFCC 53160 Platycladus orientalis China MW418414 MW422905 MW422917 MW422929 MW422941
Cytospora elaeagni CFCC 89632 Elaeagnus angustifolia China KR045626 KU710995 KU710955 KU710918 KR045667
Cytospora elaeagni CFCC 89633 Elaeagnus angustifolia China KF765677 KU710996 KU710956 KU710919 KR045668
Cytospora elaeagnicola CFCC 52882T Elaeagnus angustifolia China MK732341 MK732344 MK732347 NA NA
Cytospora elaeagnicola CFCC 52883 Elaeagnus angustifolia China MK732342 MK732345 MK732348 NA NA
Cytospora erumpens CFCC 50022 Prunus padus China MH933627 MH933534 NA MH933502 MH933569
Cytospora erumpens CFCC 53163 Prunus padus China MK673059 MK673029 MK673000 MK672948 MK672975
Cytospora eucalypti CBS 144241 Eucalyptus globulus USA MG971907 MG972056 NA MG971617 NA
Cytospora euonymicola CFCC 50499T Euonymus kiautschovicus China MH933628 MH933535 MH933598 MH933503 MH933570
Cytospora euonymicola CFCC 50500 Euonymus kiautschovicus China MH933629 MH933536 MH933599 MH933504 MH933571
Cytospora euonymina CFCC 89993T Euonymus kiautschovicus China MH933630 MH933537 MH933600 MH933505 MH933590
Cytospora euonymina CFCC 89999 Euonymus kiautschovicus China MH933631 MH933538 MH933601 MH933506 MH933591
Cytospora fraxinigena MFLU 17-0880 T Fraxinus ornus Italy NR154859 NA NA NA NA
Cytospora fugax CXY 1371 Populus simonii China KM034852 NA NA NA KM034891
Cytospora fugax CXY 1381 Populus ussuriensis China KM034853 NA NA NA KM034890
Cytospora fusispora NFCCI 4372 NA India MN227694 NA NA NA NA
Cytospora galegicola MFLUCC 18-1199T Galega officinalis Italy MK912128 MN685810 MN685820 NA NA
Cytospora gigalocus CFCC 89620T Juglans regia China KR045628 KU710997 KU710957 KU710920 KR045669
Cytospora gigalocus CFCC 89621 Juglans regia China KR045629 KU710998 KU710958 KU710921 KR045670
Cytospora gigaspora CFCC 50014 Juniperus procumbens China KR045630 KU710999 KU710959 KU710922 KR045671
Cytospora gigaspora CFCC 89634T Salix psammophila China KF765671 KU711000 KU710960 KU710923 KR045672
Cytospora globosa MFLU 16-2054T Abies alba Italy MT177935 NA MT432212 MT454016 NA
Cytospora granati CBS 144237T Punica granatum USA MG971799 MG971949 NA MG971514 NA
Cytospora haidianensis CFCC 54056 Euonymus alatus China MT360041 MT363978 MT363987 MT363997 MT364007
Cytospora haidianensis CFCC 54057T Euonymus alatus China MT360042 MT363979 MT363988 MT363998 MT364008
Cytospora hippophaës CFCC 89639 Hippophaë rhamnoides China KR045632 KU711001 KU710961 KU710924 KR045673
Cytospora hippophaës CFCC 89640 Hippophaë rhamnoides China KF765682 KF765730 KU710962 KP310865 KR045674
Cytospora japonica CFCC 89956 Prunus cerasifera China KR045624 KU710993 KU710953 KU710916 KR045665
Cytospora japonica CFCC 89960 Prunus cerasifera China KR045625 KU710994 KU710954 KU710917 KR045666
Cytospora joaquinensis CBS 144235 Populus deltoides USA MG971895 MG972044 NA MG971605 NA
Cytospora junipericola MFLU 17-0882T Juniperus communis Italy MF190125 NA NA MF377580 NA
Cytospora juniperina CFCC 50501T Juniperus przewalskii China MH933632 MH933539 MH933602 MH933507 NA
Cytospora juniperina CFCC 50502 Juniperus przewalskii China MH933633 MH933540 MH933603 MH933508 MH933572
Cytospora kantschavelii CXY 1383 Populus maximowiczii China KM034867 NA NA NA NA
Cytospora kuanchengensis CFCC 52464T Castanea mollissima China MK432616 MK442940 MK578076 NA NA
Cytospora kuanchengensis CFCC 52465 Castanea mollissima China MK432617 MK442941 MK578077 NA NA
Cytospora leucosperma CFCC 89622 Pyrus bretschneideri China KR045616 KU710988 KU710944 KU710911 KR045657
Cytospora leucosperma CFCC 89894 Pyrus bretschneideri China KR045617 KU710989 KU710945 KU710912 KR045658
Cytospora longispora CBS 144236T Prunus domestica USA MG971905 MG972054 NA MG971615 NA
Cytospora longistiolata MFLUCC 16-0628 Salix × fragilis Russia KY417734 KY417700 KY417802 NA NA
Cytospora lumnitzericola MFLUCC 17-0508T Lumnitzera racernosa Tailand MG975778 MH253457 MH253461 NA NA
Cytospora mali CFCC 50028 Malus pumila China MH933641 MH933548 MH933606 MH933513 MH933577
Cytospora mali CFCC 50029 Malus pumila China MH933642 MH933549 MH933607 MH933514 MH933578
Cytospora mali-spectabilis CFCC 53181T Malus spectabilis China MK673066 MK673036 MK673006 MK672953 MK672982
Cytospora melnikii CFCC 89984 Rhus typhina China MH933644 MH933551 MH933609 MH933515 MH933580
Cytospora myricicola CFCC 59323T Myricaria paniculate China OR769868 OR767324 OR767338 OR767364 OR767351
Cytospora myricicola CFCC 59324 Myricaria paniculate China OR769869 OR767325 OR767339 OR767365 OR767352
Cytospora myricicola CFCC 59325 Myricaria paniculate China OR769870 OR767326 OR767340 OR767366 OR767353
Cytospora myrtagena CFCC 52454 Castanea mollissima China MK432614 MK442938 MK578074 NA NA
Cytospora myrtagena CFCC 52455 Castanea mollissima China MK432615 MK442939 MK578075 NA NA
Cytospora nivea MFLUCC 15-0860 Salix acutifolia Russia KY417737 KY417703 KY417805 NA NA
Cytospora nivea CFCC 89641 Elaeagnus angustifolia China KF765683 KU711006 KU710967 KU710929 KR045679
Cytospora notastroma NE_TFR5 Populus tremuloides USA JX438632 NA NA JX438543 NA
Cytospora notastroma NE_TFR8 Populus tremuloides USA JX438633 NA NA JX438542 NA
Cytospora ochracea CFCC 53164T Cotoneaster sp. China MK673060 MK673030 MK673001 MK672949 MK672976
Cytospora oleicola CBS 144248T Olea europaea USA MG971944 MG972098 NA MG971660 NA
Cytospora olivacea CFCC 53174 Prunus cerasifera China MK673058 MK673028 MK672999 NA MK672974
Cytospora olivacea CFCC 53175 Prunus dulcis China MK673062 MK673032 MK673003 NA MK672978
Cytospora palm CXY 1276 Cotinus coggygria China JN402990 NA NA KJ781296 NA
Cytospora palm CXY 1280T Cotinus coggygria China JN411939 NA NA KJ781297 NA
Cytospora paracinnamomea CFCC 55453T Salix matsudana China MZ702594 OK303456 OK303515 OK303576 OK303643
Cytospora paracinnamomea CFCC 55455T Salix matsudana China MZ702598 OK303460 OK303519 OK303580 OK303647
Cytospora parakantschavelii MFLUCC 15-0857T Populus × sibirica Russia KY417738 KY417704 KY417806 NA NA
Cytospora parapistaciae CBS 144506T Pistacia vera USA MG971804 MG971954 NA MG971519 NA
Cytospora paraplurivora FDS-439 Prunus armeniaca Canada OL640182 OL631586 NA OL631589 NA
Cytospora paraplurivora FDS-564T Prunus persica var. nucipersica Canada OL640183 OL631587 NA OL631590 NA
Cytospora parasitica CFCC 53173 Berberis sp. China MK673070 MK673040 MK673010 MK672957 MK672986
Cytospora paratranslucens MFLUCC 15-0506T Populus alba var. bolleana Russia KY417741 KY417707 KY417809 NA NA
Cytospora paratranslucens MFLUCC 16-0627 Populus alba Russia KY417742 KY417708 KY417810 NA NA
Cytospora phialidica MFLUCC 17-2498 Alnus glutinosa Italy MT177932 NA MT432209 MT454014 NA
Cytospora piceae CFCC 52841T Picea crassifolia China MH820398 MH820406 MH820395 MH820402 MH820387
Cytospora piceae CFCC 52842 Picea crassifolia China MH820399 MH820407 MH820396 MH820403 MH820388
Cytospora pingbianensis MFLUCC 18-1204T Undefined wood China MK912135 MN685817 MN685826 NA NA
Cytospora pistaciae CBS 144238T Pistacia vera USA MG971802 MG971952 NA MG971517 NA
Cytospora platycladi CFCC 50504T Platycladus orientalis China MH933645 MH933552 MH933610 MH933516 MH933581
Cytospora platycladi CFCC 50505 Platycladus orientalis China MH933646 MH933553 MH933611 MH933517 MH933582
Cytospora platycladicola CFCC 50038T Platycladus orientalis China KT222840 MH933555 MH933613 MH933519 MH933584
Cytospora platycladicola CFCC 50039 Platycladus orientalis China KR045642 KU711008 KU710973 KU710931 KR045683
Cytospora plurivora CBS 144239T Olea europaea USA MG971861 MG972010 NA MG971572 NA
Cytospora populi CFCC 55472 T Populus sp. China MZ702609 OK303471 OK303530 OK303591 OK303658
Cytospora populi CFCC 55473 Populus sp. China MZ702610 OK303472 OK303531 OK303592 OK303659
Cytospora populicola CBS 144240 Populus deltoides USA MG971891 MG972040 NA MG971601 NA
Cytospora populina CFCC 89644T Salix psammophila China KF765686 KU711007 KU710969 KU710930 KR045681
Cytospora populina CFCC 58856 Prunus cerasifera China OR769873 OR767329 OR767343 OR767369 NA
Cytospora populinopsis CFCC 50032T Sorbus aucuparia China MH933648 MH933556 MH933614 MH933520 MH933585
Cytospora populinopsis CFCC 50033 Sorbus aucuparia China MH933649 MH933557 MH933615 MH933521 MH933586
Cytospora predappioensis MFLUCC 17-2458T Platanus hybrida Italy MG873484 NA NA NA NA
Cytospora predappioensis MFLU 17-0327 Platanus hybrida Italy MH253451 MH253449 MH253450 NA NA
Cytospora prunicola MFLU 17-0995T Prunus sp. Italy MG742350 MG742353 MG742352 NA NA
Cytospora pruni-mume CFCC 53179 Prunus armeniaca China MK673057 MK673027 NA MK672947 MK672973
Cytospora pruni-mume CFCC 53180T Prunus mume China MK673067 MK673037 MK673007 MK672954 MK672983
Cytospora pruinopsis CFCC 50034T Ulmus pumila China KP281259 KP310836 KU710970 KP310849 KP310819
Cytospora pruinopsis CFCC 53153 Ulmus pumila China MN854451 MN850763 MN850752 MN850759 MN861121
Cytospora pruinosa CFCC 50036 Syringa oblata China KP310800 KP310832 NA KP310845 KP310815
Cytospora pruinosa CFCC 50037 Syringa oblata China MH933650 MH933558 NA MH933522 MH933589
Cytospora pubescentis MFLUCC 18-1201T Quercus pubescens Italy MK912130 MN685812 MN685821 NA NA
Cytospora punicae CBS 144244 Punica granatum USA MG971943 MG972091 NA MG971654 NA
Cytospora quercicola MFLU 17-0881 Quercus sp. Italy MF190128 NA NA NA NA
Cytospora ribis CFCC 50026 Ulmus pumila China KP281267 KP310843 KU710972 KP310856 KP310826
Cytospora ribis CFCC 50027 Ulmus pumila China KP281268 KP310844 NA KP310857 KP310827
Cytospora rosae MFLU 17-0885 Rosa canina Italy MF190131 NA NA NA NA
Cytospora rosicola CF 20197024T Rosa sp. China MK673079 MK673049 MK673019 MK672965 MK672995
Cytospora rosigena MFLUCC 18-0921T Rosa sp. Russia MN879872 NA NA NA NA
Cytospora rostrata CFCC 89909 Salix cupularis China KR045643 KU711009 KU710974 KU710932 KR045684
Cytospora rostrata CFCC 89910 Salix cupularis China KR045644 KU711010 KU710975 KU710933 NA
Cytospora rusanovii MFLUCC 15-0853 Populus × sibirica Russia KY417743 KY417709 KY417811 NA NA
Cytospora rusanovii MFLUCC 15-0854T Salix babylonica Russia KY417744 KY417710 KY417812 NA NA
Cytospora salicacearum MFLUCC 15-0509 Salix alba Russia KY417746 KY417712 KY417814 NA NA
Cytospora salicacearum MFLUCC 15-0861 Salix × fragilis Russia KY417745 KY417711 KY417813 NA NA
Cytospora salicicola MFLUCC 14-1052T Salix alba Russia KU982636 KU982637 NA NA NA
Cytospora salicicola MFLUCC 15-0866 Salix sp. Thailand KY417749 KY417715 KY417817 NA NA
Cytospora salicina MFLUCC 15-0862 Salix alba Russia KY417750 KY417716 KY417818 NA NA
Cytospora salicina MFLUCC 16-0637 Salix × fragilis Russia KY417751 KY417717 KY417819 NA NA
Cytospora schulzeri CFCC 50042 Malus pumila China KR045650 KU711014 KU710981 KU710937 KR045691
Cytospora sibiraeae CFCC 50045T Sibiraea angustata China KR045651 KU711015 KU710982 KU710938 KR045692
Cytospora sibiraeae CFCC 50046 Sibiraea angustata China KR045652 KU711016 KU710983 KU710939 KR045693
Cytospora sibiraeicola CFCC 59100T Sibiraea angustata China OR769871 OR767327 OR767341 OR767367 OR767354
Cytospora sibiraeicola CFCC 59101 Sibiraea angustata China OR769872 OR767328 OR767342 OR767368 OR767355
Cytospora sophorae CFCC 50047 Styphnolobium japonicum China KR045653 KU711017 KU710984 KU710940 KR045694
Cytospora sophorae CFCC 89598 Styphnolobium japonicum China KR045654 KU711018 KU710985 KU710941 KR045695
Cytospora sophoricola CFCC 89596 Styphnolobium japonicum China KR045656 KU711020 KU710987 KU710943 KR045697
Cytospora sophoricola CFCC 89595T Styphnolobium japonicum China KR045655 KU711019 KU710986 KU710942 KR045696
Cytospora sophoriopsis CFCC 55469 Salix matsudana China MZ702583 OK303445 OK303504 OK303565 OK303632
Cytospora sophoriopsis CFCC 89600 Styphnolobium japonicum China KR045623 KU710992 KU710951 KU710915 KP310817
Cytospora sorbi MFLUCC 16-0631T Sorbus aucuparia Russia KY417752 KY417718 KY417820 NA NA
Cytospora sorbicola MFLUCC 16-0584T Acer pseudoplatanus Russia KY417755 KY417721 KY417823 NA NA
Cytospora sorbicola MFLUCC 16-0633 Cotoneaster melanocarpus Russia KY417758 KY417724 KY417826 NA NA
Cytospora sorbina CF 20197660T Sorbus tianschanica China MK673052 MK673022 NA MK672943 MK672968
Cytospora spiraeae CFCC 50049T Spiraea salicifolia China MG707859 MG708196 MG708199 NA NA
Cytospora spiraeae CFCC 50050 Spiraea salicifolia China MG707860 MG708197 MG708200 NA NA
Cytospora spiraeicola CFCC 53138T Spiraea salicifolia China MN854448 NA MN850749 MN850756 MN861118
Cytospora spiraeicola CFCC 53139 Tilia nobilis China MN854449 NA MN850750 MN850757 MN861119
Cytospora tamaricicola CFCC 50507 Rosa multifolora China MH933651 MH933559 MH933616 MH933525 MH933587
Cytospora tamaricicola CFCC 50508T Tamarix chinensis China MH933652 MH933560 MH933617 MH933523 MH933588
Cytospora tanaitica MFLUCC 14-1057T Betula pubescens Russia KT459411 KT459413 NA NA NA
Cytospora thailandica MFLUCC 17-0262T Xylocarpus moluccensis Thailand MG975776 MH253459 MH253463 NA NA
Cytospora thailandica MFLUCC 17-0263T Xylocarpus moluccensis Thailand MG975777 MH253460 MH253464 NA NA
Cytospora tibetensis CF 20197026 Cotoneaster sp. China MK673076 MK673046 MK673016 MK672962 MK672992
Cytospora tibetensis CF 20197029 Cotoneaster sp. China MK673077 MK673047 MK673017 MK672963 MK672993
Cytospora tibouchinae CPC 26333T Tibouchina semidecandra France KX228284 NA NA NA NA
Cytospora translucens CXY 1351 Populus davidiana China KM034874 NA NA NA KM034895
Cytospora translucens CXY 1359 Populus × beijingensis China KM034871 NA NA NA KM034894
Cytospora ulmi MFLUCC 15-0863T Ulmus minor Russia KY417759 NA NA NA NA
Cytospora verrucosa CFCC 53157 T Platycladus orientalis China MW418408 NA MW422911 MW422923 MW422935
Cytospora verrucosa CFCC 53158 Platycladus orientalis China MW418410 MW422901 MW422913 MW422925 MW422937
Cytospora vinacea CBS 141585T Vitis interspecific USA KX256256 NA NA KX256277 KX256235
Cytospora viridistroma CBS 202.36T Cercis canadensis USA MN172408 NA NA MN271853 NA
Cytospora viticola Cyt2 Vitis interspecific USA KX256238 NA NA KX256259 KX256217
Cytospora viticola CBS 141586T Vitis vinifera USA KX256239 NA NA KX256260 KX256218
Cytospora xinjiangensis CFCC 53182 Rosa sp. China MK673064 MK673034 MK673004 MK672951 MK672980
Cytospora xinjiangensis CFCC 53183T Rosa sp. China MK673065 MK673035 MK673005 MK672952 MK672981
Cytospora xinglongensis CFCC 52458 Castanea mollissima China MK432622 MK442946 MK578082 NA NA
Cytospora xinglongensis CFCC 52459 Castanea mollissima China MK432623 MK442947 MK578083 NA NA
Cytospora xylocarpi MFLUCC 17-0251T Xylocarpus granatum Thailand MG975775 MH253458 MH253462 NA NA
Cytospora zhaitangensis CFCC 56227 T Euonymus japonicus China OQ344750 OQ410623 OQ398733 OQ398760 OQ398789
Cytospora zhaitangensis CFCC 57537 Euonymus japonicus China OQ344751 OQ410624 OQ398734 OQ398761 OQ398790
Diaporthe vaccinii CBS 160.32 Vaccinium macrocarpon USA KC343228 JQ807297 NA KC343954 KC344196

Ex-type strains are indicated with (T) after the collection number; “NA” indicates unavailable sequences; sequences produced in the current study are in bold.
Figure 1. 

Maximum Likelihood tree generated from combined ITS, act, rpb2, tef1 and tub2 sequence data. Bootstrap support values ≥ 50% and Bayesian posterior probabilities ≥ 0.90 are demonstrated at the branches. Ex-type cultures are marked with (*).

Taxonomy

Cytospora myricicola Ning Jiang, sp. nov.

MycoBank No: MycoBank No: 850240
Fig. 2

Etymology

“myrici” refers to the host genus Myricaria and “-cola” means inhabiting.

Figure 2. 

Cytospora myricicola (CAF800083, holotype) A, B canker disease symptom C conidioma D transverse section through a conidioma E longitudinal section through a conidioma F conidiophores and conidia G, H conidia. Scale bars: 2000 µm (B); 1000 µm (C, D); 500 µm (E); 10 µm (F–H).

Holotype

CAF800083.

Description

Associated with branch canker disease of Myricaria paniculate. Sexual morph: Undetermined. Asexual morph: Pycnidial stromata ostiolated, semi-immersed in the host bark, scattered, discoid, with multiple locules. Conceptacle dark brown to black, circular surrounded stromata. Ectostromatic disc dark yellow, circular to ovoid, (250–)350–450(–550) μm diam., with one ostiole per disc. Ostioles dark, at the same level as the disc, (35–)55–85(–100) μm diam. Locule numerous, arranged circularly or elliptically with independent walls (245–)300–450(–550) μm diam. Peridium comprising a few layers of cells of textura angularis, with innermost layer brown, outer layer brown to dark brown. Conidiophores hyaline, branched, thin-walled, filamentous. Conidiogenous cells enteroblastic polyphialidic, 6.5–35.5 × 1.5–2.5 μm. Conidia hyaline, allantoid, smooth, aseptate, thin-walled, (4.4–)4.7–5.6(–5.8) × 1.4–1.7 μm (x̄ = 5.2 × 1.6 μm).

Culture characteristics

Colonies on PDA flat, with flocculent aerial mycelium and entire edge, initially white, becoming dark and reaching 90 mm diameter after 10 days at 25 °C, sterile.

Materials examined

China, Tibet Tibetan Autonomous Region, Lhasa City, Mozhugongka County, Riduo Township, Zen Village, on cankered branches of Myricaria paniculate, 28 July 2022, Jin Peng, Liu Yuanyuan, Jiang Ning and Liu Min (CAF800083, holotype); ex-type culture CFCC 59323. China, Tibet Tibetan Autonomous Region, Lhasa City, Mozhugongka County, Riduo Township, Renqinglin Village, on cankered branches of Myricaria paniculate, 28 July 2022, Jin Peng, Liu Yuanyuan, Jiang Ning and Liu Min (XZ010B); cultures CFCC 59324 and CFCC 59325.

Notes

Phylogenetically, Cytospora myricicola is close to C. fraxinigena, C. junipericola, C. pubescentis, C. quercicola and C. rosae (Fig. 1). Of these six species, only C. myricicola, C. pubescentis and C. rosae have asexual morph descriptions; C. myricicola (4.7–5.6 × 1.4–1.7 μm) is different from C. pubescentis (5.8–7.5 × 1.3–1.6 μm) by shorter conidia and from C. rosae (3–5 × 0.5–1 μm) by larger conidia (Senanayake et al. 2017; Shang et al. 2020). In addition, C. myricicola can be distinguished from the other five species by host and distribution (C. myricicola from Myricaria paniculate in China vs. C. fraxinigena from Fraxinus ornus in Italy vs. C. junipericola from Juniperus communis in Italy vs. C. pubescentis from Quercus pubescens in Italy vs. C. quercicola from Quercus sp. in Italy vs. C. rosae from Rosa canina in Italy) (Senanayake et al. 2017; Shang et al. 2020).

Cytospora populina (Pers.) Rabenh., Deutschl. Krypt.-Fl. (Leipzig) 1: 148. 1844

Fig. 3

Description

Associated with branch canker disease of Prunus cerasifera. Sexual morph: Stromata immersed in bark. Ascostromata, erumpent through the surface of bark, lenticular, extending to a large circular area, (750–)900–1200(–1350) μm diam. Disc grey to black, circular to ovoid, (85–)100–150(–195) μm in diameter. Ostioles numerous, dark brown to black, at the same level as the disc, (25–)31–46(–52) μm diam. Locules dark brown, arranged circularly, flask-shaped to spherical, (180–)195–285(–340) μm diam. Asci clavate to elongate obovoid, (45–)55.5–62.5(–67) × (6.5–)8–12(–16) μm, 4-spored. Ascospores biseriate, elongate-allantoid, thin-walled, hyaline, aseptate, (15–)18.5–23.5(–25.5) × (4–)4.5–5.5(–6.5) μm (x̄ = 20.4 × 5.1 μm). Asexual morph: Undetermined.

Figure 3. 

Cytospora populina (CAF800085) A, B canker disease symptom C ascostromata D transverse section through an ascostroma E asci and Ascospores F ascospores. Scale bars: 2000 µm (B); 500 µm (C); 200 µm (D); = 10 µm (E–F).

Culture characteristics

Colonies on PDA flat, with flocculent aerial mycelium and entire edge, initially white, becoming luteous and reaching 80 mm diameter after 10 days at 25 °C, sterile.

Materials examined

China, Tibet Tibetan Autonomous Region, Shigatse City, Sangzhuzi District, Gongjuelinka Park, on cankered branches of Prunus cerasifera, 2 August 2022, Jin Peng, Jiang Ning and Liu Min (XZ063); culture CFCC 58856.

Notes

Cytospora populina has been reported from Populus canadensis in Argentina, Salix psammophila in Shaanxi Province of China and Acer pubescens Rubus sp. in Uzbekistan (Farr 1973; Fan et al. 2015; Gafforov 2017). This fungus is distinguished from the other Cytospora species by its 4-ascospored asci and undiscovered asexual state (Fan et al. 2015). In the present study, we firstly found this fungus causing cankered branches of Prunus cerasifera in Tibet, China.

Cytospora sibiraeicola Ning Jiang, sp. nov.

MycoBank No: MycoBank No: 850241
Fig. 4

Etymology

“sibiraei” refers to the host genus Sibiraea and “-cola” means inhabiting.

Holotype

CAF800084.

Description

Associated with branch canker disease of Sibiraea angustata. Sexual morph: Undetermined. Asexual morph: Pycnidial stromata ostiolated, immersed or semi-immersed in the host bark, scattered, discoid, with multiple locules. Conceptacle black, circular surrounded stromata. Ectostromatic disc black, circular to ovoid, (200–)300–450(–500) μm diam., with one ostiole per disc. Ostioles dark, at the same level as the disc, (30–)60–80(–95) μm diam. Locule numerous, arranged circularly or elliptically with independent walls, (200–)250–380(–500) μm diam. Peridium comprising few layers of cells of textura angularis, with innermost layer brown, outer layer brown to dark brown. Conidiophores hyaline, unbranched, thin-walled, filamentous. Conidiogenous cells enteroblastic polyphialidic, 12.5–32.5 × 2–3.5 μm. Conidia hyaline, allantoid, smooth, aseptate, thin-walled, (3.3–)3.4–4.3(–4.5) × 1.2–1.6 μm (x̄ = 3.9 × 1.5 μm).

Figure 4. 

Cytospora sibiraeicola (CAF800084, holotype) A, B canker disease symptom C conidioma D transverse section through a conidioma E longitudinal section through a conidioma F conidiophores and conidia G, H conidia. Scale bars: 2000 µm (B); 1000 µm (C–E); 10 µm (F–H).

Culture characteristics

Colonies on PDA flat, with flocculent aerial mycelium and undulate margin, initially white, becoming olivaceous grey and reaching 90 mm diameter after 10 days at 25 °C, sterile.

Materials examined

China, Tibet Tibetan Autonomous Region, Lhasa City, Mozhugongka County, Riduo Township, Zen Village, on cankered branches of Sibiraea angustata, 28 July 2022, Jin Peng, Liu Yuanyuan, Jiang Ning and Liu Min (CAF800083, holotype); ex-type cultures CFCC 59100 and CFCC 59101.

Notes

Cytospora sibiraeicola is phylogenetically close to C. phialidica and C. viticola (Fig. 1). Morphologically, C. sibiraeicola (3.4–4.3 × 1.2–1.6 μm) and C. phialidica (3.5–5 × 1–2 μm) have much shorter conidia than C. viticola (5.2–7 × 0.9–1.6 μm) (Lawrence et al. 2017; Li et al. 2020). In addition, these three species can be distinguished by the host and distribution (C. sibiraeicola from Sibiraea angustata in China vs. C. phialidica from Alnus glutinosa in Italy vs. C. viticola from Vitis vinifera in the USA) (Lawrence et al. 2017; Li et al. 2020).

Discussion

Cytospora is a species-rich genus occurring on various plant hosts (Fotouhifar et al. 2010; Aiello et al. 2019; Jayawardena et al. 2019; Úrbez-Torres et al. 2020; Hanifeh et al. 2022). However, in the third pole of the Earth named Qinghai-Tibet Plateau, canker pathogens, such as Cytospora, have been seldom surveyed previously. In the comprehensive study on the genus Cytospora in China, only one species C. chrysosperma was recorded from Ulmus pumila in Tibet (Fan et al. 2020). Subsequently, Cytospora cotoneastricola and C. tibetensis from Cotoneaster sp. and Cytospora rosicola from Rosa sp. were discovered in Tibet (Pan et al. 2020). The current study introduces two new species named C. myricicola from Myricaria paniculate and C. sibiraeicola from Sibiraea angustata in Tibet, China. In addition, a new host record of C. populina on Prunus cerasifera was discovered.

To our knowledge, Cytospora myricicola is the first species of Cytospora discoved on the host genus Myricaria (Fan et al. 2020). Cytospora sibiraeicola and C. sibiraeae have been recorded from the host species Sibiraea angustata (Liu et al. 2015). Cytospora sibiraeae was described, based only on the sexual morph and is currently impossible to be distinguished from C. sibiraeicola morphologically (Liu et al. 2015). However, these two species occurring on Sibiraea angustata are phylogenetically obviously distinct (Fig. 1).

Species of Cytospora are known as opportunistic pathogens mainly infecting woody hosts and some of the species occur on a wide host range (Adams et al. 2005; Fan et al. 2020). The Cytospora species and their host association have been revealed in this study; however, further studies are required to confirm the fungal pathogenicity.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This research was funded by the Longterm Ecological Observation Study of Alpine Pine in southeast Tibet (Science and Technology Innovation Base, XZ202301JD0001G), the flexible talent introduction projects of the Key Laboratory of Forest Ecology in Tibet Plateau, Ministry of Education, Tibet Agricultural and Animal Husbandry University (2022–2023) and the National Microbial Resource Center of the Ministry of Science and Technology of the People’s Republic of China (NMRC-2022-7).

Author contributions

Conceptualization: JRL, JTL, NJ. Methodology: NJ. Formal analysis: JRL. Investigation: JRL, JTL, NJ. Resources: JRL, JTL, NJ. Data Curation: JRL, JTL. Writing - Original draft: JRL. Writing - Review and Editing: NJ. Visualization: JTL, NJ.

Author ORCIDs

Jiangrong Li https://orcid.org/0000-0002-6679-5227

Jieting Li https://orcid.org/0009-0001-8984-7261

Ning Jiang https://orcid.org/0000-0002-9656-8500

Data availability

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

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