Abstract
The potato cyst nematodes (PCN) Globodera rostochiensis and G. pallida are among the most important pests causing significant yield loss in potato production. Cultivating resistant cultivars of potato is the most effective and environmentally safe method for protecting potato crops against nematodes. However, widespread cultivation of cultivars resistant to G. rostochiensis can affect the reproduction of G. pallida. Therefore, breeding for resistance to nematodes remains among the major aims of potato breeding programmes. Many wild Solanum species could be valuable sources of nematode resistance. This study examined the resistance to G. pallida identified in two accessions of the wild species Solanum gourlayi. Both accessions demonstrated resistance to pathotypes Pa2 and Pa3, but show asymmetric distribution of resistance among the progeny clones. The presented distributions of resistance scores indicate quantitative nature of resistance to G. pallida. Furthermore, this resistance is specific to each pathotype and may be controlled by different genes. We also conclude that there is a need for independent evaluation of resistance for both pathotypes of G. pallida (Pa2 and Pa3).
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
The potato cyst nematodes (PCN) Globodera rostochiensis and G. pallida are the most important pests that feed on potato roots (Evans and Trudgill 1992). Yield loss caused by PCN is estimated to be as high as 50% (Nicol et al. 2011). Both PCN species are included in the list of quarantine pathogens in many countries (Smith et al. 1992). Growing resistant cultivars is economically the most effective and environmentally safe method for protecting potato crops against PCN (EPPO/OEPP 2004). However, the widespread cultivation of cultivars resistant to only G. rostochiensis may increase the reproduction of G. pallida. In recent years, the increased spread of G. pallida among populations of nematodes has been observed in Europe (Širca et al. 2012; EPPO 2012, 2013; Nježić et al. 2014). The cultivation of potato cultivars with resistance to multiple Globodera species may effectively provide protection against the wide spectrum of PCN pathotypes.
Resistance to nematodes was not initially found within Solanum tuberosum ssp. tuberosum. Thus, breeding for resistance to nematodes is based on resistance identified in other Solanum species (Dalamu et al. 2012). The dominant gene Gpa2 associated with resistance to G. pallida pathotype Pa2 was found in S. tuberosum ssp. andigena (van der Voort et al. 1999). The dominant gene H2 was found in S. multidissectum, which confers resistance against G. pallida pathotype Pa1 (Dunnett 1961; Strachan et al. 2019). Quantitative resistance was identified in the wild species S. tuberosum ssp. andigena, together with the large effect QTL GpaIVsadg (Bradshaw et al. 1998; Bryan et al. 2004), and in S. vernei together with Gpa5 (van der Voort et al. 2000; Bryan et al. 2002). However, both these genes confer only partial levels of resistance to G. pallida pathotypes Pa2 and Pa3. Caromel et al. (2005) identified that cooperating resistance loci GpaVsspl and GpaXIsspl originating from S. sparsipilum resulted in a strong hypersensitive response on the roots infected with G. pallida Pa2/3. However, many loci conferring resistance to G. pallida originate from wild species accessions that have not been introduced into advanced breeding material.
Solanum gourlayi (grl) is one of the sources of resistance to G. pallida identified among accessions of wild Solanum species (Ruiz de Galarreta et al. 1998; Castelli et al. 2005). The major aim of our research was to examine the nematode resistance identified in two accessions of the wild species S. gourlayi.
Materials and Methods
Plant Material
Two accessions of S. gourlayi (grl) were obtained in the form of seeds from the Centre for Genetic Resources, the Netherlands (CGN): CGN22342 and CGN17592. Both of these accessions were described as resistant to pathotypes Pa2 and Pa3 of G. pallida (CGN gene bank description n.d.; links in references). Clone Sg 3/3 was obtained from seeds of accession CGN22342 (2n = 24 chromosomes), and clone Sg 2/7 was obtained from seeds of accession CGN17592 (2n = 24 chromosomes). The resistance of these clones was confirmed in a glasshouse test, and then these clones were used as resistant parents in crosses with the susceptible diploid clone DW 94-4235 (resistance score 1), obtained in a crossing programme performed in Młochów Research Centre. One hundred and forty progeny clones were obtained from the cross DW 94-4235 × Sg 2/7 and 104 progeny clones were obtained from the cross DW 94-4235 × Sg 3/3.
Test for Nematode Resistance
The test was performed according to Przetakiewicz and Milczarek (2017). The resistance screening was conducted in two independent phenotypic tests. Ten tubers per genotype were planted separately in pots with 1 l of soil (Universal Kronenerde soil) containing nematode cysts (5 eggs × ml−1 of soil) of either G. pallida Pa2 (5 tubers) or Pa3 (5 tubers). The pathotypes used for inoculation were the Pa3 population “Chavornay” and pathotype Pa2 obtained from the collection of the Federal Research Centre for Cultivated Plants, Germany (JKI). Plants were grown in a glasshouse for 3 months and then the plants (with soil) were removed and the cysts counted. The relative susceptibility of the tested accessions/progeny clones was calculated according to the following formula:
where Pf is the mean number of cysts determined by counting all cysts from all replicates; cv. Desiree was used as a susceptible standard.
Resistance was scored on a 9-grade scale, where score 9 indicates the highest level of resistance according to the EU Council Directive 2007/33/EC. The progeny clone was regarded as resistant when the score was higher than 5-moderate resistance score (Table 1).
Statistical Analyses
The Pearson correlation coefficient for resistance to pathotypes Pa2 and Pa3 was performed with the STATISTICA data analysis software system, version 10 (www.statsoft.com).
Results
After inoculation with the G. pallida pathotypes Pa2 and Pa3, the mean cyst count over the replicates was established for each tested genotype. The cyst count ranged from 0 to 528 cysts for pathotype Pa2 and from 0 to 532 cysts for pathotype Pa3. The susceptible control (Desiree) developed on average 458 cysts of pathotype Pa2 and 468 cysts of pathotype Pa3. The mean number of cysts counted per tested genotype was used for calculation of resistance scores. The clone was regarded as resistant when the score was higher than 5 (under 45 and 47 cysts counted for Pa2 and Pa3, respectively).
Clone Sg 3/3 was highly resistant to pathotype Pa2 (resistance score 8) and to pathotype Pa3 (resistance score 9). Clone Sg 2/7 was highly resistant to pathotype Pa2 (resistance score 9) and resistant to pathotype Pa3 (resistance score 7).
Cyst count and the resistance score for each tested progeny clone are shown in Supplementary Table 1. Among the progeny of DW 94-4235 × Sg 3/3, 95 (95%) of the clones were resistant to pathotype Pa2 (resistance score > 5). Only 11 (12%) of the clones were resistant to Pa3 (Fig. 1). From among 95 clones resistant to pathotype Pa2, 11 clones were resistant to pathotype Pa3. The Pearson correlation coefficient for resistance to pathotypes Pa2 and Pa3 was r = 0.26* in population DW 94-4235 × Sg 3/3.
Among the progeny of DW 94-4235 × Sg 2/7, the distribution of resistance to pathotype Pa2 was bimodal (Fig. 2). In general, 23 (17%) of the clones from this progeny were resistant to pathotype Pa2 whereas a total of 80 (61%) of the clones were found to be resistant to Pa3 (Fig. 2). From among 80 clones resistant to pathotype Pa3, 15 clones were resistant to pathotype Pa2. The Pearson correlation coefficient for resistance to pathotypes Pa2 and Pa3 was r = 0.08 in population DW 94-4235 × Sg 2/7.
Discussion
Cultivating resistant cultivars of potato is the most effective and environmentally safe method for protecting potato crops against pests and diseases. Potato breeding for resistance is partially based on introgression of resistance genes from wild potato species (Gebhardt and Valkonen 2001). Among Solanum spp. evaluated for nematode resistance, S. gourlayi was recognised as a source of resistance to G. pallida (Dalamu et al. 2012). Van Soest et al. (1983) concluded that both resistant and susceptible accessions can be found in the gene pool of S. gourlayi. Uhrig and Wenzel (1981) found that the percentage of resistant clones in the S. gourlayi hybrids was higher compared with the S. vernei hybrids. Chavez et al. (1988) in their research-derived hybrids of tetraploid S. gourlayi rated high resistance to P4A, with > 50% resistant in crosses with S. tuberosum ssp. andigena, and over 97% in crosses with ssp. tuberosum, but susceptible to P5A. In that investigation, two populations of G. pallida from South America were used, which are designated P4A and P5A according to the pathotype scheme of Canto-Saenz and de Scurrah (1977). The results of our work indicate that the evaluated accessions of S. gourlayi are sources for nematode resistance that can be incorporated into practical potato breeding programmes.
European populations of G. pallida are divided into three groups of pathotypes, namely Pa1, Pa2 and Pa3, based on their different pathogenic characteristics (Kort et al. 1977). Many authors, while evaluating sources of resistance, treat the pathotypes Pa2 and Pa3 as one. Resistance to the G. pallida pathotypes Pa2/Pa3 is used to indicate resistance to pathotypes Pa2 and/or Pa3 (Sattarzadeh et al. 2006). However, taking into account the results of this work, we conclude that resistance tests should be conducted independently for every pathotype. Although the evaluated resistant parental forms (grl accessions) demonstrated resistance to both pathotypes Pa2 and Pa3, this resistance was segregated among the progeny clones. Figures 1 and 2 show the asymmetric distributions of resistances to each tested pathotype of G. pallida in the evaluated progenies. Most of the clones tested from the progeny of DW 94-4235 × Sg 3/3 were highly resistant to pathotype Pa2 and susceptible to pathotype Pa3. In turn, most of the clones tested from the progeny of DW 94-4235× Sg 2/7 were highly resistant to pathotype Pa3 but susceptible to pathotype Pa2. The Pearson correlation coefficients for resistance to pathotypes Pa2 and Pa3 for these populations were low. The presented distributions of resistance scores (Figs. 1 and 2) indicate the quantitative nature of resistance to G. pallida. Furthermore, this resistance is specific to each pathotype and may be controlled by different genes. There is a need of further investigation of the genetic basis of this resistance.
References
Bradshaw JE, Hackett CA, Meyer RC, Milbourne D, McNicol JW, Phillips MS, Waugh R (1998) Identification of AFLP and SSR markers associated with quantitative resistance to Globodera pallida (Stone) in tetraploid potato (Solanum tuberosum subsp. tuberosum) with a view to marker-assisted selection. Theor Appl Genet 97:202–210
Bryan G, McLean K, Bradshaw J, De Jong W, Phillips M, Castelli L, Waugh R (2002) Mapping QTLs for resistance to the cyst nematode Globodera pallida derived from the wild potato species Solanum vernei. Theor Appl Genet 105:68–77
Bryan GJ, McLean K, Pande B, Purvis A, Hackett CA, Bradshaw JE, Waugh R (2004) Genetical dissection of H3-mediated polygenic PCN resistance in a heterozygous autotetraploid potato population. Mol Breed 14:105–116
Canto-Saenz MA, de Scurrah MM (1977) Races of the potato cyst nematode in the Andean region and a new system of classification. Nematologica 23:340–349
Caromel B, Mugniéry D, Kerlan MC, Andrzejewski S, Palloix A, Ellissèche D, Rousselle-Bourgeois F, Lefebvre V (2005) Resistance quantitative trait loci originating from Solanum sparsipilum act independently on the sex ratio of Globodera pallida and together for developing a necrotic reaction. MPMI 18:1186–1194
Castelli L, Bryan G, Blok VC, Ramsay G, Phillips MS (2005) Investigation of resistance specificity amongst fifteen wild Solanum species to a range of Globodera pallida and G. rostochiensis populations. Nematology 7:689–699
CGN gene bank descriptions (n.d.) https://cgngenis.wur.nl/AccessionDetails.aspx? ID=muwqtoir&acnumber=CGN22342; https://cgngenis.wur.nl/AccessionDetails.aspx?acnumber=CGN17592)
Chavez R, Jackson MT, Schmiediche PE, Franco J (1988) The importance of wild potato species resistant to the potato cyst nematode, Globodera pallida, pathotypes Pa4 and Pa5, in potato breeding. I Resistance studies. Euphytica 37:9–14
Dalamu BV, Umamaheshwari R, Shrama R, Kaushik SK, Joseph TA, Singh BP, Gebhardt C (2012) Potato cyst nematode (PCN) resistance: genes, genotypes and markers – an update. SABRAO J Breed Genet 44:202–228
de Galarreta R, Carrasco A, Salazar A, Barrena I, Iturritxa E, Marquinez R, Legorburu FJ, Ritter E (1998) Wild Solanum species as resistance sources against different pathogens of potato. Potato Res 41:57–68
Dunnett J (1961) Inheritance of resistance to potato root eelworm in a breeding line stemming from Solanum multidissectum Hawkes. In: Report of the Scottish plant breeding station, pp 39–46
EPPO Reporting Service (2012) Situation of Globodera pallida in Finland in 2011
EPPO Reporting service (2013) First report of Globodera pallida in Denmark
EPPO/OEPP (2004) Diagnostic protocols for regulated pests, European and Mediterranean plant protection organization. OEPP/EPPO Bull 34:309–314
Evans K, Trudgill DL (1992) Pest aspects of potato production. Part 1. The nematode pests of potato. In: Harris P (ed) The potato crop, 2nd edn. Chapman and Hall, London, pp 438–475
Gebhardt C, Valkonen JP (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102
Kort J, Ross H, Stone AR, Rumpenhorst HJ (1977) An international scheme for identifying and classifying pathotypes of potato cyst-nematodes Globodera rostochiensis and G. pallida. Nematologica 23:333–339
Nicol JM, Turner SJ, Coyne DL, den Nijs L, Hockland S, Tahna Maafi Z (2011) Current nematode threats to world agriculture. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer, Berlin, pp 21–43
Nježić B, Stare BG, Širca S, Grujic N (2014) First report of the pale potato cyst nematode Globodera pallida from Bosnia and Herzegovina. Plant Dis 98:575–575
Przetakiewicz A, Milczarek D (2017) Evaluation of potato cultivars and breeding lines for resistance to Globodera rostochiensis and Globodera pallida. Plant Breed Seed Sci 76:3–8
Sattarzadeh A, Achenbach U, Lübeck J, Strahwald J, Tacke E, Hofferbert HR, Rothsteyn T, Gebhardt C (2006) Single nucleotide polymorphism (SNP) genotyping as basis for developing a PCR-based marker highly diagnostic for potato varieties with high resistance to Globodera pallida pathotype Pa2/3. Mol Breed 18:301–312
Širca S, Stare BG, Strajnar P, Urek G, Lautar IM (2012) First report of the pale potato cyst nematode Globodera pallida from Slovenia. Plant Dis 96:773–773
Smith IM, McNamara DG, Scott PR, Harris KM (1992) Quarantine pests for Europe. CAB Int & EPPO
Strachan SM, Armstrong MR, Kaur A, Wright KM, Lim TY, Baker K, Jones J, Bryan G, Blok V, Hein I (2019) Mapping the H2 resistance effective against Globodera pallida pathotype Pa1 in tetraploid potato. Theor Appl Genet 132(4):1283–1294
Uhrig U, Wenzel G (1981) Solanum gourlayi Hawkes as a source of resistance against the white potato cyst nematode Globodera pallida Stone. Zeitschrift fuer Pflanzenzuechtung 86:148–157
van der Voort JR, Kanyuka K, van der Vossen E, Bendahmane A, Mooijman P, Klein-Lankhorst R, Stiekema W, Baulcombe D, Bakker J (1999) Tight physical linkage of the nematode resistance gene Gpa2 and the virus resistance gene Rx on a single segment introgressed from the wild species Solanum tuberosum subsp. andigena CPC 1673 into cultivated potato. MPMI 12:197–206
van der Voort JR, Van der Vossen E, Bakker E, Overmars H, Van Zandvoort P, Hutten R, Klein Linkhorst R, Bakker J (2000) Two additive QTLs conferring broad-spectrum resistance in potato to Globodera pallida are localized on resistance gene clusters. Theor Appl Genet 101:1122–1130
Van Soest LJM, Rumpenhorst HJ, Huijsman CA (1983) Resistance to potato cyst-nematodes in tuber-bearing Solanum species and its geographical distribution. Euphytica 32:65–74
Funding
This work was partly supported by the project BH 4-3-00-6-02 of the Ministry of Agriculture and Rural Development.
Author information
Authors and Affiliations
Contributions
D.M. conceived and coordinated the project and co-wrote the paper. A.P.P. carried out phenotyping studies. B.F., B.T. and J.P. participated in the design of the studies and co-wrote the paper. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Statement of Human and Animal Right
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(XLSX 194 kb)
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Milczarek, D., Tatarowska, B., Plich, J. et al. Solanum gourlayi—a Source of Cyst Nematode Resistance in Potato Breeding. Potato Res. 63, 589–595 (2020). https://doi.org/10.1007/s11540-020-09459-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11540-020-09459-9