vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-24-21vavilov-4087Research ArticleИММУНИТЕТ РАСТЕНИЙ К БОЛЕЗНЯМPLANT IMMUNITYIn silico поиск R-генов у примитивных культурных видов картофеляIn silico search for and analysis of R gene variation in primitive cultivated potato speciesГуринаА. А.GurinaA. A.

Санкт-Петербург

St. Petersburg

a.gurina@vir.nw.ruГанчеваМ. С.GanchevaM. S.

Санкт-Петербург

St. Petersburg

АлпатьеваН. В.AlpatievaN. V.

Санкт-Петербург

St. Petersburg

РогозинаЕ. В.RogozinaE. V.

Санкт-Петербург

St. Petersburg

Федеральный исследовательский центр Всероссийский институт генетических ресурсов растений им. Н.И. Вавилова (ВИР)РоссияFederal Research Center the N.I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR)Russian FederationСанкт-Петербургский государственный университетРоссияSt. Petersburg State UniversityRussian Federation202411042024282175184Copyright © Гурина А.А., Ганчева М.С., Алпатьева Н.В., Рогозина Е.В., 20242024Гурина А.А., Ганчева М.С., Алпатьева Н.В., Рогозина Е.В.Gurina A.A., Gancheva M.S., Alpatieva N.V., Rogozina E.V.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4087

Ключевую роль в защите растений от патогенов играют рецепторы, кодируемые R-генами. Они являются генетической основой для селекции многих сельскохозяйственных культур, в том числе картофеля. Множество генов устойчивости у картофеля стало известно и было вовлечено в селекцию благодаря изучению широкого разнообразия диких сородичей картофеля. Использование примитивных культурных видов (ПКВ), относящихся к первичному генофонду картофеля, также перспективно. Как наиболее близкие к ранним доместицированным формам картофеля, ПКВ представляют особый интерес для исследования эволюции генов устойчивости. Целью настоящего исследования стали поиск и анализ R-генов у ПКВ картофеля, геномы которых с различным качеством сборки представлены в базе данных NCBI. Исследовано 27 образцов, относящихся к трем видам: Solanum phureja Juz. & Bukasov, S. stenotomum Juz. & Bukasov и S. goniocalyx Juz. & Bukasov. Проведен in silico поиск последовательностей, гомологичных 26 R-генам, идентифицированных у различных по филогенетической отдаленности от ПКВ картофеля видов: паслёна (S. americanum Mill.), североамериканских (S. bulbocasta num Dunal., S. demissum Lindl.) и южноамериканских (S. venturii Hawkes & Hjert., S. berthaultii Hawkes) диких видов, а также видов культурного картофеля (S. tuberosum L., S. andigenum Juz. & Bukasov). Гомологи кодирующих последовательностей всех исследованных генов обнаружены у ПКВ картофеля с относительно высокой степенью сходства (85–100 %). Впервые у примитивных культурных видов картофеля найдены гомологи генов R3b, Rpi-amr3 и Rpi- ber1. Для 15 R-генов проведен анализ полиморфизма нуклеотидных и аминокислотных последовательностей. Приведены отличия в частоте замен у ПКВ картофеля при анализе R-генов, референсные последовательности которых идентифицированы у разных видов. Для всех изученных NBS-LRR генов доля замещенных аминокислот в LRR-домене превосходит этот показатель для NBS-домена. Показана потенциальная перспективность использования ПКВ картофеля в качестве источников устойчивости к вертициллёзному увяданию. 

Pathogen recognition receptors encoded by R genes play a key role in plant protection. Nowadays, R genes are a basis for breeding many crops, including potato. Many potato R genes have been discovered and found suitable for breeding thanks to the studies of a wide variety of wild potato species. The use of primitive cultivated potato species (PCPS) as representatives of the primary gene pool can also be promising in this respect. PCPS are the closest to the early domesticated forms of potato; therefore, their investigation could help understand the evolution of R genes. The present study was aimed at identifying and analyzing R genes in PCPS listed in the open database of NCBI and Solomics DB. In total, the study involved 27 accessions belonging to three species: Solanum phureja Juz. & Bukasov, S. stenotomum Juz. & Bukasov and S. goniocalyx Juz. & Bukasov Materials for the analysis were the sequencing data for the said three species from the PRJNA394943 and PRJCA006011 projects. An in silico search was carried out for sequences homologous to 26 R genes identified in potato species differing in phylogenetic distance from PCPS, namely nightshade (S. americanum), North- (S. bulbocastanum, S. demissum) and South-American (S. venturii, S. berthaultii) wild potato species, as well as the cultivated potato species S. tuberosum and S. andigenum. Homologs of all investigated protein-coding sequences were discovered in PCPS with a relatively high degree of similarity (85–100 %). Homologs of the Rpi-R3b, Rpi-amr3 and Rpi-ber1 genes have been identified in PCPS for the first time. An analysis of polymorphism of nucleotide and amino acid sequences has been carried out for 15 R genes. The differences in frequencies of substitutions in PCPS have been demonstrated by analysis of R genes, the reference sequences of which have been identified in different species. For all the studied NBS-LRR genes, the proportion of substituted amino acids in the LRR domain exceeds this figure for the NBS domain. The potential prospects of using PCPS as sources of resistance to Verticillium wilt have been shown.

R-геныNBS-LRRполиморфизмSolanum phurejaS. stenotomumR genesNBS-LRRpolymorphismSolanum phurejaS. stenotomum.The work was supported by the Russian Science Foundation Project No. 22-26-00111 “Genes of potato resistance to late blight in the context of the evolution of cultivated and wild tuber-bearing species of Solanum L.”ReferencesArmstrong 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(2):540-549. DOI 10.1111/pbi.12997Armstrong 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(2):540-549. DOI 10.1111/pbi.12997Ballvora A., Ercolano M.R., Weiß J., Meksem K., Bormann C.A., Oberhagemann P., Salamini F., Gebhardt C. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 2002;30(3):361-371. DOI 10.1046/J.1365-313X.2001.01292.XBallvora A., Ercolano M.R., Weiß J., Meksem K., Bormann C.A., Oberhagemann P., Salamini F., Gebhardt C. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 2002;30(3):361-371. DOI 10.1046/J.1365-313X.2001.01292.XBendahmane A., Kanyuka K., Baulcombe D.C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell. 1999;11(5):781-791. DOI 10.1105/tpc.11.5.781Bendahmane A., Kanyuka K., Baulcombe D.C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell. 1999;11(5):781-791. DOI 10.1105/tpc.11.5.781Bolger A.M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-2120. DOI 10.1093/bioinformatics/btu170Bolger A.M., Lohse M., Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-2120. DOI 10.1093/bioinformatics/btu170Bradeen J.M., Kole C. (Eds.). Genetics, Genomics and Breeding of Potato. CRC Press, 2011. DOI 10.1201/b10881Bradeen J.M., Kole C. (Eds.). Genetics, Genomics and Breeding of Potato. CRC Press, 2011. DOI 10.1201/b10881Bradshaw J.E. Potato Breeding: Theory and Practice. Cham (Switzerland): Springer, 2021. DOI 10.1007/978-3-030-64414-7Bradshaw J.E. Potato Breeding: Theory and Practice. Cham (Switzerland): Springer, 2021. DOI 10.1007/978-3-030-64414-7Deng Y., Ning Y., Yang D.-L., Zhai K., Wang G.-L., He Z. Molecular basis of disease resistance and perspectives on breeding strategies for resistance improvement in crops. Mol. Plant. 2020;13(10):14021419. DOI 10.1016/j.molp.2020.09.018Deng Y., Ning Y., Yang D.-L., Zhai K., Wang G.-L., He Z. Molecular basis of disease resistance and perspectives on breeding strategies for resistance improvement in crops. Mol. Plant. 2020;13(10):14021419. DOI 10.1016/j.molp.2020.09.018Fang Y., Jiang J., Hou X., Guo J., Li X., Zhao D., Xie X. Plant proteincoding gene families: Their origin and evolution. Front. Plant Sci. 2022;13:995746. DOI 10.3389/fpls.2022.995746Fang Y., Jiang J., Hou X., Guo J., Li X., Zhao D., Xie X. Plant proteincoding gene families: Their origin and evolution. Front. Plant Sci. 2022;13:995746. DOI 10.3389/fpls.2022.995746FAO. The Second Report on the World’s Plant Genetic Resources for Food and Agriculture. Rome, 2010FAO. The Second Report on the World’s Plant Genetic Resources for Food and Agriculture. Rome, 2010FAO. Land Use Statistics and Indicators. Global, Regional and Country Trends, 2000–2020. No. 48. Rome: FAOSTAT analytical Brief, 2020FAO. Land Use Statistics and Indicators. Global, Regional and Country Trends, 2000–2020. No. 48. Rome: FAOSTAT analytical Brief, 2020Foster S.J., Park T.H., Pel M., Brigneti G., Sliwka J., Jagger L., van der Vossen E., Jones J.D.G. Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol. Plant Microbe Interact. 2009;22(5):589-600. DOI 10.1094/MPMI-22-5-0589Foster S.J., Park T.H., Pel M., Brigneti G., Sliwka J., Jagger L., van der Vossen E., Jones J.D.G. Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii, confers resistance to potato late blight. Mol. Plant Microbe Interact. 2009;22(5):589-600. DOI 10.1094/MPMI-22-5-0589Gurina A.A., Alpatieva N.V., Chalaya N.A., 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(12):1473-1484. DOI 10.1134/S1022795422120043Gurina A.A., Alpatieva N.V., Chalaya N.A., 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(12):1473-1484. DOI 10.1134/S1022795422120043Hardigan 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., Veilleux R.E., Buell C.R. Genome diversity of tuberbearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proc. Natl. Acad. Sci. USA. 2017;114(46):E9999-E10008. DOI 10.1073/pnas.1714380114Hardigan 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., Veilleux R.E., Buell C.R. Genome diversity of tuberbearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proc. Natl. Acad. Sci. USA. 2017;114(46):E9999-E10008. DOI 10.1073/pnas.1714380114Hawkes J.G. The Potato: Evolution, Biodiversity and Genetic Resources. Belhaven Press, 1990Hawkes J.G. The Potato: Evolution, Biodiversity and Genetic Resources. Belhaven Press, 1990Huang S., van der Vossen E.A.G., Kuang H., Vleeshouwers V.G.A.A., Zhang N., Borm T.J.A., van Eck H.J., Baker B., Jacobsen E., Visser R.G.F. Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 2005;42(2):251-261. DOI 10.1111/J.1365-313X.2005.02365.XHuang S., van der Vossen E.A.G., Kuang H., Vleeshouwers V.G.A.A., Zhang N., Borm T.J.A., van Eck H.J., Baker B., Jacobsen E., Visser R.G.F. Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 2005;42(2):251-261. DOI 10.1111/J.1365-313X.2005.02365.XHuang J., Wu X., Sun K., Gao Z. Structure and function analysis of a CC-NBS-LRR protein AT1G12290. Biochem. Biophys. Res. Commun. 2021;1(534):206-211. DOI 10.1016/j.bbrc.2020.11.111Huang J., Wu X., Sun K., Gao Z. Structure and function analysis of a CC-NBS-LRR protein AT1G12290. Biochem. Biophys. Res. Commun. 2021;1(534):206-211. DOI 10.1016/j.bbrc.2020.11.111Jones J., Foster S.J., Chu Z., Park T.H., Pel M.A. Late Blight Resistance Genes and Methods. US Patent WO 2009013468 A3.2013Jones J., Foster S.J., Chu Z., Park T.H., Pel M.A. Late Blight Resistance Genes and Methods. US Patent WO 2009013468 A3.2013Jupe F., Pritchard L., Etherington G.J., MacKenzie K., Cock P.J.A., Wright F., Sharma S.K., Bolser D., Bryan G.J., Jones J.D.G., Hein I. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics. 2012;13:75. DOI 10.1186/14712164-13-75Jupe F., Pritchard L., Etherington G.J., MacKenzie K., Cock P.J.A., Wright F., Sharma S.K., Bolser D., Bryan G.J., Jones J.D.G., Hein I. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics. 2012;13:75. DOI 10.1186/14712164-13-75Koboldt D.C., Chen K., Wylie T., Larson D.E., McLellan M.D., Mardis E.R., Weinstock G.M., Wilson R.K., Ding L. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics. 2009;25(17):2283-2285. DOI 10.1093/Bioinformatics/BTP373Koboldt D.C., Chen K., Wylie T., Larson D.E., McLellan M.D., Mardis E.R., Weinstock G.M., Wilson R.K., Ding L. VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics. 2009;25(17):2283-2285. DOI 10.1093/Bioinformatics/BTP373Kourelis J., van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell. 2018;30(2):285-299. DOI 10.1105/tpc.17.00579Kourelis J., van der Hoorn R.A.L. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell. 2018;30(2):285-299. DOI 10.1105/tpc.17.00579Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35(6):1547-1549. DOI 10.1093/MOLBEV/MSY096Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35(6):1547-1549. DOI 10.1093/MOLBEV/MSY096Ladunga I. Finding similar nucleotide sequences using Network BLAST searches. Curr. Protoc. Bioinformatics. 2017;58(1):3.3.1-3.3.25. DOI 10.1002/CPBI.29Ladunga I. Finding similar nucleotide sequences using Network BLAST searches. Curr. Protoc. Bioinformatics. 2017;58(1):3.3.1-3.3.25. DOI 10.1002/CPBI.29Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9(4):357-359. DOI 10.1038/nmeth.1923Langmead B., Salzberg S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods. 2012;9(4):357-359. DOI 10.1038/nmeth.1923Li G., Huang S., Guo X., Li Y., Yang Y., Guo Z., Kuang H., Rietman H., Bergervoet M., Vleeshouwers V.G.G.A., van der Vossen E.A.G., Qu D., Visser R.G.F., Jacobsen E., Vossen J.H. Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. 2011;24(10): 1132-1142. DOI 10.1094/MPMI-11-10-0276Li G., Huang S., Guo X., Li Y., Yang Y., Guo Z., Kuang H., Rietman H., Bergervoet M., Vleeshouwers V.G.G.A., van der Vossen E.A.G., Qu D., Visser R.G.F., Jacobsen E., Vossen J.H. Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. 2011;24(10): 1132-1142. DOI 10.1094/MPMI-11-10-0276Li Y., Colleoni C., Zhang J., Liang Q., Hu Y., Ruess H., Simon R., Liu Y., Liu H., Yu G., Schmitt E., Ponitzki C., Liu G., Huang H., Zhan F., Chen L., Huang Y., Spooner D., Huang B. Genomic analyses yield markers for identifying agronomically important genes in potato. Mol. Plant. 2018;11(3):473-484. DOI 10.1016/j.molp.2018.01.009Li Y., Colleoni C., Zhang J., Liang Q., Hu Y., Ruess H., Simon R., Liu Y., Liu H., Yu G., Schmitt E., Ponitzki C., Liu G., Huang H., Zhan F., Chen L., Huang Y., Spooner D., Huang B. Genomic analyses yield markers for identifying agronomically important genes in potato. Mol. Plant. 2018;11(3):473-484. DOI 10.1016/j.molp.2018.01.009Liu Z. Diversity of NB-LRR genes in the genome of Solanum stenotomum subsp. goniocalyx. Thesis. Montreal: McGill University, 2020Liu Z. Diversity of NB-LRR genes in the genome of Solanum stenotomum subsp. goniocalyx. Thesis. Montreal: McGill University, 2020Lokossou 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., van der Vossen E.A.G. 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(6):630-641. DOI 10.1094/MPMI-22-6-0630Lokossou 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., van der Vossen E.A.G. 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(6):630-641. DOI 10.1094/MPMI-22-6-0630Lokossou A.A., Rietman H., Wang M.Q., Krenek P., Schoot H., Henken B., Hoekstra R., Vleeshouwers V.G.A.A., van der Vossen E.A.G., Visser R.G.F., Jacobsen E., Vosman B. Diversity, distribution, and evolution of Solanum bulbocastanum late blight resistance genes. Mol. Plant Microbe Interact. 2010;23(9):1206-1216. DOI 10.1094/MPMI-23-9-1206Lokossou A.A., Rietman H., Wang M.Q., Krenek P., Schoot H., Henken B., Hoekstra R., Vleeshouwers V.G.A.A., van der Vossen E.A.G., Visser R.G.F., Jacobsen E., Vosman B. Diversity, distribution, and evolution of Solanum bulbocastanum late blight resistance genes. Mol. Plant Microbe Interact. 2010;23(9):1206-1216. DOI 10.1094/MPMI-23-9-1206Lozano R., Ponce O., Ramirez M., Mostajo N., Orjeda G. Genomewide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS One. 2012;7(4):e34775. DOI 10.1371/journal.pone.0034775Lozano R., Ponce O., Ramirez M., Mostajo N., Orjeda G. Genomewide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS One. 2012;7(4):e34775. DOI 10.1371/journal.pone.0034775Monino-Lopez D., Nijenhuis M., Kodde L., Kamoun S., Salehian H., Schentsnyi K., Stam R., Lokossou A., Abd-El-Haliem A., Visser R.G.F., Vossen J.H. Allelic variants of the NLR protein Rpi-chc1 differentially recognize members of the Phytophthora infestans PexRD12/31 effector superfamily through the leucine-rich repeat domain. Plant J. 2021;107(1):182-197. DOI 10.1111/tpj.15284Monino-Lopez D., Nijenhuis M., Kodde L., Kamoun S., Salehian H., Schentsnyi K., Stam R., Lokossou A., Abd-El-Haliem A., Visser R.G.F., Vossen J.H. Allelic variants of the NLR protein Rpi-chc1 differentially recognize members of the Phytophthora infestans PexRD12/31 effector superfamily through the leucine-rich repeat domain. Plant J. 2021;107(1):182-197. DOI 10.1111/tpj.15284Muratova (Fadina) 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(1):73-83. DOI 10.30901/2227-8834-2020-1-73-83Muratova (Fadina) 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(1):73-83. DOI 10.30901/2227-8834-2020-1-73-83Oosumi T., Rockhold D.R., Maccree M.M., Deahl K.L., McCue K.F., Belknap W.R. Gene Rpi-bt1 from Solanum bulbocastanum confers resistance to late blight in transgenic potatoes. Am. J. Pot. Res. 2009; 86:456-465. DOI 10.1007/s12230-009-9100-4Oosumi T., Rockhold D.R., Maccree M.M., Deahl K.L., McCue K.F., Belknap W.R. Gene Rpi-bt1 from Solanum bulbocastanum confers resistance to late blight in transgenic potatoes. Am. J. Pot. Res. 2009; 86:456-465. DOI 10.1007/s12230-009-9100-4Paal J., Henselewski H., Muth J., Meksem K., Menéndez C.M., Salamini F., Ballvora A., Gebhardt C. Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J. 2004;38(2):285-97. DOI 10.1111/j.1365-313X.2004.02047.xPaal J., Henselewski H., Muth J., Meksem K., Menéndez C.M., Salamini F., Ballvora A., Gebhardt C. Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J. 2004;38(2):285-97. DOI 10.1111/j.1365-313X.2004.02047.xPark T.H., Gros J., Sikkema A., Vleeshouwers V.G., Muskens M., Allefs S., Jacobsen E., Visser R.G., van der Vossen E.A. The late blight resistance locus Rpi-bib3 from Solanum bulbocastanum belongs to a major late blight R gene cluster on chromosome 4 of potato. Mol. Plant Microbe Interact. 2005;18(7):722-729. DOI 10.1094/MPMI-18-0722Park T.H., Gros J., Sikkema A., Vleeshouwers V.G., Muskens M., Allefs S., Jacobsen E., Visser R.G., van der Vossen E.A. The late blight resistance locus Rpi-bib3 from Solanum bulbocastanum belongs to a major late blight R gene cluster on chromosome 4 of potato. Mol. Plant Microbe Interact. 2005;18(7):722-729. DOI 10.1094/MPMI-18-0722Paysan-Lafosse T., Blum M., Chuguransky S., Grego T., Pinto B.L., Salazar G.A., Bileschi M.L., … Sillitoe I., Thanki N., Thomas P.D., Tosatto S.C.E., Wu C.H., Bateman A. InterPro in 2022. Nucleic Acids Res. 2023;51(D1):D418-D427. DOI 10.1093/NAR/GKAC993Paysan-Lafosse T., Blum M., Chuguransky S., Grego T., Pinto B.L., Salazar G.A., Bileschi M.L., … Sillitoe I., Thanki N., Thomas P.D., Tosatto S.C.E., Wu C.H., Bateman A. InterPro in 2022. Nucleic Acids Res. 2023;51(D1):D418-D427. DOI 10.1093/NAR/GKAC993Potato Genome Sequencing Consortium; Xu X., Pan S., Cheng S., Zhang B., Mu D., Ni P., Zhang G., Yang S., ... Kloosterman B., van Eck H., Datema E., Hekkert Bt., Goverse A., van Ham R.C., Visser R.G. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475(7355):189-195. DOI 10.1038/nature10158Potato Genome Sequencing Consortium; Xu X., Pan S., Cheng S., Zhang B., Mu D., Ni P., Zhang G., Yang S., ... Kloosterman B., van Eck H., Datema E., Hekkert Bt., Goverse A., van Ham R.C., Visser R.G. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475(7355):189-195. DOI 10.1038/nature10158Prakash 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(1):11392. DOI 10.1038/s41598-020-67848-zPrakash 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(1):11392. DOI 10.1038/s41598-020-67848-zQuinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841-842. DOI 10.1093/bioinformatics/btq033Quinlan A.R., Hall I.M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841-842. DOI 10.1093/bioinformatics/btq033Rairdan G.J., Collier S.M., Sacco M.A., Baldwin T.T., Boettrich T., Moffett P. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell. 2008;20(3):739-751. DOI 10.1105/tpc.107.056036Rairdan G.J., Collier S.M., Sacco M.A., Baldwin T.T., Boettrich T., Moffett P. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell. 2008;20(3):739-751. DOI 10.1105/tpc.107.056036Rogozina E.V., Khavkin E.E. Interspecific potato hybrids as donors of durable resistance to pathogens. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2017;21(1):30-41. DOI 10.18699/VJ17.221 (in Russian)Rogozina E.V., Khavkin E.E. Interspecific potato hybrids as donors of durable resistance to pathogens. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2017;21(1):30-41. DOI 10.18699/VJ17.221 (in Russian)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(2):273. DOI 10.3390/plants12020273Rogozina 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(2):273. DOI 10.3390/plants12020273Sliwka J., Jakuczun H., Chmielarz M., Hara-Skrzypiec A., Tomczyńska I., Kilian A., Zimnoch-Guzowska E. A resistance gene against potato late blight originating from Solanum × michoacanum maps to potato chromosome VII. Theor. Appl. Genet. 2012;124(2):397-406. DOI 10.1007/s00122-011-1715-4Sliwka J., Jakuczun H., Chmielarz M., Hara-Skrzypiec A., Tomczyńska I., Kilian A., Zimnoch-Guzowska E. A resistance gene against potato late blight originating from Solanum × michoacanum maps to potato chromosome VII. Theor. Appl. Genet. 2012;124(2):397-406. DOI 10.1007/s00122-011-1715-4Slootweg E., Koropacka K., Roosien J., Dees R., Overmars H., Lankhorst R.K., van Schaik C., Pomp R., Bouwman L., Helder J., Schots A., Bakker J., Smant G., Goverse A. Sequence exchange between homologous NB-LRR genes converts virus resistance into nematode resistance, and vice versa. Plant Physiol. 2017;175(1): 498-510. DOI 10.1104/pp.17.00485Slootweg E., Koropacka K., Roosien J., Dees R., Overmars H., Lankhorst R.K., van Schaik C., Pomp R., Bouwman L., Helder J., Schots A., Bakker J., Smant G., Goverse A. Sequence exchange between homologous NB-LRR genes converts virus resistance into nematode resistance, and vice versa. Plant Physiol. 2017;175(1): 498-510. DOI 10.1104/pp.17.00485Song Y., Zhang Z., Seidl M.F., Majer A., Jakse J., Javornik B., Thomma B.P.H.J. Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. 2017;18(2):195-209. DOI 10.1111/MPP.12390Song Y., Zhang Z., Seidl M.F., Majer A., Jakse J., Javornik B., Thomma B.P.H.J. Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. 2017;18(2):195-209. DOI 10.1111/MPP.12390Spooner 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. DOI 10.1007/s12229-014-9146-ySpooner 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. DOI 10.1007/s12229-014-9146-yTang D., Jia Y., Zhang J., Li H., Cheng L., Wang P., Bao Z., Liu Z., Feng S., Zhu X., Li D., Zhu G., Wang H., Zhou Y., Zhou Y., Bryan G.J., Buell C.R., Zhang C., Huang S. Genome evolution and diversity of wild and cultivated potatoes. Nature. 2022;606(7914): 535-541. DOI 10.1038/s41586-022-04822-xTang D., Jia Y., Zhang J., Li H., Cheng L., Wang P., Bao Z., Liu Z., Feng S., Zhu X., Li D., Zhu G., Wang H., Zhou Y., Zhou Y., Bryan G.J., Buell C.R., Zhang C., Huang S. Genome evolution and diversity of wild and cultivated potatoes. Nature. 2022;606(7914): 535-541. DOI 10.1038/s41586-022-04822-xUsadel B. Solanaceae pangenomes are coming of graphical age to bring heritability back. aBIOTECH. 2022;3(4):233-236. DOI 10.1007/s42994-022-00087-0Usadel B. Solanaceae pangenomes are coming of graphical age to bring heritability back. aBIOTECH. 2022;3(4):233-236. DOI 10.1007/s42994-022-00087-0van der Vossen E.A., van der Voort J.N., Kanyuka K., Bendahmane A., Sandbrink H., Baulcombe D.C., Bakker J., Stiekema W.J., KleinLankhorst R.M. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 2000;23(5):567-576. DOI 10.1046/j.1365-313x.2000.00814.x. PMID: 10972883van der Vossen E.A., van der Voort J.N., Kanyuka K., Bendahmane A., Sandbrink H., Baulcombe D.C., Bakker J., Stiekema W.J., KleinLankhorst R.M. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 2000;23(5):567-576. DOI 10.1046/j.1365-313x.2000.00814.x. PMID: 10972883van der Vossen E., Sikkema A., Hekkert Bt., Gros J., Stevens P., Muskens M., Wouters D., Pereira A., Stiekema W., Allefs S. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 2003;36(6):867-882. DOI 10.1046/j.1365-313x.2003.01934.xvan der Vossen E., Sikkema A., Hekkert Bt., Gros J., Stevens P., Muskens M., Wouters D., Pereira A., Stiekema W., Allefs S. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 2003;36(6):867-882. DOI 10.1046/j.1365-313x.2003.01934.xvan der Vossen E.A.G., 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(2):208-222. DOI 10.1111/j.1365-313X.2005.02527.xvan der Vossen E.A.G., 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(2):208-222. DOI 10.1111/j.1365-313X.2005.02527.xVleeshouwers V.G.A.A., Rietman H., Krenek P., Champouret N., Young C., Oh S.K., Wang M., Bouwmeester K., Vosman B., Visser R.G.F., Jacobsen E., Govers F., Kamoun S., van der Vossen E.A.G. Effector genomics accelerates discovery and functional profiling of potato disease resistance and phytophthora infestans avi rulence genes. PLoS One. 2008;3(8):2875. DOI 10.1371/journal.pone.0002875Vleeshouwers V.G.A.A., Rietman H., Krenek P., Champouret N., Young C., Oh S.K., Wang M., Bouwmeester K., Vosman B., Visser R.G.F., Jacobsen E., Govers F., Kamoun S., van der Vossen E.A.G. Effector genomics accelerates discovery and functional profiling of potato disease resistance and phytophthora infestans avi rulence genes. PLoS One. 2008;3(8):2875. DOI 10.1371/journal.pone.0002875Vossen 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(9):1785-1796. DOI 10.1007/S00122-016-2740-0Vossen 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(9):1785-1796. DOI 10.1007/S00122-016-2740-0Wingett S.W., Andrews S. FastQ Screen: A tool for multi-genome mapping and quality control. F1000Res. 2018;7:1338. DOI 10.12688/f1000research.15931.2Wingett S.W., Andrews S. FastQ Screen: A tool for multi-genome mapping and quality control. F1000Res. 2018;7:1338. DOI 10.12688/f1000research.15931.2Witek K., Lin X., Karki H.S., Jupe F., Witek A.I., Steuernagel B., Stam R., van Oosterhout C., Fairhead S., Heal R., Cocker J.M., Bhanvadia S., Barrett W., Wu C.H., Adachi H., Song T., Kamoun S., Vleeshouwers V.G.A.A., Tomlinson L., Wulff B.B.H., Jones J.D.G. A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat. Plants. 2021;7(2):198-208. DOI 10.1038/S41477-021-00854-9Witek K., Lin X., Karki H.S., Jupe F., Witek A.I., Steuernagel B., Stam R., van Oosterhout C., Fairhead S., Heal R., Cocker J.M., Bhanvadia S., Barrett W., Wu C.H., Adachi H., Song T., Kamoun S., Vleeshouwers V.G.A.A., Tomlinson L., Wulff B.B.H., Jones J.D.G. A complex resistance locus in Solanum americanum recognizes a conserved Phytophthora effector. Nat. Plants. 2021;7(2):198-208. DOI 10.1038/S41477-021-00854-9Zhang R., Zheng F., Wei S., Zhang S., Li G., Cao P., Zhao S. Evolution of disease defense genes and their regulators in plants. Int. J. Mol. Sci. 2019;20(2):335. DOI 10.3390/ijms20020335Zhang R., Zheng F., Wei S., Zhang S., Li G., Cao P., Zhao S. Evolution of disease defense genes and their regulators in plants. Int. J. Mol. Sci. 2019;20(2):335. DOI 10.3390/ijms20020335

The authors declare that there are no conflicts of interest present.