Next Article in Journal
Genetic Diversity and Geographic Distribution of Cucurbit-Infecting Begomoviruses in the Philippines
Previous Article in Journal
Physiological and Full-Length Transcriptome Analyses Reveal the Dwarfing Regulation in Trifoliate Orange (Poncirus trifoliata L.)
Previous Article in Special Issue
Identification of Long-Distance Transport Signal Molecules Associated with Plant Maturity in Tetraploid Cultivated Potatoes (Solanum tuberosum L.)
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Diversity of Late Blight Resistance Genes in the VIR Potato Collection

N.I. Vavilov Institute of Plant Genetic Resources (VIR), St. Petersburg 190000, Russia
Institute of Phytopathology, Bol’shiye Vyazemy, Moscow 143050, Russia
Institute of Agricultural Biotechnology, Moscow 127550, Russia
Author to whom correspondence should be addressed.
Plants 2023, 12(2), 273;
Received: 9 December 2022 / Revised: 26 December 2022 / Accepted: 3 January 2023 / Published: 6 January 2023
(This article belongs to the Special Issue Genetics and Breeding of Cultivated Potato (Solanum tuberosum L.))


Late blight (LB) caused by the oomycete Phytophthora infestans (Mont.) de Bary is the greatest threat to potato production worldwide. Current potato breeding for LB resistance heavily depends on the introduction of new genes for resistance to P. infestans (Rpi genes). Such genes have been discovered in highly diverse wild, primitive, and cultivated species of tuber-bearing potatoes (Solanum L. section Petota Dumort.) and introgressed into the elite potato cultivars by hybridization and transgenic complementation. Unfortunately, even the most resistant potato varieties have been overcome by LB due to the arrival of new pathogen strains and their rapid evolution. Therefore, novel sources for germplasm enhancement comprising the broad-spectrum Rpi genes are in high demand with breeders who aim to provide durable LB resistance. The Genbank of the N.I. Vavilov Institute of Plant Genetic Resources (VIR) in St. Petersburg harbors one of the world’s largest collections of potato and potato relatives. In this study, LB resistance was evaluated in a core selection representing 20 species of seven Petota series according to the Hawkes (1990) classification: Bulbocastana (Rydb.) Hawkes, Demissa Buk., Longipedicellata Buk., Maglia Bitt., Pinnatisecta (Rydb.) Hawkes, Tuberosa (Rydb.) Hawkes (wild and cultivated species), and Yungasensa Corr. LB resistance was assessed in 96 accessions representing 18 species in the laboratory test with detached leaves using a highly virulent and aggressive isolate of P. infestans. The Petota species notably differed in their LB resistance: S. bulbocastanum Dun., S. demissum Lindl., S. cardiophyllum Lindl., and S. berthaultii Hawkes stood out at a high frequency of resistant accessions (7–9 points on a 9-point scale). Well-established specific SCAR markers of ten Rpi genes—Rpi-R1, Rpi-R2/Rpi-blb3, Rpi-R3a, Rpi-R3b, Rpi-R8, Rpi-blb1/Rpi-sto1, Rpi-blb2, and Rpi-vnt1—were used to mine 117 accessions representing 20 species from seven Petota series. In particular, our evidence confirmed the diverse Rpi gene location in two American continents. The structural homologs of the Rpi-R2, Rpi-R3a, Rpi-R3b, and Rpi-R8 genes were found in the North American species other than S. demissum, the species that was the original source of these genes for early potato breeding, and in some cases, in the South American Tuberosa species. The Rpi-blb1/Rpi-sto1 orthologs from S. bulbocastanum and S. stoloniferum Schlechtd et Bché were restricted to genome B in the Mesoamerican series Bulbocastana, Pinnatisecta, and Longipedicellata. The structural homologs of the Rpi-vnt1 gene that were initially identified in the South American species S. venturii Hawkes and Hjert. were reported, for the first time, in the North American series of Petota species.

1. Introduction

The potato belongs to major staple crops that sustainably feed the world [1,2]. To attain this goal, current potato breeding heavily relies on the incessant inflow of new genes that stand for durable resistance to abiotic and biotic adverse factors and higher tuber yield of better quality.
In Russia, with its annual potato production of about 22 million metric tons and consumption of 110 kg per capita per year (; assessed on 4 January 2023), this crop is the mainstay of food security. Here, as well as worldwide, late blight (LB) caused by the oomycete Phytophthora infestans (Mont.) de Bary is a major threat to potato crops, and the dominant race-specific genes for resistance to P. infestans (Rpi genes) have been most vigorously searched for by geneticists and explored by breeders [3,4,5,6,7,8,9]. These genes are found in wild, primitive, and cultivated tuber-bearing species of Solanum L. (section Petota Dumort.), and many of these genes have been successfully introgressed into potato cultivars by sexual and somatic hybridization or by genetic transformation. By now, over 20 Rpi genes, all belonging to the CC-NB-LRR group, have been established and investigated in great detail in diverse Petota species, particularly those belonging to the North American and Mesoamerican series Bulbocastana (Rydb.) Hawkes, Demissa Buk. and Longipedicellata Buk. and to the South American series Tuberosa (Rydb.) Hawkes [2,5,6,9,10,11,12,13,14]. Outside two American continents and beyond the section Petota, we find the homologous Rpi genes in such widespread species as S. americanum Mill. and S. nigrum L. [15,16].
Novel sources of LB resistance for germplasm enhancement are in high demand with breeders because of pathogen migration and rapid evolution; therefore, preferred are potato species and Rpi genes that have not been previously involved in large-scale breeding. With the advent of the “omics” era, the molecular genetic approach to broadening the basic germplasm resource for potato breeding is speedily gaining momentum. Especially significant in this context is new knowledge on the structure and function of the Rpi genes; no less important are the advanced technologies of mining for these genes in germplasm collections and introducing the beneficial genes to practical breeding. As a result, even although most Petota species have not been sufficiently researched, we evidence the expanding list of prospective breeding sources, with many promising accessions and particular individuals further maintained as clones that contribute new valuable alleles for germplasm enrichment [2,10,17,18,19,20,21,22,23,24,25].
Several World Genbanks in Europe and America maintain vast genetic collections of tuber-bearing Solanum species, and numerous accessions of these species have been screened for LB resistance with specific and well-characterized pathogen isolates. The wild potato germplasm maintained in the local collections seems to present another exciting treasure trove of the Rpi genes. As a result, many resistant accessions have been earmarked across the Petota species [25,26,27,28,29,30,31].
To mine for the Rpi genes, researchers utilize such specific technologies as PCR amplification, e.g., with the sequence characterized amplified region (SCAR) markers [3,22,32,33,34], and the resistance gene enrichment sequencing technologies [7,15,35,36]. An alternative approach, effectoromics, employs avirulence (Avr) genes of P. infestans matching the corresponding Rpi genes [5] as a tool for recognizing new Rpi genes and, what is most significant, discerning between the functional genes and their structural homologs, which may possess yet unknown functions. The outcome of such screening is most vividly exemplified in the cases of the gene cluster on chromosome 4 comprising the Rpi-R2 gene and its numerous orthologs in the Mexican species S. bulbocastanum Dun., S. demissum Lindl., S. edinense Berth., S. hjertingii Hawkes, and S. schenckii Bitter [12,37,38], the orthologous Rpi-blb1/Rpi-sto1 genes on chromosome 8 in the Mexican species S. bulbocastanum, S. stoloniferum Schlechtd. et Bché, S. papita Rydb. and S. polytrichon Rydb. [3,5,38,39], and several Rpi genes in the cluster on the distal part of chromosome 9, including Rpi-R8 and Rpi-R9a from S. demissum, Rpi-vnt1 from S. venturii Hawkes and Hjert. and Rpi-ver1 from S. verrucosum Schlechtd [40,41,42,43,44].
The VIR Genbank is one of the five largest ex situ collections of potato and related tuber-bearing species, with its oldest accessions traced back to 1926–1927 [45]. It is one of the world’s best collections of wild, primitive, and cultivated species, which have been widely deployed in germplasm improvement. In this collection, the North American potato species are classified according to Bukasov [46], and the South American wild species according to Gorbatenko [47]. However, for the convenience of the foreign reader, in this communication, we list the names of species and their series positions in accordance with the system by Hawkes [48].
The goal of our study was a first reconnaissance of the VIR potato collection in order to select the most attractive genotypes for further detailed research. For such selection, we combined two independent strategies: the phenotypical evaluation of late blight resistance in the detached leaf test with a highly virulent and already sufficiently investigated P. infestans isolate—and the molecular screening with well-validated SCAR markers. Both technologies are open to many criticisms; nevertheless, when combined, such data are very practical for the wide-range screening of new plant germplasm.
Here we report the evidence from our study of LB resistance in the core selection from the VIR collection of wild potatoes (Table S1). The study covered 20 species of seven Petota series according to the classification by Hawkes [48]: Bulbocastana (Rydb.) Hawkes, Demissa Buk., Longipedicellata Buk., Maglia Bitt., Pinnatisecta (Rydb.) Hawkes, Tuberosa (Rydb.) Hawkes (wild and cultivated species), and Yungasensa Corr., with a total of 201 accessions (plant IDs are assigned to the collecting numbers). Each plant ID is represented by one or two genotypes. LB resistance was assayed in the laboratory test (163 assessments). SCAR marker analysis covered 263 genotypes. Using this selection, 117 accessions representing 17 wild and cultivated Solanum species from seven Petota series were screened with SCAR markers of ten Rpi genes: Rpi-R1, Rpi-R2/Rpi-blb3, Rpi-R3a, Rpi-R3b, Rpi-R8, Rpi-blb1/Rpi-sto1, Rpi-blb2, and Rpi-vnt1. This communication also includes some data from our previous studies of the VIR collection and as of to date presents the most comprehensive description of this collection as regards LB resistance.
Because of broad race specificity, the Rpi-blb1/Rpi-sto1, Rpi-blb2, Rpi-R2, and Rpi-vnt1 genes are currently most popular as the basis of durable LB resistance [49,50,51,52] and discovering new alleles of these genes would greatly benefit potato breeding. These genes became the focus of the present study. The patterns of plant response to P. infestans and the profiles of Rpi genes are discussed regarding the location of investigated species and their systematic position. Some data to be found below have been previously reported at several Euroblight workshops (; assessed on 4 January 2023)

2. Results

2.1. LB Resistance

The frequency of resistant accessions (7–9 points by 9-point scale) varied from 0.11 to 0.71 depending on Solanum species (Table 1). The North American species S. bulbocastanum, S. demissum, and S. cardiophyllum Lindl. clearly predominated among the resistant forms. Among the South American species, the best was S. berthaultii Hawkes, with the frequency of resistant genotypes of 0.5.
LB resistance varied within species and even within accessions (between individual genotypes). In S. bulbocastanum, the accessions k-19981, k-21266, and k-21274 were resistant, k-24866 was susceptible, the accession k-24855 was weakly affected by artificial infection, whereas each of the accessions k-23174 and 25351 comprised both resistant and weakly affected forms (Table S2). In S. pinnatisectum Dun., the accessions k-24239, k-24243, and 24415 were resistant; three accessions were moderately resistant or slightly affected by artificial infection (Table S3). In S. demissum, most accessions were resistant in all experiments, though the accessions k-15174, k-15175, and k-24887 were slightly affected by the pathogen in all tests (Table S8). In S. berthaultii, the accession k-19961 was resistant, in all other cases, plant response varied from weak damage to resistance. Similarly, in S. verrucosum, the accession k-24990 was resistant, the accessions k-24991 and k-24992 were susceptible, and in all other cases plants were moderately resistant to LB infection (Table S5). Accessions of S. stoloniferum greatly vary in their LB response: we observed a considerable diversity of phenotypes within individual accessions k-3554, 24973 and high LB resistance in the accessions k-3360, k-21618 and k-24981 (Table S9). The accessions of S. venturii k-12658, 25394, 25396, 25397, 25398 were obtained as seeds from the accessions CGN 17999, CGN 17998, CGN 18109, CGN 18279, and CGN 22703, respectively. Among them, the accessions κ-12658 and κ-25398 were resistant, whereas within the S. venturii accession k-25397, plants considerably differed in their response to infection: from susceptible to highly resistant. The variation within the accession κ-25394 was less prominent, from weakly affected to resistant (Table S5).

2.2. Rpi Genes

The data for particular Petota accessions are combined in Tables S2–S9; they are summed up per species and per series in Table 2 and Table 3.
As anticipated, the most prominent in the Petota set under study were the patterns of SCAR markers recognizing the Rpi-R1, Rpi-2, Rpi-R3a, Rpi-3b, and Rpi-R8 genes, which were initially found in S. demissum [4,6,9,14]; below we will call these genes demissoid. In S. demissum, the marker frequencies for these genes varied from 0.18 (Rpi-R3a-1380) and 0.17 (Rpi-R8-1258) to 0.9 (Rpi-R3b-378). Many of these genes or their structural homologs were also recognized in other North American series at comparable frequencies (the species are listed in the descending frequency order): Rpi-R1 in S. stoloniferum and S. polytrichon, Rpi-R2 in S. stoloniferum, S. polytrichon, S. bulbocastanum, S. pinnatisectum, and S. cardiophyllum, Rpi-R3a in S. cardiophyllum and S. cardiophyllum ssp. ehrenbergii Bitt., S. bulbocastanum and S. stoloniferum, Rpi-3b in all Pinnactisecta species included in this study, as well as in S. stoloniferum and S. bulbocastanum, and Rpi-R8 in S. stoloniferum (Table 2 and Table 3). Several S. stoloniferum accessions each comprised markers for two or even three demissoid genes; such plants were usually highly resistant to P. infestans (Table S9). Notable is the presence of putative structural homologs of demissoid genes in the series Tuberosa: Rpi-R2 in S. avilesii Hawkes et Hjerting, S. venturii, S vernei Bitt. et Wittm., Rpi-R3a in S. microdontum ssp. simplicifolium Bitt., Rpi-3b in S. venturii and S. phureja Juz. et Buk. and Rpi-R8 in many Tuberosa species. Nevertheless, the functional activity of these genes, especially beyond S. demissum, will demand further investigation.
In S. bulbocastanum, we observe a high frequency of the markers for three Rpi genes initially discovered in this potato species: Rpi-blb1-821 (0.48), Rpi-blb2-976 (0.8) and Rpi-blb3-305 (0.75). The frequency of Rpi-sto1-890, the marker of Rpi-sto1 orthologous to Rpi-blb1, was 0.53 in S. bulbocastanum, similar to the frequency of the marker Rpi-blb1-821. Most S. bulbocastanum plants containing these markers were highly resistant to P. infestans (Table S2): however, our marker analysis did not include the susceptible accession k-23181 (two genotypes). In S. bulbocastanum, we also found a high frequency of the markers for demissoid genes Rpi-R2, Rpi-3a, and Rpi-3b.
To screen for the Rpi-blb1 gene, we usually employ several markers covering different regions of this gene. The marker of this gene, Rpi-blb1-821, and the marker of its orthologue, Rpi-sto1-890, which are located widely apart on the gene sequence, were tightly linked in S. bulbocastanum accessions and two Longipedicellata accessions (Tables S2 and S9). The sequences of Rpi-blb1/Rpi-sto1 amplicons corresponding to these markers (the NCBI Genbank accessions KP317986–KP317990) were 100% identical to the prototype genes AY426259 and EU884421 [53]. In this study, we also discovered both markers, Rpi-blb1-821 and Rpi-sto1-890, in the S. cardiophyllum accession k-24203-435 (Table S3). The fragments cloned from this accession were 99% identical to the prototype genes and differed by several SNPs (see also [53]). The function of these fragments has not yet been established.
In addition to S. bulbocastanum, the marker for Rpi-blb2 was found in S. cardiophyllum (Table 2). The cloned amplicon differed from the prototype gene from S. bulbocastanum by several insertions. Less expected putative homologs of this gene in S. alandiae Card. (OP903197), S. okadae Hawkes et Hjerting and S. microdontum (Table 3; see also [54]) await further elucidation. In particular, the Rpi-blb2 amplicon cloned from S. alandiae differed from its S. bulbocastanum prototype by deletion and several substitutions and was apparently a dysfunctional homolog [54].
The Rpi-R2 gene from S. demissum and S. schenckii (FJ536325 and GU563975) is 96–99% identical to its ortholog Rpi-blb3 from S. bulbocastanum (FJ536346) [39]. The markers of Rpi-blb3 and Rpi-R2 cover different regions of these orthologous sequences and do not always match in the three Solanum series. Most important, the frequencies of the two markers considerably diverge in different species (Table 2). We, therefore, presume that many individual plants, foremost in Bulbocastana and also in Longipedicillata, Pinnatisecta, and probably Tuberosa (e.g., S. venturii), each comprise both orthologs (Tables S2, S3, S5 and S9). Among the Tuberosa species, Rpi-R2 homologs from S. alandiae (OP 749981 and OP 903199) and S. okadae were 94–97% identical to the prototype genes from S. demissum and S. bulbocastanum. Characteristically, the homologs from S. bulbocastanum, S. alandiae, and S. okadae differed from the demissum prototype Rpi-R2 gene by several SNPs and a six-nucleotide insertion [54]. In the case of S cardiophyllum and S. cardiophyllum ssp. ehrenbergii, we registered the different frequencies of the Rpi-R2 gene marker (χ2 = 5.5, p < 0.02).
To our surprise, the frequencies of the marker for the Rpi-R8 gene in many Tuberosa species considerably exceeded those in S. demissum and S. stoloniferum (Table 2). The fragments of the Rpi-R8 gene cloned from S. alandiae (OP762711) and S. okadae [54] were 99% identical to the corresponding region in the prototype gene in S. demissum (KU530153). Two former sequences differed by several SNPs.
Diploid S. bulbocastanum and polyploid North American species significantly differed in the frequencies of Rpi gene markers. Such is the case of the Rpi-R1 gene in S. bulbocastanum vs. S. demissum (χ2 = 20.5, p < 0.001) and vs. S. stoloniferum (χ2 = 10.4, p < 0.002). In the case of the Rpi-3b, Rpi-R8, and Rpi-blb2 genes, the frequencies of the markers in S. bulbocastanum significantly differed from those in S. stoloniferum (χ2 = 7.0, p = 0.008; χ2 = 8.5, p = 0.004; χ2 = 8.9, p = 0.003, respectively).
The marker of Rpi-vnt1 was found in all accessions of S. bulbocastanum and S. stoloniferum and absent from S. demissum, with the sole exception of the accession k-19997; in this aspect, marker frequencies in two former species significantly differed (χ2 = 16.4, p < 0.001, χ2 = 13.8, p < 0.001, respectively). The sequences from S. bulbocastanum (PI255516, PI275194), S. cardiophyllum (PI283062), and S. stoloniferum (PI195169, k-24420) were 92–96% identical to the prototype gene and differed from it by 5–9 SNPs.

3. General Discussion and Conclusions

3.1. Polymorphisms of Wild Potatoes in the VIR Collection

In the course of long evolution of tuber-bearing potatoes, the initial whole genome duplication and allopolyploidization by interspecific hybridization were followed by extensive gene diversification during Solanum speciation and plant adjustment to highly diverse habitats in North and South America. The characteristic case of series Tuberosa also included the adaptation to pathogens and selection under the pressure of informed breeding and cultivation. In particular, on the basis of his studies of LB-resistant potato forms, Budin [55] identified four centers of potato breeding: the Mexican, Colombian-Ecuadorian, Bolivian and Argentinean, which coincided with the natural habitats of P. infestans-resistant forms under the climates most favorable for pathogen dissemination. Sometimes new environments have been widely different from those in the areas of initial potato domestication and cultivation. All these processes of further gene evolution comprised tandem duplications, intergenic and intragenic recombination, selective retention, and neofunctionalization of retained key loci [56,57,58,59,60,61,62,63]. As an outcome, we observe a multihued landscape of agronomically important genes in the cultivated Solanum species and landraces along with the structural homologs of these genes of yet unknown functions in the wild species, especially in the aboriginal forms confined to the South American habitats and maintained in the local genetic collections [64]. The evolutionary analyses of this landscape would substantially promote and accelerate the search for the variation sought after by both evolution researchers and breeders [65]. This context helps elucidate the evolution of Rpi genes, assess their present diversity, and grasp the prospects to discover new beneficial alleles both in genetic collections of wild species [10,25,66] and in already existing multi-parent hybrids, which accumulated germplasm from numerous wild species introgressed sometimes many years ago [52].
The diversity of potatoes and their wild relatives has been repeatedly discussed against different taxonomies of the Petota section as the latter was revised to match the volumes of series and species and to include new, previously unknown species. The species systems were developed by Correll [67], Bukasov [46], and Hawkes [48]. Gorbatenko [47] took into account new species discovered at the end of the 20th century in Peru and Bolivia to develop the species system for South America. To classify potato species growing in the North, Central, and southern part of South America, Spooner et al. [68] combined the classical morphophysiological approach with the evidence obtained with several molecular technologies. Current systems of the Petota section widely differ in the number and composition of supraspecific taxa (series according to the classification by Correll, Bukasov, Hawkes, and Gorbatenko vs. groups according to the classification by Spooner) as well as in the number and grouping of species.
These revisions in the Petota taxonomy have split the ex situ potato world. While such depositary as the International Potato Center (CIP) organizes its collection according to the taxonomy by Hawkes, other major potato genebanks, such as the USDA-ARS Potato Genebank NRSP-6, adopted the classification by Spooner. Potato curators in all genebanks acknowledge the revision by Spooner as a significant advance in the field, yet the taxa by Hawkes are employed to manage their ex situ collections [69].
On the basis of early cytogenetic data, the genomes of most Petota species explored in this study are AA and AAAA in diploid and autotetrapoid Tuberosa, BB in diploid Bulbocastana and Pinnatisecta and AABB in allotetraploid Longipedicellata. Two hypotheses based on classical cytogenetic data and genomic in situ hybridization presume that the genome A in Longipedicellata originated either from S. chacoense or S. verrucosum (see [48,68] for detailed discussion); however, both hypotheses have not been extensively tested with the latest molecular methods. The systematic affiliation of three genomes of S. demissum has also been under active discussion [68]. Hopefully, these genome disputes will be finally resolved as more and more Petota genomes are completely deciphered [70,71,72,73,74,75,76].
The study of the VIR potato collection was started in 1921 by S.M. Bukasov and his colleagues and considerably expanded when wild potato tubers collected by the VIR expeditions to two American continents started to arrive in 1927 [77]. The present VIR collection maintains 8150 Petota accessions, including 1990 accessions of wild species, 3200 accessions of cultivated species, 2360 cultivars, and 600 advanced clones [45]. From the very beginning, the work with the collection has focused on mobilizing the germplasm pool of potatoes and related species and the genetic studies of these resources, as well as selecting the most valuable plant accessions and developing new sources for potato breeding. For this study, we selected Petota series and species from two dissimilar potato groups representing the North American and South American centers of genetic diversity. We focused on the accessions that produced tubers under our experimental conditions; thus, our study could proceed for several years.

3.2. LB Resistance

The VIR accessions of Petota species have been repeatedly assessed for LB resistance, and new sources of LB resistance were identified [20,53,77,78,79]. Leaf LB resistance is characteristic of the North American species from series Demissa (S. demissum, S. guerreroense Corr. and S. hougasii Corr.), Pinnatisecta (S. pinnatisectum and S. tarnii Hawkes et Hjerting), S. bulbocastanum and S. stoloniferum and the South American species S. vernei and S. berthaultii
In several cases, the assessments of LB resistance of the potato accessions in the VIR collection can be matched up against the evidence reported by other authors. We compared our data to the evidence from the laboratory tests carried out in the US Genbank (these evaluation data are provided by the Germplasm Resource Information Network (GRIN) database (; assessed on 4 January 2023).). An excellent agreement was established for 94 accessions of wild and cultivated potato species from two collections: Spearman’s correlation coefficient was 0.76 (p = 0.05). Another illustration is the LB resistance of S. venturii: our evidence is in good agreement with the data for the accessions CGN 18279, CGN 22703 and CGN 18109 reported by Foster et al. [40]. When Bachman-Pfabe et al. [29] tested the potato collection from the IPK Genebank (; assessed on 4 January 2023).) for tuber resistance to P. infestans, the most prominent, similar to the present study, were the accessions of S. bulbocastanum, S. pinnatisectum, and S. stoloniferum.

3.3. Diversity of the Rpi Genes

A considerable part of potato genomes is represented by the genes that determine resistance to numerous diseases and pests. Among them, the dominant Rpi genes apparently evolved from the NB-LRR predecessor structures (protogenes) when the Solanum species were adjusting to the particular habitats in both American continents and co-evolving with the local repertoires of P. infestans [9,80,81,82,83].
Recent advances in the phylogenetic and phylogeographic studies of this diversity of Rpi genes in the numerous wild and cultivated Solanum species and landraces also owe much to the sequencing of complete genomes [70,71,72,73,74,75,76] and transcriptomes [72,84,85,86]. The big data from sequencing are supplemented with the evidence obtained by extensive screening of nuclear DNA with various anonymous and gene-specific markers [3,34,57,68,75,87,88,89,90,91]. Another kind of evidence is obtained by researching into the polymorphisms of individual genes and rapidly evolving clusters of NB-LRR resistance genes [14,59,80,83,92].
In hexaploid S. demissum, only one haplotype (genome) comprised the functional Rpi-R1 gene, and its structural homologs (pseudogenes) in two other genomes might act as a reservoir of gene sequences for further evolution [92]. The distribution of other Rpi genes between haplotypes of S. demissum has not been explicitly established.
The gene Rpi-blb1 was firmly established as the marker of genome B in the series Bulbocastana and Longipedicellata rather than Pinnatisecta [3,53]. There are, however, several exceptions. Lokossou. [39] found the marker Rpi-blb1-821 in two Mexican accessions of S. cardiophyllum (CGN 18326 and CGN 22387). Similar evidence is reported in this communication (Table S3). Tiwari et al. [33] registered an 846-bp homolog (KJ472309) from S. cardiophyllum with 82% identity to the prototype Rpi-blb1 gene. Previously Pankin et al. [93,94,95] cloned from S. cardiophyllum several DNA fragments corresponding to the CC region of the Rpi-blb1 gene; among them, two sequences over 1 kb in length (JN688099 and JN698894), cloned from the accession k16828-390 were 94% similar to the prototype gene. In addition to S. cardiophyllum, a full-length homolog of the Rpi-blb1 gene was found in the genome of S. pinnatisectum [75], its sequence (CP047564) is 84% identical to Rpi-blb1. Fadina et al. [53] did not find the SCAR markers of the Rpi-blb1/Rpi-sto1 genes in the accessions of Demissa and Pinnatisecta (with exception of a single S. cardiophyllum accession k-24207, GLKS2152, 420). The markers of Rpi-blb1/Rpi-sto1 were also absent from resistant S. verrucosum accessions comprising the RBver homolog [96].
Other Rpi genes in the wild Petota collection maintained in the VIR Genbank have been previously researched in our laboratory. Sokolova et al. [32] screened over 200 wild Solanum accessions (half of them from the VIR collection) representing 21 species of six Petota series with the SCAR markers for the Rpi-R1 and Rpi-R3a genes. As a whole, these genes were restricted to the Mexican species: the Rpi-R1 gene was reported in the series Demissa and Longipedicellata, whereas the Rpi-R3a gene was also found in several accessions of S. bulbocastanum, S. cardiophyllum, and S. cardiophyllum ssp. ehrenbergii. S. microdontum was the only South American species comprising Rpi-R3a. Later the same researchers reported the SCAR marker of the Rpi-R3b gene in many Pinnatisecta accessions [97]. Beketova et al. [98] screened numerous accessions of S. demissum, S. stoloniferum, S. papita, and S. polytrichon (two latter species are included in S. stoloniferum sensu Spooner) from the VIR collection using three Rpi-R1 markers. With the marker Rpi-R1-1205, they found the gene and/or its putative homologs in all these species. Next, more specific markers Rpi-R1-517 and Rpi-R1-513 were employed to discriminate between the Rpi-R1 alleles putatively characteristic of S. demissum and S. stoloniferum, respectively. The deduced amino acid sequences of two alleles differed by three substitutions. The marker Rpi-R1-517 was found in all S. demissum accessions, whereas the presumable stoloniferum allele recognized with the marker Rpi-R1-513 was registered only in some stoloniferum accessions. Zoteeva et al. [78] reported the marker of the Rpi-R3a gene in the Mexican species S. guerreroense (Demissa, Iopetala group), accession k-18407.
Foster et al. [40] and Pel et al. [41] identified three functional alleles of the Rpi-vnt1 gene in S. venturiii. Using allele mining with specific PCR primers, Pel [99] recognized the functional and non-functional homologs of this gene in many South American species. The list of species comprising these homologs was recently complemented with S. alandiae (OP889280) and S. okadae (OP903198) [62] and with S. phureia and S. stenotomum [100]. In the current study, the marker of the Rpi-vnt1 gene was also registered in two Tuberosa species absent from the Pel’s list: S. alandiae and S. berthaultii (Table 2). Pel [99] presumed that the Rpi-vnt1 gene is restricted to the series Tuberosa; however, Tiwari et al. [75] reported a structural homolog of Rpi-vnt1 (CP047560) on chromosome 9 in the recently sequenced genome of S. pinnatisectum Dun. (CGN17745). In the present study, the marker Rpi-vnt1-612 was found in other North American species: S. bulbocastanum, S. cardiophyllum, and S. stoloniferum and even in one accession of S. demissum (Table 2; Figure S1). The frequencies of this marker in the Mesoamerican species (Table 2) exceeded those reported for the South American species [99]. Remarkably, the only North American species from the series Tuberosa, S. verrucosum, was devoid of this marker (Table 2).
When we compared the Rpi-vnt1 homologs obtained in this study with the prototype gene and its numerous homologs (pseudogenes) (Figure S1), they were distinctly divided into two clusters: the translated and most probably functional genes and the pseudogenes (Figure S1). Cluster 1 of translated sequences is subdivided into two subclusters. The subcluster 1a comprises the prototype alleles Rpi-vnt1.1, Rpi-vnt1.2, and Rpi-vnt1.3 (vnt_FJ423044, vnt_FJ423045, vnt_FJ423046) and Rpi-vnt1 sequence tub_OP617268 from S. tuberosum cultivar Alouette (this cultivar contains the Rpi-vnt1-3 allele [36]) and also non-translatable sequences of Rpi-vnt1.1 pseudogenes from S. venturii (vnt__GU386358), from S. tarijense (tar_GU338324 and tar_GU338326) and from S. microdontum ssp. gigantophyllum (mcd_GU338312). These pseudogenes are 94–97% identical to the prototype gene. The pseudogene from S. venturii (GU386358) comprises a 3-bp insertion encoding a stop codon. Subcluster 1b comprises the translatable sequences from the North American species S. bulbocastanum, S. cardiophyllum, and S. stoloniferum cloned in this study, with the identity to the prototype gene of 92–96%. These sequences contain a characteristic deletion in position 43–47 bp, which restores the proper reading frame. The region of 1–42 bp in Rpi-vnt1 from the North American species is quite different from all other homologs of this gene in the NCBI Genebank. The second cluster in Figure S1 combines pseudogenes found by Pel [99] in the South American Tuberosa species. Three outgroup sequences are 86–93% identical to the prototype gene.
The divergent evolution and specialization of the Rpi-blb1 protogene(s) in Petota species left the functional homologs considerably different from Rpi-blb1/Rpi-sto1, such as Rpi-bt1 in S. bulbocastanum (with the identity of 87% to Rpi-blb1) and RBver in S. verrucosum (the identity of 89%); several polymorphisms prevent recognition of these genes by the marker Rpi-blb1-821 [53]. NCBI Genebank database comprises many Tuberosa homologs of this gene with an identity below 90%. Notably, when using SCAR markers other than Rpi-blb1-821 and Rpi-sto1-890, many footprints of the Rpi-blb1 gene of unknown functions were reported in diverse Solanum and even Capsicum species. While in S. bulbocastanum these genome fragments were linked to resistance to P. infestans, in other species such a relationship was not observed [33,93,94]. The structural homologs of Rpi-vnt1 initially identified in S. venturii were found in many South and North American species ([54,99,100] and this communication); most probably they are pseudogenes.
Quite apart stands S. verrucosum; this North American species is combined by taxonomists in one clade with the southern South American Tuberosa [48,101,102]. Such treatment is not recognized universally, and Bukasov [46] even put this species into the separate series Verrucosa. Several accessions of S. verrucosum are highly resistant to P. infestans, and here Liu and Halterman [96] discovered the functional homologs of Rpi-blb1; these RBver sequences shared up to 89% nucleotide identity with the former gene. Using the specific Avr genes, these investigators demonstrated that most S. verrucosum accessions resistant to P. infestans also comprised the functional homologs of the Rpi-R8 and/or Rpi-R9 genes [103]. More recently, Chen et al. [44] applied two complementary enrichment strategies that targeted resistance genes (RenSeq) and single/low-copy number genes (generic-mapping enrichment sequencing; GenSeq), respectively, to investigate Rpi genes of S. verrucosum. Here, on the distal end of chromosome 9 rich in the NB-LRR sequences [80], many Rpi genes have previously been identified, including Rpi-vnt1 from S. venturii [40,41]. The new gene, named Rpi-ver1, was different from the well-known set of demissum genes Rpi-R1–Rpi-R11, the bulbocastanum genes Rpi-blb1 and Rpi-blb2 and also from the Rpi-vnt1 gene.
In S. demissum (k-15175, k-19997) and S. stoloniferum (k-3360, 21616, 23652, 24420, 24981, 24972, 24976), we registered SCAR markers for several Rpi genes per accession. Two accessions of S. stoloniferum k-24263 and k-24981 combined the markers for five genes (Tables S8 and S9). Two accessions of S. stoloniferum k-3554 and k-23652 combined the markers for three demissoid genes (Tables S8 and S9). The cases of several Rpi genes in one plant are especially promising sources for pyramiding/stacking technologies of breeding for broad-spectrum and durable disease resistances, including potato LB resistance [42,49,52].
In marker analysis, we find numerous homologs of specific Rpi genes in various species of the section Petota. The question arises as to their origin. One reason for the presence of “alien” homologs with an identity of over 90% is a cross-pollination of wild Solanum species with their cultivated and wild relatives. The expanded wild introgressions following polyploidy brought in alleles from outside of the geographic origin of particular species. As reported by Hardigan et al. [58] and Bethke et al. [23], 73% of alleles characteristic of wild species are found in North American potato varieties. Accessions of the same species may widely vary when they were collected from different habitats [10]. Another reason may be the divergent evolution of protogens: the structures that preceded the differentiation of the genomes of tuberous potato species went through a series of mutations. Functional Rpi genes arose during the further evolution of Solanum species, when, in the course of dispersal on the American mainland, the species adapted to different habitats with local pathogen repertoires. Recent studies show that the recombination level at resistance gene clusters is increased following pathogen infection, suggesting a mechanism that induces temporary genome instability in response to extremal stress conditions [39,82].
One way to characterize putative protogens is to study Rpi homologs in susceptible Tuberosa species with well-characterized genomes. The Solynthus potato variety [104] was bred to a unique level of homozygosity. Its genome has been fully sequenced, but the analysis of its individual genes is just beginning. Nevertheless, the BLAST analysis revealed in this genome the structural homologs of all the genes studied in our work; these homologs are 87–95% similar to the prototype genes. As a caveat, one should note that even after nine cycles of selfing, Solynthus has noticeable heterozygosity, possibly due to the preferential selection of heterozygous plants in the selection process [104].
Notwithstanding the ongoing progress in gene mining and allele identification, the attempts to directly link the Rpi gene activities to plant LB resistance have not been always convincing, even when gene functions were established by effectoromics and genetic transformation of plants susceptible to P. infestans. The situation is especially complicated in plants combining several Rpi genes of different specificity toward P. infestans races. Thus, in our case, the relationship between the presence of Rpi genes and plant resistance to P. infestans is qualitatively visible although not statistically significant, especially in S. bulbocastanum. In some cases, such a lack of significant relationship presumes that highly resistant plants comprise Rpi genes other than scored presently with our markers. Apparently, these Solanum species have not been adequately studied by molecular methods: hopefully, such potato accessions contain as yet unknown Rpi genes or new alleles of known Rpi genes. We believe that this problem will be overcome by using the new screening technologies directly recognizing the functional alleles of the Rpi genes.
The characteristic dichotomy in the geographic distribution of the Rpi genes may help elucidate their evolution in tuber-bearing potatoes. Our evidence confirmed the diverse location of the functional Rpi gene in two American continents. The structural homologs of the Rpi-R2, Rpi-R3a, Rpi-R3b, and Rpi-R8 genes were found in the North American species other than S. demissum, the very species which was the original source of these genes for early potato breeding, and in some cases, in the South American Tuberosa species. In contrast, the Rpi-blb1/Rpi-sto1 orthologs from S. bulbocastanum and S. stoloniferum were restricted to the Mesoamerican series Bulbocastana, Longipedicellata and possibly Pinnatisecta. Particularly interesting are the structural homologs of Rpi-vnt1. The functional gene was initially identified in S. venturii, and its homologs were found in many South American species, whereas here we report these homologs, for the first time, in the North American Petota series. Future studies will probably reveal whether such homologs are footprints of NB-LRR gene functionalization in the expanding area of tuber-bearing potatoes rather than protogenes rejected by Rpi gene specialization in particular disease landscapes.

4. Materials and Methods

Clonal collections of wild Solanum species were developed from seed accessions obtained from the N.I. Vavilov Institute of Plant Genetic Resources (VIR), Russia ( assessed on 4 January 2023), the US Potato Genebank NRSP-6 (; assessed on 4 January 2023), CIP (International Potato Center, assessed on 4 January 2023) and the CGN potato collection (; assessed on 4 January 2023) and were further maintained in VIR as tuber progenies (Table S1).
Resistance to P. infestans was assayed in the laboratory test with detached leaves according to the Eucablight protocol (; assessed on 4 January 2023) see also [105]). In this test, we employed a highly virulent and aggressive isolate of P. infestans N161 collected in the Moscow region and maintained in the Institute of Phytopathology (mating type A1; race 1,2,3,4,5,6,7,8,9,10,11; virulence genes avr1, Avr2K, Avr2-likeMI, avr3aEM, avr4, Avr8, Avr-Smira1 (I, II), Avr-blb1 (I, II), Avr-blb2, Avr-vnt1 [106]) and potato variety Santé as a standard. The resistance indices of individual accessions and clones which were also screened with the SCAR markers of ten Rpi genes are listed in Tables S2–S9.
Specific SCAR markers of Rpi genes employed in screening wild Solanum accessions were designed by other authors and verified against the prototype Rpi genes characteristic of particular Solanum species (Table 4).
When discerned in other Petota series, DNA fragments amplified with these markers are referred to as structural homologs rather than orthologues of the prototype genes. In several cases, to evaluate the structural relationship with the prototype genes, the amplicons from remote species were cloned using pGEMT Easy Vector System I (Promega, Madison, WI, USA) or pAL2-T vector (Evrogen, Moscow, Russia;; assessed on 4 January 2023) and sequenced with a nucleic acid analyzer ABI PRISM 3130xl (Applied Biosystems, Foster City, CA, USA) in the Institute of Agricultural Biotechnology or with an ABI PRISM 3500 (Applied Biosystems) in the Evrogen. BLAST (; assessed on 4 January 2023) was used to mine genomic databases for Rpi genes and their homologs. SeqMan, Lasergene 7.0 programs, and MEGA version 10.2.1 [112] were employed to assemble sequence fragments.
The data were statistically processed by the parametric and nonparametric statistics methods using the Statistica StatSoft 13 software package (; assessed on 4 January 2023).

Supplementary Materials

The following supporting information can be downloaded at:, Figure S1: Phylogenetic analysis of the nucleotide sequences of the Rpi-vnt1 gene and its structural homologs in Solanum species section Petota.; Table S1: Solanum species and accessions studied; Table S2: Screening S. bulbocastanum with SCAR markers of the Rpi genes and for late blight resistance; Table S3: Screening Solanum species Pinnatisecta series with SCAR markers of the Rpi genes and for late blight resistance; Table S4: Screening S. chacoesne (Yungasensa series) with SCAR markers of the Rpi genes and for late blight resistance; Table S5: Screening Solanum species Tuberosa (wild species) series with SCAR markers of the Rpi genes and for late blight resistance; Table S6: Screening Solanum species Tuberosa (cultivated species) series with SCAR markers of the Rpi genes and for late blight resistance; Table S7: Screening Solanum maglia (Maglia series) with SCAR markers of the Rpi genes and for late blight resistance; Table S8: Screening S. demissum (Demissa series) with SCAR markers of the Rpi genes and for late blight resistance; Table S9: Screening Solanum species Longipedicellata series with SCAR markers of the Rpi genes and for late blight resistance.

Author Contributions

E.E.K., M.A.K. and E.V.R. conceived and designed the research. N.A.C. and A.A.G. maintained potato species collection. M.A.K. and N.M.Z. evaluated LB resistance in the laboratory tests, M.P.B., P.E.D., O.A.M. and E.A.S. ran the marker and bioinformatics analyses. E.E.K. and E.V.R. wrote and revised the manuscript. E.V.R. provided funding. All authors have read and agreed to the published version of the manuscript.


This research was supported by Russian Science Foundation, project No 22-26-00111 “Genes for resistance to potato late blight in the context of the evolution of cultured and wild tuber-forming Solanum species”.

Data Availability Statement

Not applicable.


The authors thank the Center for Collective Use of Equipment “Biotechnology” at the Institute of Agricultural Biotechnology, Moscow, for sequencing Solanum genome fragments and the Center for Collective Use of the State Collection of Plant Pathogenic Microorganisms, Indicator Plants and Differential Cultivars at the Institute of Phytopathology for making available the equipment for phytopathological assessments. The authors are most grateful to three anonymous reviewers for their meticulous analysis of the manuscript and most constructive suggestions.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Birch, P.R.J.; Bryan, G.J.; Fenton, B.; Gilroy, E.M.; Hein, I.; Jones, J.T.; Prashar, A.; Taylor, M.A.; Torrance, L.; Toth, I.K. Crops that feed the world 8: Potato: Are the trends of increased global production sustainable? Food Secur. 2012, 4, 477–508. [Google Scholar] [CrossRef]
  2. Bradshaw, J.E. Review and analysis of limitations in ways to improve conventional potato breeding. Potato Res. 2017, 60, 171–193. [Google Scholar] [CrossRef]
  3. Wang, M.; Allefs, S.; van den Berg, R.G.; Vleeshouwers, V.G.; van der Vossen, E.A.; Vosman, B. Allele mining in Solanum: Conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum. Theor. Appl. Genet. 2008, 116, 933–943. [Google Scholar] [CrossRef]
  4. Hein, I.; Birch, P.R.J.; Danan, S.; Lefebvre, V.; Odeny, D.A.; Gebhardt, C.; Trognitz, F.; Bryan, G.J. Progress in mapping and cloning qualitative and quantitative resistance against Phytophthora infestans in potato and its wild relatives. Potato Res. 2009, 52, 215–227. [Google Scholar] [CrossRef][Green Version]
  5. Vleeshouwers, V.G.; Raffaele, S.; Vossen, J.H.; Champouret, N.; Oliva, R.; Segretin, M.E.; Rietman, H.; Cano, L.M.; Lokossou, A.; Kessel, G.; et al. Understanding and exploiting late blight resistance in the age of effectors. Annu. Rev. Phytopathol. 2011, 49, 507–531. [Google Scholar] [CrossRef] [PubMed][Green Version]
  6. Rodewald, J.; Trognitz, B. Solanum resistance genes against Phytophthora infestans and their corresponding avirulence genes. Mol. Plant Pathol. 2013, 14, 740–757. [Google Scholar] [CrossRef] [PubMed]
  7. van Weymers, P.S.M.; Baker, K.; Chen, X.; Harrower, B.; Cooke, D.E.L.; Gilroy, E.M.; Birch, P.R.J.; Thilliez, G.J.A.; Lees, A.K.; Lynott, J.S.; et al. Utilizing “omic” technologies to identify and prioritize novel sources of resistance to the oomycete pathogen Phytophthora infestans in potato germplasm collections. Front. Plant Sci. 2016, 7, 672. [Google Scholar] [CrossRef][Green Version]
  8. Khavkin, E.E. Plant–pathogen molecular dialogue: Evolution, mechanisms and agricultural implementation. Russ. J. Plant Phys. 2021, 68, 197–211. [Google Scholar] [CrossRef]
  9. Blossei, J.; Gaebelein, R.; Hammann, T.; Uptmoor, R. Late blight resistance in wild potato species—Resources for future potato (Solanum tuberosum) breeding. Plant Breed. 2022, 141, 314–331. [Google Scholar] [CrossRef]
  10. Bethke, P.C.; Halterman, D.A.; Jansky, S. Are we getting better at using wild potato species in light of new tools? Crop. Sci. 2017, 57, 1241–1258. [Google Scholar] [CrossRef]
  11. Machida-Hirano, R.; Niino, T. Potato genetic resources. In The Potato Genome; Kumar, C.S., Xie, C., Kumar, T.J., Eds.; Springer: Cham, Switzerland, 2017; pp. 11–30. [Google Scholar] [CrossRef]
  12. Aguilera-Galvez, C.; Champouret, N.; Rietman, H.; Lin, X.; Wouters, D.; Chu, Z.; Jones, J.; Vossen, J.; Visser, R.; Wolters, P.J.; et al. Two different R gene loci co-evolved with Avr2 of Phytophthora infestans and confer distinct resistance specificities in potato. Stud. Mycol. 2018, 89, 105–115. [Google Scholar] [CrossRef] [PubMed]
  13. Ortiz, R. Genomic-led potato breeding for increasing genetic gains: Achievements and outlook. Crop. Breed. Genet. Genom. 2020, 2, e200010. [Google Scholar] [CrossRef]
  14. Paluchowska, P.; Śliwka, J.; Yin, Z. Late blight resistance genes in potato breeding. Planta 2022, 255, 127. [Google Scholar] [CrossRef] [PubMed]
  15. Witek, K.; Lin, X.; Karki, H.S.; Jupe, F.; Witek, A.I.; Steuernagel, B.; Jones, J.D. A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat. Plants 2021, 7, 198–208. [Google Scholar] [CrossRef]
  16. Lin, X.; Jia, Y.; Heal, R.; Prokchorchik, M.; Sindalovskaya, M.; Olave-Achury, A.; Makechemu, M.; Fairhead, S.; Noureen, A.; Heo, J.; et al. The Solanum americanum pangenome and effectoromics reveal new resistance genes against potato late blight. bioRxiv 2022. [Google Scholar] [CrossRef]
  17. Vossen, J.H.; Jo, K.-R.; Vosman, B. Mining the genus Solanum for increasing disease resistance. In Genomics of Plant Genetic Resources; Crop Productivity, Food Security and Nutritional Quality; Tuberosa, R., Graner, A., Frison, E., Eds.; Springer: Dordrecht, The Netherlands, 2014; Volume 2, pp. 27–46. [Google Scholar] [CrossRef]
  18. Hardigan, M.A.; Bamberg, J.; Buell, C.R.; Douches, D.S. Taxonomy and genetic differentiation among wild and cultivated germplasm of Solanum sect. Petota. Plant Genome 2015, 8. [Google Scholar] [CrossRef] [PubMed][Green Version]
  19. Machido-Hirano, R. Diversity of potato genetic resources. Breed. Sci. 2015, 65, 26–40. [Google Scholar] [CrossRef][Green Version]
  20. Kiru, S.D.; Rogozina, E.V. Mobilization, conservation and study of cultivated and wild potato genetic resources. Vavilov J. Genet. Breed. 2017, 21, 7–15. [Google Scholar] [CrossRef]
  21. Jansky, S.H.; Spooner, D.M. The evolution of potato breeding. Plant Breed. Rev. 2018, 41, 169–214. [Google Scholar] [CrossRef]
  22. Li, Y.; Colleoni, C.; Zhang, J.; Liang, Q.; Hu, Y.; Ruess, H.; Simon, R.; Liu, Y.; Liu, H.; Yu, G.; et al. Genomic analyses yield markers for identifying agronomically important genes in potato. Mol. Plant 2018, 11, 473–484. [Google Scholar] [CrossRef][Green Version]
  23. Bethke, P.C.; Halterman, D.; Jansky, S. Potato germplasm enhancement enters the genomics era. Agronomy 2019, 9, 575. [Google Scholar] [CrossRef][Green Version]
  24. Ghislain, M.; Douches, D.S. The genes and genomes of the potato. In The Potato Crop; Campos, H., Ortiz, O., Eds.; Springer: Cham, Switzerland, 2020; pp. 139–162. [Google Scholar] [CrossRef]
  25. Karki, H.S.; Jansky, S.H.; Halterman, D.A. Screening of wild potatoes identifies new sources of late blight resistance. Plant Dis. 2021, 105, 368–376. [Google Scholar] [CrossRef] [PubMed]
  26. Pérez, W.; Salas, A.; Raymundo, R.; Huaman, Z.; Nelson, R.; Bonierbale, M. Evaluation of wild potato species for resistance to late blight. CIP Program Rep. 1999, 2000, 49–62. [Google Scholar]
  27. Pérez, W.; Ñahui, M.; Ellis, D.; Forbes, G.A. Wide phenotypic diversity for resistance to Phytophthora infestans found in potato landraces from Peru. Plant Dis. 2014, 98, 1530–1533. [Google Scholar] [CrossRef] [PubMed][Green Version]
  28. Khiutti, A.; Spooner, D.M.; Jansky, S.H.; Halterman, D.A. Testing taxonomic predictivity of foliar and tuber resistance to Phytophthora infestans in wild relatives of potato. Phytopathol. 2015, 105, 1198–1205. [Google Scholar] [CrossRef][Green Version]
  29. Bachmann-Pfabe, S.; Hammann, T.; Kruse, J.; Dehmer, K.J. Screening of wild potato genetic resources for combined resistance to late blight on tubers and pale potato cyst nematodes. Euphytica 2019, 215, 48. [Google Scholar] [CrossRef]
  30. Duan, Y.; Duan, S.; Xu, J.; Zheng, J.; Hu, J.; Li, X.; Li, B.; Li, G.; Jin, L. Late blight resistance evaluation and genome-wide assessment of genetic diversity in wild and cultivated potato species. Front. Plant Sci. 2021, 12, 710468. [Google Scholar] [CrossRef]
  31. Pérez, W.; Alarcon, L.; Rojas, T.; Correa, Y.; Juarez, H.; Andrade-Piedra, J.L.; Anglin, N.L.; Ellis, D. Screening South American potato landraces and potato wild relatives for novel sources of late blight resistance. Plant Dis. 2022, 106, 1845–1856. [Google Scholar] [CrossRef]
  32. Sokolova, E.; Pankin, A.; Beketova, M.; Kuznetsova, M.; Spiglazova, S.; Rogozina, E.V.; Yashina, I.; Khavkin, E. SCAR markers of the R-genes and germplasm of wild Solanum species for breeding late blight-resistant potato cultivars. Plant Genet. Res. 2011, 9, 309–312. [Google Scholar] [CrossRef]
  33. Tiwari, J.K.; Devi, S.; Sharma, S.; Chandel, P.; Rawat, S.; Singh, B.P. Allele mining in Solanum germplasm: Cloning and characterization of RB-homologous gene fragments from late blight resistant wild potato species. Plant Mol. Biol. Rep. 2015, 33, 1584–1598. [Google Scholar] [CrossRef]
  34. Ramakrishnan, A.P.; Ritland, C.E.; Sevillano, R.H.B.; Riseman, A. Review of potato molecular markers to enhance trait selection. Am. J. Potato Res. 2015, 92, 455–472. [Google Scholar] [CrossRef]
  35. Jupe, F.; Witek, K.; Verweij, W.; Sliwka, J.; Pritchard, L.; Etherington, G.J.; MacLean, D.; Cock, P.J.; Leggett, R.M.; Bryan, G.J.; et al. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 2013, 76, 530–544. [Google Scholar] [CrossRef] [PubMed][Green Version]
  36. Armstrong, M.R.; Vossen, J.; Lim, T.Y.; Hutten, R.C.B.; Xu, J.; Strachan, S.M.; Harrower, B.; Champouret, N.; Gilroy, E.M.; Hein, I. Tracking disease resistance deployment in potato breeding by enrichment sequencing. Plant Biotechnol. J. 2019, 17, 540–549. [Google Scholar] [CrossRef] [PubMed]
  37. Champouret, N. Functional Genomics of Phytophthora Infestans Effectors and Solanum Resistance Genes. Ph.D. Thesis, Wageningen University, Wageningen, The Netherlands, 2010; 154p. [Google Scholar]
  38. Lokossou, A.A.; Rietman, H.; Wang, M.; Krenek, P.; van der Schoot, H.; Henken, B.; Hoekstra, R.; Vleeshouwers, V.G.A.A.; van der Vossen, E.A.G.; Visser, R.G.F.; et al. Diversity, distribution, and evolution of Solanum bulbocastanum late blight resistance genes. Mol. Plant-Microbe Inter. 2010, 23, 1206–1216. [Google Scholar] [CrossRef][Green Version]
  39. Lokossou, A.A. Dissection of the Major Late Blight Resistance Cluster on Potato Linkage Group IV. Ph.D. Thesis, Wageningen University, Wageningen, The Netherlands, 2010; 142p. [Google Scholar]
  40. Foster, S.J.; Park, T.H.; Pel, M.; Brigneti, G.; Sliwka, J.; Jagger, L.; Van der Vossen, E.; Jones, J.D. Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol. Plant-Microbe Inter. 2009, 22, 589–600. [Google Scholar] [CrossRef][Green Version]
  41. Pel, M.A.; Foster, S.J.; Park, T.H.; Rietman, H.; Van Arkel, G.; Jones, J.D.G.; Van Eck, H.J.; Jacobsen, E.; Visser, R.G.F.; Van Der Vossen, E.A.G. Mapping and cloning of late blight resistance genes from Solanum venturii using an interspecific candidate gene approach. Mol. Plant-Microbe Interact. 2009, 22, 601–615. [Google Scholar] [CrossRef][Green Version]
  42. Jo, K.R.; Visser, R.G.F.; Jacobsen, E.; Vossen, J.H. Characterisation of the late blight resistance in potato diferential MaR9 reveals a qualitative resistance gene, R9a, residing in a cluster of Tm-2 (2) homologs on chromosome IX. Theor. Appl. Genet. 2015, 128, 931–941. [Google Scholar] [CrossRef][Green Version]
  43. Vossen, J.H.; Van Arkel, G.; Bergervoet, M.; Jo, K.-R.; Jacobsen, E.; Visser, R.G.F. The Solanum demissum R8 late blight resistance gene is an Sw-5 homologue that has been deployed worldwide in late blight resistant varieties. Theor. Appl. Genet. 2016, 129, 1785–1796. [Google Scholar] [CrossRef]
  44. Chen, X.; Lewandowska, D.; Armstrong, M.R.; Baker, K.; Lim, J.T.-Y.; Bayer, M.; Harrower, B.; McLean, K.; Jupe, F.; Witek, K.; et al. Identification and rapid mapping of a gene conferring broad-spectrum late blight resistance in the diploid potato species Solanum verrucosum through DNA capture technologies. Theor. Appl. Genet. 2018, 131, 1287–1297. [Google Scholar] [CrossRef][Green Version]
  45. Nagel, M.; Dulloo, M.E.; Bissessur, P.; Gavrilenko, T.; Bamberg, J.; Ellis, D.; Giovannini, P. Global Strategy for the Conservation of Potato; Global Crop Diversity Trust: Bonn, Germany, 2022; pp. 1–159. [Google Scholar] [CrossRef]
  46. Bukasov, S.M. Systematics of the potato. Proc. Appl. Bot. Genet. Breed. 1978, 62, 3–35. (In Russian) [Google Scholar]
  47. Gorbatenko, L.E. Potato species of South America: Ecology, Geography, Introduction, Taxonomy, and Breeding Value; Russian Academy of Agricultural Sciences, State Scientific Centre of the Russian Federation: St. Petersburg, Russian, 2006; pp. 1–456. (In Russian) [Google Scholar]
  48. Hawkes, J.G. The Potato: Evolution, Biodiversity and Genetic Resources; Belhaven Press: London, UK, 1990; pp. 1–259. [Google Scholar]
  49. Haesaert, G.; Vossen, J.H.; Custers, R.; De Loose, M.; Haverkort, A.; Heremans, B.; Hutten, R.; Kessel, G.; Landschoot, S.; van Droogenbroeck, B.; et al. Transformation of the potato variety Desiree with single or multiple resistance genes increases resistance to late blight under field conditions. Crop. Prot. 2015, 77, 163–175. [Google Scholar] [CrossRef]
  50. Haverkort, A.J.; Boonekamp, P.M.; Hutten, R.; Jacobsen, E.; Lotz, L.A.P.; Kessel, G.J.T.; Vossen, J.H.; Visser, R.G.F. Durable late blight resistance in potato through dynamic varieties obtained by cisgenesis: Scientific and societal advances in the DuRPh project. Potato Res. 2016, 59, 35–66. [Google Scholar] [CrossRef][Green Version]
  51. Ghislain, M.; Byarugaba, A.A.; Magembe, E.; Njoroge, A.; Rivera, C.; Román, M.L.; Tovar, J.C.; Gamboa, S.; Forbes, G.A.; Kreuze, J.F.; et al. Stacking three late blight resistance genes from wild species directly into African highland potato varieties confers complete field resistance to local blight races. Plant Biotech. J. 2019, 17, 1119–1129. [Google Scholar] [CrossRef] [PubMed][Green Version]
  52. Rogozina, E.V.; Beketova, M.P.; Muratova, O.A.; Kuznetsova, M.A.; Khavkin, E.E. Stacking resistance genes in multiparental interspecific potato hybrids to anticipate late blight outbreaks. Agronomy 2021, 11, 115. [Google Scholar] [CrossRef]
  53. Fadina, O.A.; Beketova, M.P.; Kuznetsova, M.A.; Rogozina, E.V.; Khavkin, E.E. Polymorphisms and evolution of Solanum bulbocastanum genes for broad-spectrum resistance to Phytophthora infestans. Russ. J. Plant Physiol. 2019, 66, 950–957. [Google Scholar] [CrossRef]
  54. Muratova, O.A.; Beketova, M.P.; Kuznetsova, M.A.; Rogozina, E.V.; Khavkin, E.E. South American species Solanum alandiae Card. and S. okadae Hawkes et Hjerting as potential sources of genes for potato late blight resistance. Proc. Appl. Bot. Genet. Breed. 2020, 181, 73–83. [Google Scholar] [CrossRef][Green Version]
  55. Budin, K.Z. Genetic foci of Solanum species, Petota Dumort, resistant to Phytophthora infestans (Mont.) De Bary. Genet. Resour. Crop. Evol. 2002, 49, 229–235. [Google Scholar] [CrossRef]
  56. Moore, R.C.; Purugganan, M.D. The evolutionary dynamics of plant duplicate genes. Curr. Opin. Plant Biol. 2005, 8, 122–128. [Google Scholar] [CrossRef]
  57. Hardigan, M.A.; Crisovan, E.; Hamilton, J.P.; Kim, J.; Laimbeer, P.; Leisner, C.P.; Manrique-Carpintero, N.C.; Newton, L.; Pham, G.M.; Vaillancourt, B.; et al. Genome reduction uncovers a large dispensable genome and adaptive role for copy number variation in asexually propagated Solanum tuberosum. Plant Cell 2016, 28, 388–405. [Google Scholar] [CrossRef][Green Version]
  58. Hardigan, M.A.; Laimbeer, F.P.E.; Newton, L.; Crisovan, E.; Hamilton, J.P.; Vaillancourt, B.; Wiegert-Rininger, K.; Wood, J.C.; Douches, D.S.; Farré, E.M.; et al. Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proc. Natl. Acad. Sci. USA 2017, 114, E9999–E10008. [Google Scholar] [CrossRef][Green Version]
  59. Qian, L.H.; Zhou, G.C.; Sun, X.Q.; Lei, Z.; Zhang, Y.M.; Xue, J.Y.; Hang, Y.Y. Distinct patterns of gene gain and loss: Diverse evolutionary modes of NBS-encoding genes in three Solanaceae crop species. G3 Genes|Genomes|Genet. 2017, 7, 1577–1585. [Google Scholar] [CrossRef][Green Version]
  60. Cheng, F.; Wu, J.; Cai, X.; Liang, J.; Freeling, M.; Wang, X. Gene retention, fractionation and subgenome differences in polyploid plants. Nat. Plants 2018, 4, 258–268. [Google Scholar] [CrossRef]
  61. Barragan, A.C.; Weigel, D. Plant NLR diversity: The known unknowns of pan-NLRomes. Plant Cell 2021, 33, 814–831. [Google Scholar] [CrossRef] [PubMed]
  62. Tang, D.; Jia, Y.; Zhang, J.; Li, H.; Cheng, L.; Wang, P.; Bao, Z.; Liu, Z.; Feng, S.; Zhu, X.; et al. Genome evolution and diversity of wild and cultivated potatoes. Nature 2022, 606, 535–541. [Google Scholar] [CrossRef] [PubMed]
  63. Hoopes, G.; Meng, X.; Hamilton, J.P.; Achakkagari, S.R.; de Alves, F.G.F.; Bolger, M.E.; Coombs, J.J.; Esselink, D.; Kaiser, N.R.; Kodde, L.; et al. Phased, chromosome-scale genome assemblies of tetraploid potato reveal a complex genome, transcriptome, and predicted proteome landscape underpinning genetic diversity. Mol. Plant 2022, 15, 520–536. [Google Scholar] [CrossRef] [PubMed]
  64. Janzen, G.M.; Wang, L.; Hufford, M.B. The extent of adaptive wild introgression in crops. New Phytol. 2019, 221, 1279–1288. [Google Scholar] [CrossRef][Green Version]
  65. Morrell, P.L.; Buckler, E.S.; Ross-Ibarra, J. Crop genomics: Advances and applications. Nature Rev. Genet. 2012, 13, 85–96. [Google Scholar] [CrossRef]
  66. Spanoghe, M.; Marique, T.; Nirsha, A.; Esnault, F.; Lanterbecq, D. Genetic Diversity Trends in the Cultivated Potato: A Spatiotemporal Overview. Biology 2022, 11, 604. [Google Scholar] [CrossRef]
  67. Correll, D.S. The potato and its wild relatives. Contr. Texas Res. Found. Bot. Stud. 1962, 4, 606. [Google Scholar]
  68. Spooner, D.M.; Ghislain, M.; Simon, R.; Jansky, S.H.; Gavrilenko, T. Systematics, diversity, genetics, and evolution of wild and cultivated potatoes. Bot. Rev. 2014, 80, 283–383. [Google Scholar] [CrossRef]
  69. Ellis, D.; Salas, A.; Chavez, O.; Gomez, R.; Anglin, N. Ex situ conservation of potato [Solanum section Petota (Solanaceae)] Genetic Resources in Genebanks. In The Potato Crop; Campos, H., Ortiz, O., Eds.; Springer: Cham, Switzerland, 2020. [Google Scholar] [CrossRef]
  70. Potato Genome Sequencing Consortium. Genome sequence and analysis of the tuber crop potato. Nature 2011, 475, 189–195. [Google Scholar] [CrossRef] [PubMed][Green Version]
  71. Aversano, R.; Contaldi, F.; Ercolano, M.R.; Grosso, V.; Iorizzo, M.; Tatino, F.; Xumerle, L.; Molin, A.D.; Avanzato, C.; Ferrarini, A.; et al. The Solanum commersonii genome sequence provides insights into adaptation to stress conditions and genome evolution of wild potato relatives. Plant Cell 2015, 27, 954–968. [Google Scholar] [CrossRef] [PubMed][Green Version]
  72. Gálvez, J.H.; Tai, H.H.; Barkley, N.A.; Gardner, K.; Ellis, D.; Strömvik, M.V. Understanding potato with the help of genomics. AIMS Agricult. Food 2017, 2, 16–39. [Google Scholar] [CrossRef]
  73. Leisner, C.P.; Hamilton, J.P.; Crisovan, E.; Manrique-Carpintero, N.C.; Marand, A.P.; Newton, L.; Pham, G.M.; Jiang, J.; Douches, D.S.; Jansky, S.H.; et al. Genome sequence of M6, a diploid inbred clone of the high-glycoalkaloid-producing tuber-bearing potato species Solanum chacoense, reveals residual heterozygosity. Plant J. 2018, 94, 562–570. [Google Scholar] [CrossRef][Green Version]
  74. Kyriakidou, M.; Achakkagari, S.R.; López, J.H.G.; Zhu, X.; Tang, C.Y.; Tai, H.H.; Anglin, N.L.; Ellis, D.; Strömvik, M.V. Structural genome analysis in cultivated potato taxa. Theor. Appl. Genet. 2020, 133, 951–966. [Google Scholar] [CrossRef][Green Version]
  75. Tiwari, J.K.; Rawat, S.; Luthra, S.K.; Zinta, R.; Sahu, S.; Varshney, S.; Kumar, V.; Dalamu, D.; Mandadi, N.; Manoj Kumar, M.; et al. Genome sequence analysis provides insights on genomic variation and late blight resistance genes in potato somatic hybrid (parents and progeny). Mol. Biol. Rep. 2021, 48, 623–635. [Google Scholar] [CrossRef]
  76. Wang, F.; Xia, Z.; Zou, M.; Zhao, L.; Jiang, S.; Zhou, Y.; Zhang, C.; Ma, Y.; Bao, Y.; Sun, H.; et al. The autotetraploid potato genome provides insights into highly heterozygous species. Plant Biotech. J. 2022, 20, 1996–2005. [Google Scholar] [CrossRef]
  77. Kiru, S.D. 80 years of the VIR potato collection. Proc. Appl. Bot. Genet. Breed. 2007, 183, 5–21. (In Russian) [Google Scholar]
  78. Zoteyeva, N.; Mezaka, I.; Vilcâne, D.; Carlson-Nilsson, U.; Skrabule, I.; Rostoks, N. Assessment of genes R1 and R3 conferring resistance to late blight and of gene Rysto conferring resistance to potato virus Y in two wild species accessions and their hybrid progenies. Proc. Latv. Acad. Sci. Sect. B 2014, 68, 133–141. [Google Scholar] [CrossRef]
  79. Enciso-Maldonado, G.A.; Lozoya-Saldaña, H.; Colinas-Leon, M.T.; Cuevas-Sanchez, J.A.; Sanabria-Velázquez, A.D.; Bamberg, J.; Raman, K.V. Assessment of wild Solanum species for resistance to Phytophthora infestans (Mont.) de Bary in the Toluca valley, Mexico. Am. J. Potato Res. 2022, 99, 25–39. [Google Scholar] [CrossRef]
  80. Jupe, F.; Pritchard, L.; Etherington, G.J.; Mackenzie, K.; Cock, P.J.; Wright, F.; Kumar, S.S.; Bolser, D.; Bryan, G.J.; Jones, J.D. Identifcation and localisation of the NB–LRR gene family within the potato genome. BMC Genom. 2012, 13, 75. [Google Scholar] [CrossRef][Green Version]
  81. Quirin, E.A.; Mann, H.; Meyer, R.S.; Traini, A.; Chiusano, M.L.; Litt, A.; Bradeen, J.M. Evolutionary meta-analysis of Solanaceous resistance gene and Solanum resistance gene analog sequences and a practical framework for cross-species comparisons Mol. Plat-Microbe Inter. 2012, 25, 603–612. [Google Scholar] [CrossRef] [PubMed][Green Version]
  82. Stam, R.; Silva Arias, G.A.; Tellier, A. Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats. New Phytol. 2019, 224, 367–379. [Google Scholar] [CrossRef] [PubMed]
  83. Prakash, C.; Trognitz, F.C.; Venhuizen, P.; von Haeseler, A.; Trognitz, B. A compendium of genome-wide sequence reads from NBS (nucleotide binding site) domains of resistance genes in the common potato. Sci. Rep. 2020, 10, 11392. [Google Scholar] [CrossRef]
  84. Kloosterman, B.; Abelenda, J.A.; Gomez, M.D.M.C.; Oortwijn, M.; de Boer, J.M.; Kowitwanich, K.; Horvath, B.M.; van Eck, H.J.; Smaczniak, C.; Prat, S.; et al. Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 2013, 495, 246–250. [Google Scholar] [CrossRef]
  85. Duan, Y.; Duan, S.; Armstrong, M.R.; Xu, J.; Zheng, J.; Hu, J.; Chen, X.; Hein, I.; Li, G.; Jin, L. Comparative transcriptome profiling reveals compatible and incompatible patterns of potato toward Phytophthora infestans. G3 Genes|Genomes|Genet. 2020, 10, 623–634. [Google Scholar] [CrossRef] [PubMed][Green Version]
  86. Petek, M.; Zagorščak, M.; Ramšak, Ž.; Sanders, S.; Tomaž, Š.; Tseng, E.; Zouine, M.; Coll, A.; Gruden, K. Cultivar-specific transcriptome and pan-transcriptome reconstruction of tetraploid potato. Sci. Data 2020, 7, 249. [Google Scholar] [CrossRef] [PubMed]
  87. Jacobs, M.M.; Smulders, M.J.; van den Berg, R.G.; Vosman, B. What’s in a name; genetic structure in Solanum section Petota studied using population-genetic tools. BMC Evol. Biol. 2011, 11, 1–20. [Google Scholar] [CrossRef] [PubMed][Green Version]
  88. Gebhardt, C. Bridging the gap between genome analysis and precision breeding in potato. Trends Genet. 2013, 29, 248–256. [Google Scholar] [CrossRef]
  89. Tiwari, J.K.; Siddappa, S.; Singh, B.P.; Kaushik, S.K.; Chakrabarti, S.K.; Bhardwaj, V.; Chandel, P. Molecular markers for late blight resistance breeding of potato: An update. Plant Breed. 2013, 132, 237–245. [Google Scholar] [CrossRef]
  90. Sharma, S.K.; Bryan, G.J. Genome sequence-based marker development and genotyping in potato. In The Potato Genome; Springer: Cham, Switzerland, 2017; pp. 307–326. [Google Scholar] [CrossRef]
  91. Monte, M.N.; Rey Burusco, M.F.; Carboni, M.F.; Castellote, M.A.; Sucar, S.; Norero, N.S.; Colman, S.L.; Massa, G.A.; Colavita, M.L.; Feingold, S.E. Genetic diversity in Argentine Andean potatoes by means of functional markers. Am. J. Potato Res. 2018, 95, 286–300. [Google Scholar] [CrossRef]
  92. Kuang, H.; Wei, F.; Marano, M.R.; Wirtz, U.; Wang, X.; Liu, J.; Shum, W.P.; Zaborsky, J.; Tallon, L.J.; Rensink, W.; et al. The R1 resistance gene cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant J. 2005, 44, 37–51. [Google Scholar] [CrossRef] [PubMed]
  93. Pankin, A.A.; Sokolova, E.A.; Rogozina, E.V.; Kuznetsova, M.A.; Deahl, K.L.; Jones, R.W.; Khavkin, E.E. Searching Among Wild Solanum Species for Homologues of RB/Rpiblb1/Rpi-bt1 Gene Conferring Durable Late Blight Resistance; PAGV-Special Report; Schepers, H.T.A.M., Ed.; DLO Foundation: Wageningen, The Netherlands, 2010; Volume 14, pp. 277–284. [Google Scholar]
  94. Pankin, A.; Sokolova, E.; Rogozina, E.; Kuznetsova, M.; Deahl, K.; Jones, R.; Khavkin, E. Allele mining in the gene pool of wild Solanum species for homologues of late blight resistance gene RB/Rpi-blb1. Plant Genet. Res. 2011, 9, 305–308. [Google Scholar] [CrossRef]
  95. Fadina, O.A.; Belyantseva, T.V.; Khavkin, E.E.; Pankin, A.A.; Rogozina, E.V.; Kuznetsova, M.A.; Jones, R.W.; Deahl, K.L. SCAR Markers for the RB/Rpi-blb1 Gene of Potato Late Blight Resistance; PAGV-Special Report; Schepers, H.T.A.M., Ed.; DLO Foundation: Wageningen, The Netherlands, 2014; Volume 16, pp. 215–220. [Google Scholar]
  96. Liu, Z.; Halterman, D. Identification and characterization of RB-orthologous genes from the late blight resistant wild potato species Solanum verrucosum, Physiol. Mol. Plant Pathol. 2006, 69, 230–239. [Google Scholar] [CrossRef]
  97. Sokolova, E.A.; Fadina, O.A.; Khavkin, E.E.; Rogozina, E.V.; Kuznetsova, M.A.; Jones, R.W.; Deahl, K.L. Structural Homologues of CC-NBS-LRR Genes for Potato Late Blight Resistance in Wild Solanum Species; PAGV-Special Report; Schepers, H.T.A.M., Ed.; DLO Foundation: Wageningen, The Netherlands, 2014; Volume 16, pp. 247–253. [Google Scholar]
  98. Beketova, M.P.; Sokolova, E.A.; Rogozina, E.V.; Kuznetsova, M.A.; Khavkin, E.E. Two orthologs of late blight resistance gene R1 in wild and cultivated potato. Russ. J. Plant Physiol. 2017, 64, 718–727. [Google Scholar] [CrossRef]
  99. Pel, M.A. Mapping, Isolation and Characterization of Genes Responsible for Late Blight Resistance in Potato. Ph.D. Thesis, Wageningen University, Wageningen, The Netherlands, 2010; pp. 1–200. Available online: (accessed on 4 January 2023).
  100. Gurina, A.A.; Alpatieva, N.V.; Chalaya, N.V.; Mironenko, N.V.; Khiutti, A.V.; Rogozina, E.V. Homologs of late blight resistance genes in representatives of tuber-bearing species of the genus Solanum L. Russ. J. Genet. 2022, 58, 1473–1484. [Google Scholar] [CrossRef]
  101. Huang, B.; Ruess, H.; Liang, Q.; Colleoni, C.; Spooner, D.M. Analyses of 202 plastid genomes elucidate the phylogeny of Solanum section Petota. Sci. Rep. 2019, 9, 4454. [Google Scholar] [CrossRef][Green Version]
  102. Hosaka, A.J.; Sanetomo, R.; Hosaka, K. A de novo genome assembly of Solanum verrucosum Schlechtendal, a Mexican diploid species geographically isolated from other diploid A-genome species of potato relatives. G3 Genes|Genomes|Genet. 2022, 12, jkac166. [Google Scholar] [CrossRef]
  103. Liu, Z.; Halterman, D. Different genetic mechanisms control foliar and tuber resistance to Phytophthora infestans in wild potato Solanum verrucosum. Am. J. Potato Res. 2009, 86, 476–480. [Google Scholar] [CrossRef]
  104. van Lieshout, N.; van der Burgt, A.; de Vries, M.E.; ter Maat, M.; Eickholt, D.; Esselink, D.; van Kaauwen, M.P.W.; Kodde, L.P.; Visser, R.G.F.; Lindhout, P.; et al. Solyntus, the new highly contiguous reference genome for potato (Solanum tuberosum). G3 Genes|Genomes|Genet. 2020, 10, 3489–3495. [Google Scholar] [CrossRef]
  105. Zoteyeva, N.; Chrzanowska, M.; Flis, B.; Zimnoch-Guzowska, E. Resistance to pathogens of the potato accessions from the collection of NI Vavilov Institute of Plant Industry (VIR). Am. J. Potato Res. 2012, 89, 277–293. [Google Scholar] [CrossRef]
  106. Chizhik, V.K.; Martynov, V.V.; Sokolova, E.A.; Kuznetsova, M.A.; Rogozina, E.V.; Khavkin, E.E. The Repertoire of Avr Genes in Two East European Populations of Phytophthora Infestans; PAGV-Special Report; Schepers, H.T.A.M., Ed.; DLO Foundation: Wageningen, The Netherlands, 2019; Volume 19, pp. 231–240. [Google Scholar]
  107. Jo, K.R.; Kim, C.J.; Kim, S.J.; Kim, T.Y.; Bergervoet, M.; Jongsma, M.A.; Visser, R.G.; Jacobsen, E.; Vossen, J.H. Development of late blight resistant potatoes by cisgene stacking. BMC Biotechnol. 2014, 14, 50. [Google Scholar] [CrossRef] [PubMed][Green Version]
  108. Van der Vossen, E.A.G.V.D.; Gros, J.; Sikkema, A.; Muskens, M.; Wouters, D.; Wolters, P.; Pereira, A.; Allefs, S. The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J. 2005, 44, 208–222. [Google Scholar] [CrossRef]
  109. Lenman, M.; Ali, A.; Mühlenbock, P.; Carlson-Nilsson, U.; Liljeroth, E.; Champouret, N.; Vleeshouwers, V.; Andreasson, E. Effector-driven marker development and cloning of resistance genes against Phytophthora infestans in potato breeding clone SW93-1015. Theor. Appl. Genet. 2015, 129, 105–115. [Google Scholar] [CrossRef] [PubMed]
  110. Lokossou, A.A.; Park, T.-H.; van Arkel, G.; Arens, M.; Ruyter-Spira, C.; Morales, J.; Whisson, S.C.; Birch, P.R.J.; Visser, R.G.F.; Jacobsen, E.; et al. Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol. Plant Microbe Interact. 2009, 22, 630–641. [Google Scholar] [CrossRef] [PubMed][Green Version]
  111. Kim, H.-J.; Lee, H.-R.; Jo, K.-R.; Mortazavian, S.M.M.; Huigen, D.J.; Evenhuis, B.; Kessel, G.; Visser, R.G.F.; Jacobsen, E.; Vossen, J.H. Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes. Theor. Appl. Genet. 2012, 124, 923–935. [Google Scholar] [CrossRef][Green Version]
  112. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
Table 1. Resistance of wild potato species accessions to P. infestans in the laboratory test.
Table 1. Resistance of wild potato species accessions to P. infestans in the laboratory test.
SeriesSpeciesFrequency of Resistant Accessions * (the Total Number)The Average Score
BulbocastanaS. bulbocastanum0.71 (14)6.7
PinnatisectaS. pinnatisectum0.50 (6)6.0
S. cardiophyllum0.60 (5)6.4
S. cardiophyllum
ssp. ehrenbergii
0.17 (12)4.7
S. jamesii0.11 (9)5.1
S. stenophyllidium0 (2)3.0
YungasensaS. chacoense0.33 (6)4.8
MagliaS. maglian.d.**
Tuberosa (wild)S. alandiae0 (2)4.5
S. avilesii0.5 (2)5.5
S. berthaultii0.50 (8)6.5
S. microdontum0.20 (5)5.8
S. microdontum ssp. gigantophyllum, syn. simplicifolium 0.20 (5)5.8
S. sucrensen.d.
S. venturii0.29 (17)6.6
S. vernei0 (5)5.0
S. verrucosum0.37 (8)5.4
Tuberosa (cultivated)S. phureja0 (3)4.3
S. stenotomum0 (2)6.4
DemissaS. demissum0.58 (12)6.7
LongipedicellataS. stoloniferum0.25 (20)5.4
S. polytrichon0 (13)4.4
* 7–9 points by the 1–9 resistance scale (1, susceptible; 9, resistant); ** n.d.—no data.
Table 2. Screening Solanum species with SCAR markers of the Rpi genes. Frequency of the markers (the number of accessions analyzed).
Table 2. Screening Solanum species with SCAR markers of the Rpi genes. Frequency of the markers (the number of accessions analyzed).
Markers (the Numbers of Scored Accession Are Shown in Parenthesis)
Rpi-R1-1205Rpi-R2-1137Rpi-blb3-305Rpi-R3a-1380Rpi-R3b-378Rpi-R8-1258Rpi-blb1-821Rpi-sto1-890Rpi-blb2- 976Rpi-vnt1-612
BulbocastanaS. bulbocastanum0 (34)0.37 (16)0.75 (16)0.29 (34)0.42(24)0 (13)0.48 (25)0.53 (15)0.80 (15)1.0 (15)
PinnatisectaS. pinnatisectum0 (9)0.5 (6)0.28 (7)0 (9)0.33 (6)0 (6)0 (6)0 (6)0 (6)1.0 (6)
S. cardiophyllum0 (7)0.14 (7)0.28 (7)0.28 (7)0.17 or 1.0 (6)0 (6)0.17 (6)0.17 (6)0.33 (6)0.66 (6)
S. cardiophyllum ssp. ehrenbergii0 (15)0.75 (8) 0.12 (8)0.26 (15)0.78 (14)0 (4)0 (12)0 (8)0.14 (7)1 (4)
S. jamesii0 (12)0 (1)0 (1)0 (12)0.37 (8)n.d.0 (2)0 (1)0 (1)n.d.
S. stenophyllidium0 (3)1.0 (2)0 (2)0 (3)0.33 (3)n.d.0 (2)0 (2)0 (2)n.d.
YungasensaS. chacoense0 (11)0 (11)0 (11)0 (11)0.36 (11)0 (11)0 (11)0 (11)0 (11)0 (11)
MagliaS. maglia0 (3)0 (3)0 (3)0 (3)0 (3)1 (3)0 (3)0 (3)0 (3) 0 (3)
Tuberosa (wild)S. alandiae0 (5)0 (4)0 (4)0 (5)0 (3)0.6 (5)0 (4)0 (4)0.8 (5)0.2 (5)
S. avilesii0 (2)0.5 (2)0 (2)0 (2)0 (2)1 (2)0 (2)0 (2)1.0 (2)1.0 (2)
S. berthaultii0.09 (11)0 (5)0 (5)0 (11)0 (6)1 (4)0 (5)0 (5)0.4 (5)0.6 (5)
S. microdontum0 (9)0 (8)0 (8)0 (8)0 (8)0.43 (7)0 (8)0 (7)0 (7)0.37 (7)
S. microdontum ssp. gigantophyllum, syn. simplicifolium0 (4)0 (3)0 (3)0.25(4)0 (3)0.33 (3)0 (3)0 (2)0.33 (1)0.66 (3)
S. sucrense0 (2)0 (2) 0 (2)0 (2)0 (2)0.5 (2)0 (2)0 (1)0 (2)0.5 (2)
S. venturii0 (6)0.17 (6)0.17 (6)0 (6)0.17 (6)0.83 (6)0 (6)0 (6)0.33 (6)1.0 (6)
S. vernei0 (5)0.2 (5)0 (5)0 (5)0 (5)0.6 (5)0 (5)0 (5)0 (4)0.4 (5)
S. verrucosum0 (15)0.08 (12)0 (12)0 (15)0.07 (14)0 (12)0 (14)0 (12)0 (12)0 (12)
Tuberosa (cultivated)S. phureja0 (6)0 (6)0 (6)0 (6)0.33 (6)0.66 (6)0 (6)0 (6)0 (6)0.66 (6)
S. stenotomum0 (2)0 (2)0 (2)0 (2)0 (2)0.5 (2)0 (2)0 (2)0 (2)0.5 (2)
DemissaS. demissum0.46 (37)0.5 (6)0.33 (6)0.18 (38)0.9 (10)0.17(6)0 (8)0 (6)0 (6)0.17 (6)
LongipedicellataS. stoloniferum0.26 (46)0.67 (18)0.5 (18)0.2 (46)0.79 (24)0.5 (12)0.33 (24)0.22 (18)0.28 (18)1.0 (12)
S. polytrichon0.17 (12)1.0 (5)0.2 (5)0.08 (12)0.33 (9)0.33 (3)0.28 (7)0 (5) 0.4 (5)0.67 (3)
Table 3. Screening Solanum species from the seven taxonomic series of Section Petota Dum. with SCAR markers of the Rpi genes. Frequency of the markers (the number of accessions analyzed).
Table 3. Screening Solanum species from the seven taxonomic series of Section Petota Dum. with SCAR markers of the Rpi genes. Frequency of the markers (the number of accessions analyzed).
Markers (the Numbers of Scored Accession Are Shown in Parenthesis)
Bulbocastana0 (34)0.37 (16)0.75 (16)0.29 (34)0.42(24)0 (13)0.48 (25)0.53 (15)0.80 (15)1.0 (15)
Pinnatisecta0 (46) 0.50 (24)0.20 (25)0.13 (46)0.55 (31) *0.06 (16)0.03 (28)0.04 (23)0.14 (22)0.87 (16)
Yungasensa0 (11)0 (11)0 (11)0 (11)0.36 (11)0 (11)0 (11)0 (11)0 (11)0 (11)
Maglia0 (3)0 (3)0 (3)0 (3)0 (3)1.0 (3)0 (3)0 (3)0 (3) 0 (3)
Tuberosa (wild)0.02 (62)0.08 (50)0.02 (50)0.02 (61)0.04 (50)0.51 (49)0 (52)0 (48)0.22 (49)0.40 (50)
Tuberosa (cultivated)0 (8)0 (8)0 (8)0 (8)0.25 (8)0.62 (8)0 (8)0 (8)0 (8)0.62 (8)
Demissa0.46 (37)0.50 (6)0.33 (6)0.18 (38)0.9 (10)0.17 (6)0 (8)0 (6)0 (6)0.17 (6)
Longipedicellata0.24 (58)0.74 (23)0.43 (23)0.17 (58)0.66 (33)0.47 (15)0.32 (31)0.17 (23)0.30 (23)0.93 (15)
* without of S. cardiophyllum.
Table 4. SCAR markers of the Rpi genes used in this study.
Table 4. SCAR markers of the Rpi genes used in this study.
GeneSolanum Species, Gene Accession Numbers in the NCBI GenBankMarker, Length, bpMarker Position on the Gene, bpAnneal. Temp., °CPrimer SequencesReferences
RB/Rpi-blb1S. bulbocastanum, AY426259Rpi-blb1-8214989–580962F-aacctgtatggcagtggcatg
Rpi-sto1S. stoloniferum, EU884421Rpi-sto1-890241–113065F-accaaggccacaagattctc
Rpi-blb2S. bulbocastanum, DQ122125Rpi-blb2-9764004–497958F-ggactgggtaacgacaatcc
Rpi-R1S. demissum, AF447489Rpi-R1-12065126–633161F-cactcgtgacatatcctcacta
Rpi-R2S. demissum, FJ536325Rpi-R2-11371277–241360F-aagatcaagtggtaaaggctgatg
Rpi-blb3S. bulbocastanum, FJ536346Rpi-blb3-3055551–585563.5F-agctttttgagtgtgtaattgg
Rpi-R3aS. demissum, AY849382Rpi-R3a-13801677–305664F-tccgacatgtattgatctccctg
Rpi-R3bS. demissum, JF900492Rpi-R3b-37894,818–95,19564F-gtcgatgaatgctatgtttctcgaga
Rpi-R8S. demissum, KU530153Rpi-R8-125873,693–74,95062.5F-aacaagagatgaattaagtcggtagc
[43] modif.
Rpi-vnt1S. venturii, FJ423044–FJ423046Rpi-vnt1-61289–70058F-ccttcctcatcctcacatttag
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Rogozina, E.V.; Gurina, A.A.; Chalaya, N.A.; Zoteyeva, N.M.; Kuznetsova, M.A.; Beketova, M.P.; Muratova, O.A.; Sokolova, E.A.; Drobyazina, P.E.; Khavkin, E.E. Diversity of Late Blight Resistance Genes in the VIR Potato Collection. Plants 2023, 12, 273.

AMA Style

Rogozina EV, Gurina AA, Chalaya NA, Zoteyeva NM, Kuznetsova MA, Beketova MP, Muratova OA, Sokolova EA, Drobyazina PE, Khavkin EE. Diversity of Late Blight Resistance Genes in the VIR Potato Collection. Plants. 2023; 12(2):273.

Chicago/Turabian Style

Rogozina, Elena V., Alyona A. Gurina, Nadezhda A. Chalaya, Nadezhda M. Zoteyeva, Mariya A. Kuznetsova, Mariya P. Beketova, Oksana A. Muratova, Ekaterina A. Sokolova, Polina E. Drobyazina, and Emil E. Khavkin. 2023. "Diversity of Late Blight Resistance Genes in the VIR Potato Collection" Plants 12, no. 2: 273.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop