Alternate host ranges of Cronartium flaccidum and Cronartium ribicola in Northern Europe

Abstract

Attached and detached leaves of 60 potential host species were inoculated in the greenhouse and laboratory with aeciospores of Cronartium ribicola J.C. Fisch. from six Finnish locations and of Cronartium flaccidum (Alb. & Schw.) Wint. from 20 locations in Finland and Sweden in 2011. Candidate hosts represented 16 plant families: Solanaceae, Verbenaceae, Asclepiadaceae, Grossulariaceae, Paeoniaceae, Balsaminaceae, Gentianaceae, Scrophulariaceae, Loasaceae, Tropaeolaceae, Acanthaceae, Myricaceae, Phrymaceae, Plantaginaceae, Orobanchaceae, and Apocynaceae. Inoculations of C. flaccidum produced uredinia after 2 weeks and (or) telia after 4 weeks of incubation on 25 hosts. Inoculation trials identified several new hosts for C. flaccidum in Fennoscandia, namely Impatiens balsamina, Swertia fedtschenkoana, Loasa tricolor, Myrica gale, Verbena canadensis, Saxifraga spp., Paeonia obovata, and Veronica daurica. Myricaceae and Saxifragaceae represent new host families for these rusts. Cronartium ribicola formed uredinia or telia on 10 species: Ribes spp. (7 species/cultivars), Pedicularis palustris subsp. palustris, Bartsia alpina, and Loasa triphylla. Results suggest wider alternate host ranges for both C. flaccidum and C. ribicola than previously recognized. Spores were virulent regardless of their source location, suggesting a lack of host-specificity among Fennoscandian populations of Cronartium.

Full text

Alternate host ranges of Cronartium flaccidum and
Cronartium ribicola in northern Europe
Juha Kaitera, Ritva Hiltunen, and Berit Samils
Abstract: Attached and detached leaves of 60 potential host species were inoculated in the greenhouse and laboratory with
aeciospores of Cronartium ribicola J.C. Fisch. from six Finnish locations and of Cronartium flaccidum (Alb. & Schw.)
Wint. from 20 locations in Finland and Sweden in 2011. Candidate hosts represented 16 plant families: Solanaceae, Verbe-
naceae, Asclepiadaceae, Grossulariaceae, Paeoniaceae, Balsaminaceae, Gentianaceae, Scrophulariaceae, Loasaceae, Tropaeo-
laceae, Acanthaceae, Myricaceae, Phrymaceae, Plantaginaceae, Orobanchaceae, and Apocynaceae. Inoculations of
C. flaccidum produced uredinia after 2 weeks and (or) telia after 4 weeks of incubation on 25 hosts. Inoculation trials iden-
tified several new hosts for C. flaccidum in Fennoscandia, namely Impatiens balsamina,Swertia fedtschenkoana,Loasa tri-
color,Myrica gale,Verbena canadensis,Saxifraga spp., Paeonia obovata, and Veronica daurica. Myricaceae and
Saxifragaceae represent new host families for these rusts. Cronartium ribicola formed uredinia or telia on 10 species: Ribes
spp. (7 species/cultivars), Pedicularis palustris subsp. palustris,Bartsia alpina, and Loasa triphylla. Results suggest wider
alternate host ranges for both C. flaccidum and C. ribicola than previously recognized. Spores were virulent regardless of
their source location, suggesting a lack of host-specificity among Fennoscandian populations of Cronartium.
Key words: alternate hosts, Scots pine blister rust, white pine blister rust.
Résumé : Les auteurs ont inoculé les feuilles détachées et attachées de 60 espèces d’hôtes potentiels en serre et au labora-
toire avec les écidiospores du Cronartium ribicola J.C. Fisch., provenant de six localités finlandaises et du Cronartium flac-
cidum (Alb. & Schw.) Wint. provenant de vingt localités suèdoises et finlandaises en 2011. Les hôtes candidats représentent
16 familles de plantes : Solanaceae, Verbenaceae, Asclepiadaceae, Grossulariaceae, Paeoniaceae, Balsaminaceae, Gentiana-
ceae, Scrophulariaceae, Loasaceae, Tropaeolaceae, Acanthaceae, Myricaceae, Phrymaceae, Plantaginaceae, Orobanchaceae et
Apocynaceae. Les inoculations avec le C. flaccidum produisent des urédinies après deux semaines et (ou) des télies après
quatre semaines d’incubation sur 25 hôtes. Les essais d’inoculation ont permis d’identifier plusieurs nouveaux hôtes du
C. flaccidum Fennoscandie, nommément les Impatiens balsamina,Swertia fedtschenkoana,Loasa tricolor,Myrica gale,Ver-
bena canadensis,Saxifraga spp., Paeonia obovata et Veronica daurica. Les Myricaceae et les Saxifragaceae représentent de
nouvelles familles hôtes pour ces rouilles. Le C. ribicola forme des urédinies ou des télies sur 10 espèces : Ribes spp. (7 es-
pèces/cultivars), Pedicularis palustris ssp. palustris,Bartsia alpina et Loasa triphylla. Les résultats suggèrent une amplitude
élargie d’hôtes alternatifs pour le C. flaccidum aussi bien que le C. Ribicola par rapport a ce qu’on a reconnu auparavant.
Les spores se sont avérées virulentes indépendamment de la localisation de leur source, suggérant une absence de spécificité
àl’hôte chez les populations fennoscandiennes du genre Cronartium.
Mots‐clés : hôtes alternatifs, rouille vésiculeuse du pin sylvestre, rouille vésiculeuse du pin blanc.
[Traduit par la Rédaction]
Introduction
Cronartium ribicola J.C. Fisch. causes white pine blister
rust (WPBR), a severe disease affecting five-needle pines in
the northern hemisphere (Stephan and Hyun 1983; Blada
1990; Stephan 2004). In Finland, WPBR destroyed most of
the five-needle pine plantations in the 1800s and 1900s (Liro
1908; Heikinheimo 1956; Lähde et al. 1984), but susceptible
species can still be found growing in arboreta, botanical gar-
dens, parks, and along roadsides. The rust spreads mainly via
species of Ribes,Pedicularis, and Castilleja (Yokota et al.
1975; Yokota and Uozumi 1976; La and Yi 1976; Patton
and Spear 1989; McDonald et al. 2006; Kim et al. 2010;
Zhang et al. 2010). In Finland, the rust infects Ribes L. spp.,
Pedicularis palustris L. subsp. palustris, and some species of
Orobanchaceae, Loasaceae, Apocynaceae, and Tropaeolaceae
(Kaitera and Nuorteva 2006a, 2006b; Kaitera and Hiltunen
2011, 2012).
Cronartium flaccidum (Alb. & Schw.) Wint. affects two-
needle pines throughout Europe, especially in northern Fen-
noscandia where it has caused extensive damage over the
last 20–30 years (Diamandis and De Kam 1986; Greig 1987;
Kaitera 2000; Samils et al. 2011). The rust spreads via spe-
Received 10 February 2012. Accepted 6 April 2012. Published at www.nrcresearchpress.com/cjb on 27 June 2012.
J. Kaitera. Finnish Forest Research Institute, Oulu, P.O. Box 413, FI-90014 University of Oulu, Finland.
R. Hiltunen. Botanical Gardens, University of Oulu, P.O. Box 3000, FI-90014 Oulu, Finland.
B. Samils. Department of Forest Mycology and Plant Pathology, Box 7026, Swedish University of Agriculture, SE-75007 Uppsala,
Sweden.
Corresponding author: Juha Kaitera (e-mail: juha.kaitera@metla.fi).
694
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cies of Vincetoxicum,Melampyrum,Gentiana,Paeonia,Ped-
icularis,Loasa,Nemesia,Impatiens,Grammatocarpus,Schi-
zanthus,Tropaeolum,Verbena, and Euphrasia (Hylander et
al. 1953; Gäumann 1959; Kaitera and Hiltunen 2012). Ac-
cording to Ragazzi (1983), its main alternate host in southern
Europe is Vincetoxicum hirundinaria Medicus. Among a
number of suitable hosts in northern Europe (Kaitera et al.
1999, 2005; Kaitera and Hiltunen 2011, 2012), Melampyrum
sylvaticum L. is the most important.
The aim of this study was to clarify the alternate host
ranges of C. flaccidum and C. ribicola in Fennoscandia by
screening a suite of candidate species from the native and
exotic flora with live aeciospore inocula.
Materials and methods
Inocula and plant material
Locations from which sample inocula of C. ribicola and
C. flaccidum were obtained are indicated in Table 1. Viable
aeciospores of C. ribicola (locality codes 1–6) were collected
from fresh and unopened aecia on multiple hosts in two loca-
tions of southern Finland in late May 2011. Spores were col-
lected from a single lesion by cutting the surface with a
sterile scalpel and dusting the contents into a Petri dish. Ae-
cial remnants were removed from the spore mass with for-
ceps before being placed into storage at 5 °C for 5–8 weeks.
After 24 h incubation on 1.5% water agar, 11%–35% of ae-
ciospores had germinated.
Eleven samples of C. flaccidum spores were obtained from
three locations in southern and northern Finland. Intact aecia
were transported on cut branches to the laboratory where
spores were collected in a laminar flow hood (locality codes
1a–3e). Each sample consisted of all spores collected from 1–
7 lesions per location. Nine Petri dish samples from Sweden
(locality codes 4a–4i) were obtained by incision and dusting
of one lesion per location in the field. Aeciospore germina-
tion varied between 37%–100% after 24 h incubation on
1.5% water agar. The spores were stored at 5 °C for 1–
8 weeks prior to inoculation. Samples were collected during
early–mid June in Finland, late May in southern Sweden, mid
June in central Sweden, and late June in northern Sweden.
Plants were grown from seed in the greenhouse. Detached
green and healthy leaves were also collected from plants in
the systematic collection of the Botanical Gardens at the Uni-
versity of Oulu. Test plants comprised 60 species in 16 fami-
lies (Tables 2 and 3).
Inoculation of leaves
Live plants were inoculated in the greenhouse at the Bota-
nical Gardens of the University of Oulu between late June
and mid July 2011. Plants first received a misting with water
and then had lower leaf surfaces dusted with aeciospores at a
density of ~75/mm2. Inoculated plants were covered with a
moistened plastic bag and incubated for 48 h. After the incu-
bation period, bags were removed and test plants were then
left on the greenhouse table under artificial light at an aver-
age of 19–21 °C (monthly averages) and irrigated for 3 s
every 30 min for 6–8 weeks.
In a second experiment, detached leaves were placed on
water in Petri dishes, inoculated, and incubated for 8 weeks
Table 1. Source locality data of Cronartium spores used as inocula.
Locality
code
Source
species
Date of
collection Host plant Collection location
No. of
lesions
Spore
germination (%)
1C. ribicola 19-5-2011 Pinus strobus Viikki arboretum, southern Finland 1 20
2C. ribicola 19-5-2011 Pinus strobus Viikki arboretum, southern Finland 1 35
3C. ribicola 19-5-2011 Pinus strobus Viikki arboretum, southern Finland 1 11
4C. ribicola 19-5-2011 Pinus strobus Viikki arboretum, southern Finland 1 24
5C. ribicola 19-5-2011 Pinus strobus Viikki arboretum, southern Finland 1 32
6C. ribicola 19-5-2011 Pinus monticola Botanical Gardens of Helsinki, southern Finland 1 17
1a C. flaccidum 1-6-2011 Pinus sylvestris Naantali, southern Finland 4 96
2a C. flaccidum 16-6-2011 Pinus sylvestris Kolari, northern Finland 1 85
2b C. flaccidum 16-6-2011 Pinus sylvestris Kolari, northern Finland 2 92
2c C. flaccidum 16-6-2011 Pinus sylvestris Kolari, northern Finland 7 86
2d C. flaccidum 16-6-2011 Pinus sylvestris Kolari, northern Finland 3 37
2e C. flaccidum 16-6-2011 Pinus sylvestris Kolari, northern Finland 3 63
3a C. flaccidum 17-6-2011 Pinus sylvestris Juomukuru, northern Finland 1 56
3b C. flaccidum 17-6-2011 Pinus sylvestris Juomukuru, northern Finland 1 76
3c C. flaccidum 17-6-2011 Pinus sylvestris Juomukuru, northern Finland 1 99
3d C. flaccidum 17-6-2011 Pinus sylvestris Juomukuru, northern Finland 1 60
3e C. flaccidum 17-6-2011 Pinus sylvestris Juomukuru, northern Finland 5 88
4a C. flaccidum 27-5-2011 Pinus sylvestris Ar (Gotland), southern Sweden 1 90
4b C. flaccidum 27-5-2011 Pinus sylvestris Ar (Gotland), southern Sweden 1 88
4c C. flaccidum 27-5-2011 Pinus sylvestris Ardre (Gotland), southern Sweden 1 96
4d C. flaccidum 19-5-2011 Pinus sylvestris Uppsala, central Sweden 1 100
4e C. flaccidum 19-5-2011 Pinus sylvestris Uppsala, central Sweden 1 99
4f C. flaccidum 25-5-2011 Pinus sylvestris Tjärby, southern Sweden 1 94
4g C. flaccidum 16-6-2011 Pinus sylvestris Sorunda, central Sweden 1 98
4h C. flaccidum 22-6-2011 Pinus sylvestris Övertorneå, northern Sweden 1 72
4i C. flaccidum 22-6-2011 Pinus sylvestris Övertorneå, northern Sweden 1 52
Kaitera et al. 695
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Table 2. Uredinia and telia formation on detached leaves of test plants inoculated in the laboratory after 8 weeks of incubation in 2011.
Spore source
Cronartium ribicola Cronartium flaccidum
Spore locality code
Species 1 2 3 4 5 6 1a 2a 2b 2c 2d 2e 3a 3b 3c 3d 3e 4a 4b 4c 4d 4e 4f 4g 4h 4i
Antirrhinum majus1nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Verbena canadensis2nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes nigrum ’Ola’3nt +/–nt +/–+/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes nigrum ‘Mortti’3nt +/+ nt +/+ +/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes nigrum ’Hedda’3nt +/–nt +/+ +/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes nigrum ’Wild type’3nt +/+ nt +/–+/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes spicatum subsp. spicatum3nt +/–nt +/–+/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes atropurpureum3nt +/+ nt +/+ –/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Ribes laxiflorum3nt +/–nt +/–+/+ nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica chamaedrys4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica longifolia4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica gentianoides4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica spicata subsp. spicata4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica incana4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Veronica spicata4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Plantago media4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Plantago lanceolata4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Digitalis grandiflora4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Chaenorhinum minus4nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt nt nt nt
Scopolia carniolica5nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Lycium barbarum5nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Paeonia lactiflora6nt –/–nt –/––/–nt +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/–nt +/–+/+ +/–nt nt +/+ +/–nt +/+ +/+ +/+
Paeonia anomala6nt –/–nt –/––/–nt +/–+/–+/+ +/–+/–+/+ +/+ +/–nt –/–+/+ –/–nt nt +/––/–nt +/+ +/+ +/+
Paeonia officinalis6nt –/–nt –/––/–nt +/–+/+ +/+ +/+ +/+ +/+ +/+ +/+ nt +/+ +/+ +/–nt nt –/–+/+ nt +/–+/+ +/+
Paeonia obovata6nt –/–nt –/––/–nt +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ nt +/+ +/+ +/+ nt nt +/+ +/+ nt +/+ +/+ +/+
Rhinanthus minor7nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Melampyrum pratense7nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Melampyrum sylvaticum7nt –/–nt –/––/–nt +/–+/+ +/+ +/+ +/+ +/+ –/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Pedicularis sceptrum-carolinum7nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/+
Heuchera cylindra8nt –/–nt –/––/–nt –/––/––/––/––/––/––/–– nt –/––/––/–nt nt –/––/–nt –/––/––/–
Saxifraga cespitosa8nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–+/––/––/––/––/––/––/––/––/––/––/––/–
Saxifraga exarata8nt –/–nt –/––/–nt –/––/––/––/––/––/––/–+/+ nt –/––/––/–nt nt –/––/–nt –/––/–+/+
Saxifraga hostii8nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt +/––/–nt +/––/––/–
Vincetoxicum hirundinaria12 nt –/–nt –/––/–nt +/––/–+/+ +/+ +/+ +/+ +/+ +/+ nt –/–+/+ +/–nt nt +/+ +/–nt +/+ +/–+/+
Penstemon confertus13 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Verbascum phoeniceum13 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Scrophularia nodosa13 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Verbascum thapsus13 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Gentiana asclepiadea14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Gentiana affinis14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Gentiana septemfida14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Gentiana lutea14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Gentiana purpurea14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt nt nt nt
Swertia fedtschenkoana14 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/––/––/––/––/–+/+ –/––/––/––/–+/––/–+/+
Acanthus balcanicus15 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/–nt –/––/––/–nt nt –/––/–nt –/––/––/–
Impatiens noli-tangere16 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/–
Impatiens glandulifera16 nt –/–nt –/––/–nt –/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/–
Impatiens balsamina16 nt –/–nt –/––/–nt –/–+/+ +/+ +/––/–+/–+/+ –/–nt +/+ –/–+/+ nt nt –/–+/+ nt +/–+/+ +/+
Note: See Table 1 for spore locality data. First column represents uredinia and the second column telia. +, present; –, absent; nt, not tested. Supersrcipt numbers represent the following plant families 1Phrymaceae, 2Verbenaceae, 3Grossulariaceae, 4Planta-
ginaceae, 5Solanaceae, 6Paeoniaceae, 7Orobanchaceae, 8Saxifragaceae, 9Myricaceae, 10Loasaceae, 11Tropaeolaceae, 12Apocynaceae, 13Scrophulariaceae, 14Gentianaceae, 15Acanthaceae, and 16Balsaminaceae.
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at 18 °C under artificial light in a climate chamber (Clima-
cell). After 4 weeks, plants were rearranged inside the cham-
ber to homogenize the conditions received by each leaf.
Disease assessment
Following Gäumann (1959), rust symptoms on inoculated
leaves were assessed for the formation of uredinia, telia, and
basidia using a stereomicroscope. Inoculated test plants were
examined every 2 weeks. Rust samples from Finland were
collected from the same Cronartium populations studied ear-
lier with respect to their pathogenicity (Kaitera and Nuorteva
2006a, 2006b; Kaitera and Hiltunen 2011, 2012) and genetic
identity (Hantula et al. 1998; Kaitera et al. 2010). Spores
from the Swedish populations in Uppsala and Övertorneå
have also been genetically profiled (Samils et al. 2011).
Results
Inoculation with Cronartium ribicola
No uredinia or telia developed on test plants of 13 families
(Solanaceae, Verbenaceae, Plantaginaceae, Phrymaceae,
Paeoniaceae, Balsaminaceae, Gentianaceae, Acanthaceae,
Myricaceae, Scrophulariaceae, Apocynaceae, Tropaeolaceae,
and Saxifragaceae) when inoculated with spores of C. ribi-
cola. Plants bearing fruitbodies were found in three families:
Grossulariaceae (7 species and cultivars), Orobanchaceae (2
species), and Loasaceae (1 species). All Ribes spp. (Grossu-
lariaceae) were infected (Table 2), and abundant uredinia
were formed on detached leaves of four commercial cultivars,
a wild type of Ribes nigrum L., and on Ribes spicatum Rob-
son subsp. spicatum (Figs. 1–5). Uredinia developed on
Ribes atropurpureum C.A. Meyer and Ribes laxiflorum
Pursh. (Fig. 6) after 2–4 weeks of incubation for all three
spore samples (Table 4). Telia developed less frequently than
uredinia on three cultivars of Ribes nigrum, and on
Ribes atropurpureum and Ribes laxiflorum. Their first ap-
pearance occurred 4 weeks after inoculation and with in-
creasing frequency until disease assessment was terminated 8
weeks after inoculation.
Although telia did not develop, some uredinia were ob-
served on one leaf of Loasa triphylla Juss. after 6 weeks of
incubation (Tables 3 and 4). On species of Orobanchaceae,
uredinia developed for two spore samples on 8%–27% of
leaves of Pedicularis palustris subsp. palustris after 4 weeks
of incubation. After 8 weeks, telia developed on 3% of leaves
inoculated with one of the spore samples. Uredinia developed
on Bartsia alpina L. (Orobanchaceae), when inoculated with
all six spore samples (Fig. 7). On this host, 1%–10% of ino-
culated leaves carried uredinia after 8 weeks of incubation,
but telia did not develop. The remaining test species of Oro-
banchaceae and Loasaceae were not infected.
Inoculation with Cronartium flaccidum
No uredinia or telia developed on test plants of Solana-
ceae, Grossulariaceae, Phrymaceae, Scrophulariaceae, or
Acanthaceae when inoculated with spores of C. flaccidum.
Fruiting stages developed on 25 species in 11 families, of
which 12 were new hosts for C. flaccidum in Fennoscandia.
In Verbenaceae, uredinia developed after 2 weeks and telia
after 4 weeks of incubation on less than 1% of attached
leaves of Verbena canadensis (L.) Britt. when inoculated
Table 3. Uredinia and telia formation on attached leaves of test plants inoculated in the greenhouse after 8 weeks of incubation in 2011.
Spore source
Cronartium ribicola Cronartium flaccidum
Spore locality code
Species 1234561a2a2b2c2d2e3a3b3c3d3e4a4b4c4d4e4f4g4h4i
Antirrhinum majus1nt nt nt nt nt nt –/––/–nt nt nt nt –/–nt nt nt nt –/–nt nt nt nt nt –/–nt nt
Verbena canadensis2nt nt nt –/–nt nt –/–+/+ nt nt nt nt nt nt nt nt nt –/–nt nt nt nt nt nt nt nt
Veronica longifolia4nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt +/+
Veronica daurica4nt nt nt –/–nt nt –/––/–nt nt nt nt –/–nt nt nt nt +/–nt nt nt nt nt nt –/–nt
Solanum lycopersicum5nt nt nt nt nt nt nt –/–nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt
Bartsia alpina7+/–+/–+/–+/–+/–+/–+/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/–+/+ +/–+/+ +/+ –/––/–+/+
Melampyrum pratense7nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt +/+ –/–nt
Pedicularis palustris subsp. palustris7nt nt nt +/–+/+ nt +/+ +/+ nt nt nt nt +/+ nt nt nt nt +/–nt nt nt nt nt +/+ +/+ –/–
Pedicularis dolichorrhiza7nt nt nt –/–nt nt nt +/–nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt
Euphrasia stricta7nt nt nt nt nt nt nt +/+ nt nt nt nt nt nt nt nt nt +/+ nt nt nt nt nt nt nt nt
Saxifraga rotundifolia8nt nt nt –/–nt nt –/––/–nt nt nt nt –/–nt nt nt nt –/–nt nt nt nt nt –/––/––/–
Myrica gale9nt nt nt nt nt nt nt +/+ nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt nt
Caiophora lateritia10 nt nt nt –/–nt nt +/–+/–nt nt nt nt +/–nt nt nt nt +/–nt nt nt nt nt nt –/–nt
Loasa tricolor10 nt nt nt –/–nt nt –/–+/+ nt nt nt nt +/+ nt nt nt nt +/+ nt nt nt nt nt nt nt nt
Loasa triphylla10 –/––/––/–+/––/––/–+/–+/+ nt nt nt nt –/–nt nt nt nt +/+ nt nt nt nt nt nt –/–nt
Tropaeolum majus11 nt nt nt –/–nt nt +/–+/–nt nt nt nt +/–nt nt nt nt +/–nt nt nt nt nt +/–+/–nt
Vincetoxicum hirundinaria12 nt nt nt nt nt nt +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ nt nt +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+ +/+
Impatiens noli-tangere16 nt nt nt nt nt nt –/––/–nt nt nt nt nt nt nt nt nt –/–nt nt nt nt nt –/–nt nt
Impatiens glandulifera16 –/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/––/–
Note: See Table 1 for spore locality data. First column represents uredinia and the second column telia. +, present; –, absent; nt, not tested. Superscript numbers represent plant families as defined in Table 2.
Kaitera et al. 697
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with one spore sample (Fig. 16). In Plantaginaceae, two po-
tential host species were infected. On Veronica longifolia L.,
both uredinia and telia developed in small patches on a few
attached leaves when inoculated with one spore sample after
2–4 weeks of incubation (Fig. 10). Uredinia developed simi-
larly on Veronica daurica Stev. after 2 weeks of incubation,
but telia did not develop (Table 4). All test subjects of the
Paeoniaceae, one of the main alternate host families of
C. flaccidum, were successfully infected. Uredinia were
formed abundantly after 2 weeks of incubation and telia after
4 weeks on Paeonia obovata Maximovicz for all 16 spore
samples tested (Fig. 15). Similarly, uredinia and telia devel-
oped from most spore samples used to inoculate Paeonia of-
ficinalis L. (Fig. 14), Paeonia anomala L. (Fig. 13), and
Paeonia lactiflora Pall. (Fig. 12). Among species of Paeonia,
Paeonia lactiflora was the most resistant based on the fre-
quency and coverage of fruiting structures on inoculated
leaves (data not shown). Inoculated leaves of Vincetoxicum
hirundinaria, the only candidate host of Apocynaceae, were
frequently infected. Most spore samples, regardless of their
geographic origin, formed uredinia after 2 weeks and telia
after 4 weeks of incubation (Fig. 8). In Orobanchaceae, seven
of eight test species were infected by C. flaccidum;Rhinan-
thus minor L. was the exception. All species of Pedicularis
were infected, among which Pedicularis palustris subsp. pal-
ustris (Fig. 19) was the most susceptible host. Six of seven
spore samples formed uredinia and telia on attached leaves
of Pedicularis palustris subsp. palustris, regardless of their
geographic origin. A few telia occasionally developed on de-
tached leaves of Pedicularis sceptrum-carolinum L. after 4
weeks of incubation for one of the 16 spore samples. How-
ever, no uredinia developed on this host. One spore sample
developed some uredinia on attached leaves of Pedicularis do-
lichorrhiza Schrenk after 2 weeks of incubation (Fig. 22). On
other species of Orobanchaceae, two spore samples yielded
abundant uredinia and telia on attached leaves of Euphrasia
stricta Wolff ex. Lehm. after 2 weeks of incubation
(Fig. 21). Either uredinia or telia developed on Bartsia alpina
for 16 of 18 spore samples (Fig. 24). Uredinia were formed
after 2 weeks and telia after 4 weeks of incubation on that
host. A few attached leaves of a known resistant species,
Melampyrum pratense L., carried uredinia and telia after 4–
6 weeks of incubation when inoculated with one of the spore
samples (Table 4). However, none of 18 spore samples suc-
cessfully infected the detached leaves of this host. Although
spore infections from the six Finnish locations frequently
and rapidly led to both uredinia and telia on detached leaves
of Melampyrum sylvaticum (Fig. 18), Swedish spores did not.
Disease symptoms were recognized in species belonging to
two new host families for C. flaccidum: Saxifragaceae and
Myricaceae. Among the four species of Saxifraga tested, ure-
dinia developed after 2–4 weeks of incubation on detached
leaves of Saxifraga exarata Vill. (Fig. 17), Saxifraga hostii
Tausch, and Saxifraga cespitosa L. Sporulation was, how-
ever, rare and occurred on only a few individual leaves per
plant. On Saxifraga, spore infections from two samples de-
veloped telia on Saxifraga exarata after 4 weeks of incuba-
tion. Both uredinia and telia developed on attached leaves of
Myrica gale L. after 6 weeks of incubation (Fig. 25). The
formation of fruiting structures was slower on Myrica gale
than on other hosts, but necrosis of inoculated leaves had be-
gun before they were fully developed. In Loasaceae, a known
alternate host family of C. flaccidum, three species were ino-
culated and all became infected. Infections of all spore sam-
ples formed either uredinia or telia on Loasa triphylla
(Fig. 26), Loasa tricolor Lindl. (Fig. 23), and Caiophora lat-
eritia Benth. On these hosts, both uredinia and telia devel-
oped after 2 weeks of incubation. In Tropaeolaceae, uredinia
developed on leaves of whole plants of Tropaeolum majus
L. after 2 weeks of incubation for six spore samples tested
(Fig. 20). On this host, a low number (2%) of inoculated
leaves became infected but failed to form telia. In Gentiana-
ceae, all five species of Gentiana tested proved to be resist-
ant. Swertia fedtschenkoana Pissjank. was infected, and
either uredinia or telia developed on detached leaves after 2–
4 weeks of incubation for three spore samples (Fig. 11). In
Impatiens (Balsaminaceae), two of three species tested were
resistant but 11 of 16 spore samples frequently led to both
uredinia and telia on detached leaves of Impatiens balsamina
L. after 4 weeks of incubation (Fig. 9).
Among the candidate hosts, Impatiens noli-tangere L., Im-
patiens glandulifera Royle, Veronica chamaedrys L., Veron-
ica gentianoides Vahl., Veronica spicata subsp. spicata L.,
Verbascum thapsus L., Gentiana septemfida Pall., Genti-
ana lutea L., Gentiana purpurea L., Plantago lanceolata L.,
Digitalis grandiflora Mill., Scrophularia nodosa L., Acan-
thus balcanicus Heywood & I.B.K. Richardson, Plantago
media L., Chaenorrhinum minus (L.) Lange, Veronica incana
L., Veronica spicata L., Penstemon confertus Douglas et
Lindl., Scopolia carniolica Jacq., Lycium barbarum L., Heu-
chera cylindra L., Gentiana affinis Griseb., Gentiana ascle-
piadea L. Verbascum phoeniceum L., Solanum lycopersicum
L., and Saxifraga rotundifolia L. were resistant to aeciospore
infections of C. flaccidum.
Discussion
In this study, both Cronartium rusts (C. ribicola and
C. flaccidum) showed a wider host range than reported ear-
lier (Stephan and Hyun 1983; Kaitera and Nuorteva 2006b).
Results confirmed the recent inoculation results on Pedicula-
ris palustris,Loasa triphylla, and Bartsia alpina (Kaitera and
Hiltunen 2011, 2012). Both the Asian (Yokota et al. 1975; La
and Yi 1976) and North American (Patton and Spear 1989;
McDonald et al. 2006) C. ribicola are known to be virulent
on several hosts of Grossulariaceae and Orobanchaceae in-
cluding Ribes and Pedicularis, which were also susceptible
hosts in this study. Among the new hosts, Loasa and Bartsia
(Kaitera and Hiltunen 2012) were only slightly susceptible to
C. ribicola, but their distribution suggests they could support
C. ribicola and its spread.
To summarize the inoculations, uredinia of C. ribicola
formed abundantly on most Ribes but telia were scarcely de-
veloped. This is typical for local Cronartium cultured under
artificial conditions (e.g., Kaitera and Nuorteva 2006a), and
the high susceptibility of Ribes nigrum was clear and in ac-
cordance with Zambino (2010). Based on results presented
here and in our earlier work (Kaitera and Hiltunen 2011,
2012), it seems that many alternate hosts of variable suscept-
ibility exist in Grossulariaceae and Orobanchaceae and there
are perhaps many more awaiting detection.
Cronartium flaccidum infected and sporulated on 25 hosts
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1 mm
1 mm
1 mm
1 mm1 mm
1 mm 1 mm
1
34
567
2
Figs. 1–26. Uredinia (white arrows) and telia (white arrow heads) of Cronartium ribicola (Figs. 1–7) and Cronartium flaccidum (Figs. 8–26)
on the lower leaf surface of inoculated test plants in 2011. Fig. 1. Uredinia on Ribes nigrum ‘Ola’. Fig. 2. Uredinia on Ribes nigrum ‘Mortti’.
Fig. 3. Uredinia on Ribes nigrum ‘Hedda’. Fig. 4. Uredinia on Ribes nigrum ‘Wild type’. Fig. 5. Uredinia on Ribes spicatum subsp. spicatum.
Fig. 6. Uredinia on Ribes laxiflorum. Fig. 7. Uredinia on Bartsia alpina. Fig. 8. Uredinia and telia on Vincetoxicum hirundinaria. Fig. 9.
Uredinia and telia on Impatiens balsamina. Fig. 10. Uredinia and telia on Swertia fedschenkoana. Fig. 11. Uredinia and telia on Veronica
longifolia. Fig. 12. Uredinia on Paeonia lactiflora. Fig. 13. Uredinia on Paeonia anomala. Fig. 14. Uredinia on Paeonia officinalis. Fig. 15.
Uredinia on Paeonia obovata. Fig. 16. Uredinia and telia on Verbena canadensis. Fig. 17. Uredinia and telia on Saxifraga exarata. Fig. 18.
Uredinia on Melampyrum sylvaticum. Fig. 19. Uredinia and telia on Pedicularis palustris subsp. palustris. Fig. 20. Uredinia on Tropaeolum
majus. Fig. 21. Uredinia and telia on Euphrasia stricta. Fig. 22. Uredinia on Pedicularis dolichorrhiza. Fig. 23. Uredinia and telia on Loasa
tricolor. Fig. 24. Uredinia and telia on Bartsia alpina. Fig. 25. Telia on Myrica gale. Fig. 26. Uredinia on Loasa triphylla.
Kaitera et al. 699
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in 11 families. Of these, Veronica,Bartsia,Euphrasia,Impa-
tiens,Pedicularis,Melampyrum, and Myrica are common in
natural forests and likely serve as alternate hosts. Gäumann
(1959) cited species of Euphrasia,Impatiens, and Verbena
as alternate hosts for C. flaccidum but considerable variation
between species within genera (e.g., Impatiens and Veronica)
and within families obscures any general pattern from being
observed. Species of Gentiana (Gentianaceae) were fully re-
sistant to C. flaccidum, supporting the notion that some de-
gree of host restriction exists for this rust (Gäumann 1959).
It is interesting to note that Swertia, also within Gentiana-
ceae, is a known host for Cronartium himalayense Bagchee
(Bakshi 1976) and was infected by C. flaccidum here. Cro-
nartium himalayense is believed to belong to a complex in-
cluding C. flaccidum (Hiratsuka 1995), so the implied
susceptibility of Swertia to Cronartium generally may be
somewhat exaggerated by taxonomy. Another new host for
C. flaccidum,Myrica gale, is similarly known as an alternate
host for Cronartium comptoniae Arth. (Ziller 1974). Disease
symptoms developed more slowly on Myrica gale than other
hosts, which may account for why this species was not de-
tected as a potential host in earlier experiments (Kaitera and
Hiltunen 2012). Nevertheless, C. flaccidum and its congeners
evidently share hosts.
1 mm
1 mm
1 mm1 mm1 mm
1 mm 1 mm
1 mm 1 mm
8910
11 12 13
14 15 16
Figs. 1–26. (continued).
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In line with recent studies (Kaitera and Hiltunen 2011,
2012), the present study showed that C. flaccidum frequently
forms uredinia and telia on Vincetoxicum hirundinaria,Paeo-
nia spp, Pedicularis sp., and Melampyrum sp. Among spe-
cies of Melampyrum,Melampyrum sylvaticum was highly
susceptible to C. flaccidum while fruiting stages developed
only rarely on Melampyrum pratense, a species known to be
resistant. This agrees with the results of earlier inoculation
1 mm
1 mm1 mm
1 mm
1 mm
1 mm1 mm
1 mm 1 mm 1 mm
17
20
23
18
21
24
19
22
25 26
Figs. 1–26. (concluded).
Kaitera et al. 701
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studies (Kaitera and Nuorteva 2003a, 2003b) and those based
on damaged pine stands (Kaitera et al. 2005). All of the
above mentioned species can spread C. flaccidum efficiently
in natural and urban environments, and they are thus impor-
tant alternate hosts in practice. The ability of some new hosts
found in gardens (e.g., Tropaeolum,Loasa) or narrowly dis-
tributed in the north (e.g., Swertia,Saxifraga,Verbena)to
spread C. flaccidum is unknown. It is also possible that these
rusts may never be observed on the new hosts growing in
natural habitats. The cause(s) of the epidemics of C. flacci-
dum in northern Fennoscandia remain poorly understood.
The hypothesis that northern rust populations are generally
less host-specific than southern ones (Kaitera and Nuorteva
2003a) was not supported by the present study, and spore
samples from within Sweden and Finland were equally viru-
lent on most candidate hosts including those known to be
susceptible (e.g., Vincetoxicum,Pedicularis,Paeonia).
Combining the results of this and two recent studies (Kai-
tera and Hiltunen 2011, 2012), we have demonstrated that the
spectrum of alternate hosts for C. ribicola and C. flaccidum
is considerably wider than previously described. As such, we
believe there is a need to study the natural distribution and
density of Cronartium rusts and their hosts to understand the
factors that spread the disease and create epidemics. Further-
more, sporulation on the newly detected hosts under natural
conditions must also be determined.
Table 4. Proportion of leaves with uredinia and telia of Cronartium ribicola and Cronartium flaccidum after inoculation of attached or
detached leaves in 2011.
Incubation
Weeks 2 Weeks 4 Weeks 6 Weeks 8
% of leaves
Inoculation
No. of spore
sources Uredinia Telia Uredinia Telia Uredinia Telia Uredinia Telia
C. ribicola
Ribes atropurpureum33 0 01701703333
Ribes nigrum ‘Ola’33 83 0 83 0 83 0 83 0
Ribes nigrum ‘Hedda’33 100 0 100 0 100 0 100 17
Ribes nigrum ’Mortti’33 100 0 100 17 100 17 100 50
Ribes nigrum ‘Wild type’33 67 0 67 0 67 0 67 17
Ribes spicatum. subsp. spicatum33 67 0 67 0 67 0 67 0
Ribes laxiflorum33 83 0 83 0 83 0 100 17
Pedicularis palustris subsp. palustris72 0 0100100103
Bartsia alpina76+0303040
Loasa triphylla10 6 0 0 0 0 0.2 0 0.2 0
C. flaccidum
Verbena canadensis216 + 0 0.1 0 0.1 0 1 1
Veronica longifolia416 0 0++++++
Veronica daurica45+0+0+0+0
Paeonia obovata616 47 0 100 88 100 88 100 97
Paeonia lactiflora616 310783878389759
Paeonia anomala616 410663166316663
Paeonia officinalis616 560885388538863
Melampyrum pratense716 0 0 + 0 + 7 no no
Melampyrum sylvaticum716 399443844384641
Euphrasia stricta72++++++1414
Bartsia alpina720 +0++++6 5
Pedicularis sceptrum-carolinum716 00060606
Pedicularis palustris subsp.palustris77 6 0 8 9 9 10 10 10
Pedicularis dolichorrhiza71+0+0+0nono
Saxifraga exarata816 30666666
Saxifraga hostii816 00636363
Saxifraga cespitosa820 0 0+0+0+0
Myrica gale91000044nono
Caiophora lateritia10 4+0+0+0+0
Loasa tricolor10 4++222255
Loasa triphylla10 5++323253
Tropaeolum majus11 6+0+0+020
Vincetoxicum hirundinaria12 19 + 0 6 2 8 6 13 13
Swertia fedtschenkoana14 20 30969696
Impatiens balsamina16 16 0 0 30 15 30 15 48 33
Note: +, uredinia or telia present; no, not observed. Superscript numbers represent plant families as defined in Table 2.
702 Botany, Vol. 90, 2012
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Acknowledgements
We thank staff of the Botanical Gardens of the University
of Oulu for providing plant material and greenhouse space
for this study. Irene Murtovaara helped us prepare the figures
and Michael Hardman checked the language.
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