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The rust genus
Frommee¨lla
revisited: a later synonym of
Phragmidium
after all
Hye Young Yun
Andrew M. Minnis
Systematic Mycology & Microbiology Laboratory, USDA-
ARS, B010A, 10300 Baltimore Avenue, Beltsville,
Maryland 20705
Young Ho Kim
Department of Agricultural Biotechnology, Seoul
National University, Seoul 151-921, Korea
Lisa A. Castlebury
Systematic Mycology & Microbiology Laboratory, USDA-
ARS, B010A, 10300 Baltimore Avenue, Beltsville,
Maryland 20705
M. Catherine Aime
1
Department of Plant Pathology and Crop Physiology,
Louisiana State University Agricultural Center, 302
Life Sciences Building, Baton Rouge, Louisiana 70803
Abstract
:
Frommee¨lla
(Phragmidiaceae, Pucciniales,
Basidiomycota), which currently includes two species
and is typified by
F. tormentillae
, causes rust on
members of tribe
Potentilleae
(Rosaceae). The genus
has been distinguished from
Phragmidium
on the
basis of having only one germ pore per teliospore cell
rather than two or three and by aecial characters.
Phylogenetic analyses of both currently accepted
Frommee¨lla
spp. with nLSU rDNA data suggest that
Frommee¨lla
was derived from within a clade represent-
ing
Phragmidium
. Thus
Frommee¨lla
should be consid-
ered to be a later generic synonym of
Phragmidium
.
Analyses also indicate that
Frommee¨lla tormentillae
on
Potentilla
species includes two taxa recognized herein
as
Phragmidium potentillae-canadensis
and
P. tormen-
tillae
.
Frommee¨lla mexicana
on
Potentilla
spp. formerly
classified in
Duchesnea
, is distinct from but sister to
the other two species. Based on data regarding type
specimens that were presented in a study by McCain
and Hennen, the new combination
Phragmidium
mexicanum
is proposed as the correct name for this
species. Necessary studies of original material were
made, and
Phragmidium potentillae-canadensis
is
lectotpyified and epitypified. Although considered
and expanded here, further examination of species
boundaries and host ranges of the fungi formerly
classified in
Frommee¨lla
is warranted.
Key words:
cinquefoil pathogens, fungal taxono-
my, rDNA systematics, rust fungi, Uredinales
INTRODUCTION
The Phragmidiaceae (Pucciniales, Basidiomycota) is
an economically important family of rust fungi that
occurs primarily on Rosaceae.
Phragmidium
, which is
a well known bane of
Rosa
and
Rubus
, is characterized
by dark brown teliospores that are typically festooned
with several transverse septa and 2–3 germ pores per
teliospore cell and usually
Caeoma
-type aecia with
catenulate aeciospores. Arthur (1917) segregated
species having one germ pore per teliospore cell
and
Uredo
-type aecia with aeciospores born singly
rather than in chains into the newly erected genus
Frommea
. Unfortunately numerous mycologists at the
time were confusing two taxa on
Potentilla
,
Phragmi-
dium potentillae
that represents a true
Phragmidium
and a morphological species representing the type of
the new genus
Frommea
that Arthur (1917) called
Frommea obtusa
(Laundon 1975). Because
Frommea
obtusa
was actually a synonym of
Phragmidium
potentillae
the new genus
Frommea
, typified by
F.
obtusa
, was also a synonym of
Phragmidium
(Laundon
1975). Cummins and Hiratsuka (1983) remedied this
situation when they erected the new genus
From-
mee¨lla
, which was typified by
F. tormentillae
, for the
taxa fitting Arthur’s concept of
Frommea
. Two species,
Frommee¨lla tormentillae
and
F. mexicana
, were includ-
ed in the latest revision of the genus (McCain and
Hennen 1990), and this was reiterated by Hennen et
al. (2005) who followed the study in their summary of
the genus.
The uredinial stage of an unknown rust fungus was
found recently on
Potentilla hebiichigo
(;
Duchesnea
chrysantha
) in Korea. Based on morphology and host,
the fungus was identified tentatively as
Phragmidium
potentillae
, which was reported previously on
D.
chrysantha
from Japan (Shirai and Miyake 1917). A
subsequent BLASTn analysis on GenBank with newly
generated nLSU rDNA (LSU) sequence data however
revealed the Korean rust was more closely related to
but distinct from a taxon represented by an existing
sequence identified as
Frommee¨lla mexicana
, a wide-
spread fungus on
Potentilla
species formerly placed in
the genus
Duchesnea
, rather than other species of
Phragmidium
. Hiratsuka et al. (1992) did not list
Phragmidium potentillae
on
Duchesnea
, and Shirai’s
and Miyake’s record (1917) might represent a
misidentification of host, fungus, or both. A detailed
taxonomic study of
Frommee¨lla
was made subsequently
with morphological data from new and existing
herbarium collections as well as newly generated
Submitted 13 Apr 2011; accepted for publication 20 May 2011.
1
Corresponding author. E-mail: maime@agcenter.lsu.edu
Mycologia,
103(6), 2011, pp. 1451–1463. DOI: 10.3852/11-120
#
2011 by The Mycological Society of America, Lawrence, KS 66044-8897
1451
DNA sequence data to enhance the current under-
standing of the genus. When necessary, studies of
original material and typifications were performed.
MATERIALS AND METHODS
Taxon sampling.—
New collections of rust fungi including
materials representing
Frommee¨lla
spp. bearing uredinial
and telial stages were made and preserved following the
methods of Cummins and Hiratsuka (1983) and deposited
into herbaria BPI and LSUM. Historical material examined
for morphological characters is housed at BPI. (See Farr
and Rossman 2011 for additional collection data not found
in the specimens examined section or T
ABLE I.) Herbaria
acronyms follow Thiers (2011).
Morphology.—
Light microscopy (LM) was used to observe
microscopic characters of specimens. Herbarium materials
were rehydrated and viewed in 3% KOH. Whenever possible
a minimum of 15–30 structures were measured. Scion
Image beta 4.0.2 software (Scion Corp., Frederick, Mary-
land) was used to obtain the measurement data. Scanning
electron microscopy (SEM) images were produced accord-
ing to the methods of Yun et al. (2007). Color notes based
on both study of macroscopic and microscopic features are
based on terminology of Macbeth (2000) and indicated by
the notation (M) or they are general terminology from
collector or author notes and are not indicated by
parentheses.
DNA extraction, PCR amplification and sequencing.—
LSU
sequence data were generated from Korean material
according to the methods of Yun et al. (2007). Methods
and primers for DNA extraction, PCR and sequencing of
the LSU and in some cases the internal transcribed spacer
region 2 (ITS2) rDNA followed Aime (2006). Briefly, sori
were excised individually from dried herbarium material
and extracted with the UltraClean Plant DNA Isolation Kit
(MoBio Laboratories Inc., Solana Beach, California).
Primers Rust2inv (Aime 2006) and LR5 or LR6 (Vilgalys
and Hester 1990) were used for amplification and sequenc-
ing. Sequences were generated on an ABI 3130 genetic
analyzer (Applied Biosystems) from ethanol-precipitated
sequencing reactions, or PCR products were sent to
Macrogen Inc. (Korea) for sequencing on an ABI 3730XL.
Collection data for new material and GenBank accession
numbers for sequences used in this study are provided
(T
ABLE I).
Data editing and phylogenetic analysis.—
Sequences were
edited in Sequencher 4.1.4 (Gene Codes Corp., Ann Arbor,
Michigan). Additional sequences were obtained from
GenBank (http://www.ncbi.nlm.nih.gov/, T
ABLE I) to con-
tain as inclusive a representation of Phragmidiaceae and
Phragmidium
taxa as possible, including the type of
Phragmidium
,
P. mucr onatum
.
Kweilin gia divina
(Syd.)
Buritica´ was included as an outgroup given its supported
relationship as sister to Phragmidiaceae in Aime (2006).
After trimming the ends 979 bp of LSU were aligned with
MAFFT 6.5 with Q-INS-I (Katoh and Toh 2008) and assessed
visually in Se-Al 2.0a11 (Andrew Rambaut, Dept. Zoology,
Univ. Oxford, UK; http://evolve.zoo.ox.ac.uk/). Align-
ments are available from the corresponding author or
through TreeBASE (S11511). Maximum parsimony (MP)
analyses were conducted in PAUP* 4.0b10 (Swofford 2002)
as heuristic searches with 1000 random addition replicates
and TBR branch swapping. Support for branches was
evaluated by bootstrap analysis derived from 1000 MP
replicates with 10 random addition replicates each. Maxi-
mum likelihood (ML) analyses were conducted in RAxML-
HPC2 7.2.7 (Stamatakis 2006) via the CIPRES portal (Miller
et al. 2011) with default parameters adjusting for 1000
bootstrapping replicates.
RESULTS
Data matrix and phylogenetic analysis.—
ITS2 data
were obtainable only for seven of the 37 samples
selected for analyses, and these were not alignable
across the family; therefore this region was not used
in phylogenetic analyses. The LSU was completely
alignable across 979 bp of which 180 characters were
parsimony informative, 774 were constant and 25
were variable but uninformative. Thirty-six equally
parsimonious trees were found with a tree score of
392. ML and MP analyses were congruent in
supporting the species formerly placed in
Frommee¨lla
within
Phragmidium
and in consistently describing
three reciprocally monophyletic species within the
Frommee¨lla
group (FIG. 1). Differences between the
three
Frommee¨lla
species occur as SNPs or short indels
that appear fixed within species despite the broad
geographic range of samples.
TAXONOMY
Phragmidium Link, Magazin der Gesellschaft Natur-
forschenden Freunde Berlin 7:30. 1816. Typus
genericus:
Phragmidium mucronatum
(Pers.)
Schltdl.
5
Frommea
Arthur, Bull. Torrey Bot. Club 44:503. 1917.
Typus genericus:
Frommea obtusa
(F. Strauss) Arthur
5
Phragmidium potentillae
(Pers.) Grev. Note: Laundon
(1975) discussed the correct author citation for
P.
potentillae
.
5 Frommee¨lla
Cummins & Y. Hirats., Illus. Gen. Rust
Fungi, Revised Ed.: 120. 1983.
Typus genericus:
Frommee¨lla tormentillae
(Fuckel)
Cummins & Y. Hirats.
Phragmidium mexicanum (Mains) H.Y. Yun, Minnis
& Aime, comb. nov. F
IG.2
MycoBank MB561256
;
Frommea mexicana
Mains, Bull. Torrey Bot. Club
66:618. 1939 (basionym).
;
Frommee¨lla mexicana
(Mains) J.W. McCain & J.F.
Hennen, Mycotaxon 39:250. 1990.
1452 MYCOLOGIA
TABLE I. Collections used in phylogenetic analysis, locality, host, GenBank number and origin
Species Collection/Voucher No. Locality Host GenBank No. Origin
Gymnoconia peckiana
(Howe) Trotter
LD 1003
/BPI 879271 USA: MD
Rubus
sp. GU058010 Dixon et al. 2010.
" U-349
/BPI 747600 USA: MN
Rubus allegheniensis
JF907677 This study.
Kuehneola uredinis
(Link) Arthur
MCA 2830
/BPI 871104 USA: NC
Rubus argutus
DQ354551 Aime 2006.
" PBM 2577
NA NA AY745696 Unpublished.
Kweilingia divina MCA 2887
/BPI 871105 Costa Rica
Bambusa
sp. DQ354554 Aime 2006.
Phragmidium
biloculare
Dietel
& Holw.
U-564
/BPI 881121 USA: WA
Potentilla flabellifolia
JF907670 This study.
Phragmidium fragariae
(DC.) G. Winter
WM 1317
Europe
Potentilla sterilis
AF426217 Maier et al. 2003.
Phragmidium
fusiforme
J. Schro¨t.
NA Switzerland
Rosa pendulina
AJ715522 Ritz et al. 2005.
Phragmidium
ivesiae
Syd. & P. Syd.
U-35
/BPI 863637 USA: UT
Potentilla gracilis
JF907672 This study.
" U-1212
/BPI 877968 USA: ID
Potentilla gracilis
JF907673 This study.
Phragmidium
mexicanum
HY104
/BPI 881108 Korea
Potentilla hebiichigo
JF907671 This study.
" MCA 2495
/BPI 843829 USA: VA
Potentilla indica
JF907659 This study.
" MCA 2496
/BPI 843961 USA: MD
Potentilla indica
JF907660 This study.
" MCA 2812
/BPI 877884 USA: TN
Potentilla indica
JF907664 This study.
" MCA 3343
/LSUM
00127236
USA: TN
Potentilla indica
JF907665 This study.
" MCA 3674
/LSUM
00127238
USA: LA
Potentilla indica
JF907661 This study.
" MCA 3678
/LSUM
00127237
USA: LA
Potentilla indica
JF907662 This study.
" U-64
/BPI 843393 USA: MD
Potentilla indica
JF907663 This study.
Phragmidium
montivagum
Arthur
FO 47828
Europe
Rosa
cf.
woodsii
AF426213 Maier et al. 2003.
Phragmidium
mucronatum
C2
/TUB 012076 Germany
Rosa corymbifera
AJ715519 Ritz et al. 2005.
" P15
/TUB 012082 Germany
Rosa corymbifera
AJ715514 Ritz et al. 2005.
Phragmidium
potentillae-canadensis
MCA 2616
/BPI 877886 USA: NC
Potentilla
sp. JF907667 This study.
" MCA 2858
/BPI 877887 USA: NY
Potentilla
sp. JF907666 This study.
" MCA 2987
/BPI 877885 USA: MD
Potentilla canadensis
JF907668 This study.
Phragmidium rubi-idaei
(DC.) P. Karst.
WM 1024
Europe
Rubus idaeus
AF426215 Maier et al. 2003.
Phragmidium
sanguisorbae
(DC.) J.
Schro¨t.
ML 957
Europe
Sanguisorba minor
AF426216 Maier et al. 2003.
" U-1008
/BPI 872232 Germany
Sanguisorba minor
JF907674 This study.
Phragmidium
tormentillae
MCA 2786
/BPI 877888 USA: TN
Potentilla simplex
JF907669 This study.
"U-3
/BPI 843392 USA: MD
Potentilla canadensis
DQ354553 Aime 2006.
Phragmidium
tuberculatum
J.B. Mu¨ll.
M8
Germany
Rosa canina
AJ715511 Ritz et al. 2005.
" U-486
/BPI 877981 Germany
Rosa
sp. JF907675 This study.
Phragmidium violaceum
(Schultz) G. Winter
MCA 2922
/BPI 877816 USA: CA
Rubus pensilvanicus
EF672358 Aime and
Rossman 2007.
" WM 1037
Europe
Rubus fruticosus
AF426214 Maier et al. 2003.
Trachyspora intrusa
(Grev.) Arthur
MCA 2384
/BPI 843828 Switzerland
Alchemilla vulgaris
DQ354550 Aime 2006.
YUN ET AL.: THE GENUS
F
ROMMEE
¨
LLA
REVISITED 1453
5
Frommee¨lla mexicana
var.
indicae
J.W. McCain & J.F.
Hennen, Mycotaxon 39:251. 1990.
Anamorphic names:
Uredo duchesneae
(Arthur) J.W. McCain & J.F.
Hennen, Mycotaxon 39:252. 1990 as ‘(Arthur)
Sacc. & Trotter’. This combination cited by McCain
and Hennen (1990) does not exist in the cited
work, but inadvertently they were the first to validly
publish the combination since the requirements of
ICBN Art. 33 (McNeill et al. 2006) were fulfilled.
;
Kuehneola duchesneae
Arthur, N. Amer. Fl. 7:185. 1912.
;
Phragmidium duchesneae
(Arthur) P. Syd. & Syd.,
Monographia Uredinearum Vol. 3:93. 1915.
;
Frommea duchesneae
(Arthur) Arthur, Bull. Torrey Bot.
Club 44:504. 1917.
;
Frommea obtusa
f.
duchesneae
(Arthur) Arthur, Manual
of the Rusts in United States and Canada: 93. 1934.
Arthur (1934) did not clearly indicate the rank where
he made the new combination, but he mentions the
rank of form in the discussion of this taxon.
;
Frommee¨lla duchesneae
(Arthur) Yohem, Cummins &
Gilb., Mycotaxon 22:452. 1985.
;
Frommee¨lla obtusa-duchesneae
(Arthur) Buritica´, Rev.
Acad. Colomb. Cienc. 20:225. 1996. This name would
be invalid under ICBN Art. 35.1 as an infraspecific
taxon because there is no clear indication of rank and
illegitimate under ICBN Art. 52 via superfluous as a
nom. nov. The intention of Buritica´andPardo-
Cardona (1996) is unclear due to an erroneous use
of the hyphen perpetuated in some literature after
Arthur (1934) introduced a name at the rank of form.
Description.
Spermogonia epiphyllous on brown
necrotic spots, intraepidermal. Uredinia hypophyllous,
scattered to gregarious, at times becoming confluent,
subepidermal and erumpent becoming pulverulent,
circular, yellow (M) to reddish yellow (M), 0.1–1 mm
diam. Paraphyses present or absent, peripheral,
cylindrical, at times capitate, hyaline, walls thin and
smooth. Urediniospores 16.9–22.9 3 12.9–20.1
mm,
non-catenulate, globoid to obovoid, contents yellow
when fresh, walls hyaline, echinulate, 0.8–1.8
mmthick,
pores indistinct. Telia hypophyllous, scattered to
gregarious, at times becoming confluent, subepider-
mal and erumpent becoming pulverulent, circular,
brown (M) to dark reddish brown (M), 0.3–0.8 mm
diam. Paraphyses absent. Teliospores 51.4–84.3 3
23.1–28.4
mm, non-catenulate, clavate, cylindrical or
fusiform, at times slightly curved, obtuse at apices,
obtuse or tapering below at bases, 3–5(mostly 4)-celled
with transverse septa, walls constricted at septa, reddish
yellow (M), smooth, 4.8–6.5
mm thick at apices, 0.7–
2.2
mm thick on sides, pores one per cell with pores
central and apical in apical cells and pores immedi-
ately below apical septa in subapical cells, pedicels
persistent, terete or slightly tapering below, yellowish
or hyaline above and hyaline below, up to 72
mmlong.
Habitat and distribution.
Known primarily from
Potentilla indica
(
Duchesnea indica
). This is the first
report of this fungus on another host,
Potentilla
hebiichigo
(
Duchesnea chrysantha
), which also was
reclassified (Yonekura et al. 2008). Based on the
databases of Farr and Rossman (2011), this fungus is
widely distributed with reports from Africa, Asia,
Europe, North America, Oceania, South America,
etc. This represents the first report from Korea.
Collections examined
. REPUBLIC OF KOREA. GANG-
WON PROVINCE: Chuncheon, on
Potentilla hebiichigo
,21
Apr 2007, leg.
H
.
Y
.
Yun
,
HY104
(BPI 881108). USA.
LOUISIANA: East Baton Rouge Parish, Baton Rouge,
approx. 2 miles from LSU campus, Chris Clark residence,
on
Potentilla indica
, 12 Feb 2009, leg.
M
.
C
.
Aime
,
MCA 3674
(LSUM 00127238); 23 Mar 2009, leg.
M
.
C
.
Aime
,
MCA 3678
(LSUM 00127237, duplicate BPI 881496). MARYLAND:
Great Falls, Bear Island and C&O Canal, on
Potentilla
indica
, 10 Apr 2004, leg.
M
.
C
.
Aime
,
MCA 2496
(BPI 843961
as
Frommee¨lla mexicana
); Baltimore County, Granite, on
Potentilla indica
, 13 Oct 2001, leg.
J
.
R
.
Herna´ndez
,
JRH
2001-29
(U-64, BPI 843393 as
Frommee¨lla mexicana
).
TENNESSEE: Cosby, Gabes Mountain Trail, Great Smoky
Mountains National Park, on
Potentilla indica
, 29 Jun 2007,
leg.
M
.
C
.
Aime
,
MCA 3343
(LSUM 00127236); Knoxville,
University of Tennessee campus, outside Hesler Building,
on
Potentilla indica
, 08 Sep 2004, leg.
M
.
C
.
Aime
,
MCA 2812
(BPI 877884 as
Frommee¨lla mexicana
). VIRGINIA: Rich-
mond, on
Potentilla indica
, 27 Mar 2004, leg.
M
.
C
.
Aime
,
MCA 2495
(BPI 843829 as
Frommee¨lla mexicana
).
Notes.
Arthur (1912) was the first to recognize this
taxon as a distinct species,
Kuehneola duchesneae
,on
Duchesnea indica
,but
Duchesnea
is now classified in
Potentilla
(Erikkson et al. 2003). McCain and Hennen
(1990) provided the most recent taxonomic and
nomenclatural revision of this species, and they
recognized two varieties,
F. mexicana
var.
mexicana
and
F. mexicana
var.
indicae
, which were differentiated
primarily by the number of cells per teliospore with 2–
TABLE I. Continued
Species Collection/Voucher No. Locality Host GenBank No. Origin
" WM 1019
Europe
Alchemilla vulgaris
AF426219 Maier et al. 2003.
Triphragmium
ulmariae
(DC.) Link
MCA 2378
/BPI 881364 Italy undetr. Rosaceae JF907676 This study.
‘‘ WM 1027
Europe
Filipendula ulmaria
AF426219 Maier et al. 2003.
1454 MYCOLOGIA
4 in the former and 3–5 in the latter. McCain and
Hennen (1990) also noted that
F. mexicana
var.
mexicana
lacked uredinial paraphyses while
F. mex-
icana
var.
indicae
had a few. Because McCain and
Hennen (1990) treated the Mains (1939) species
based on
Frommea mexicana
and the Arthur (1912)
species based on
Kuehneola duchesneae
as a single
species with two varieties the new teleomorphic name,
FIG. 1. Phylogenetic tree based on maximum likelihood analyses of LSU sequences of Phragmidiaceae showing species
formerly placed in
Frommee¨lla
as derived from within
Phragmidium
. Origins of sequences are provided (TABLE I).
Kweilingia
divina
selected as outgroup. Numbers above branches indicate bootstrapping support (1000 replicates) for each node as ML/
MP.
YUN ET AL.: THE GENUS
F
ROMMEE
¨
LLA
REVISITED 1455
Frommee¨lla mexicana
var.
indicae
, had to be introduced
at that time because all homotypic synonyms of the
Arthur name were based on a type specimen bearing
only the anamorphic, uredinial stage in spite of
Arthur’s (1912) description of a telial state (ICBN
Art. 59).
At this time one species,
Phragmidium mexicanum
,
with no varieties is recognized because the presence
or absence of uredinial paraphyses was variable in the
studied material and no sequence differences were
found that would warrant the recognition of two
infraspecific taxa. Arthur (1925) similarly noted the
variable presence or absence of uredinial paraphyses
in this species. Additionally in the material on
Potentilla indica
examined for this study, five-celled
teliospores were not consistently encountered. Based
FIG. 2. Macroscopic and microscopic features of
Phragmidium mexicanum
. A. Uredinia on
Potentilla hebiichigo
(BPI
881108). B. Uredinia on
Potentilla hebiichigo
(BPI 881108). C. Surface structure of uredinium by SEM (scanning electron
microscopy). Bar 5 100
mm (BPI 881108). D. Surfaces of urediniospores by SEM. Bar 5 20 mm (BPI 881108). E. Surface of
urediniospore by SEM. Bar 5 2
mm (BPI 881108). F. Urediniospores by LM (light microscopy). Bar 5 20 mm (BPI 843393). G.
Telia on
Potentilla indica
(BPI 843393). H. Teliospores by LM. Bar 5 50 mm (BPI 843393).
1456 MYCOLOGIA
on the anamorphic nature of the type specimen of
Kuehneola duchesneae
that was reported by McCain
and Hennen (1990), we propose the new combina-
tion
Phragmidium mexicanum
for this fungus because
its basionym has priority at the species rank for the
holomorph (ICBN Arts. 11, 59).
Although the type locality of
Phragmidium mexica-
num
is Mexico, the host,
Potentilla indica
, is native to
andwidespreadintemperateandtropicalAsia,
especially southern and southeastern Asia (USDA
2011). The present Korean collection of this rust
species from another host,
Potentilla hebiichigo
, which
is confirmed with DNA sequence data, probably
represents a record of this fungus from near its
geographical origin.
Phragmidium potentillae-canadensis Dietel, Hedwigia
42:179. 1903. F
IG.3
Lectotypus of
Phragmidium potentillae-canadensis
(hic
designatus): USA. OHIO: Toledo, on leaves of
Potentilla canadensis
, 6 Sep 1902, leg.
F
.
D
.
Kelsey
,
Micromycetes Rariores Selecti Praecipere Scandi-
navici No. 634 (BPI 881493).
Epitypus of
Phragmidium potentillae-canadensis
(hic
designatus): USA. NEW YORK: Lake Erie State
Park, Brocton, on
Potentilla
sp., 19 Sep 2004, leg.
M
.
C
.
Aime
,
MCA 2858
(BPI 877887 as
Frommee¨lla
mexicana
).
Study of
Phragmidium potentillae-canadensis
(desig-
nated lectotype): Spermogonia were not observed.
Uredinia hypophyllous, scattered, subepidermal and
erumpent becoming pulverulent, circular, pale yellow
(M), 0.2–0.3 mm diam. Paraphyses absent. Uredinio-
spores 21.4–25 3 17.9–21.7
mm, non-catenulate,
globoid to obovoid, contents hyaline in old material,
walls hyaline, echinulate, 1.3–1.7
mm thick, pores
indistinct. Telia hypophyllous, scattered to gregari-
ous, subepidermal and erumpent becoming pulveru-
lent, circular, yellowish red (M), 0.1–0.4 mm diam.
Paraphyses absent. Teliospores 48.1–86.8 3 30.1–
33.3
mm, non-catenulate clavate, cylindrical or fusi-
form, at times slightly curved, obtuse at apices, obtuse
or tapering below at bases, 2–4(mostly 3)-celled with
transverse septa, walls constricted at septa, reddish
yellow (M) or yellowish brown, smooth, 5.0–5.7
mm
thick at apices, 1.7–2.8
mm thick on sides; pores one
per cell with pores central and apical in apical cells
and pores immediately below apical septa in subapical
cells, pedicels persistent, terete or slightly tapering
below, yellowish or hyaline above and hyaline below,
up to 61
mm long.
Description.
Spermogonia epiphyllous on dark red
necrotic spots, intraepidermal. Uredinia hypophyllous,
scattered to gregarious, at times becoming confluent,
subepidermal and erumpent becoming pulverulent,
circular, pale yellow (M), 0.1–0.5 mm diam. Paraphyses
present or absent, 34.4–41.2 3 9.1–10.6
mm, cylindri-
cal, at times capitate, hyaline, walls thin and smooth.
Urediniospores 19.6–24.3 3 17.5–22.5
mm, non-caten-
ulate, globoid to obovoid, contents yellow when fresh,
walls hyaline, echinulate, 1.4–1.5
mm thick, pores
indistinct. Telia hypophyllous, scattered to gregarious,
at times becoming confluent, subepidermal and
erumpent becoming pulverulent, circular, yellowish
red (M), 0.1–0.5 mm diam. Paraphyses absent.
Teliospores 50.1–94.2 3 27–35
mm, non-catenulate
clavate, cylindrical or fusiform, at times slightly curved,
obtuse at apices, obtuse or tapering below at bases, 2–
4(mostly 2–3)-celled with transverse septa, walls
constricted at septa, reddish yellow (M) or yellowish
brown, smooth, 4.3–6.0
mm thick at apices, 1.0–2.8 mm
thick on sides; pores one per cell with pores central
and apical in apical cells and pores immediately below
apical septa in subapical cells, pedicels persistent,
terete or slightly tapering below, yellowish or hyaline
above and hyaline below, up to 62
mmlong.
Habitat and distribution.
Known from
Potentilla
spp., especially
Potentilla canadensis
. This species is
known with certainty from eastern USA. This fungus is
reported for the first time from MD, NC and NY.
Collections examined
. USA. OHIO: Toledo, on leaves of
Potentilla canadensis
, 6 Sep 1902, leg.
F
.
D
.
Kelsey
, Micro-
mycetes Rariores Selecti Praecipere Scandinavici No. 634
(BPI 881493, designated lectotype). MARYLAND: Catoctin
Mountain National Park, Visitor Center, approx. 1000 ft.
elev., on
Potentilla canadensis
, 15 Sep 2005, leg.
M
.
C
.
Aime
and
C
.
Park
,
MCA 2987
(BPI 877885 as
Frommee¨lla
mexicana
). NORTH CAROLINA: near Asheville, 3100 ft.
elev., on
Potentilla
sp., 17 Jul 2004, leg.
M
.
C
.
Aime
,
MCA
2616
(BPI 877886 as
Frommee¨lla mexicana
). NEW YORK:
Lake Erie State Park, Brocton, on
Potentilla
sp., 19 Sep 2004,
leg.
M
.
C
.
Aime
,
MCA 2858
(BPI 877887 as
Frommee¨lla
mexicana
, designated epitype).
Notes.
Mycologists including Dietel (1903) and
Sydow and Sydow (1915) recognized two species on
Potentilla
as it was defined then that would be included
in the generic concept of
Frommee¨lla
. The first,
Phragmidium potentillae-canadensis
, was thought to be
an American species characterized by having relatively
fewer cells per teliospore (2–4) (Dietel 1903, Sydow
and Sydow 1915). The second,
Phragmidium tormentil-
lae
, was the well known European species, which is
characterized generally as having greater and more
variable numbers of cells per teliospore (2–7) (Sydow
and Sydow 1915). Arthur (1917) provided an extensive
synonym list for these taxa under
Frommea obtusa
and
stated that after observing teliospore cell numbers from
numerous collections there was no such difference.
Based on phylogenetic analyses,
Phragmidium
potentillae-canadensis
is one of two taxa recognized
Y
UN ET AL.: THE GENUS
F
ROMMEE
¨
LLA
REVISITED 1457
on
Potentilla
, exclusive of host species formerly
classified in
Duchesnea
, with
Frommee¨lla
characters.
Although the present sampling is small, the telio-
spores observed for this taxon correspond morpho-
logically to the previous concept of the American
species with 2–4 cells per teliospore (Dietel 1903,
Sydow and Sydow 1915). The teliospores of
P.
potentillae-canadensis
, which Sydow and Sydow
(1915) noted, tend to be somewhat more darkly
pigmented. The original material of
P. potentillae-
canadensis
was distributed in Vestegren’s exsiccatae
set, Micromycetes Rariores Selecti Praecipere Scandi-
navici, and it is conspecific based on morphology with
the sequenced collections. One of two of the
exsiccatae housed at BPI is designated as the
lectotype, and the telia-bearing collection associated
with DNA sequence data is designated as the epitype
to stabilize the application of this name. After
examining the list of synonyms provided by Sydow
and Sydow (1915) for this species and the original
material of
Aregma triarticulatum
(see
P. tormentillae
),
the correct name for this taxon is accepted as
Phragmidium potentillae
-
canadensis
, which we here
recognize as a distinct species.
FIG. 3. Macroscopic and microscopic features of
Phragmidium potentillae
-
canadensis
. A. Telia on
Potentilla
sp. (BPI 877887,
designated epitype). B. Teliospore by LM (light microscopy). Bar 5 50
mm. (BPI 877887, designated epitype). C. Uredinia on
Potentilla canadensis
(BPI 877885). D. Urediniospores and paraphyses by LM. Bar 5 20 mm (BPI 877885). E. Paraphyses of
uredinia by LM. Bar 5 30
mm (BPI 877885). F. Surface of urediniospore by LM. Bar 5 20 mm (BPI 881493, designated
lectotype). G. Teliospore by LM. Bar 5 50
mm (BPI 881493, designated lectotype). H. Teliospore by LM. Bar 5 50 mm (BPI
881493, designated lectotype).
1458 MYCOLOGIA
Phragmidium tormentillae Fuckel, Jahrb. Nas-
sauischen Vereins Naturk. 23–24:46. 1870. F
IG.4
;
Xenodochus tormentillae
(Fuckel) Magnus, Ber.
Deutsch. Bot. Ges. 17:179. 1899.
;
Kuehneola tormentillae
(Fuckel) Arthur, Re´sultats
Scientifiques du Congre`s International de Botanique
Vienne 1905: 342. 1906.
;
Frommee¨lla tormentillae
(Fuckel) Cummins & Y. Hirats.,
Illus. Gen. Rust Fungi, Revised Ed.: 147. 1983.
5
Aregma triarticulatum
Berk. & M.A. Curtis, Grevillea
3:51. 1874.
;
Phragmidium triarticulatum
(Berk. & M.A. Curtis) Farl.,
Bull. Bussey Inst. 1:433. 1876 as ‘(Berk. & M.A. Curtis)
Newton’. Farlow (1876) provided no indication that
Newton provided this name.
Study of
Phragmidium tormentillae
(original materi-
al): Spermogonia were not observed. Uredinia hypo-
phyllous, scattered, subepidermal and erumpent
becoming pulverulent, circular, pale yellow (M),
0.2–0.5 mm diam. Urediniospores 20.7–25.7 3 17.6–
21.7
mm, non-catenulate, globoid to obovoid, contents
hyaline in old material, walls hyaline, echinulate, 1.2–
1.9
mm thick, pores indistinct. Paraphyses absent.
Telia hypophyllous, scattered to gregarious, at times
becoming confluent, subepidermal and erumpent
FIG. 4. Macroscopic and microscopic features of
Phragmidium tormentillae
. A. Sori on
Potentilla canadensis
(BPI 843392). B.
Uredinia on
Potentilla canadensis
(BPI 843392). C. Urediniospores by LM (light microscopy). Bar 5 20 mm (BPI 843392). D.
Telium on
Potentilla simplex
(BPI 877888). E. Teliospores by LM. Bar 5 30 mm (BPI 877888). F. Teliospore by LM. Bar 5 30 mm
(Fungi Rhenani No. 2227, original material of
Phragmidium tormentillae
, BPI). G. Teliospore by LM. Bar 5 30 mm (Fungi
Rhenani No. 2227, original material of
Phragmidium tormentillae
, BPI).
YUN ET AL.: THE GENUS
F
ROMMEE
¨
LLA
REVISITED 1459
becoming pulverulent, circular, dark reddish brown
(M), 0.2–0.5 mm diam. Paraphyses absent. Telio-
spores 49.1–75.3 3 29.1–34.6
mm, non-catenulate,
clavate, cylindrical or fusiform, at times slightly
curved, obtuse at apices, obtuse or tapering below at
bases, 2–3(mostly 3)-celled with transverse septa, walls
slightly constricted at septa, brownish yellow, smooth,
4.3–5.4
mm thick at apices, 1.5–2.5 mm thick on sides,
pores one per cell with pores central and apical in
apical cells and pores immediately below apical septa
in subapical cells, pedicels persistent, terete or slightly
tapering below, yellowish or hyaline above and
hyaline below, up to 26 mm long.
Study of
Aregma triarticulatum
(original material):
Spermogonia were not observed. Uredinia hypophyl-
lous, scattered to gregarious, at times becoming
confluent, subepidermal and erumpent becoming
pulverulent, circular, pale yellow (M), 0.1–0.5 mm
diam. Urediniospores 16.1–26.9 3 15.8–26.8
mm, non-
catenulate, globoid to obovoid, contents hyaline in
old material, walls hyaline, echinulate, 1.5–1.8
mm
thick, pores indistinct. Paraphyses absent. Telia
hypophyllous, scattered to gregarious, at times be-
coming confluent, subepidermal and erumpent be-
coming pulverulent, circular, brown (M), 0.1–0.5 mm
diam. Paraphyses absent. Teliospores 50.4–95.3 3
29.1–36.5
mm, non-catenulate, clavate, cylindrical or
fusiform, at times slightly curved, obtuse at apices,
obtuse or tapering below at bases, 2–5(mostly 3–4)-
celled with transverse septa, walls slightly constricted
at septa, brownish yellow, smooth, 5–9.5
mm thick at
apices, 1.5–3
mm thick on sides, pores one per cell
with pores central and apical in apical cells and pores
immediately below apical septa in subapical cells,
pedicels persistent, terete or slightly tapering below,
yellowish or hyaline above and hyaline below, up to
71.5
mm long.
Description.
Spermogonia epiphyllous, on purple
necrotic spots, intraepidermal. Aecia epiphyllous and
otherwise like uredinia. Uredinia hypophyllous and
petiolicolous, scattered to gregarious, at times becom-
ing confluent, subepidermal and erumpent becoming
pulverulent, circular, yellowish, 0.3–0.5 mm diam.
Paraphyses absent. Urediniospores 20.3–25.7 3 18.3–
21.6
mm, non-catenulate, globoid to obovoid, contents
yellow when fresh, walls hyaline, echinulate, 1.0–1.7
mm
thick, pores indistinct. Paraphyses absent. Telia hypo-
phyllous, scattered to gregarious, at times becoming
confluent, subepidermal and erumpent becoming
pulverulent, circular, dark brown (M), 0.1–0.2 mm
diam. Teliospores 41.4–92.3 3 27–34.7
mm, non-
catenulate, clavate, cylindrical or fusiform, at times
slightly curved, obtuse at apices, obtuse or tapering
below at bases, 2–6(mostly 3–4)-celled with transverse
septa, walls slightly constricted at septa, reddish-yellow
(M) or brownish yellow, smooth, 4.1–6.3
mm thick at
apices, 1.0–2.7
mm thick on sides, pores one per cell
with pores central and apical in apical cells and pores
immediately below apical septa in subapical cells,
pedicels persistent, terete or slightly tapering below,
yellowish or hyaline above and hyaline below, up to
45
mmlong.
Habitat and distribution.
Known from several spe-
cies of
Potentilla
. Based on the databases of Farr and
Rossman (2011), this fungus is known from Europe,
North America, and Oceania, but historical records
must be considered with caution considering confu-
sion with other taxa. This work also confirms reports of
P. tormentillae
(as
Frommea obtusa
) in MD, PA and TN
(Arthur 1934).
Collections examined
. CZECHOSLOVAKIA. Bohemia,
Velenka, near Sadska´, on leaves of
Potentilla tormentillae
,
05 Sep 1901, leg.
F. Buba´k
(BPI 127734); Moravia, between
Za´bøeh and Lupene, on
Potentilla tormentillae
, 21 Oct 1896,
leg.
F. Buba´k
(BPI 127732); Vydrholec, near U
´
valy, on
Potentilla tormentillae
, Oct 1899, leg.
F. Buba´k
(BPI 127733).
GERMANY. In sylva Hostrichiensi, on
Potentilla tormentillae
,
autumn, Fungi Rhenani No. 2227 (original material of
Phragmidium tormentillae
, BPI). USA. MARYLAND: Cun-
ningham Falls, on
Potentilla canadensis
, 30 Apr 2003, leg.
J
.
R
.
Herna´ ndez
and
M
.
C
.
Aime
,
JRH 2003-002
(U-3, BPI
843392 as
Frommee¨lla
sp.). PENNSYLVANIA: on
Potentilla
(original material of
Aregma triarticulatu m
, in Michener
Collection at BPI as
Aregma breve
; see Berkeley [1874]).
TENNESSEE: Great Smoky Mountains National Park,
Greenbriar area, 1699 ft. elev., on
Potentilla simplex
, 6 Sep
2004, leg.
M
.
C
.
Aime
,
MCA 2786
(BPI 877888).
Notes.
This is the well known type species of
Frommee¨lla
(Cummins and Hiratsuka 1983) that was
described originally from Europe as
Phragmidium
tormentillae
(Fuckel 1870) and has been accepted
variously as
Frommea obtusa
(Arthur 1917, 1934; Wilson
and Henderson 1966) in the misapplied sense
(Laundon 1975) and
Frommee¨lla tormentillae
(Cum-
mins and Hiratsuka 1983, Parmelee 1986, McCain and
Hennen 1990) and frequently confused with
Phragmi-
dium potentillae
(Laundon 1975).
The phylogenetic data presented here support the
hypothesis that there are at least two taxa on
Potentilla
, exclusive of host species formerly classified
in
Duchesnea
, that fit the generic concept of
Frommee¨lla
. Examined teliospores of this taxon
revealed a greater and more variable number of cells
per teliospore (2–6) than
Phragmidium potentillae-
canadensis
as well as somewhat lighter pigmented
teliospores. The original material of
Phragmidium
tormentillae
was distributed in Fuckel’s exsiccatae set,
Fungi Rhenani. Morphological study of it and other
European collections indicates conspecificity with the
examined American collections. The description is
based on American material that represents the type
1460 M
YCOLOGIA
species of
Frommee¨lla
as it has been applied in North
America (Parmelee 1986). Here we accept it as
Phragmidium tormentillae
.
Uncertain or excluded taxa:
Dicaeoma potentillae
Kuntze. Revisio Generum Plan-
tarum 3:470. 1898 as ‘(Schwein.) Kuntze’. This is a
nom. nov. because
Puccinia potentillae
Schwein. is a
nom. illeg.
;
Kuehneola potentillae
(Kuntze) Arthur, Re´sultats
Scientifiques du Congre`s International de Botanique
Vienne 1905:342. 1906 as ‘(Fuckel) Arthur’.
;
Puccinia potentillae
Schwein. Trans. Amer. Phil. Soc.
4:297. 1832 non
Puccinia potentillae
Pers. : Pers., Syn-
opsis Methodica Fungorum 1:229. 1801.
Notes.
Schweinitz (1832) described this species as a
new taxon on
Potentilla canadensis
, but his name was a
later homonym of a previously described species.
Unfortunately there are no detailed data on micro-
scopic characters in the protolog. Although Kuntze
(1898) and Arthur (1906) as well as others addressed
this species, we could find no additional data about
microscopic characters of the original material. Sydow
and Sydow (1915) listed this species under their
concept of an American species on
Potentilla
(
Phrag-
midium potentillae
-
canadensis
). Because we were un-
able to examine original material after attempting to
locate it at BPI, DWC and PH and that confusion
about
Phragmidium
taxa on
Potentilla
is pervasive in
older literature we prefer to list the taxonomic status
of this taxon as uncertain.
KEY TO THE SPECIES OF
PHRAGMIDIUM
WITH ONE GERM
PORE PER TELIOSPORE CELL
1. On
Potentilla
hosts formerly classified in
Duches-
nea
.........................
P. mexicanum
1. On
Potentilla
hosts, exclusive of species formerly
classified in
Duchesnea
.................... 2
2. Teliospores brownish yellow to yellowish
brown, typically with 2–3 up to 4 cells per
teliospore . . . .......
P. potentillae-canadensis
2. Teliospores brownish yellow, with 2–6 and
typically 3–4 cells per teliospore . . .
P. tormentillae
DISCUSSION
In summary,
Frommee¨lla
is derived from within a
monophyletic
Phragmidium
, revealing it as a later
generic synonym. Some species of
Phragmidium
are
known to have
Uredo
-type aecia (Cummins and
Hiratsuka 2003). The remaining major historical
difference between
Frommee¨lla
and
Phragmidium
of
the number of germ pores per teliospore cell is not
informative at generic rank. Within
Phragmidium
Arthur (1934) divided the genus into two sections,
Euphragmidium
(should be section
Phragmidium
according to the current ICBN Art. 22) and
Earlea
(Arthur) Arthur, when he demoted the genus
Earlea
Arthur to a lower rank.
Earlea
was described originally
by Arthur (1906) for species that lacked uredinial
stages in their life cycles. Arthur (1934) abandoned
this as a generic character, but he still thought
differences including a relative lack of abundance of
paraphyses in aecia, usually smooth or relatively
smooth instead of verrucose teliospores, and firmer,
more or less non-hygroscopic pedicels warranted
section
Earlea
as a distinct grouping. Based on our
preliminary sampling of
Phragmidium
, sections
Phrag-
midium
and
Earlea
do not form natural groupings. It
also appears likely that there have been multiple
jumps onto
Potentilla
during
Phragmidium
evolution
(e.g.
P. biloculare
and
P. ivesiae
,FIG. 1).
In terms of species recognition, the two previously
recognized species of
Frommee¨lla
(McCain and Hen-
nen 1990) are considered to be distinct taxa correctly
classified in
Phragmidium
, and an additional species
on non-
Duchesnea
members of
Potentilla
is recog-
nized, although bootstrap support is low. Because the
LSU region is considered conservative additional
sampling from more variable loci likely would
increase support for these species. Regarding host
associations, observed genetic variation correlated
with host identity as
Phragmidium mexicanum
always
was found to occur on host species formerly classified
in
Duchesnea
and
P. potentillae-canadensis
and
P.
tormentillae
were found on non-
Duchesnea
members
of
Potentilla
. As for morphological characters, we
found no significant uredinial characters that could
be used to readily distinguish the three species.
Uredinial paraphyses were difficult to observe due
to their relatively low abundance, and it is difficult to
know whether not observing them meant they were
really absent and whether this was significant. Some
variation in teliospore pigmentation and numbers of
cells per teliospore was observed. However a large
number of teliospores need to be examined to see the
full range, and this is seldom easy to do with sparse
material. Future work should continue to examine
species boundaries and host ranges of
Phragmidium
species formerly classified in the
Frommee¨lla
group,
especially because
Duchesnea
is now considered a
synonym of
Potentilla
(Eriksson et al. 2003).
ACKNOWLEDGMENTS
The authors thank Chris Clark (Louisiana material), Raman
Kaur (technical assistance at LSU), Karen Hughes and Ed
Lickey (logistics and support for collecting in Great Smoky
Mountains National Park), and USDA-APHIS and the
YUN ET AL.: THE GENUS
F
ROMMEE
¨
LLA
REVISITED 1461
Louisiana Board of Regents for support of molecular work
done at LSU. Two anonymous reviewers are credited with
helpful comments, especially encouragement to study
additional original material, which improved the quality of
this manuscript.
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