Standardizing the nomenclature for clonal lineages of the sudden oak death pathogen, Phytophthora ramorum.
ABSTRACT Phytophthora ramorum, the causal agent of sudden oak death and ramorum blight, is known to exist as three distinct clonal lineages which can only be distinguished by performing molecular marker-based analyses. However, in the recent literature there exists no consensus on naming of these lineages. Here we propose a system for naming clonal lineages of P. ramorum based on a consensus established by the P. ramorum research community. Clonal lineages are named with a two letter identifier for the continent on which they were first found (e.g., NA = North America; EU = Europe) followed by a number indicating order of appearance. Clonal lineages known to date are designated NA1 (mating type: A2; distribution: North America; environment: forest and nurseries), NA2 (A2; North America; nurseries), and EU1 (predominantly A1, rarely A2; Europe and North America; nurseries and gardens). It is expected that novel lineages or new variants within the existing three clonal lineages could in time emerge.
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ABSTRACT: Given the lack of a resistant genetic pool in host plants, the introduction of exotic invasive pathogens can result in epidemics that affect a specific ecosystem and economy. Plant quarantine, which is designed to protect endemic plant resources, is a highly invaluable safeguard that should keep biosecurity with increasing international trade and global transportation. A total of 34 species of plant pathogens including Phytophthora infestans were documented as introduced from other countries into Korea from 1900 to 2010. The genus Phytophthora, classified in oomycetes, includes more than 120 species that are mostly recognized worldwide as highly invasive plant pathogens. After 2000, over 50 new species of Phytophthora were identified internationally as plant pathogens occurring in crops and forest trees. In Korea, Phytophthora is also one of the most serious plant pathogens. To date, 22 species (about one-fifth of known species) of the genus have been identified and reported as plant pathogens in the country. The likelihood of new exotic Phytophthora species being introduced into Korea continues to increase, thus necessitating intensive plant quarantine inspections. As new potential threats to plant health in Korea, six Phytophthora species, namely, P. alni, P. inundata, P. kernoviae, P. pinifolia, P. quercina, and P. ramorum, are discussed in this review with focus on history, disease, biology, management, and plant quarantine issues.The plant pathology journal 12/2014; 30(4):331-42. · 0.76 Impact Factor
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Letter to the Editor
Standardizing the Nomenclature for Clonal Lineages
of the Sudden Oak Death Pathogen, Phytophthora ramorum
Niklaus J. Grünwald, Erica M. Goss, Kelly Ivors, Matteo Garbelotto, Frank N. Martin, Simone Prospero, Everett Hansen,
Peter J. M. Bonants, Richard C. Hamelin, Gary Chastagner, Sabine Werres, David M. Rizzo, Gloria Abad, Paul Beales,
Guillaume J. Bilodeau, Cheryl L. Blomquist, Clive Brasier, Stephan C. Brière, Anne Chandelier, Jennifer M. Davidson,
Sandra Denman, Marianne Elliott, Susan J. Frankel, Ellen M. Goheen, Hans de Gruyter, Kurt Heungens, Delano James,
Alan Kanaskie, Michael G. McWilliams, Willem Man in ‘t Veld, Eduardo Moralejo, Nancy K. Osterbauer,
Mary E. Palm, Jennifer L. Parke, Ana Maria Perez Sierra, Simon F. Shamoun, Nina Shishkoff,
Paul W. Tooley, Anna Maria Vettraino, Joan Webber, and Timothy L. Widmer
First and second authors: Horticultural Crops Research Laboratory, USDA-ARS, Corvallis, OR 97330; third author: North Carolina State
University, Mills River, NC 28759; fourth author: Department of Environmental Science, Policy, and Management, University of
California, Berkeley, CA; fifth author: Crop Improvement and Protection Unit, USDA-ARS, Salinas, CA 93905; sixth author: WSL Swiss
Federal Research Institute, 8903 Birmensdorf, Switzerland; seventh author: Botany and Plant Pathology, Oregon State University,
Corvallis OR 97331; eighth author: Plant Research International, Wageningen UR, Wageningen, The Netherlands; ninth author: Natural
Resources Canada, Department of Forest Sciences, The University of British Columbia, Vancouver, British Columbia, Canada; tenth
author: Department of Plant Pathology, Washington State University, Research and Extension Center, Puyallup, WA 9837; eleventh author:
Julius Kuehn Institut (JKI), Institute for Plant Protection in Horticulture and Forests, Braunschweig, Germany; twelfth author: University
of California at Davis, Davis, CA 95616; thirteenth author and thirty-third authors: USDA APHIS, Beltsville, MD 20705; fourteenth
author: Central Sciences Laboratory, York YO41 1LZ, N Yorkshire, England; fifteenth author: USDA-ARS, Salinas, CA, 93905; sixteenth
author: California Department of Food and Agriculture, Sacramento, CA 95832; seventeenth, twenty-first, and fortieth authors: Forest
Research, Alice Holt Lodge, Farnham, Surrey GU10 4LH, UK; eighteenth author: Canadian Food Inspection Agency, Ottawa, ON
Canada; nineteenth author: Walloon Agricultural Research Centre (CRAW), B-5030 Gembloux, Belgium; twentieth author: University of
Hawaii, Honolulu, HI 96822; twenty-second author: Washington State University, Puyallup, WA 98371; twenty-third author: USDA Forest
Service, Pacific Southwest Research Station, Albany, CA 94710; twenty-fourth author: USDA Forest Service, Central Point, OR 97502;
twenty-fifth and thirtieth authors: Plant Protection Service, Wageningen, 6700 HC, The Netherlands; twenty-sixth author: Institute for
Agricultural and Fisheries Research (ILVO), 9820 Merelbeke, Belgium; twenty-seventh author: Canadian Food Inspection Agency,
Sidney, BC V8L 1H3, Canada; twenty-eighth and twenty-ninth authors: Oregon Department of Forestry, Salem, OR 97310; thirty-first
author: Instituto Mediterráneo de Estudios Avanzados, IMEDEA (CSIC-UIB), 07190, Esporles, Balearic Islands, Spain; thirty-second
author: Oregon Department of Agriculture, Salem, OR 97310; thirty-fourth author: Dept. of Crop and Soil Science, Oregon State
University, Corvallis, OR 97331; thirty-fifth author: Instituto Agroforestal Mediterráneo, Universidad Politécnica de Valencia (IAM-
UPV), 46022 Valencia, Spain; thirty-sixth author: Natural Resources Canada, Canadian Forest Service, Pacific Forestry Centre, Victoria,
BC V8Z 1M5 Canada; thirty-seventh, thirty-eighth, and fourty-first authors: USDA-ARS FDWSRU, Fort Detrick, MD 21702; and thirty-
ninth author: Department of Plant Protection, University of Tuscia, Viterbo, 01100 Italy.
Accepted for publication 8 March 2009.
Grünwald, N. J., Goss, E. M., Ivors, K., Garbelotto, M., Martin, F. N.,
Prospero, S., Hansen, E., Bonants, P. J. M., Hamelin, R. C., Chastagner,
G., Werres, S., Rizzo, D. M., Abad, G., Beales, P., Bilodeau, G. J.,
Blomquist, C. L., Brasier, C., Brière, S. C., Chandelier, A., Davidson, J.
M., Denman, S., Elliott, M., Frankel, S. J., Goheen, E. M., de Gruyter, H.,
Heungens, K., James, D., Kanaskie, A., McWilliams, M. G., Man in ‘t
Veld, W., Moralejo, E., Osterbauer, N. K., Palm, M. E., Parke, J. L., Perez
Sierra, A. M., Shamoun, S. F., Shishkoff, N., Tooley, P. W., Vettraino, A.
M., Webber, J., and Widmer, T. L. 2009. Standardizing the nomenclature
for clonal lineages of the sudden oak death pathogen, Phytophthora
ramorum. Phytopathology 99:792-795.
Phytophthora ramorum, the causal agent of sudden oak death and
ramorum blight, is known to exist as three distinct clonal lineages which
can only be distinguished by performing molecular marker-based analyses.
However, in the recent literature there exists no consensus on naming of
these lineages. Here we propose a system for naming clonal lineages of P.
ramorum based on a consensus established by the P. ramorum research
community. Clonal lineages are named with a two letter identifier for the
continent on which they were first found (e.g., NA = North America;
EU = Europe) followed by a number indicating order of appearance.
Clonal lineages known to date are designated NA1 (mating type: A2;
distribution: North America; environment: forest and nurseries), NA2
(A2; North America; nurseries), and EU1 (predominantly A1, rarely A2;
Europe and North America; nurseries and gardens). It is expected that
novel lineages or new variants within the existing three clonal lineages
could in time emerge.
Additional keywords: exotic pathogen, forensics, molecular ecology,
phylogeography, population genetics.
Phytophthora ramorum Werres, De Cock & Man in’t Veld is
the exotic pathogen responsible for causing sudden oak death of
coast live oak and tanoak in native forests of the Western United
States and in other trees in Europe and the United States. It also
causes ramorum blight of trees and woody ornamentals such as
rhododendron and camellia in forest, retail or wholesale nursery,
and garden environments in North America and Europe (4,13,
Corresponding author: N. J. Grünwald; E-mail address: Nik.Grunwald@ars.usda.gov
*The e-Xtra logo stands for “electronic extra” and indicates that the online version
contains supplemental information providing the materials and methods used for
producing Figure 1.
This article is in the public domain and not copyrightable. It may be freely re-
printed with customary crediting of the source. The American Phytopathological
Vol. 99, No. 7, 2009 793
23,31,34,35,39). P. ramorum isolates examined to date comprise
three distinct clonal lineages based on a range of molecular
marker systems including amplified fragment length polymor-
phism (AFLP), microsatellites (SSR), mitochondrial and nuclear
sequences, and single nucleotide polymorphisms (SNPs) (1,26,
27,29,32,33). However, the nomenclature used for these lineages
is not consistent in the literature (Table 1). Thus, the objective of
this letter is to provide a consensus nomenclature for P. ramorum
clonal lineages based on current phenotypic and genotypic
(molecular marker based) information.
All marker systems used to date have revealed the existence of
these three clonal lineages. Figure 1 shows the three distinct evo-
lutionary lineages of P. ramorum in dendrograms with significant
bootstrap support based on either multilocus microsatellite (Fig.
1A) or mitochondrial sequence (Fig. 1B) data. Lineages are
named with a two letter identifier for the continent on which they
were first found (e.g., NA = North America; EU = Europe)
followed by a number indicating order of identification. Lineage
NA1, found in North America in nursery and forest environments,
is mating type A2 and is the lineage first detected in California
(Table 2). Lineage EU1 is now found both in Europe and North
America, and is predominantly A1 mating type with rare findings
of A2 isolates in Belgium (37) (Table 2). The third clonal lineage,
NA2, currently is found only in North America in nurseries and is
mating type A2 (Table 2). NA2 isolates were simultaneously
found in California and Washington in nurseries (26) and have
also been detected in Canada (11). Although both mating types
are known to coexist in United States nurseries, the segregation of
alleles that one would expect as a result of sexual reproduction
between lineages has not yet been observed in any genotyped
isolate (22,26,31). While production of oospores in controlled
crosses of A1 and A2 mating types is documented (2,5), there are
no published reports demonstrating viability of these oospores.
There is evidence of historical recombination in at least two genes
(19). However, it appears that the three P. ramorum clonal
lineages have been reproductively isolated for at least 150,000
years if not longer based on nuclear sequence analyses (19).
Genes in the mitochondrial DNA (31) and certain microsatellite
loci (26,33) exhibit fixed lineage-specific alleles that easily dis-
tinguish the lineages at the molecular level. However, isolates
within a given lineage have diverged considerably for other fast-
evolving microsatellites (Fig. 1A). Mitochondrial sequences gen-
erally have slower mutation rates than microsatellites (Fig. 1B;
after ) and accordingly there is little variation in mitochon-
drial haplotypes within lineages. The three distinct clonal lineages
and recent divergence within lineages are in agreement across all
molecular marker based analyses published to date including
AFLP (27), microsatellites (24,32,34), SNPs (1,31), mitochon-
drial sequences (27,31,33), and nuclear sequences (19,23,34).
Regardless of the differences in the rate of divergence at these
loci, isolates of these lineages can best be distinguished by per-
forming either mitochondrial or microsatellite analyses.
Differences in sequences of mitochondrial loci have been found
in isolates within lineages, e.g., NA1 isolates recovered from
Oregon forests differ in one SNP and have been named NA1a and
NA1b (31). Thus, we propose naming genetically distinct strains
within lineages based on SNPs by adding a letter to the lineage
and strain designation, e.g., NA1a and NA1b in order of
We do not propose standardizing nomenclature for differences
in genotypes for more variable markers systems such as micro-
satellites or AFLP given the rapid rate of divergence observed.
The three lineages show some differences in phenotype. Iso-
lates belonging to lineages NA2 and EU1 exhibit faster mean
radial growth in culture than those belonging to lineage NA1
(3,6,26,38). Isolates of the NA1 lineage show more phenotypic
variation in terms of growth morphology in petri dish culture or
disease severity assays and instability of phenotype than those of
the EU1 lineage (6,38). Results on differences in pathogenicity
among lineages are inconclusive at this point: there is some evi-
dence that EU1 isolates are on average significantly more patho-
Fig. 1. Representative Phytophthora ramorum isolates from its known geo-
graphic range cluster into three distinct clonal lineages based on nuclear and
mitochondrial molecular marker systems. Although some genetic diversity
exists within a lineage, the lineages are clonal. The origins of isolates are
listed in the online supplement. A, Neighbor-joining phylogram based on
Nei’s chord distance across six microsatellite loci. Bootstrap support values
greater than 75% based on 1,000 bootstrap samples are shown (modified from
Goss et al.  as described in supplement). B, Maximum likelihood tree for
each P. ramorum mitochondrial haplotype for approximately 5 kb of DNA
sequence from eight mitochondrial regions (modified from Martin  as
described in supplement). The tree is rooted with P. hibernalis and bootstrap
support values are based on 500 samples.
TABLE 2. Current nomenclature and characteristics of the known Phytoph-
thora ramorum clonal lineages (adapted from Ivors et al. )
NA1 North America Forests,
aBased upon measurements of radial growth of representative isolates of each
lineage grown on cornmeal or V8 juice agar (3,6,26,38).
bLineage EU1 is predominantly of A1 mating type with rare findings of A2
isolates in Belgium (37).
cIn the United States, the EU1 lineage is only found in nurseries, but is not
very common relative to the NA1 lineage.
TABLE 1. Placement of previously named genotypes of Phytophthora
ramorum into the clonal lineages NA1, NA2, and EU1
Clonal lineage Ivors et al. (26) Prospero et al. (33) Martin (31)
Haplotype IIa, IIb
genic to mature tree stems compared with NA1 isolates (6);
however, other studies have revealed no differences in pathogeni-
city of isolates in different lineages to foliage or shoots (7,25,36).
Clearly, phenotype is not a suitable diagnostic test of clonal
lineage; only molecular characterization can unambiguously place
individuals within a lineage (23).
The clonal structure of P. ramorum is reminiscent of that of P.
infestans and P. cinnamomi. Although P. infestans is known to
exist as a sexually reproducing population in Europe and central
Mexico (12,20,21), its population structure in the United States is
clonal (15,16,18). Interestingly, the P. infestans US-1 clonal
lineage known to exist in the United States prior to recent
introductions has since been displaced by more fit clonal lineages
such as US-8 (16,17,28). Like P. ramorum, P. cinnamomi exists as
distinct clonal lineages in Australia, South Africa, and elsewhere
(8,24,30). In a geographic area where both mating types coexist,
Phytophthora populations can be sexually recombining as is the
case for P. infestans in Europe (9,10), or remain clonal as is the
case for P. infestans in the United States and P. cinnamomi in
Australia (14,22–24). It is expected that novel lineages or new
variants of the existing three clonal lineages differing in the traits
described herein could in time emerge.
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