Content uploaded by Raghvendra Singh
Author content
All content in this area was uploaded by Raghvendra Singh on Jan 09, 2024
Content may be subject to copyright.
Submitted 23 September 2023, Accepted 18 October 2023, Published 26 December 2023
Corresponding Author: Raghvendra Singh – e-mail – drsinghtaxon@gmail.com, singhr.bot@bhu.ac.in 523
Nyssopsoraceae, a new family of Pucciniales to accommodate
Nyssopsora spp.
Yadav S1, Singh G2, Rajwar S1, Verma SK1, Gupta SK3, Singh R1,
Kharwar RN1 and Kumar S4
1Centre of Advanced Study in Botany, Institute of Science, Banaras Hindu University, Varanasi, U.P. 221005, India
2Department of Botany, Deen Dayal Upadhyay Gorakhpur University, Gorakhpur, U.P. 273009, India
3305-P, Balajeepuram, Bypass Road, Nakaha No.1, PO- Basharatpur, Gorakhpur, U.P.273004, India
4Forest Pathology Department, KSCSTE-Kerala Forest Research Institute, Peechi, Thrissur, Kerala 680653, India
Yadav S, Singh G, Rajwar S, Verma SK, Gupta SK, Singh R, Kharwar RN, Kumar S 2023 –
Nyssopsoraceae, a new family of Pucciniales to accommodate Nyssopsora spp. Current Research
in Environmental & Applied Mycology (Journal of Fungal Biology) 13(1), 523–549,
Doi 10.5943/cream/13/1/20
Abstract
A new species of rust fungi Nyssopsora toonae discovered on living leaves of Toona sinensis
(≡ Cedrela sinensis) from Uttarakhand, India, is described and illustrated. N. cedrelae is also
reported on the same host plant, but differs from N. toonae which has a wide range of cells (1–4)
and diverse teliospores shapes. Such features are not reported in any other species of the
Nyssopsora. In a phylogenetic analyses based on partial 28S large subunit (LSU), 18S smaller
subunit (SSU), cytochrome c-oxidase subunit 3 (CO3) and complete internal transcribed spacer
(ITS) sequence data, all the Nyssopsora spp. along with N. toonae clustered together and form a
separate and independent monophyletic lineage sister to Pucciniaceae in Pucciniales. The new
family Nyssopsoraceae is introduced to accommodate this lineage based on the phylogenetic
evidence and morphological differences from other known families. Nyssopsoraceae is
characterised by its teliospores borne singly on a pedicel, with simple or branched projections all
over the surface, composed of 1–4 cells (mostly 3-celled), and diverse shape. The teliospores
spherical to subspherical (1-celled), dumbbell (2-celled), linearly arranged to triquetrous (3-celled),
or T-shaped to tetrahedron (4-celled). A comparison of the morphological features, host plants and
geographical distribution of all validly accepted species of Nyssopsora is provided.
Keywords – Phylogeny – Plant pathogenic – Rust fungi – Taxonomic novelty
Introduction
The rust fungi (Pucciniales) are obligate phyto-pathogens and represent one of the largest
orders in Basidiomycota. They are a monophyletic group with more than 7000 species (Kirk et al.
2008) distributed globally. Diseases caused by rust fungi have drastically impacted human
agriculture and history through time. These fungi have a broader host range from pteridophytes
(ferns) to higher plants including gymnosperms and angiosperms, although individual species
usually have a restricted host range. Rust fungi can have a microcyclic and autoecious life cycle to
a macrocyclic life cycle with up to five spore states. Heteroecious species requires two unrelated
hosts, although the life cycle can be modified and reduced (Cummins & Hiratsuka 2003). From
India, 640 species of rust fungi have been recorded belonging to 69 genera and 16 families
(Gautam et al. 2021).
Current Research in Environmental & Applied Mycology (Journal of Fungal Biology)
13(1): 523–549 (2023) ISSN 2229-2225
www.creamjournal.org Article
Doi 10.5943/cream/13/1/20
524
Initially, rust fungi were classified into families based on characteristics of basidia and
teliospores (Cunningham 1931). Later, teliospores were the most important spore state to
distinguish genera and families in the classical taxonomy of Pucciniales (Cummins & Hiratsuka
2003, Maier et al. 2003, Aime 2006, van der Merwe et al. 2007, Beenken & Wood 2015). Arthur
(1906) established the genus Nyssopsora with N. Echinata (Lév.) Arthur as the type species.
Nyssopsora is characterized by 3-celled teliospores with a basal pedicellate cell surmounted by two
further cells and bearing conspicuous projections (spines) on its surface. Both Lütjeharms (1937)
and Lohsomboon et al. (1990) have monographed the genus Nyssopsora. Nyssopsora was originally
included in Triphragmium Link (1825). The main characteristics of Triphragmium were
subglobose, 3-celled, pedicellate teliospores divided by transverse and longitudinal septa and with
subepidermal telia. Both Nyssopsora and Triphragmium were originally assigned to
Sphaerophragmiaceae Cummins & Y. Hirats. because of their three celled teliopsores with
triangular arrangement (Cummins & Hiratsuka 1983).
Cummins & Hiratsuka (1983) established Sphaerophragmiaceae, covering the genera
Cumminsina Petr., Hapalophragmium Syd. & P. Syd. (= Hapalophragmiopsis Thirum., = Triactella
Syd.), Hennenia Buriticá, Nyssopsora Arthur (= Oplophora Syd.), Sphaerophragmium Magnus,
Triphragmiopsis Naumov (= Nyssopsorella Syd.) and Triphragmium Link. These genera were
mainly based on pedicellate teliospores with three or more spherically arranged cells. The
connections between Nyssopsora and Sphaerophragmium were noted by Lohsomboon et al. (1994).
Cummins & Hiratsuka (2003) merged the Sphaerophragmiaceae into Raveneliaceae Leppik.
McTaggart et al. (2016) showed that the type species of Sphaerophragmium, S. acacieae (Cook)
Magnus, was separated from Raveneliaceae. Therefore, Sphaerophragmiaceae was re-erected by
McTaggart et al. (2016). Sphaerophragmiaceae did not contain any genera except
Sphaerophragmium in the original description by Cummins & Hiratsuka (1983). Currently
Sphaerophragmiaceae consists of Austropuccinia Beenken, Dasyspora Berk. & M.A. Curtis,
Puccorchidium Beenken, Sphenorchidium Beenken and Sphaerophragmium (Beenken 2017, Aime
& McTaggart 2020). The current status of Nyssopsora is not resolved and it remains incertae sedis
within Uredinineae, recovered as sister to Sphaerophragmiaceae (Aime & McTaggart 2020).
Based on multi-gene sequence analysis, a stable and resolved higher-rank classification for
the rust fungi (Pucciniales) was given by Aime & McTaggart (2020) that comprising 7 suborders
and 18 families. Aime & McTaggart (2020) discussed the evolutionary trends that led to
diversification and current status within Pucciniales, but some families/genera Pucciniastrum and
Pucciniastraceae; Raveneliaceae; and Allodus, Neopuccinia, and Nyssopsora, could not be
confidently resolved.
In December 2018, a survey was conducted to explore the diversity of phytopathogenic fungi
in Chamoli district of Uttarakhand, India. During this survey, an interesting rare rust fungus was
discovered on living leaves of Toona sinensis (Juss.) M. Roem. that caused blackish brown pustules
as rusty masses restricted to the lower surface of leaves. This fungus was identified as a new
species of Nyssopsora due to the presence of 1–4-celled (mostly 3-celled) pedicellate teliospores
bearing conspicuous projections on its surface. There are12 validly accepted species of Nyssopsora
(www.indexfungorum.org and www.mycobank.org; accessed 15 September, 2023). In light of the
above, the present study focused on the phylogenetic analyses using more species and genera
including Nyssopsora and Triphragmium, to find out exact placement of all the Nyssopsora spp.
under Pucciniales. The present communication provides a comparative account of major
morphological features, spore states, hosts and geographical distribution of the validly accepted
species of Nyssopsora (Tables 1, 2).
Materials & Methods
Isolates and morphology
During a survey an interesting rare foliicolous rust was encountered on Toona sinensis from
Uttarakhand, India, in December 2018. The infected leaves were collected in sterile polybag in
525
between blotting papers and brought to the laboratory along with collection details. Close-up
photographs of infection spots for different developmental stages of spores were captured using
camera (CatCam300EF) attached to a Magnus Stereo Zoom Trinocular Olympus Microscope
(MSZ-TR). Slides were prepared by hand sectioning and scraping from infection spots of freshly
collected leaves and mounted in both lactophenol cotton-blue mixture and 50% glycerine. Fungal
propagules were photographed using an Olympus compound microscope (CH20i-TR) equipped
with Magnus camera (MIPS CMOS). Scanning electron microscopy (SEM) was done with a Carl
Zeiss EVO 18. Detailed observations of morphological characters were carried out at different
magnifications through light microscopy (450× and 1000×) and scanning electron microscopy (up
to ~35K×). For SEM micrographs specimens were coated with gold-palladium using a POLARON
Sputter coater (180 sec in nitrogen atmosphere of 20 mA, 30 mm distance from the electrode) and
examined with SEM. Measurements were made for 25 of each morphological feature of
urediniospores and teliospores. Holotype material is deposited in the Ajrekar Mycological
Herbarium (AMH), Agharkar Research Institute (ARI), Pune, India and isotype material is retained
in the Mycological Herbarium of the Department of Botany of Banaras Hindu University, Varanasi,
U.P., India (MH-BHU).
DNA extraction
Genomic DNA was extracted from spores scrapped from the heavily infected surface of
leaves using a sterile scalpel blade. Harvested spores and mycelium about 150 mg was transferred
to a 2 ml polypropylene centrifuge tube kept in liquid nitrogen for 2 min and then grinded to make
fine powder using a mortar and pestle. From powdered form, DNA was isolated using Himedia
DNA isolation Kit (HiPurA™ Fungal DNA Purification Kit) following the manufacturers’
protocols. Isolated DNA fragments were visualised by electrophoresis in 1% agarose gel (w/v)
stained with ethidium bromide under Gel Documentation system (Bio-Rad Universal Hood II) and
DNA concentration was quantified by using Nano Drop microvolume spectrophotometer
(ThermoScientificTMNanoDropTM One/OneC Microvolume UV-Vis Spectrophotometer with Wi-
Fi).
Polymerase chain reaction (PCR) and sequencing
The internal transcribed spacer (ITS) region, large subunit (LSU) and smaller subunit (SSU)
of nrDNA were amplified using Rust2inv (5′-GATGAAGAACACAGTGAAA-3′)/ITS4rust (5′-
CAGATTACAAATTTGGGCT-3′) (Aime 2006, Beenken et al. 2012), LROR (5'-
ACCCGCTGAACTTAAGC-3')/LR6 (5’-CGCCAGTTCTGCTTACC-3’) (Vilgalys & Hester
1990) and NS1 (5′-GTAGTCATATGCTTG TCTC-3′)/NS4 (5′-CTTCCGTCAATTCCTTTAAG-
3′) (White et al. 1990) primer pairs, respectively. PCRs were carried out in 50 μL reaction mixture
containing 5 μL Taq buffer containing MgCl2, 1 μL dNTPs (10 mM), 1 μL each forward and
reverse primer (10 μmol/μL), 5 μL of DNA template (~35 ng/μL), 0.3 μL of Taq DNA polymerase
(5 Unit/μL) and 36.7 μL of milli-Q water. The PCRs were carried out in Thermal Cycler (Bio-Rad
T100™). Conditions for the PCRs amplification consisted of an initial denaturation at 95 °C for 5
min; followed by 35 cycles of denaturation at 94 °C for 1 min; annealing at 53 °C for ITS, 65 °C
for LSU and 55 °C for SSU for 1 min, extension at 72 °C for 1 min. The final extension step was
done at 72 °C for 8 min. The amplified amplicons were run in 1.2% agarose gel and visualised in
the Gel Documentation system (Bio-Rad Universal Hood II) for the product size and purity. PCR
products were cleaned and sequenced with the amplification primers at AgriGenome Labs Private
Ltd., Kerala by the Sanger sequencing method using BigDye® Terminator v3.1 Cycle sequencing
Kit and ABI 3100 DNA analyzer.
Phylogenetic analysis
The obtained ITS, LSU and SSU sequences from type materials were assembled and edited
with Chromas v.2.6.6. The manually edited sequences were submitted to NCBI GenBank (Table 1)
and were subjected to a megablast search of the NCBI GenBank nucleotide database. The most
526
homologous sequences of related strains were retrieved. Reference sequences were also selected
based on sequence availability from relevant published literature (Table 1). Sequence
alignmentswere generated using MAFFT v.6.864b (Katoh & Toh 2010) whereas BioEdit v.7.0.9
(Hall 2007) and MEGA-X v.10.1.8 (Kumar et al. 2018) were used to manually check, improve and
concatenate the aligned sequences. Sequence alignments were deposited as electronic
supplementary materials in TreeBASE, study number 29662.
The phylogenetic methods used in this study included a Bayesian analysis (BI) performed
with MrBayes v.3.2.7 (Ronquist et al. 2012) and maximum likelihood (ML) analysis performed
with RAxML v.8.2.10 (Stamatakis 2014). The phylogenetic analyses were individually applied to
the two datasets: dataset 1 consisted of concatenated alignments of LSU, SSU and CO3 sequences
whereas datasets 2 consisted of concatenated alignments of LSU, SSU, CO3 and ITS sequences
from 18 families currently belonging to Pucciniales. The sequences of taxa containing weak
aligned portions, incomplete data, missing sequence data and gaps were removed. The overview
trees were rooted with Eocronartium muscicola, from the sister order to Pucciniales (Aime et al.
2006).
Bayesian inference was implemented with the GTR+I+G model. Bayesian inference was
calculated using a Markov chain Monte Carlo (MCMC) algorithm with Bayesian posterior
probabilities (Rannala & Yang 1996). The analysis was performed up to 2300000 generations till
the standard deviation of split frequency came down below 0.01. The first 25% of generated trees
representing the burn-in phase were discarded, and the remaining trees were used to calculate
posterior probabilities of the majority rule consensus tree. ML analysis was also performed using a
GTR model of site substitution, including GAMMA+P-Invar model of rate heterogeneity and a
proportion of invariant sites (Stamatakis 2014). The ML support values were evaluated with a
bootstrapping method of 1000 replicates. These analyses involved 102 nucleotide sequences.
Presented trees were obtained with the ML approach. Tree reconstruction, visualization and
editing were done using FigTree v.1.4.4 and TreeGraph_2.15.0. The multigene phylograms are
shown in Figs 9, 10.
Results
The data for the trees conducted in different analyses are shown in Table 1. Phylogenetic
trees obtained from combined genes analyses are supplied below.
Dataset 1 (LSU, SSU and CO3 phylogeny)
This dataset consisted of a concatenated alignment of three loci (LSU, SSU and CO3). The
final alignment contained a total of 1987 characters divided in to three partitions containing 1006
(LSU), 437 (SSU) and 544 (CO3) characters, respectively including the alignment gaps.
Phylogenetic trees generated from Bayesian analyses (BI) and maximum likelihood (ML) produced
trees with overall similar topology. A best scoring RAxML tree is presented in Fig. 9, with the
likelihood value of −23481.773327.
In this analysis, the exact placement of Nyssopsora spp. that were earlier not resolved,
clustered together and recovered as sister to Pucciniaceae and delineate a separate independent
lineage with strong bootstrap support within Pucciniales. The ML tree (Fig. 9) was mostly
congruent with prior studies of more limited taxon and locus sampling (Aime 2006, Beenken &
Wood 2015, McTaggart et al. 2016, Beenken 2017, Aime et al. 2017, 2018, Souza et al. 2018).
Dataset 2 (LSU, SSU, CO3 and ITS phylogeny)
This dataset consisted of a concatenated alignment of four loci (LSU, SSU, CO3 and ITS).
The final alignment of this dataset contained a total of 2662 characters divided into four partitions
containing 1006 (LSU), 437 (SSU), 544 (CO3) and 675 (ITS) characters, respectively including the
alignment gaps. Phylogenetic trees generated from Bayesian analyses and maximum likelihood
(ML) produced trees with an overall similar topology. A best scoring RAxML tree is presented
(Fig. 10), with the likelihood value of −31766.255887.
527
Table 1 Taxa included in molecular phylogenetic analyses and their GenBank accession numbers. The sequences in bold were generated in this study.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Araucariomycetaceae
Araucaromyces
fragiformis
BRIP 68996
MW049245
MW049292
MW036497
NA
Agathis robusta
Aime & McTaggart
(2020)
Coleosporiaceae
Chrysomyxa
arctostaphyli
CUW CFB
22246
AF522163
AY657009
NA
NA
NA
Aime & McTaggart
(2020)
Chrysomyxa reticulata
PDD 92535
KX985767
NA
NA
KX985767
Rhododendron sp.
sect. Vireya
Padamsee & McKenzie
(2017)
Chrysomyxa rhododendri
PDD 102088
KJ698630
KJ746824
NA
NA
Rhododendron sp.
Padamsee & McKenzie
(2014)
Coleosporium inulae
BPI 871127
MG907223
NA
NA
NA
Inula fragilis
Aime et al. (2018)
Coleosporium melampyri
PUR N16579
MG907224
NA
NA
NA
Rhinanthus
aristatus
Aime et al. (2018)
Coleosporium senecionis
PDD 98309
KJ716348
KJ746818
NA
KJ716348
Senecio sp.
Padamsee & McKenzie
(2014), Aime &
McTaggart (2020)
Coleosporium
tussilaginis
PUR N16713
MG907228
NA
NA
MG907228
Sonchus sp.
Aime et al. (2018)
Thekopsora areolata
NA
KJ546894
NA
NA
NA
Picea engelmannii
Aime & McTaggart
(2020)
Crossopsoraceae
Crossopsora fici
BRIP 58118
MH047207
MH047212
MH047204
NA
Ficus virens var.
sublanceolata
Aime & McTaggart
(2020)
Crossopsora ziziphi
BPI 877877
MG744558
NA
NA
NA
Ziziphus
mucronata
Souza et al. (2018)
Kweilingia bambusae
PUR F18200
MW147026
NA
NA
NA
Bambusa sp.
Aime & McTaggart
(2020)
Gymnosporangiaceae
Gymnosporangium
clavariiforme
BRIP 59471
MW049261
MW049296
MW036499
NA
Crataegus sp.
Aime & McTaggart
(2020)
Gymnosporangium gracile
20140326-1-GR-
P25
KM486544
NA
NA
KM486542
Juniperus oxycedrus
Fernandez & Alvarado
(2016)
Melampsoraceae
Melampsora abietis-
populi
HMAS 247978
MK064529
NA
NA
MK028579
Populus wilsonii
Zheng et al. (2019)
528
Table 1 Continued.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Melampsora epitea
DAOM 240968
HQ317514
NA
NA
HQ317514
Salix candida
Liu et al. (2015)
Melampsora euphorbiae
BPI 863501
DQ437504
DQ789986
MW036501
NA
Euphorbia
macroclada
Aime (2006), Matheny et
al. (2006), Aime &
McTaggart (2020)
Melampsora hypericorum
PDD 97325
KJ716353
KJ746828
NA
KJ716353
Hypericum
androsaemum
Padamsee & McKenzie
(2014)
Melampsora laricis-
populina
HMAS 247976
MK064525
NA
NA
MK028584
Populus simonii
Zhenget al. (2019)
Melampsora sp.
SAL103
EF192205
NA
NA
NA
Salix amygdaloides
Bennett et al. (2011)
Milesinaceae
Milesia polypodii
KR-M-0043190
MK302190
NA
NA
MH908415
Polypodium vulgare
Bubner et al. (2019)
Milesina kriegeriana
KR-M-0048480
MK302207
NA
NA
MH908452
Dryopteris dilatata
Bubner et al. (2019)
Milesina philippinensis
BRIP 58421
KM249868
NA
NA
NA
Nephrolepis sp.
McTaggart et al. (2014)
Milesina thailandica
IBAR 11436
LC498526
NA
NA
LC498526
Lygodium flexuosum
Onoet al. (2020)
Milesina vogesiaca
PURN659a
MG907235
NA
NA
NA
Polystichum
aculeatum
Aime et al. (2018)
Naohidemyces vaccinii
BPI 871754
DQ354563
DQ354562
NA
NA
Vaccinium ovatum
Aime (2006)
Uredinopsis osmundae
BPI 872258
MG907245
NA
NA
NA
Osmunda
claytoniana
Aime et al. (2018)
Nyssopsoraceae
Nyssopsora echinata
KR-0012164
(U1022),
ESS244
MW049272
U77061
NA
NA
Meum
athamanticum
Aime & McTaggart
(2020)
Nyssopsora koelreuteriae
BBSW-1
NA
NA
NA
KT750965
Koelreuteria
bipinnata
Yang et al. (2016)
Nyssopsora thwaitesii
AMH 9528
KF550283
NA
NA
KF550283
Schefflera
wallichiana
Baiswar et al. (2014)
Nyssopsora toonae
AMH 10124
MT712660
ON641038
NA
MT712662
Toona sinensis
Present study
Ochropsoraceae
Aplopsora nyssae
BPI 877823
MW049244
NA
NA
NA
Nyssa sylvatica
Aime & McTaggart
(2020)
Ochropsora ariae
KR-0015027
MW049273
NA
NA
NA
Anemone nemorosa
Aime & McTaggart
(2020)
Phakopsoraceae
Cerotelium fici
UACH107
MF580676
NA
NA
NA
Ficus carica
Solano-Báez et al. (2017)
529
Table 1 Continued.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Masseeëlla capparis
BRIP 56844
JX136798
NA
KT199413
NA
Flueggea
virosa
McTaggart et al. (2016)
Phakopsora myrtacearum
PREM 61155
KP729473
NA
KT199414
KP729468
Eucalyptus grandis
Maier et al. (2016),
McTaggart et al. (2016)
Phakopsora pachyrhizi
BRIP 56941
KP729475
MW049300
MW036503
NA
Neonotonia wightii
Maier et al. (2016),
Aime & McTaggart
(2020)
Phragmidiaceae
Gerwasia rubi
BRIP 58369
KT199397
NA
KT199408
NA
Rubus sp.
McTaggart et al. (2016)
Gymnoconia interstitialis
BPI 747600
JF907677
DQ521422
NA
NA
Rubus
allegheniensis
Yun et al. (2011),
Aime & McTaggart
(2020)
Gymnoconia peckiana
BPI 879271
GU058010
NA
NA
GU058010
Rubus sp.
Dixon et al. (2010)
Hamaspora acutissima
BRIP 55606
KT199398
KT199385
KT199409
NA
Rubus
moluccanus
McTaggart et al. (2016)
Kuehneola uredinis
BPI 871104
DQ354551
DQ092919
NA
DQ354551
Rubus argutus
Aime (2006),
Aime & McTaggart
(2020)
Phragmidium barnardii
BRIP 56945
KT199402
NA
KT199415
NA
Rubus
multibracteatus
McTaggart et al. (2016)
Phragmidium
sanguisorbae
BPI 872232
JF907674
NA
NA
NA
Sanguisorba minor
Yun et al. (2011)
Phragmidium tormentillae
BPI 843392
DQ354553
DQ354552
MG907265
MG907214
Potentilla
canadensis
Aime (2006),
Aime et al. (2018)
Phragmidium violaceum
BPI 879276
GU058015
NA
NA
GU058015
Rubus parviflorus
Dixon et al. 2010
Trachyspora intrusa
BPI 843828
DQ354550
DQ354549
MW036508
DQ354550
Alchemilla vulgaris
Aime (2006),
Aime & McTaggart
(2020)
Triphragmium ulmariae
BPI 881364
JF907676
AY125401
NA
NA
Filipendulaulmaria
Wingfield et al. (2004),
Yun et al. 2011
Pileolariaceae
Pileolaria brevipes
PUR N16525,
BPI 877989
MG907216
MW049301
MG907267
NA
Toxicodendron sp.
Aime et al. (2018),
Aime & McTaggart
(2020)
Pileolaria pistaciae
PURN11945
KY314266
NA
NA
MG860928
Pistacia chinensis
Ishaq et al. (2020)
530
Table 1 Continued.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Pileolaria toxicodendri
BPI 871761
DQ323924
NA
NA
NA
Toxicodendron sp.
Scholler & Aime 2006,
Aime & McTaggart
(2020)
Pucciniaceae
Aecidium kalanchoe
BPI 843633
AY463163
DQ354524
NA
NA
Kalanchoe
blossfeldiana
Hernandez et al. (2004),
Aime (2006)
Ceratocoma jacksoniae
BRIP 57762
KT199394
KT199382
KT199405
NA
Daviesia sp.
McTaggart et al. (2016)
Cumminsiella
mirabilissima
BPI 871101
DQ354531
DQ354530
NA
NA
Mahonia aquifolium
Aime (2006)
Endophylloides
portoricensis
BPI 844288
DQ354516
AY125389
NA
DQ354516
Mikania micrantha
Aime & McTaggart
(2020)
Leptopuccinia
malvacearum
BRIP 57522
KU296888
NA
KX999924
NA
Malva parviflora
Aime & McTaggart
(2020)
Miyagia pseudosphaeria
BPI 842230
DQ354517
AY125411
NA
NA
Sonchus oleraceus
Aime & McTaggart
(2020)
Puccinia andropogonis
BPI 871763
GU057993
NA
NA
NA
Andropogon sp.
Dixon et al. (2010)
Puccinia coronate
BPI 844300
DQ354526
DQ354525
NA
NA
Rhamnus cathartica
Aime (2006)
Puccinia coronate var.
avenae
BRIP 57635
MW147047
NA
MW139657
NA
Avena sativa
Aime & McTaggart
(2020)
Puccinia graminis
BRIP 60137
KM249852
MW049302
MW036505
NA
Glyceria maxima
Deadman et al. (2011),
Aime & McTaggart
(2020)
Puccinia hordei
BPI 871109
DQ354527
DQ415278
NA
NA
Unidentified
Poaceae
Aime (2006),
Aime et al. (2006)
Puccinia platyspora
BPI 091376
KT827311
NA
NA
NA
Sphaeralcea sp.
Demers et al. (2015)
Puccinia porri
BRIP 64600
KY849820
NA
NA
KY849820
Allium porrum
McTaggart et al. (2017)
Puccinia sherardiana
BPI 871783
KT827315
NA
NA
NA
Sphaeralcea sp.
Demers et al. (2015)
Puccinia windsoriae
BPI 871790
GU057995
NA
NA
NA
Tridens sp.
Dixon et al. (2010)
Pucciniosira solani
RS25
EU851140
NA
NA
NA
Solanum nigrum
Zuluaga et al. (2011)
Uromyces plumbarius
NA
KP313731
NA
NA
KP313731
Gaura lindheimeri
Blomquist et al. (2015b)
Pucciniastraceae
Hyalopsora aspidiotus
PUR N4641
MW049264
NA
NA
NA
Gymnocarpium
dryopteris
Aime & McTaggart
(2020)
Melampsoridium
betulinum
BPI 871107
DQ354561
AY125391
NA
NA
Alnus sp.
Wingfield et al. (2004),
Aime (2006)
531
Table 1 Continued.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Pucciniastrum epilobii
PUR N11088
MW049277
NA
NA
NA
Epilobium
angustifolium
Aime & McTaggart
(2020)
Pucciniastrum minimum
BRIP 57654
MG907242
KT199391
KT199422
NA
Vaccinium
corymbosum
McTaggart et al. (2016),
Aime et al. (2018)
Raveneliaceae
Diorchidium woodii
U1475
MW111538
MW111533
NA
NA
Millettia grandis
Aime & McTaggart
(2020)
Endoraecium
auriculiforme
BRIP 56548
KJ862298
NA
KJ862432
KJ862355
Acacia
auriculiformis
McTaggart et al. (2015)
Endoraecium parvum
BRIP 57524
KJ862316
KJ862409
KJ862445
KJ862369
Acacia leiocalyx
McTaggart et al. (2015)
Kernkampella breyniae
BRIP 56909
KJ862346
KJ862428
KJ862459
NA
Breynia cernua
McTaggart et al. (2015)
Maravalia limoniformis
BRIP 59649
MW049266
NA
MW036500
NA
Austrosteenisia
blackii
Aime & McTaggart
(2020)
Olivea scitula
BPI 871108
DQ354541
DQ354540
NA
NA
Vitex doniana
Aime (2006)
Porotenus biporus
ZT Myc 3414
JF263494
JF263510
NA
NA
Memora flavida
Beenken et al. (2012)
Prospodium tuberculatum
BRIP 57630
KJ396195
KJ396196
MW036504
NA
Lantana camara
Pegg et al. (2014),
Aime & McTaggart
(2020)
Ravenelia evansii
PREM 61846
MG945993
NA
MN095321
MG945961
Vachellia luederitzii
var. retinens
Ebinghaus & Begerow
(2018), Ebinghaus et al.
(2018, 2020)
Rogerpetersoniaceae
Rogerpetersonia torreyae
BPI 877825,
BPI 877824
MG907207
MG907197
MG907254
NA
Torreya californica
Aime et al. (2018)
Skierkaceae
Skierka diploglottidis
BRIP 59646
MW049278
MW049304
MW036506
NA
Dictyoneura obtusa
Aime & McTaggart
(2020)
Skierka robusta
BPI 879954
MW049279
MW049305
NA
NA
Rhoicissus
rhomboidea
Aime & McTaggart
(2020)
Sphaerophragmiaceae
Austropuccinia psidii
BRIP 57793
KF318449
KF318457
KT199419
NA
Rhodamnia
angustifolia
Pegg et al. (2014),
McTaggart et al. (2016)
Dasyspora gregaria
ZTMyc 3397
JF263477
JF263502
JF263518
JF263477
Xylopia
cayennensis
Beenken et al. (2012)
Dasyspora segregaria
PMA MP4941
JF263488
JF263507
JF263523
JF263488
Xylopia aromatica
Beenken et al. (2012)
532
Table 1 Continued.
Taxon
Voucher ID
GenBank accession no.
Host
Source
28S
18S
CO3
ITS
Puccorchidium
polyalthiae
ZT HeRB 251
JF263493
JF263509
JF263525
JF263493
Polyalthia longifolia
Beenken et al. (2012)
Puccorchidium popowiae
ZT Myc 1976
JF263495
JF263511
JF263526
JF263495
Monanthotaxis
caffra
Beenken et al. (2012)
Sphaerophragmium
acaciae
BRIP 56910
KJ862350
KJ862429
KJ862462
NA
Albizia sp.
McTaggart et al. (2015)
Sphenorchidium
deightonii
PC 0096730
KM217350
KM217368
NA
KM217350
Xylopia aethiopica
Beenken & Wood (2015)
Sphenorchidium xylopiae
NA
KM217355
KM217372
NA
KM217355
Xylopia aethiopica
Beenken & Wood (2015)
Tranzscheliaceae
Tranzschelia
discolor
BRIP 57662
KR994891
KR994969
KR995082
NA
Prunus persica
Doungsa-ard et al. (2018)
Tranzschelia
mexicana
KR-M-0040855
KP308391
NA
NA
KP308391
Prunus salicifolia
Blomquist et al. (2015a)
Uredinineaeincertaesedis
Allodus podophylli
BPI 842277,
PUR N16753
DQ354543
DQ354544
MG907270
DQ354543
Podophyllum
peltatum
Aime (2006),
Aime et al. (2018)
Zaghouaniaceae
Achrotelium ichnocarpi
BRIP 55634
KT199393
KT199381
KT199404
NA
Ichnocarpus
frutescens
McTaggart et al. (2016)
Blastospora smilacis
PUR N270
DQ354568
DQ354567
NA
NA
Smilax sieboldii
Aime (2006)
Hemileia vastatrix
BRIP 61233
KT199399
DQ354565
KT199410
NA
Coffea robusta
Aime (2006),
McTaggart et al. (2016)
Mikronegeria fagi
PUR N16373
MW049267
MW049298
NA
NA
Nothofagus oblique
Aime & McTaggart
(2020)
Mikronegeria fuchsiae
PDD 101517
KJ716350
KJ746826
NA
KJ716350
Phyllocladus
trichomanoides
Padamsee & McKenzie
(2014)
Zaghouanianotelaeae
BRIP 58325
KT199396
KT199384
KT199407
NA
Notelaea
microcarpa
McTaggart et al. (2016)
Out group
Eocronartium muscicola
MIN796447,
DUKE:DAH(e1)
AF014825
DQ241438
NA
NA
NA
Bruns & Szaro
Unpublished,
Henk & Vilgalys et al.
(2007)
533
Table 2 Morphological details of Nyssopsora species.
Nyssopsora
spp.
Teliospores
Projecton/spores
Urediniospores
NC†
Size
(μm)
Septal
Constric-
tion
Wall
thickness
(μm)
GP†
Pedicel
(μm)
NP†
Length
(μm)
TF†
Size (μm)
WT†
(μm)
SO†
GP†
asiatica
3
26–41 ×
26–42
Slight to
moderate
1–3
1–2(3)
Up to 60
× 5–8
13–29
6–15
2–>5
–
–
–
–
cedrelae
3
29–44 ×
27–44
Slight
1–3
1–3
Up to 105
× 7–12
13–27
3–9
2–3
14–24 ×
13–21
1–2.5
E
NS
citriobati
3
28–39 ×
28–38
Slight
1–3.5
1–3
Up to 40.5
× 3–5
14–19
2.5–6
2–6
–
–
–
–
clavellosa
3
29–37 ×
26–38
Slight to
moderate
1.5–3
1–4
Up to 94
× 5–9
10–23
4–11
3–4
–
–
–
–
echinata
3
29–42 ×
27–40
Slight
1–3
1–4
Up to 56
× 4–8
14–23
4–18
1–3
–
–
–
–
eocaenica
3
33–38 ×
34–37
Moderate
–
–
Up to 6–7
Numerous
–
0
–
–
–
–
formosana
3
27–35 ×
25–35
Slight
1–2
1–3
Up to 44
× 3.5–6
11–17
5–14
2–>5
15–24 ×
13–20
0.5–2
E
NS
koelreuteriae
3
30–40 ×
28–39
Slight
1–2.5
1–3
Up to 50
× 5–7
18–30
2–10
2–4
18–35 ×
14–25
1–2
E
NS
panamensis
3
21–26 ×
20–24
Slight
1–2
2
–
8–29
4–20
1–4
19–28 ×
16–22
0.5–1
E
2
thirumalacharii
3
22–36 ×
19–30
Slight to
moderate
–
>1
Up to 15–
30
–
–
–
–
–
–
–
thwaitesii
3
28–48 ×
25–44
Strong
1–3
1–3
Up to 85
× 4.5–9
8–17
3–12(–
16)
2–4
–
–
–
–
toonae
1–4
7.5–40 ×
9–30
Strong
1.5–5
1–2
Up to 85
× 4–18
40–60
1.5–6
2–8
20–24 ×
17–27
1.2–3.8
E
NS
trevesiae
3
24–37 ×
25–36
Slight
0.5–2.5
2–3
Deciduous
and short
10–23
2–9
1–2
–
–
–
–
†NC = Number of cells in each spore, GP = The number of germ pores (usual) in each spore, NP = Number of projections on each spore, TF = Tip
furcation, WT = Wall thickness, SO = Surface ornamentation, E = Echinulate, NS = Not seen.
534
The results of analysis of dataset 2 (Fig. 10), closely supports the dataset 1 (Fig. 9). From
both datasets, it is clear that all the Nyssopsora spp. separated together as an independent, formerly
not known lineage in Pucciniales. The differences in morphology are significant enough for
retaining Nyssopsora distinct from the members of Pucciniaceae. Therefore, a new family
Nyssopsoraceae is established for all the Nyssopsora species having 1–4-celled pedicellate
teliospores with conspicuous projections (spines) on their surface. The genera Nyssopsora and
Triphragmium, which were originally assigned to Sphaerophragmiaceae, are now excluded (Figs.
9, 10) and support the current concepts of Aime & McTaggart (2020).
Taxonomy
Nyssopsoraceae Sanjay & Raghv. Singh, fam.nov.
Index Fungorum number: IF559434; Facesoffungi number: FoF12772
Etymology – named after the genus Nyssopsora.
Spermogonia unknown. Aecia, when present, uredinioid, without paraphyses; aeciospores
echinulate. Uredinia subepidermal in origin, erumpent; urediniospores borne singly on pedicels,
echinulate, germ pores not seen. Telia subepidermal in origin, erumpent; teliospores borne singly
on pedicel, composed of 1–4-cells (mostly 3-celled), spherical to subspherical (1-celled), dumbbell
(2-celled), linearly arranged to triquetrous (3-celled), T-shaped to tetrahedron (4-celled), walls
pigmented, bearing conspicuous projections, entire or branched at the tips, 1–4 germ pores in each
cell, basidia external.
Type genus – Nyssopsora Arthur (1906).
Type species – Nyssopsora echinata (Lév.) Arthur (1906).
Nyssopsoratoonae Sanjay & Raghv. Singh, sp. nov. Figs 1–8
Index Fungorum number: IF559435; Facesoffungi number: FoF12771
Etymology – species epithet is derived from the name of the host genus.
Diagnosis – Differs from all the Nyssopsora spp. due to occurrence of wide range of cells (1–
4) and diverse shape in teliospores: spherical to subspherical (1-celled), dumbbell (2-celled),
linearly arranged to triquetrous (3-celled), and T-shaped to tetrahedron (4-celled).
Holotype – AMH 10124
Spermogonia and aecidia unknown. Infection spots hypophyllous, blackish to dark blackish brown,
velvety, initially marginal, later scattered on lamina, more or less circular to subcircular, later on
coalesce to become irregular, necrotic, 1–4 mm diam. Mycelium internal. Colonies hypogenous,
subepidermal in origin and erumpent, pulverulent, dark blackish brown when spores are abundant.
Uredinia hypophyllous, 1–4 mm diam., formed in early stage of infection and telia at later stage,
loosely or densely aggregated, subepidermal in origin, erumpent and exposed early, pulverulent,
blackish brown to black. Urediniospore mostly circular to orbicular, oval, 20–24 × 17–24(–27) µm,
wall uniformly thick, (1.2–)2–3.5(–3.8) µm, pale yellow to dark brown, surface minutely
echinulate, germ pores not seen, pedicilate, pedicels up to 16 × 6–9 µm. Telia hypophyllous, 1–4
mm diam., subepidermal in origin and early exposed, densely aggregated in irregular groups,
pulverulent, blackish brown to black. Teliospores borne singly on pedicels, 1–4-celled, mostly 3-
celled with a single proximal cell and surmounted by two distal cells, 7.5–40 × 9–30 µm, diverse
shapes [1-celled (spherical to subspherical): 7.5–27 × 9–25 µm; 2-celled (dumbbell): (20–)30–32(–
35) × (14–)18–23(–25) µm, 3-celled (linearly arranged): (30–)32–35(–40) × (15–)20–22(–24)
µm;3-celled (triquetrous): (30–)32–33(–35) × (18–)20–28(–30) µm; 4-celled (T-shaped): (36–)37–
38(–40) × (19–)20–26(–28) µm and 4-celled (tetrahedron): (28–)30–33(–35) × (18–)19–24(–26)
µm], wall (1.5–)2.5–4(–5) µm thick, strongly constricted at the septa, initially light brown, dark
brown to blackish brown at maturity; with approx 40–60 projections on each spore, mostly 2–8-
furcated at tip, 1.5–6 µm long; often barely visible 1–2 germ pores in each cell, appearing near or at
the inner angles; pedicles subhyaline to olivaceous, smooth to striated, persistent, up to 85 µm long,
(4–)6–10(–18) µm wide.
535
Material examined – India, Uttarakhand, Chamoli, Govindghat, 30.6185°N, 79.5617 E, on
living leaves of Toona sinensis (Juss.) M. Roem. (Meliaceae), December 2018, coll. Sanjay Yadav,
AMH 10124 (holotype), MH-BHU 6 (isotype).
Fig. 1 – Symptoms of Nyssopsora toonae on Toona sinensis (AMH 10124, holotype). a, b Host
Plant in natural habitat. c, d Rust pustules on the lower surface of leaf. e Symptom limited to leaf
margin. f Symptom mostly limited to midrib or vein. g, h Close-up of leaf surface showing telia.
Scale bars = 10 mm.
536
Fig. 2 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a–b Telia on leaflets of
Toonasinensis. Scale bars: a = 10 µm, b = 20 µm.
Fig. 3 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a Transverse section of
uredinium with two mature teliospores. b, c Transverse section of telium. d–f Stalked
Urediniospores. g–k Urediniospores. Scale bars = 10 µm.
537
Fig. 4 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a, b 1-celled teliospores.
c–l Different forms of 2-celled teliospores. Scale bars = 10 µm.
538
Fig. 5 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a–h Different forms of 3-
celled triquetrous teliospores. Scale bars = 10 µm.
539
Fig. 6 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a–f Different forms of 3-
celled linearly arranged teliospores. Scale bars = 10 µm.
Fig. 7 – Nyssopsora toonae, microphotographs (AMH 10124, holotype). a–c Different forms of 4-
celled T-shaped teliospores. d 4-celled tetrahedron teliospore. Scale bars = 10 µm.
540
Fig. 8 – SEM characteristicsof Nyssopsora toonae (AMH 10124, holotype). a Telium.
b, c Urediniospore showing echinulate surface. d, e Different patterns of echinulation on the surface
of urediniospores. f 1-celled teliospore. g 2-celled teliospore. h 3-celled teliospore. i 4-celled
teliospore. j, k Projections on teliospores. Scale bars: a = 10 µm, b–j = 2 µm.
541
Fig. 9 – Consensus phylogram (50% majority rule) resulting from a maximum likelihood of the
combined three-gene (dataset 1: LSU-SSU-CO3) sequence alignments. The Bayesian posterior
probabilities (≥ 0.50; BI-PP) and maximum likelihood bootstrap support values (≥ 50%; ML-BS)
are given at the nodes (BI-PP/ML-BS). All taxa names are written in black, newly introduced
species is represented in bold and novel family denoted in blue. The tree is rooted with
542
Eocronartium muscicola. Families are indicated by coloured blocks; dashed lines indicate
uncertainty at the referenced nodes.
Fig. 10 – Consensus phylogram (50% majority rule) resulting from a maximum likelihood of the
combined four-gene (dataset 1: LSU-SSU-CO3-ITS) sequence alignments. The Bayesian posterior
probabilities (≥ 0.50; BI-PP) and maximum likelihood bootstrap support values (≥ 50%; ML-BS)
543
are given at the nodes (BI-PP/ML-BS). All taxa names are written in black, newly introduced
species is in bold and novel family denoted in blue. The tree is rooted with Eocronartium
muscicola. Families are indicated by coloured blocks; dashed lines indicate uncertainty at the
referenced nodes.
Discussion
In light of current concept (Aime & McTaggart 2020), the present phylogenetic analyses used
more species and genera, including Nyssopsora and Triphragmium, to find out the exact placement
of all the Nyssopsora spp. in Pucciniales. From both the datasets it is clear that all the Nyssopsora
spp. are clustered together and separated as an independent lineage with strong statistical supports,
not known in Pucciniales. Hence, it is justified to introduce a new family Nyssopsoraceae to
accommodate all the Nyssopsora and allied species having 1–4-celled pedicellate teliospores
bearing conspicuous projections (spines) on its surface (Figs 9, 10). Moreover, the members of
Nyssopsoraceae are separated as a sister lineage of Pucciniaceae Chevall. with very low statistical
supports (Figs 9, 10). Members of Pucciniaceae can be easily distinguished from Nyssopsoraceae
in having typically with 1 or 2 celled teliospores (Aime & McTaggart 2020).
The type species of the genus Triphragmium, T. ulmariae (DC.) Link clustered within the
Phragmidiaceae clade (Figs 9, 10) and was already transferred to this family by Maier et al. (2003).
The genera Nyssopsora and Triphragmium, which were originally assigned to
Sphaerophragmiaceae, are now excluded (Figs 9, 10) and support the current concepts of Aime &
McTaggart (2020).
A total of 12 valid species of Nyssopsora have been reported across the world until now
based on morphological data alone (Ngachan & Goswami 1985, Lohsomboon et al. 1990, Baiswar
et al. 2014, Carvalho et al. 2014, Phetruang et al. 2019, Tykhonenko et al. 2021). Molecular
sequence data of all species are necessary in order to get taxonomically sound decisions, but limited
molecular sequence data are available viz., N. echinate (SSU), N. koelreuteriae (ITS) and
N. thwaitesii (SSU, LSU & ITS) (Swann & Taylor 1995, Wingßeld et al. 2004, Baiswar et al.
2014).
Nyssopsora cedrelae and N. toonae both are reported on the same host species Toona sinensis
(≡ Cedrela sinensis), but the former species differs as later have wide range of cells (1–4) and
diverse forms of shape in teliospores: spherical to subspherical (1-celled), dumbbell (2-celled),
linearly arranged to triquetrous (3-celled), and T-shaped to tetrahedron (4-celled). Such features are
not reported to any species of the Nyssopsora (Tables 2, 3).
Analytical studies recognize, N. toonae as a separate and undescribed species showing strong
support of its taxonomic position within genus Nyssopsora. With blast search in GenBank, no
sequence identical to any of the investigated genes of this species was encountered. However, the
formation of wide range of cells (1–4) and the diverse forms of shape in teliospores (spherical to
subspherical, dumbbell, linear to triquetrous and T-shaped to tetrahedron shaped) are the additional
striking features of N. toonae that easily distinguish it from other Nyssopsora spp. (Table 2).
Acknowledgements
The authors are indebted to anonymous reviewers for helpful comments and the curator of
AMH for accepting material and providing an accession number there off. We express our deep
gratitude to Dr. Konstanze Bensch (Westerdijk Fungal Biodiversity Institute, Uppsalalaan,
Netherlands) for nomenclatural review. We are also thankful to the Head, and Coordinator, CAS in
Botany, Banaras Hindu University, Varanasi for Instrumental facilities. RS thanks Science &
Engineering Research Board (SERB), Department of Science & Technology (DST), Govt. of India
(Scheme No. CRG/2020/006053) and Institution of Eminence (IoE) Scheme, Ministry of Human
Resource and Development (MHRD), Govt. of India (No. R/Dev/D/IoE/Incentive/2021-22/32387)
for providing financial support.
544
Table 3 Spore states, hosts and distribution of Nyssopsora species.
I = Aecial state, II = Uredinial state, III = Telial state
Nyssopsora spp.
State
Host families
Hosts
Distribution
References
asiatica
III
Araliaceae
Acanthopanax sciadophylloides, Aralia chinensis var.
canescens, A. chinensis var. glabrescens, A. cordata, A. elata,
A. spinosa, Evodiopanax innovans, Kalopanax innovans,
Merrilliopanax listeri
East Asia, U.S.S.R.
Ito (1950), Tai (1979),
Lohsomboon et al. (1990)
cedrelae
I, II, III
Anacardiaceae
Meliaceae
Simaroubaceae
Ailanthus altissima, Cedrela serrata, C. sinensis, Cedrela sp.,
Choerospondias axillaris
South Asia, East
Asia
Ito (1950), Lütjeharms (1937),
Tai (1979), Sydow & Sydow
(1912)
citriobati
III
Pittosporaceae
Citriobatus pauciflorus, C. multiflorus
Eastern Australia
Sydow (1938)
clavellosa
III
Araliaceae
Rosaceae
Aralia nudicaulis, A. racemosa, Prunus sp.
North America
Arthur (1934), Lütjeharms (1937),
Zeller (1935)
echinata
III
Apiaceae
Coelopleurum gmelini, Conioselinum scopulorum,
C. pacificum, C. scopulorum, Ligusticum apiodorum,
L. filicinum, L. leibergii, L. mutellina, L. porteri, L. prpureum,
L. scopulorum, Ligusticum sp., Meum athamanticum,
M. mutellina, Oenanthe californica, O. sarmentosa var.
californica, Selinum pacificum
Europe, North
America
Lütjeharms (1937), Sydow &
Sydow (1912), Wilson &
Henderson (1966)
eocaenica
III
–
Sakhalinian amber of Eocene
East Asia
Tykhonenko et al. (2021)
formosana
II, III
Sapindaceae
Koelreuteria bipinnata, K. formosana
East Asia
Lütjeharms (1937),
Sawada (1931)
koelreuteriae
II, III
Sapindaceae
Koelreuteria bipinnata, K. paniculata, Koelreuteria sp.
East Asia
Sydow & Sydow (1912),
Lohsomboon et al. (1990)
panamensis
II, III
Anacardiaceae
Astronium graveolens
Central America
Carvalho et al. (2014)
thirumalacharii
III
Araliaceae
Brassaiopsis griffithii
South Asia
Ngachan & Goswami (1985)
thwaitesii
III
Araliaceae
Rubiaceae
Brassaiopsis hainla, Hedera vahlii, Heptapleurum ellipticum,
H. stellatum, H. venulosum, Heptapleurum sp., Schefflera
bengalensis, S. elliptica, S. leucantha, S. lucescens, S. odorata,
S. polybotrya, S. roxburgii, S. scandens, S. stellata, S.
venulosum, S. wallichiana, Schefflera sp., Neonauclea
bartlingii
South Asia, South-
east Asia
Monson (1974), Sydow (1921),
Tai (1979), Berkeley & Broome
(1875), Ngachan & Goswami
(1985), Bagyanarayana et al.
(1987), Baiswar et al. (2014),
Lohsomboon et al. (1990),
Phetruang et al. (2019)
toonae
II, III
Meliaceae
Toona sinensis
South Asia
In this communication
trevesiae
III
Araliaceae
Trevesia sundaica
South-east Asia
Boedijn (1959), Gäumann (1921)
545
References
Aime MC. 2006 – Toward resolving family-level relationships in rust fungi (Uredinales).
Mycoscience 47, 112–122. Doi 10.1007/S10267-006-0281-0
Aime MC, Bell CD, Wilson AW. 2018 – Deconstructing the evolutionary complexity between rust
fungi (Pucciniales) and their plant hosts. Studies in Mycology 89, 143–152.
Doi 10.1016/j.simyco.2018.02.002
Aime MC, Matheny PB, Henk DA, Frieders EM et al. 2006 – An overview of the higher-level
classification of Pucciniomycotina based on combined analyses of nuclear large and small
subunit rDNA sequences. Mycologia 98, 896–905. Doi 10.3852/mycologia.98.6.896
Aime MC, McTaggart AR. 2020 – A higher-rank classification for rust fungi, with notes on genera.
Fungal systematic and evolution 7, 21–47. Doi 10.3114/fuse.2021.07.02
Aime MC, McTaggart AR, Mondo SJ, Duplessis S. 2017 – Phylogenetics and phylogenomics of
rust fungi. Advances in Genetics100, 267–307. Doi 10.1016/bs.adgen.2017.09.011
Arthur JC. 1906 – Eine auf die Struktur und Entwicklungsgeschichte begründete Klassifikation der
Uredineen. Resultats Scientifiques du Congres International de Botanique Vienne, pp. 331–
348.
Arthur JC. 1934 – Manual of the Rusts in United States and Canada. New York, U.S.A.: Hafner
Publishing Company.
Bagyanarayana G, Subbalakshmi G, Ramachar P, Hosagoudar VB. 1987 – Nyssopsora scheflerae
sp. nov. from India. Current Science 56, 1022–1023.
Baiswar P, Ngachan SV, Chandra S. 2014 – Identification of Nyssopsora thwaitesii on Schefflera in
northeast India. Australasian Plant Disease Notes 9, 124. Doi 10.1007/s13314-014-0124-3
Beenken L. 2017 – Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed
within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa 297, 053–061.
Doi 10.11646/phytotaxa.297.1.5
Beenken L, Wood AR. 2015 – Puccorchidium and Sphenorchidium, two new genera of Pucciniales
on Annonaceae related to Puccinia psidiiand the genus Dasyspora. Mycological Progress14,
1–13. Doi 10.1007/s11557-015-1073-8
Beenken L, Zoller S, Berndt R. 2012 – Rust fungi on Annonaceae II: the genus Dasyspora Berk. &
M. A. Curtis. Mycologia 104, 659–681. Doi 10.3852/11-068
Bennett C, Aime MC, Newcombe G. 2011 – Molecular and pathogenic variation within
Melampsora on Salix in western North America reveals numerous cryptic species. Mycologia
103, 1004–1018. Doi 10.3852/10-289
Berkeley M, Broome CE. 1875 – Enumeration of the fungi of Ceylon, part 11. Journal of the
Linnean Society, Botany 14, 29–140. Doi 10.1111/j.1095-8339.1873.tb00301.x
Blomquist CL, Scholler M, Scheck HJ. 2015a – Detection of rust caused by Tranzschelia mexicana
on Prunus salicifolia in the United States. Plant Disease 99, 1856.
Doi 10.1094/PDIS-03-15-0256-PDN
Blomquist CL, Rooney-Latham S, Scheck HJ, Adler K. 2015b – First report of the rust Uromyces
plumbarius on Gaura lindheimeri in California. Plant Disease 100, 531–531.
Doi 10.1094/pdis-06-15-0682-pdn
Boedijn KB. 1959 – The Uredinales of Indonesia. Nova Hedwigia 1, 463–496.
Bubner B, Buchheit R, Friedrich F, Kummer V, Scholler M. 2019 – Species identification of
European forest pathogens of the genus Milesina (Pucciniales) using urediniospore
morphology and molecular barcoding including M. woodwardiana sp. nov. MycoKeys 48,
1–40. Doi 10.3897/mycokeys.48.30350
Carvalho Jr AA, Esquivel-Rios E, Piepenbring M. 2014 – New species of Nyssopsora (Pucciniales)
from Panama. Nova Hedwigia 99, 65–70. Doi 10.1127/0029-5035/2014/0174
Cummins GB, Hiratsuka Y. 1983 – Illustrated genera of rust fungi. 2nd ed. APS Press, St Paul,
Minnesota.
546
Cummins GB, Hiratsuka Y. 2003 – Illustrated genera of rust fungi. 3rd ed. APS Press, St. Paul,
Minnesota.
Cunningham GH. 1931 – The rust fungi of New Zealand, together with the biology, cytology and
therapeutics of the Uredinales. John McIndoe, NZ.
Deadman ML, Al Sadi AM, Al Maqbali YM, Farr DF, Aime MC. 2011 – Additions to the rust
fungi (Pucciniales) from northern Oman. Sydowia 63, 155–168.
Demers JE, Romberg MK, Castlebury LA. 2015 – Microcyclic rusts of hollyhock (Alcea rosea).
IMAfungus 6, 477–482. Doi 10.5598/imafungus.2015.06.02.11
Dixon LJ, Castlebury LA, Aime MC, Glynn NC, Comstock JC. 2010 – Phylogenetic relationships
of sugarcane rust fungi. Mycological Progress 9, 459–468. Doi 10.1007/s11557-009-0649-6
Doungsa-Ard C, McTaggart AR, Geering ADW, Shivas RG. 2018 – Diversity of gall-forming rusts
(Uromycladium, Pucciniales) on Acacia in Australia. Persoonia-Molecular Phylogeny and
Evolution of Fungi 40, 221–238. Doi 10.3767/persoonia.2018.40.09
Ebinghaus M, Begerow D. 2018 – Ravenelia piepenbringiae and Ravenelia hernandezii, two new
rust species on Senegalia (Fabaceae, Mimosoideae) from Panama and Costa Rica. MycoKeys
41, 51–63. Doi 10.3897/mycokeys.41.27694
Ebinghaus M, Maier W, Wingfield MJ, Begerow D. 2018 – New host associations and a novel
species for the gall-inducing acacia rust genus Ravenelia in South Africa. MycoKeys 43, 1–
21. Doi 10.3897/mycokeys.43.25090
Ebinghaus M, Wingfield MJ, Begerow D. 2020 – The genus Ravenelia (Pucciniales) in South
Africa. Mycological Progress 19, 259–290. Doi 10.1007/s11557-020-01556-w
Fernandez JL, Alvarado P. 2016 – First DNA sequences of Gymnosporangium amelanchieris and
G. gracile. Boletin de la Sociedad Micologica de Madrid 40, 105–119.
Gäumann E. 1921 –Mykologische Mitteilungen I. Bulletin du lardin Botanique de Buitenzorg, Ser.
111, 3(2), 121–122.
Gautam AK, Avasthi S, Verma RK, Devadatha B et al. 2021 – Current status of research on rust
fungi (Pucciniales) in India. Asian Journal of Mycology 41, 40–80.
Hall T. 2007 – Bioedit, Version 7.0.9. [Online]. Ibis Biosciences, Carlsbad, 1997–2007.
http://www.mbio.ncsu.edu/ BioEdit/bioedit.html
Henk DA, Vilgalys R. 2007 – Molecular phylogeny suggests a single origin of insect symbiosis in
the Pucciniomycetes with support for some relationships within the genus Septobasidium.
American Journal of Botany 94, 1515–1526. Doi 10.3732/ajb.94.9.1515
Hernandez J, Aime M, Newbry B. 2004 – Aecidium kalanchoe sp. nov., a new rust on Kalanchoe
blossfeldiana (Crassulaceae). Mycological Research 108, 846–848.
Doi 10.1017/S0953756204000681
Ishaq A, Aime MC, Ayala EK, Ullah S et al. 2020 – First report of Asian pistachio rust (Pileolaria
pistaciae) in Pakistan. Canadian Journal of Plant Pathology 42, 210–217.
Doi 10.1080/07060661.2019.1647882
Ito S. 1950 – Mycologicai Flora of Japan 2, no. 3. Yokendo, Tokyo, Japan.
Katoh K, Toh H. 2010 – Parallelization of the MAFFT multiple sequence alignment program.
Bioinformatics 26, 1899–1900. Doi 10.1093/bioinformatics/btq224
Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008 – Dictionary of the Fungi. Wallingford, UK:
CAB International.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018 – MEGA X: Molecular Evolutionary
Genetics Analysis across computing platforms. Molecular Biology and Evolution 35, 1547–
1549. Doi 10.1093/molbev/msy096
Link HF. 1825 – Caroli a Linné Species Plantarum exhibentesPlantas Rite Cognitas ad Genera
Relatas. 6, 1–128.
Liu M, McCabe E, Chapados JT, Carey J et al. 2015 – Detection and identification of selected
cereal rust pathogens by TaqMan® real-time PCR. Canadian Journal of Plant Pathology 37,
92–105. Doi 10.1080/07060661.2014.999123
547
Lohsomboon P, Kakishima M, Ono Y. 1990 – A revision of the genus Nyssopsora (Uredinales).
Mycological Research 94, 907–922. Doi 10.1016/S0953-7562(09)81305-1
Lohsomboon P, Kakishima M, Ono Y. 1994 – A monograph of Sphaerophragmium (Uredinales).
Mycological Research 98, 907–919. Doi 10.1016/S0953-7562(09)80262-1
Lütjeharms WJ. 1937 – Vermischte Mykologische Notizen I, Ueber die Gattung Nyssopsora
(Pucciniaceae). Blumea, Supplement 1, 142–161.
Maier W, Begerow D, Weiss M, Oberwinkler F. 2003 – Phylogeny of the rust fungi: an approach
using nuclear large subunit ribosomal DNA sequences. Canadian Journal of Botany 81,
12–23. Doi 10.1139/b02-113
Maier W, McTaggart AR, Roux J, Wingfield MJ. 2016 – Phakopsora myrtacearum sp. nov., a
newly described rust (Pucciniales) on eucalypts in eastern and southern Africa. Plant
Pathology 65, 189–195. Doi 10.1111/ppa.12406
Matheny PB, Gossmann JA, Zalar P, Kumar TA et al. 2006 – Resolving the phylogenetic position
of the Wallemiomycetes: an enigmatic major lineage of Basidiomycota. Botany 84, 1794–
1805. Doi 10.1139/b06-128
McTaggart AR, Beasley DR, Wingfield MJ, Wood AR et al. 2017 – A dynamic, web-based
resource to identify rust fungi (Pucciniales) in southern Africa. MycoKeys 26, 77–83.
Doi 10.3897/mycokeys.26.14602
McTaggart AR, Doungsa-Ard C, Geering ADW, Aime MC et al. 2015 – A co-evolutionary
relationship exists between Endoraecium (Pucciniales) and its Acacia hosts in Australia.
Persoonia 35, 50–62. Doi 10.3767/003158515X687588
McTaggart AR, Geering ADW, Shivas RG. 2014 – Uredinopsis pteridis and Desmella aneimiae,
the first rust fungi (Pucciniales) reported on ferns (Pteridophyta) in Australia. Australasian
Plant Disease Notes 9, 1–4. Doi 10.1007/s13314-014-0149-7
McTaggart AR, Shivas RG, Doungsa-ard C. 2016 – Identification of rust fungi (Pucciniales) on
species of Allium in Australia. Australasian Plant Pathology 45, 581–592.
Doi 10.1007/s13313-016-0445-0
McTaggart AR, Shivas RG, van der Nest MA, Roux J et al. 2016 – Host jumps shaped the diversity
of extant rust fungi (Pucciniales). New Phytologist 209, 1149–1158. Doi 10.1111/nph.13686
Monson HL. 1974 – The species of Triphragmium, Nyssopsora, and Triphragmiopsis.
Mycopathologia et mycologia applicata 52, 115–131. Doi 10.1007/BF02128054
Ngachan SV, Goswami RN. 1985 – Nyssopsora thirumalacharii – a new rust from India. Indian
Phytopathology 38, 186–187.
Ono Y, Ohmachi K, Unartngam J, Okane I et al. 2020 – Milesina thailandica, a second rust fungus
on an early diverged leptosporangiate fern genus, Lygodium, found in Thailand. Mycological
Progress 19, 147–154. Doi 10.1007/s11557-019-01549-4
Padamsee M, McKenzie EH. 2014 – A new species of rust fungus on the New Zealand endemic
plant, Myosotidium, from the isolated Chatham Islands. Phytotaxa 174, 223–230.
Doi 10.11646/phytotaxa.174.4.3
Padamsee M, McKenzie EHC. 2017 – The intriguing and convoluted life of a heteroecious rust
fungus in New Zealand. Plant Pathology 66, 1248–1257. Doi 10.1111/ppa.12672
Pegg GS, Giblin FR, McTaggart AR, Guymer GP et al. 2014 – Puccinia psidii in Queensland,
Australia: disease symptoms, distribution and impact. Plant Pathology 63, 1005–1021.
Doi 10.1111/ppa.12173
Phetruang W, Haituk S, Kankavee P, Cheewangkoon R. 2019 – New record of Nyssopsora
thwaitesii on Schefflera leucantha and its colonization. Plant Pathology & Quarantine 9, 185–
191. Doi 10.5943/ppq/9/1/16
Rannala B, Yang Z. 1996 – Probability distribution of molecular evolutionary trees: a new method
of phylogenetic inference. Journal of Molecular Evolution 43, 304–311.
Doi 10.1007/PL00006090
548
Ronquist F, Teslenko M, van der Mark P, Ayres D et al. 2012 – MrBayes 3.2: Effcient Bayesian
phylogenetic inference and model choice across a large model space. Systematic Biology 61,
539–542. Doi 10.1093/sysbio/sys029
Sawada Y. 1931 – Descriptive catalogue of the Formosan fungi V. Department of Agriculture
Government Research Institute Formosa, Report 51, 52.
Scholler M, Aime MC. 2006 – On some rust fungi (Uredinales) collected in an Acacia koa–
Metrosideros polymorpha woodland, Mauna Loa Road, Big Island, Hawaii. Mycoscience 47,
159–165. Doi 10.1007/S10267-006-0286-8
Solano-Baez AR, Jiménez-Jiménez B, Camacho-Tapia M, Leyva-Mir SG et al. 2017 – First
confirmed report of Cerotelium fici causing leaf rust on Ficus carica in Mexico. Plant
Pathology & Quarantine 7, 160–163. Doi 10.5943/ppq/7/2/9
Souza ESC, Aime MC, Elias SG, Pinho DB et al. 2018 – Crossopsorella, a new tropical genus of
rust fungi. Phytotaxa375, 189–202. Doi 10.11646/phytotaxa.375.3.1
Stamatakis A. 2014 – RAxML version 8: a tool for phylogenetic analysis and post-analysis of large
phylogenies. Bioinformatics 30, 1312–1313. Doi 10.1093/bioinformatics/btu033
Swann EC, Taylor JW. 1995 – Phylogenetic perspectives on basidiomycete systematics: evidence
from the 18S rRNA gene. Canadian Journal of Botany 73(S1), 862–868. Doi 10.1139/b95-
332
Sydow H. 1921 – Die Verwertung der Verwandtschaftsverhältnisse und des gegenwärtigen
Entwicklungsganges zur Umgrenzung der Gattungen bei den Uredineen. Annales mycologici
19, 161–175.
Sydow H. 1938 – Neue oder bemerkenswerte australische Micromyceten. 111. Annales mycologici
36, 295–313.
Sydow P, Sydow H. 1912 – Monographia Uredinearum 3. Lipsiae, Germany: Fratres Brotraeger.
Tai FL. 1979 – Sylloge Frtngorum Sinicorurn. Peking, China: Science Press.
Tykhonenko Y, Hayova V, Ignatov M, Vasilenko D et al. 2021 – New species of rust fungi from
the middle Eocene Sakhalinian amber. Acta Palaeontologica Polonica 66, 92–924.
Doi 10.4202/app.00917.2021
van der Merwe M, Ericson L, Walker J, Thralla PH et al. 2007 – Evolutionary relationships among
species of Puccinia and Uromyces (Pucciniaceae, Uredinales) inferred from partial protein
coding gene phylogenies. Mycological Research 111, 163–175.
Doi 10.1016/j.mycres.2006.09.015
Vilgalys R, Hester M. 1990 – Rapid genetic identification and mapping of enzymatically amplified
ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172, 4239–4246.
Doi 10.1128/JB.172.8.4238-4246.1990
White TJ, Bruns T, Taylor J. 1990 – Amplification and direct sequencing of fungal ribosomal RNA
genes for phylogenetics. In: A guide to molecular methods and applications (Innis MA,
Gelfand DH, Sninsky JJ, White JW, eds). Academic Press, New York, pp. 315–322.
Doi 10.1016/B978-0-12-372180-8.50042-1
Wilson M, Henderson DM. 1966 – British Rust Fungi. London, U.K.: Cambridge University Press.
Wingfield BD, Ericson L, Szaro T, Burdor JJ. 2004 – Phylogenetic patterns in the Uredinales.
Australasian Plant Pathology 33, 327–335. Doi 10.1071/AP04020
Yang Y, Yang Y, Yu Y, Bi C. 2016 – First report of rust disease on Koelreuteria bipinnata caused
by Nyssopsora koelreuteriae in China. Plant Disease 100, 1014–1014.
Doi 10.1094/pdis-10-15-1182-pdn
Yun HY, Minnis AM, Kim YH, Castlebury LA et al. 2011 – The rust genus Frommeëlla revisited:
a later synonym of Phragmidium after all. Mycologia 103, 1451–1463. Doi 10.3852/11-120
Zeller SM. 1935 – Some miscellaneous fungi of the Pacific Northwest. Mycologia 27, 449–466.
Doi 10.1080/00275514.1935.12017091
Zheng W, Newcombe G, Hu D, Cao Z et al. 2019 – The first record of a north American poplar leaf
rust fungus, Melampsora medusae, in China Forests 10, 182. Doi 10.3390/f10020182
549
Zuluaga C, Buritica P, Marin M. 2011 – Phylogenetic analysis of rust fungi (Uredinales) from the
Colombian Andean region using 28S ribosomal DNA sequences. Revista de biologia tropical
59, 517–540.