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Article

New Races of Hemileia vastatrix Detected in Peruvian Coffee Fields

by
Alberto Julca-Otiniano
1,
Leonel Alvarado-Huamán
1,
Viviana Castro-Cepero
2,
Ricardo Borjas-Ventura
1,
Luz Gómez-Pando
1,
Ana Paula Pereira
3,4,
Stephan Nielen
5,
Ivan Ingelbrecht
6,
Maria do Céu Silva
3,4,* and
Vítor Várzea
3,4
1
Departamento de Fitotecnia, Facultad de Agronomía, Universidad Nacional Agraria La Molina, Lima 12-056, Peru
2
Departamento de Biología, Facultad de Ciencias, Universidad Nacional Agraria La Molina, Lima 12-056, Peru
3
Centro de Investigação das Ferrugens do Cafeeiro, Instituto Superior de Agronomia, Universidade de Lisboa, Quinta do Marquês, 2784-505 Oeiras, Portugal
4
LEAF-Linking Landscape, Environment, Agriculture and Food, Associate Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal
5
Embrapa Recursos Genéticos e Biotecnologia, Brasília 70770-917, DF, Brazil
6
Plant Breeding and Genetics Laboratory, Joint FAO/IAEA Centre of Nuclear Techniques in Food and Agriculture, International Atomic Energy Agency Laboratories, 2444 Seibersdorf, Austria
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(8), 1811; https://doi.org/10.3390/agronomy14081811
Submission received: 12 June 2024 / Revised: 3 August 2024 / Accepted: 12 August 2024 / Published: 16 August 2024
(This article belongs to the Section Pest and Disease Management)
Versions Notes

Abstract

:
Coffee leaf rust (CLR), a fungal disease caused by Hemileia vastatrix, represents Peru’s most significant threat to coffee production. The CLR epidemic (2012–2013) led Peru to implement an emergency plan under which coffee plantations underwent renewal using rust-resistant varieties derived from a Timor hybrid (HDT; Coffea arabica × canephora hybrid) like Catimors. Nevertheless, new pathogenic rust races capable of infecting these varieties have been recorded. Eighteen rust samples from coffee genotypes, such as Caturra, Typica, and Catimor, were collected in various Peruvian regions and sent to CIFC/ISA/UL (Centro de Investigação das Ferrugens do Cafeeiro/Instituto Superior de Agronomia/Universidade de Lisboa) in Portugal for race characterization. Assessing the virulence spectra of rust samples on a set of 27 coffee differentials resulted in the identification of 5 known and 2 new races. This study emphasizes the significance of conducting surveys on the diversity of H. vastatrix races in Peru for effective disease management. Moreover, Catimor lines, widely cultivated in coffee-growing countries, are susceptible to the 2 new races and to races XXXIV and XXXV identified in this study. Thus, coffee farmers need to know the resistance spectrum of new varieties before introducing them to CLR-affected regions.

1. Introduction

Coffee leaf rust (CLR), a fungal disease caused by Hemileia vastatrix Berk and Broome (phylum Basidiomycota, class Pucciniomycetes, order Pucciniales), represents a primary challenge for Arabica coffee growers, leading to annual losses estimated between one and two billion US dollars worldwide [1].
The initial record of CLR dates to 1861, when an English explorer observed it on wild coffee species near Lake Victoria in East Africa. However, in 1869, CLR caused an epidemic in the Asian island of Ceylon (Sri Lanka) leading to severe social and economic repercussions [2] cited by Talhinhas et al. [3]. It took about one hundred years for the fungus to reach the Americas, first in Brazil (1970) and later in all Latin American coffee-growing countries, such as Nicaragua (1976), El Salvador (1979), Peru (1979), Honduras and Guatemala (1980), Mexico (1981), Colombia (1983), Costa Rica (1983), and Cuba (1984) [4]. In Hawaii, it was reported in 2021 [5,6].
In Peru, coffee has been widely cultivated since the late 19th century. It is the leading agricultural export commodity, with 3.826 million 60 kg bags exported in the marketing year 2023/2024 (April/March), accounting for 96.9% of the total production. Peru produces almost exclusively Arabica coffee, of which over 70% is the Typica variety, followed by Caturra (20%) and other varieties (10%) [7]. Coffee is mostly cultivated under shade on 375,000 hectares distributed in 16 regions (out of 25), and the main coffee-producing areas are localized across the eastern slope of the Andes in the regions of Cajamarca, San Martin, Junín, and Amazonas. About 75% of Peruvian coffee cultivation occurs between 1000 and 1800 m above sea level. Arabica coffee is mostly hand-picked, and sun-dried. The harvest season begins in April and runs through September. With around 90,000 hectares of certified organic coffee, Peru is the world’s leading exporter of organic coffee [7]. Coffee is a source of employment for more than 223,000 families in the country [7,8]. CLR was first reported more than 40 years ago in the district of Satipo, Junín region [9] and is still affecting almost 40% of this crop [7].
H. vastatrix is a fungal pathogen that exhibits hemicyclic characteristics, generating urediniospores, teliospores, and basidiospores. However, it is solely the urediniospores that cause the disease. These asexual, dycariotic spores can reinfect the coffee leaves under suitable environmental conditions. Teliospores are uncommon and exhibit germination in situ, giving rise to a promycelium that generates four spherical basidiospores. The sexual basidiospores are monokaryotic and germinate in vitro but cannot infect coffee leaves [3,10,11].
H. vastatrix, like other rust fungi species, functions as an obligate biotroph that relies on the presence of its living host to feed, grow, and reproduce. Rust fungi differentiate specialized infection structures called haustoria within the living host cell that are essential in the pathogen uptake of nutrients [12,13,14,15].
The infection process of H. vastatrix starts with urediniospore germination and appressorium formation over stomata on the underside of the coffee leaves, followed by the differentiation of post-penetration fungal structures (intercellular hyphae and haustoria) [16]. For optimal germination, urediniospores require water and a temperature range of 22–28 °C, while appressorium formation is accelerated at 13–16 °C. In turn, fungal penetration appears to happen faster if, after wetting the urediniospores, the temperature drops from 23 °C to around 17 °C in a few hours. These conditions are most common during the nightfall in Arabica coffee-growing regions [17].
The disease symptoms correspond to chlorotic spots, which precede the emergence of urediniosporic sori through stomata in a bouquet-like shape, resulting in defoliation and sometimes plant death. The urediniosporic sori appear as orange-colored pustules, the typical sign of this disease. Initially, the chlorotic spots are about 1–3 mm in diameter, but they continually expand and merge into larger chlorotic lesions. Sometimes, the centers of the oldest lesions become necrotic, and the sporulation zone is confined to the outermost area. The main impact of CLR is defoliation, which reduces plant photosynthetic area, thus affecting coffee production and influencing the quality of coffee [18,19]. CLR also leads to secondary losses in the years following an epidemic, as heavily defoliated branches die and can no longer produce berries [20].
Breeding rust-resistant coffee has been one of the most efficient and environmentally friendly ways to reduce yield losses and control CLR. For such a purpose, and because no single coffee-growing country holds all the races of H. vastatrix, research on CLR on a global level was centralized at CIFC/ISA/UL (Centro de Investigação das Ferrugens do Cafeeiro/Instituto Superior de Agronomia/Universidade de Lisboa) in Portugal since 1955, holding unique characterized germplasm collections of both the plant and the pathogen. Timor hybrids (HDTs), which are natural C. arabica × C. canephora hybrids, are the most widely used source of resistance to CLR. Discovered, characterized, and supplied by CIFC/ISA/UL to research institutions in coffee-growing countries around the globe, these hybrids have been incorporated into breeding programs addressing the agroecological particularities of each region [3,16,19,21,22]. More than 90% of the CLR-resistant varieties cultivated worldwide resulted from these efforts. Nonetheless, the recent emergence of new H. vastatrix races that have overcome the resistance of some coffee varieties [3,23,24] highlights the coevolutionary dynamics of the plant and the pathogen. Moreover, since 2008, Latin America and the Caribbean have experienced a series of CLR outbreaks linked to combined favorable regional meteorological conditions, namely the longer-term changes in temperature and rainfall associated with climate change, and challenging economic factors, all contributing to neglected coffee crop management [18,20,25,26].
In Peru in the 2012–2013 epidemic season, there was a 60% decrease in the coffee harvest, valued at approximately US $290 million. This drove the execution of an emergency plan, supported by a fund of around US $30 million, administered by the National Agricultural Health Service (SENASA). This occurrence resulted in the rejuvenation of coffee plantations by introducing rust-resistant varieties derived from HDT, like Catimors [27]. CLR has struck all coffee-growing regions of Peru where susceptible varieties, mainly Typica and Caturra Roja, have historically been grown. Nowadays, Peru boasts over forty commercial coffee varieties, encompassing both traditional varieties like Typica, Bourbon, Caturra, and Mundo Novo, alongside derivatives of HDT, including Catimor, Colombia, Costa Rica 95, Obatã, Marsellesa, and Limani [28].
Inheritance studies of rust resistance performed at CIFC demonstrated that the gene-for-gene theory [29] applies to coffee—H. vastatrix interactions [30,31] with the resistance of coffee plants being conditioned by at least nine major dominant genes (SH1–SH9), singly or associated. Following the same theory, it was possible to infer nine genes of virulence (v1–v9) in the pathogen [16,21]. These SH resistance genes were characterized through genetic analyses of population descendants according to Mendelian proportions. Major genes SH1, SH2, SH4, and SH5 were found in pure Arabicas of Ethiopian origin, the gene SH3 originated from C. liberica, and SH6, SH7, SH8, and SH9 were only found in HDT derivatives, therefore presumably originating from the C. canephora parent in the hybrid [16,21]. SH5 is found in Typica and Bourbon varieties and all its descendants (hybrids and/or mutants), such as Caturra, Catuaí, Mundo Novo, Pacas, San Ramón, and Villa Sarchi. SH1, alone or in association with the SH5 gene, is found in the Dilla & Alghe and Geisha varieties, respectively. SH2 is associated with SH5 in the variety Blue Mountain. SH3 is associated with the genes SH5, SH2,4, and SH2,5 in the varieties S.288, S.333, and S.795, respectively. The SH2 and SH3 genes have never been characterized alone but have always been associated with the SH5 resistance gene. In turn, the descendant populations of HDT known as Catimor (Caturra × HDT CIFC 832/1) and Sarchimor (Villa Sarchi × HDT CIFC 832/2) bear the SH6, SH7, SH8, and SH9 genes associated with the SH5 gene.
The evidence of high pathogenic variability in H. vastatrix has been known for a long time and is associated with the loss of resistance in coffee plants. Mayne, in India, was the first to describe the physiological specialization [32,33], identifying four rust races. Since the 1950s, CIFC has conducted and expanded world surveys of rust races under the leadership of its founder, Prof. D’Oliveira, using spore samples of H. vastatrix collected from various coffee-growing regions globally. In addition, distinct races or pathotypes have been identified through the differentiation of isolates in a set of coffee genotypes carrying different resistance gene combinations (differentials) [16,31,34]. Currently, more than 55 rust physiological races have been identified in a set of 27 coffee differentials, as reported by Silva et al. [24] and references therein. However, it has not yet been possible to characterize the full virulence genotype for some of the identified races due to the lack of appropriate coffee differentials [3] (CIFC database). The swift adaptation of H. vastatrix to circumvent coffee defenses is puzzling considering the pathogen’s asexual lifecycle, which typically limits the emergence of new genotypes through recombination [35] cited by Koutouleas et al. 2019 [36]. Several studies have assessed to analyze genetic variability in H. vastatrix, using molecular markers [37,38,39,40,41,42]. Findings from these studies suggest a range of genetic variability, but specific molecular markers for the different rust pathotypes have so far not been identified. Recently, through genomic research, H. vastatrix populations have been categorized into three genetically divergent lineages with strong host specialization, distinguishing rusts that infect diploid and tetraploid coffee species. Evidence of recombination and signs of introgression were also discovered, indicating the potential for virulence factors to be exchanged between different rust lineages. This could potentially increase virulence, thereby contributing to the frequent emergence of new pathotypes [24] and references therein, [43,44]. More recently [45], a genomic analysis revealed genetic variations within a global sample of rusts from Coffea arabica and interspecific hybrids. This analysis identified three divergent genetic subgroups: a low-differentiated and widely distributed rust lineage and two highly differentiated groups from Africa and East Timor.
Even though molecular studies suggested high H. vastatrix diversity within rust samples from Peru [40,41], there has been a lack of research on the interaction of the pathogen races with the coffee varieties grown in Peru, which is essential knowledge to breed more efficiently for disease resistance. This work represents the first characterization of H. vastatrix races collected from various coffee genotypes across different regions of Peru.

2. Materials and Methods

2.1. Rust Samples

Eighteen rust samples, collected from diverse coffee genotypes across various regions of Peru, were dispatched to CIFC (Portugal) for race identification: one rust sample in San Juan del Oro in the Puno region (variety Typica); eleven samples in San Ramón, Junín region (varieties Bourbon, Typica, Caturra, Catuaí and Maragogipe); two samples in Tingo Maria, Huánaco region (varieties Bourbon and Catuaí); one sample in Pichanaki, Junín region (variety Catimor); three samples in Villa Rica in the Pasco region (varieties Catuaí and Catimor). Technicians from the Ministry of Agriculture in Peru identified the coffee varieties where these rust samples were collected.
The urediniospores were harvested from infected leaves, which had been dried at room temperature. The spores were subsequently collected in gelatin capsules.
To confirm the identity of these samples, a small portion of spores from each sample was stained and mounted in lactophenol cotton blue containing three components: a phenol that kills any live organism, lactic acid that preserves the structure of the fungus, and cotton blue that stains the fungus, allowing for better identification [46]. The microscopic visualization showed that the urediniospores were reniform with a strongly warty convex side and smooth on the straight or concave side, as previously described [47,48]. Observations were made using a bright-field microscope (Leica DM-2500).

2.2. Inoculation

Urediniospores from each sample were initially multiplied on a susceptible genotype Matari (CIFC 849/1) for further inoculation on a set of 27 coffee differentials: clonal lines of 5 C. arabica selections, 16 tetraploid hybrids of C. arabica × Coffea spp., and 6 Coffea spp. selections [24]. The coffee plants were maintained in greenhouse conditions at temperatures between 15 °C and 30 °C and relative humidity of 60–80%.
On the day before inoculation, the plants were watered abundantly to ensure that the leaves were turgid. Following a standard procedure used at the CIFC [21,34,49], inoculations were carried out by placing, with a scalpel, fresh urediniospores (1 mg/pair of leaves) on the lower surface of young, fully expanded leaves from the terminal node. The urediniospores were then carefully brushed off with a camel’s hair brush. The inoculated leaves were sprayed with distilled water, wrapped in a damp plastic bag, and kept in the dark for 24 h.

2.3. Evaluation of Reaction Types

The evaluation of reaction types in the coffee differentials was done according to the following qualitative scale used at CIFC [21,34,49]:
i = Immune (no visible symptoms);
fl = Flecks (small chlorotic flecks) at the penetration sites that are well visible with a pocket lens or by holding the leaf against the light;
t = Punctiform tumefactions, often associated with flecks;
0 = Chlorotic spots, sometimes associated with small necrosis but without spore production;
1 = Rare sporulating sori always very small (sometimes only visible with a pocket lens) in chlorotic areas, sometimes associated with necrosis;
2 = Small or medium-sized pustules diffused but visible macroscopically in areas with intense chlorosis;
3 = Medium-sized or large pustules surrounded by chlorosis;
4 = Large sporulating pustules, sometimes surrounded by a slight chlorotic halo (highly susceptible or compatible);
X = Heterogeneous reaction with pustules very variable in size associated with resistant reaction types.
This qualitative scale makes it possible to characterize both the plant resistance and the virulence of H. vastatrix.
For the characterization of rust races, about forty days after the inoculation, coffee differentials were evaluated using this scoring scale, where reaction types i, fl, t, and 0 (chlorotic lesion without urediniospores on its surface) are classified as resistant, and the rust sample as avirulent. When urediniospores form on lesion surfaces, they might cover just a small part of the lesion (reactions 1 and 2), the entire lesion (reaction 4), or most of the lesion with a small non-sporulating chlorotic halo surrounding it (reaction 3). All these scenarios indicate susceptibility, and the rust sample is virulent. To ensure reliability, the inoculation of each coffee differential with all the rust samples and the subsequent qualitative assessment of the reaction types were repeated at least twice.

2.4. Inference of Virulence Genes

The virulence genes of each rust sample were inferred according to the gene-to-gene Flor theory [29]. As an example, for a rust sample that produces spores (reaction types 1–4) on a coffee differential, such as the CIFC 32/1 Kents carrying the resistance genes SH2, SH5, we inferred that the sample has the virulence genes v2 and v5. If the same sample also produces spores on coffee differential CIFC 110/5–S4 Agaro bearing the genes SH4, SH5, it means that it also has the virulence genes v4 and v5.

3. Results and Discussion

The analysis of reaction types of the Peruvian rust samples on the set of coffee differentials allowed us to characterize the following races and the corresponding virulence genes (Table 1): race I (v2,5), race XXIII (v1,2,4,5), race XXIV (v2,4,5), race XXXIV (v2,5,7 or v2,5,7,9), race XXXV (v2,4,5,7,9). Importantly, two rust races showed new virulence profiles [(v2,4,5,7,8 or v2,4,5,7,8,9) and (v1,2,4,5,7,8 or v1,2,4,5,7,8,9)]. These new races/genotypes of virulence were identified for the first time at CIFC.
Rust races tend to be distributed in patterns that correspond to the occurrence of resistance genes within local coffee populations [3] (CIFC database). Among coffee-growing countries, the v2 virulence gene is the second most widespread, following v5. The gene v2 can infect coffee varieties with resistance gene SH2, like Kents. This is the oldest variety of Arabica coffee cultivated in India, named after Mr. L. P. Kent, a British planter who first selected it in Mysore in 1920. Notably, it was the first coffee selected for CLR resistance. It has been widely cultivated in India since the 1930s but a few years later became susceptible. It belongs to the Typica family, and its characteristics of rust resistance associated with good cup quality contributed to its dissemination throughout all coffee-growing countries within Arabica coffee breeding programs, mainly in Kenya, Uganda, and Tanzania and in other East African countries as well as in Indonesia [50].
Rust races that only have the virulence gene v5 can infect the Arabica varieties carrying the resistance gene SH5, like Caturra, Bourbon, Typica, and Mundo Novo. Furthermore, the rust races carrying different associations of virulence genes v1, v2, v4, and v5 can infect all known pure Arabica varieties (different associations of resistance genes SH1, SH2, SH4 and SH5) [3,16,21,51].
The rust races I (v2,5) and XXIV (v2,4,5), characterized in this study, are widely distributed in coffee-growing countries of South and Central America, Africa, and Asia (CIFC database). The rust race XXIV (v2,4,5) was also recently reported in Hawaii [52]. Ramírez-Camejo et al. [53] reported a genotypic relationship between Central American and Jamaican populations of Hemileia vastatrix and Hawaii rust isolates recently introduced on this Island. According to their analysis, the appearance of CLR in Hawaii most likely resulted from the accidental introduction of spores or infected plant material brought in by travelers, seasonal workers, or through shipments of contaminated coffee from Central America or the Caribbean.
The race XXIV (v2,4,5) is avirulent to Arabica genotypes, such as Dilla & Alghe (SH1), Geisha (SH1,5), and S.288 (SH3,5), as well as to HDT derivatives like Catimors (Caturra CIFC 19/1 × HDT CIFC 832/1) and Sarchimors (Villa Sarchi × HDT CIFC 832/2) with different associations of resistance genes SH5, SH6, SH7, SH8 and SH9 [3,16,21].
Rust races with different associations of virulence genes v5, v6, v7, v8, and v9 with or without the virulence genes v1, v2, or v4 can infect varieties derived from HDT, like some genotypes of Catimor and Sarchimor [21,51]. The main difficulty in characterizing the spectra of virulence in H. vastatrix samples from HDT derivatives is related directly with the lack of new coffee differentials (new combinations of resistance genes) and sometimes with unstable reaction types, as observed at CIFC in Icatu [54] and in Brazil [50].
The race XXXIV (v2,5,7 or v2,5,7,9) identified in this study was also recently characterized in rust samples collected from germplasm fields in China’s major coffee-growing regions [55].
The detection of Peruvian rust races with an increasing number (2 to 7) of virulence genes, like race I (v2,5); race XXIII (v1,2,4,5); race XXIV (v2,4,5); race XXXIV (v2,5,7 or v2,5,7,9); race XXXV (v2,4,5,7,9); the new race not yet designated (v2,4,5,7,8 or v2,4,5,7,8,9); as well the new race (v1,2,4,5,7,8 or v1,2,4,5,7,8,9) shows the pathogen’s nature to evolve new virulence genes by consecutive mutations [56,57] or, eventually, by introgression or recombination events [43,44].
The level of virulence of rust races observed in coffee regions in Peru is very high and can infect all the Arabica varieties as well as many derivatives of HDT, namely the Catimor population. According to the CIFC’s experience, it is normal to find rust races with this level of virulence when pure Arabicas and Catimor are grown side by side in coffee fields as well as in germplasm banks where the selection pressure is very high. On the other hand, in regions where the Catimor variety or HDT derivatives are the most widely grown, such as East Timor, the rust races observed have the virulence genes v5, v6, v7, v8, and v9 and others yet to be determined, but do not have the virulence genes v1, v2, v3 or v4, since pure Arabica varieties are not grown in this region. This phenomenon shows the very great ability of H. vastatrix to increase virulence and points out the importance of knowing the genetic background of resistance of the varieties to be planted in coffee regions.
A gradual erosion of resistance to CLR has been detected in Catimor-derived varieties worldwide over the past 25 years, coinciding with the appearance of increasingly virulent rust races. It is important to mention that the term “Catimor” is used in an indiscriminate way to mention all the coffee genotypes from HDT while not all of them have the same background of resistance. The main reason for this nonuniformity in resistance level is due to the erosion of SH resistance genes during the selection process of the varieties once the SH genes are not homozygous in the Catimor population. On the other hand, there are several introductions of HDT in the Catimor group with different spectra of resistance like HDT CIFC 832/1, 832/2, 1343, and 2570.
From CIFC HW26/5 (Caturra CIFC 19/1 × HDT CIFC 832/1), many varieties were selected in different coffee-growing countries, like var. Costa Rica 95 (Costa Rica), var. Oeiras (Brazil), var. IHCAFE 90 (Honduras), var. Anacafé (Guatemala), var. Catisic (El Salvador), var. Lempira (Honduras), var. Oro Azteca (Mexico), etc. From CIFC H361/4 (CIFC 971/10 Villa Sarchi × HDT CIFC 832/2) were selected the varieties Obatã, Tupi, IAPAR 59, IPR 97–99, IPR 104, IPR 107–108, Acauã (Brazil), var. Cuscatleco (El Salvador), and var. Chandragiri (India). From HDT CIFC 1343 were selected the varieties Colombia, Batian, Tabi, Catillo, and Catimor 129 (Colombia). From CIFC 2570 in Brazil were selected the following varieties: Catiguá, Paraíso, Pau Brazil, and Sacramento [19,58,59,60,61,62,63].
During the selection of new varieties, coffee breeders encounter various constraints, such as limited information on the local rust population and its evolution, as well as challenges in distinguishing between plants with narrow and high spectra of resistance to rust. Without this crucial information, there is a high probability of a breeder selecting plants with good agronomic characteristics but low spectra of resistance (few SH genes). Perhaps for this reason, some Catimors show higher levels of resistance than others, even descendants of the same progenitors. The same also happens with the Sarchimors group. Thus, predicting the durability of resistance becomes challenging when the virulence of local rust races and the range of resistance in the host is unknown.
The results presented here are also relevant for current attempts to develop plants with new resistance alleles by using induced mutations. By using gamma irradiation of seeds or chemical mutagenesis of explants, mutant populations are being generated that are tested for resistance to the new races of H. vastatrix [64,65]. This strategy aims to overcome the limited gene pool available for crossing experiments.

4. Conclusions

In this study, almost all the known virulence genes (v1 to v9) were detected in Peruvian coffee fields except v3 and v6. The absence of the v3 and v6 virulence genes in this study could be due to an escape or, probably, to the absence or rarity of coffee genotypes cultivated with the corresponding SH3 (e.g., Indian varieties S.288, S.795) and SH6 resistance genes in Peru. Our results provide essential guidance to coffee growers, breeders, and allied industries in Peru and elsewhere who intend to control CLR by planting resistant varieties. Indeed, the genes v7, v8, and v9 are virulent to many HDT derivatives.
The development of rust-resistant varieties in different coffee-growing countries has been made possible by HDT, which has underpinned all the coffee breeding programs focused on CLR resistance [3,16,19,21,22]. However, in recent years, there has been a progressive breakdown in the resistance of these varieties in several countries due to the appearance of more virulent H. vastatrix races. Most of the population lines derived from HDT, such as Catimor, are widespread in coffee-growing countries. However, these lines are susceptible to the two new races, as well as to the races XXIV and XXXIV detected in this study (CIFC database). By providing Peruvian coffee growers with knowledge of the resistance profiles of commercial coffee varieties, they can successfully transition from susceptible traditional varieties like Caturra, Typica, and Bourbon to new resistant ones.

Author Contributions

Conceptualization, V.V., M.d.C.S., A.J.-O. and L.A.-H.; methodology, V.V., A.P.P., M.d.C.S., L.A.-H., V.C-C., R.B.-V. and L.G.-P.; validation, V.V., A.P.P. and M.d.C.S.; investigation, V.V., A.P.P., M.d.C.S., L.A.-H., V.C-C., R.B.-V. and L.G.-P.; resources, A.J.-O., V.V., A.P.P., M.d.C.S., L.A.-H., V.C-C., R.B.-V. and L.G.-P.; writing—original draft preparation, A.J.-O., V.V., M.d.C.S., A.P.P., L.A.-H., R.B.-V., V.C.-C., L.G.-P., S.N. and I.I.; writing—review and editing, A.J.-O., V.V., M.d.C.S., A.P.P., L.A.-H., R.B.-V., V.C.-C., L.G.-P., S.N. and I.I.; supervision, V.V., M.d.C.S., A.J.-O., S.N. and I.I. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Research Agreement between CIFC/ISA/Universidade de Lisboa and the International Atomic Energy Agency (IAEA) in the scope of the project “Efficient Screening Techniques to Identify Mutant Plants with Resistance to Disease” (CRP code: D22005), by FCT—Fundação para a Ciência e a Tecnologia, I.P., under the project reference UIDB/04129/2020 of LEAF (Linking Landscape, Environment, Agriculture and Food) Research Center and DOI identifier 10.54499/UIDB/04129/2020, and by PROCIENCIA for financing the project “Study of the genetic variability and characterization of coffee rust (Hemileia vastatrix L.) in Peru as a basis for the development of an integrated management program for the disease in a context of climate change” [Agreement No. PE501078996-2022].

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Table 1. Characterization of virulence genes in eighteen rust samples from various coffee varieties and different Peruvian regions.
Table 1. Characterization of virulence genes in eighteen rust samples from various coffee varieties and different Peruvian regions.
Rust Sample NumberCoffee VarietyRegionVirulence GenesRace
1 *Typica San Juan del Oro (Puno)v1,2,4,5XXIII
2 **Caturra AmarillaSan Ramón (Junín) BGv1,2,4,5XXIII
3 **Caturra RojoSan Ramón (Junín) BGv1,2,4,5XXIII
4 *CatuaíTingo Maria (Huánuco)v2,5I
5 *Bourbon RojoTingo Maria (Huánuco)v2,4,5XXIV
6 **CaturraSan Ramón (Junín) BGv1,2,4,5,7,8 or v1,2,4,5,7,8,9new race ***
7 **MaragogypeSan Ramón (Junín) BGv1,2,4,5,7,8 or v1,2,4,5,7,8,9new race ***
8 **CatuaíSan Ramón (Junín) BGv1,2,4,5XXIII
9 **BourbonSan Ramón (Junín) BGv1,2,4,5XXIII
10 **Typica San Ramón (Junín) BGv1,2,4,5XXIII
11 *Catimor Pichanaki (Junín)v2,4,5,7,8 or v2,4,5,7,8,9new race ***
12 *Caturra Villa Rica (Pasco)v1,2,4,5,7,8 or v1,2,4,5,7,8,9new race ***
13 *Caturra Villa Rica (Pasco)v1,2,4,5,7,8 or v1,2,4,5,7,8,9new race ***
14 *Catimor Villa Rica (Pasco)v1,2,4,5,7,8 or v1,2,4,5,7,8,9new race ***
15 **CaturraSan Ramón (Junín) BGv2,5,7 or v2,5,7,9XXXIV
16 **CaturraSan Ramón (Junín) BGv2,4,5,7,9XXXV
17 **CaturraSan Ramón (Junín) BGv2,5 I
18 **CaturraSan Ramón (Junín) BGv2,5,7 or v2,5,7,9XXXIV
* Samples collected on coffee farms. ** Samples collected in the germplasm bank of the Universidad Nacional Agraria La Molina. *** New rust race not yet designated.
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Julca-Otiniano, A.; Alvarado-Huamán, L.; Castro-Cepero, V.; Borjas-Ventura, R.; Gómez-Pando, L.; Pereira, A.P.; Nielen, S.; Ingelbrecht, I.; Silva, M.d.C.; Várzea, V. New Races of Hemileia vastatrix Detected in Peruvian Coffee Fields. Agronomy 2024, 14, 1811. https://doi.org/10.3390/agronomy14081811

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Julca-Otiniano A, Alvarado-Huamán L, Castro-Cepero V, Borjas-Ventura R, Gómez-Pando L, Pereira AP, Nielen S, Ingelbrecht I, Silva MdC, Várzea V. New Races of Hemileia vastatrix Detected in Peruvian Coffee Fields. Agronomy. 2024; 14(8):1811. https://doi.org/10.3390/agronomy14081811

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Julca-Otiniano, Alberto, Leonel Alvarado-Huamán, Viviana Castro-Cepero, Ricardo Borjas-Ventura, Luz Gómez-Pando, Ana Paula Pereira, Stephan Nielen, Ivan Ingelbrecht, Maria do Céu Silva, and Vítor Várzea. 2024. "New Races of Hemileia vastatrix Detected in Peruvian Coffee Fields" Agronomy 14, no. 8: 1811. https://doi.org/10.3390/agronomy14081811

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