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Revista mexicana de fitopatología
On-line version ISSN 2007-8080Print version ISSN 0185-3309
Rev. mex. fitopatol vol.38 n.1 Texcoco Jan. 2020 Epub Nov 27, 2020
https://doi.org/10.18781/r.mex.fit.1910-3
Scientific articles
Identification of daylily rust (Puccinia hemerocallidis) and characterization of resistance of five genotypes
1 Programa de Fitosanidad-Fitopatología, Colegio de Postgraduados, Campus Montecillo, Km 36.5 Carretera México-Texcoco, Montecillo, Texcoco, Estado de México, CP 56230, México
2 Recursos Genéticos y Productividad, Colegio de Postgraduados, Campus Montecillo, Km 36.5 Carretera México-Texcoco, Montecillo, Texcoco, Estado de México, CP 56230, México.
Daylily (Hemerocallis spp.) is attacked by the fungus Puccinia hemerocallidis. In Mexico there are no reports of this disease nor of plant material resistant to the pathogen. Since 2008, symptoms of rust on leaves of H. lilioasphodelus have been observed in the garden of a private house in the municipality of Chicoloapan de Juárez, State of Mexico, and in a nursery in Fortín de las Flores, Veracruz. The objectives of this investigation were to identify morphologically and molecularly the isolates of both locations and characterize the resistance to this disease macroscopically in five genotypes of Hemerocallis spp. under greenhouse conditions. According to the morphological characteristics of uredospores, teliospores and molecular studies, the fungus was identified as P. hemerocallidis. The genotypes evaluated were grouped into three resistance categories: H. lilioasphodelus behaved susceptible; ‘Radiant Greetings’ and ‘Stella d’Oro’ cultivars of the H. hybrida species were classified as moderately resistant; the cultivar ‘Cherry Wine’ and the species H. fulva were grouped as resistant; the latter presents a probable partial resistance sensu Parlevliet. The presence of P. hemerocallidis and the resistance of daylily genotypes are reported for the first time in Mexico.
Key words: cultivars; Hemerocallis lilioasphodelus; Hemerocallis fulva; hypersensitivity resistance; partial resistance.
El lirio de día (Hemerocallis spp.) es atacado por el hongo Puccinia hemerocallidis. En México no existen reportes de esta enfermedad o de material vegetal resistente al patógeno. Desde 2008, se han observado síntomas de roya sobre hojas de H. lilioasphodelus en el jardín de una casa particular en el municipio de Chicoloapan de Juárez, Estado de México y en un vivero de Fortín de las Flores, Veracruz. Los objetivos de esta investigación fueron identificar morfológica y molecularmente los aislamientos de ambas localidades y caracterizar la resistencia a esta enfermedad macroscópicamente en cinco genotipos de Hemerocallis spp., bajo condiciones de invernadero. De acuerdo con las características morfológicas de uredosporas, teliosporas y estudios moleculares, el hongo se identificó como P. hemerocallidis. Los genotipos evaluados se agruparon en tres categorías de resistencia: H. lilioasphodelus se comportó susceptible; los cultivares ‘Radiant Greetings’ y ‘Stella d’Oro’ de la especie H. hybrida se clasificaron como moderadamente resistentes; el cultivar ‘Cherry Wine’ y la especie H. fulva se agruparon como resistentes; esta última presenta una probable resistencia parcial sensu Parlevliet. La presencia de P. hemerocallidis y la resistencia de genotipos de lirio de día se reporta por primera vez en México.
Palabras clave: cultivares; Hemerocallis lilioasphodelus; Hemerocallis fulva; resistencia de hipersensibilidad; resistencia parcial
Daylily (Hemerocallis spp.) is one of the economically important plants in the United States and China because of its ornamental and food use, respectively. It is a perennial and very popular plant because of its long flowering period, availability in several colors, forms and sizes, ability to survive with very little care in different climates, and resistance to drought, pests and diseases (Munson, 1989; Grosvenor, 1999). In Mexico, daylily is considered a minor ornamental species but in the last years has become more important in home, hotels, parks and highways gardening, among others.
However, there are important phytopathological issues that limit daylily production. In 2000, a devastating disease was reported for the first time in the state of Georgia, United States, in the ‘Pardon Me’ cultivar, which, according to the symptoms, corresponded to the group of rusts (Williams-Woodward et al., 2001). The fungus was identified as Puccinia hemerocallidis, a pathogen originally from Asia that has caused damage in Asia, mainly in China, Japan, Korea, Russia, Taiwan and Thailand (Smith, 2009). In 2001, the fungus was detected in another 20 states of the United States (Hernández et al., 2002), and later also in Brazil (Carvalho et al., 2001), Colombia (Pardo-Cardona, 2006), South Africa (Mostert et al., 2008), Venezuela (Pardo-Cardona et al., 2008), Canada, Panama and Australia (Smith, 2009) and Portugal (Silva et al., 2016). Although there are no reports on the pathogen in Mexico, plants showing symptoms have been observed since 2008 in Aguascalientes, the State of Mexico, Morelos, Veracruz and Zacatecas. The causal agent of daylily rust and what plant material is resistant to the pathogen are currently unknown in Mexico. Therefore, the objectives of this research were to identify the causal agent of daylily rust in the State of Mexico and Veracruz, based on morphological and molecular characteristics, and evaluate the resistance of five Hemerocallis spp. genotypes to the causal agent of rust under greenhouse conditions.
Materials And Methods
Plant material. Hemerocallis lilioasphodelus adult plants infected with rust and plants with healthy appearance were collected in a private garden in the municipality of Chicoloapan de Juárez, State of Mexico, and in a greenhouse in the municipality of Fortín de las Flores, Veracruz. ‘Radiant Greetings,’ ‘Stella d’Oro’ and ‘Cherry Wine’ cultivars from the H. hybrida and H. fulva species were obtained from a garden in Mexico City, all of them with healthy appearance.
Each plant was sown in a pot containing pasteurized soil. The rust-free plants were placed on a table, and the infected plants on another table. The plants with healthy appearance were pruned to obtain new tissue, inoculate them and increase inoculum; then a resistance evaluation was performed. Irrigation was applied to each pot every other day using 200 mL of water. Each pot was fertilized with 2 g of Nitrofoska® Azul (12-12-17+Mg+S+ micronutrients) every 15 days.
Obtaining inoculum. The initial inoculum was 100 mg of P. hemerocallidis uredospores. Spores were collected by shaking the leaves with sporulation on a 20 x 20 cm foil sheet. The isolates were named according to the site where they were collected: RCH1, from the municipality of Chicoloapan de Juárez, State of Mexico, and RFOR2, from the municipality of Fortín de las Flores, Veracruz.
Inoculum increase. To evaluate the resistance, the initial inoculum of RCH1 and RFOR2 was increased. Uredospore suspensions of each isolate were prepared at a concentration of 1 × 106 mL-1 in Soltrol 170® mineral oil, and then uniformly and separately sprayed on plants of the same genotype from which the spores were obtained. The plants were sprayed using a constant-pressure sprinkler injected through a vacuum pump in the rust greenhouse of the International Maize and Wheat Improvement Center (CIMMYT, for its acronym in Spanish). After spraying the plants with the suspension, the oil was left to evaporate and the plants were placed in an incubation chamber for 18 h under complete darkness at 14 °C and 100% relative humidity, for which a Micro-Jet ULV® model 7401 was used for 20 min. Then the plants were taken to a greenhouse with average temperature of 24 °C. When the fungus sporulated, spores were collected, placed in hermetically sealed jars and kept at 5 °C.
Morphological identification. The isolates were morphologically identified based on the form and size of the uredospores and teliospores obtained from cuts of uredia and telia from the collected material. The Cummins and Hiratsuka (1996) key for genera and sections was used in the case of genus, and the descriptions of Hiratsuka et al. (1992) and Hernández et al. (2002) for species.
Molecular identification. The isolates DNA was extracted using the methodology described by Ahrens and Seemüller (1992). The DNA quality was verified through horizontal electrophoresis in 1% agarose gel (Ultrapure, Gibco, USA) and the bands were visualized using a transilluminator (Gel Doc 2000, BIO RAD®, USA). The DNA concentration was quantified using a Lambda BIO 10 (Perkin-Elmer®) spectrophotometer, and dilutions with 20 ng were used to amplify the internal transcribed spacers (ITS1 and ITS2), and the 5.8S ribosomal gene using PCR and by combining ITS4 (5’-TCCTCCGCTTATTGATATGC) and ITS5 (5’-GGAAGTAAAAGTCGTAACAAGG) universal primers. The amplified product was purified using the Wizard kit (Promega® USA) and sequenced with ABI PRISM 3700 (Applied Biosystem®, USA). The consensus sequences were assembled and edited using the CAP option (Contig Assembly Program) of BioEdit v7.0.9.1 software (Hall, 1999) and deposited in the GenBank (NCBI, 2012).
Characterization of resistance
Inoculation. Two experiments were conducted: the first in March 2018, and the second in May 2018. The old leaves of all the genotypes were cut three days before inoculation in order to inoculate only young leaves by spraying them with a suspension of RCH1 and RFOR2 fresh uredospores at a concentration of 1 × 106 mL-1. The uredospores were suspended in 96% ethanol (1 g L-1). The plants were placed in an incubation chamber under the same conditions described for inoculum increase, and in both experiments the plants were kept in a greenhouse at 24 °C average temperature. The experiment unit consisted of one pot with one plant, and five replications for each genotype and for each fungus isolate.
Measurement of resistance. The evaluated variables were the latency period (LP) (days from inoculation to sporulation) and infection type (IT), which refers to the reaction of the host tissue to the pathogen invasion and no-invasion. The plants were inspected daily between days three and 21 after inoculation (dai), and to record the IT, the following classification established by Mueller et al. (2003) was used: R=resistant, no lesions or very few lesions restricted to a hypersensitivity reaction without sporulation; MR=moderately resistant, very few lesions and production of some uredospores; MS=moderately susceptible, a slightly reduced number of lesions or delayed sporulation; S=susceptible, a considerable number of lesions and amount of sporulation.
Results And Discussion
Description of the disease signs and symptoms. The leaves of plants infected with H. lilioasphodelus that were collected in Chicoloapan, State of Mexico, showed interveinal advanced lesions yellow in color, rectangular and coalescent on the upper surface and underside, on which the development of dense, oval, rectangular or irregular shaped medium-sized subepidermal uredia with abundant bright yellow uredospores, was observed (Figure 1-A and B). The leaves of plants collected in Fortín de las Flores, Veracruz, showed initial lesions on the underside that corresponded to medium-sized, dense and circular subepidermal uredia with bright yellow uredospores that matched the upper surface with yellowish, circular or quadrangular spots (Figure 1-C).
Telia were observed only on leaves of the plants collected in Fortín de las Flores, which were black in color, erumpent and slightly long and dense (Figure 1-D). The main symptom observed when uredia and telia pustules invaded the leaf area was a general yellowing of leaves that eventually became necrosed, a fact that caused photosynthesis to slow down, thus reducing the plant growth, as well as the size and number of flowers (Figure 1-E).
Morphological identification of the fungus
Identification at the genus level. Bicellular, pedicelled and horizontally septated teliospores inside non-jelly telia were observed; no peridium in palisade was observed in uredia and telia. According to Cummins and Hiratsuka (1996), these characteristics correspond to the Puccinia genus.
Identification at the species level. Uredospores of both isolates were yellow in color, globose to ellipsoid, with hyaline and equinulated walls, and some were attached to a short pedicel that emerged from the bottom of the uredia. No germinal pores were observed. Measurements of uredospores of the RCH1 isolate were within range: 18.3-22.3 x 15.13-19.3 µm (mean = 20.06 µm ± 1.64 by 17.157 µm ± 1.41, n = 100). Measurements of uredospores of the RFOR2 isolate were: 18-22.7 x 16.4-19.3 µm (mean = 20.17 µm ± 1.81 by 17.749 µm ± 1.28, n = 100) (Figure 1-F).
Teliospores were found only in the RFOR2 isolate, which were ellipsoid and nailed, and had a rounded, angular and eccentric papillae at the apex. Most of the teliospores observed had no septa and measured 30.1-40.8 x 13.3-17.5 µm (mean = 35.887 µm ± 4.70 by 15.518 µm ± 1.67, n = 100) (Figure 1-G). Septated teliospores measured 42.1-51.2 x 14.5-21.2 µm (mean = 46.526 µm ± 3.86 by 17.544 µm ± 2.7, n = 100) (Figure 1-H). The teliospores wall was smooth and turned dark brown as it approached the apex; its sides measured 1 to 1.8 µm (mean = 1.365 µm) and 3.1-5.3 µm at the apex (mean = 4.7 µm ± 0.77, n = 20).
The morphological characteristics of uredospores and teliospores coincided with the description of P. hemerocallidis provided by Hiratsuka et al. (1992), Williams-Woodward et al. (2001) and Hernández et al. (2002). Uredospores of both isolates were slightly smaller than those described by the authors and, the same as in the other American specimens, no septated teliospores were observed. No alternate host was observed in the identified rust, but according to Hiratsuka et al. (1992), P. hemerocallidis has Type 4 spermatogonia.
Molecular identification. After amplification using ITS5 and ITS4 primers, 618 and 623 bp fragments, approximately, were obtained and then deposited in the Genbank (access numbers FJ897533 and FJ897535). The results of BLASTN confirmed that the RCH1 and RFOR2 isolates corresponded to P. hemerocallidis, since the ITS region showed 99% nucleotic similarity with P. hemerocallidis (access number AF479742).
Characterization of resistance. Based on the latency period and type of infection, the evaluated genotypes were grouped in three categories of resistance to P. hemerocallidis (Table 1). No infection differences were observed between isolates and experiments. The type of infection recorded by genotypes was uniform among isolates.
The H. lilioasphodelus species was susceptible because it initially showed abundant, humid chlorotic and bright small lesions three days after inoculation (dai), which sporulated six dai in the form of small and round bright yellow uredia that grew in extended form and had abundant sporulation on leaf upper surface and backside (10 dai) (Figure 2-A). ‘Radiant Greetings’ and ‘Stella d’Oro’ cultivars showed reddish small necrotic lesions five dai, which indicated a hypersensitivity reaction. However, at 10 and 11 dai, respectively, a yellow initial sporulation was observed on some lesions, so they were classified as moderately resistant (Figure 2-B and C). The H. fulva species showed a reduced number of small chlorotic, humid and bright lesions without sporulation at six dai, so it was classified as resistant (Figure 2-D), the same as ‘Cherry Wine’ cultivar, which had no lesions or sporulation (Figure 2-E).
The hypersensitivity reaction (HR) is an active resistance mechanism that operates after the parasite penetrates. In the broad sense, this mechanism is attributed to the presence of major resistance genes that limit the reaction of a specific parasite genotype, but they actually limit a range of interactions ranging from immunity up to a certain level of susceptibility (Jones and Clifford, 1983).
Genotipo | Aislamiento RCH1x | Aislamiento RFOR2y | ||
---|---|---|---|---|
Período delatencia (días) | Tipo de infecciónz | Período delatencia (días) | Tipo de infección | |
H. lilioasphodelus | 6 | S | 6 | S |
‘Radiant Greetings’ | 10 | MR | 10 | MR |
‘Stella d’Oro’ | 11 | MR | 11 | MR |
H. fulva | - | R | - | R |
‘Cherry Wine’ | - | R | - | R |
x Chicoloapan, State of Mexico.
y Fortín de las Flores, Veracruz.
z R= resistant; MR= moderately resistant; S= susceptible.
The genes that confer HR cause the host cell to collapse after the haustorium is formed. The cell collapses a few hours after penetration in order to interfere with the fungus nutriment supply, causing a rapid death of the infection hyphae. At first glance, this phenomenon can be observed in the form of yellowish and necrotic spots. In other cases, the collapse is slower and allows the formation of uredospores (Parlevliet and van Ommeren, 1975; Niks et al., 2011). This explains the type of infection observed in ‘Radiant Greetings’ and ‘Stella d’Oro’ cultivars, because in both cases, hypersensitivity lesions were first observed, but later uredia were detected in some lesions. The studies conducted by Mueller et al. (2003), Li et al. (2007) and Buck (2013) indicate that ‘Stella d’Oro’ cultivar was moderately resistant, resistant and highly resistant, respectively, where the type of infection was limited to necrotic lesions. The reactions observed in the experiments conducted in this study for the cultivar are similar to those reported by the authors, so it seems that there is no variation in the pathogen virulence.
The H. fulva genotype showed slow sporulation on some of the chlorotic lesions outside of the interval of the resistance evaluation, approximately 28 days after inoculation. Parlevliet and van Ommeren (1975) indicated that genotypes with partial resistance have a susceptible type of infection (complete compatibility between the pathogen and its host, which indicates the absence of hypersensitivity), and that the latency period is far longer, while the infection is less frequent compared to a susceptible host. From the established experiments, major differences can be observed in the latency period and infection frequency (not quantified), but no histological studies, as the studies conducted for cereal rusts (Niks, 1983; Moldenhauer et al., 2006), were conducted to specify the level of reaction and thus define the existence of a possible partial resistance. Based only on the coloration changes in the host’s tissue, the types of infection in ‘Radiant Greetings’ and ‘Stella d’Oro’ cultivars have only one type of hypersensitivity resistance. However, H. fulva, which showed only one latency period of approximately 28 days and null macroscopically hypersensitivity reaction, could have partial resistance sensu Parlevliet (Parlevliet and van Ommeren (1975), but this must be further studied.
The RCH1 and RFOR2 isolates inoculated in the different genotypes caused the same resistance reactions, which indicates that there are no variations in pathogenicity. However, studies conducted by Hernández et al. (2002) and Chatasiri et al. (2006) indicate that there is proof of variation in the pathogen, because by comparing the ITS region of several isolates coming from different America and Asia geographical areas, they observed genetic differences in the specimens from each continent. However, they point out that a wider sampling is needed in order to determine if there is genetic variability in the fungus.
Inoculation of different P. hemerocallidis isolates used in the study conducted by Buck (2013) confirms the presence of pathotypes with a different type of virulence in daylily cultivars in the southern area of the United States. Carvalho et al. (2018) report that the absence of the isolate found in Portugal is completely aligned with the sequences from the United States and Costa Rica, but that it differs from the reported sequences from Russia, Japan, Australia and Mexico (sequences reported in the present study).
Rusts are obliged parasites and highly specific to the host specificity; in some rust species the special forms and physiological races are defined according to the host specificity and cultivars (Li et al., 2007). In the case of P. hemerocallidis, there are no reports on its host specificity, so it would not be surprising to find such pathogenic specialization in this pathosystem, considering that it is similar to those that involve rusts in different economically important crops (Leonard and Szabo, 2005; Soto-Estrada et al., 2005; Yáñez et al., 2009), but further studies must be conducted to demonstrate this aspect.
It is known that in macrocyclic rusts, including wheat stem rust| (P. graminis f. sp. tritici) and leaf rust (P. triticina), the genetic recombination occurs in the alternate host and that this is a mechanism to create new virulence combinations. Since Patrinia villosa, an alternate P. hemerocallidis host (Ono, 2003), has not been found in Mexico, its possible influence on the development of genetic variation in the fungus is unknown.
In North America, the first report on this rust was submitted by Williams-Woodward et al. in 2001, when they detected infected material in the United States. Later, the disease quickly spread across America and it is probably present in all the countries where Hemerocallis spp. susceptible cultivars are grown.
Conclusions
The fungus that attack Hemerocallis susceptible genotypes in Mexico correspond to P. hemerocallidis. The H. lilioasphodelus species is susceptible; ‘Radiant Greetings’ and ‘Stella d’Oro’ cultivars from the H. hybrida species were classified as moderately resistant because they showed hypersensitivity resistance; the ‘Cherry Wine’ cultivar and the H. fulva species were included in the group of resistant, the latter probably having partial resistance sensu Parlevliet.
Acknowledgments
The authors wish to thank Dr. Stephen D. Koch (†) of the Colegio de Postgraduados’ Botany Program for their help in identifying the Hemerocallis species used in the present study.
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Received: October 20, 2019; Accepted: November 23, 2019