Abstract
Bacterial wilt caused by Ralstonia solanacearum is the main bacterial disease in potato. Solanum commersonii Dun. (cmm; 2n = 2x = 24, 1 EBN) is a native species to southern Brazil, Uruguay and Argentina with desirable traits for introgressive hybridisation breeding into cultivated potato such as resistance to R. solanacearum. In Uruguay, successful crosses between cmm and Solanum tuberosum Group Tuberosum (tbr; 2n = 4x = 48, 4 EBN) have been carried out with this objective, resulting in backcross 1, 2 and 3 progenies. The aim of this study was to characterise one backcross 3 progeny (BC3) using cytogenetic, genetic, morphological and agronomic descriptors. Resistance to R. solanacearum showed transgressive segregation and an association with plant architecture. Fifty-two percent of individuals had chromosome numbers close to cultivated potato with no evidence of preferential loss of cmm chromosomes. All BC3 individuals showed male sterility, probably due to nuclear-cytoplasmic interactions. Although there was wide segregation in morphological traits, most individuals resembled the recurrent tbr parents. A few more backcrosses combined with screening for bacterial wilt resistance may be necessary to allow for further recombination and removal of undesirable traits from cmm. The presence of BC3 individuals with chromosome numbers close to 2n = 48, combining morphological traits from tbr with good levels of resistance, suggests the occurrence of introgression events. This points to S. commersonii as one of the most promising genetic resources for potato breeding from the Southern Atlantic region.
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References
Baichoo Z, Jaufeerally-Fakim Y (2017) Ralstonia solanacearum upregulates marker genes of salicylic acid and ethylene signaling pathways but not those of the jasmonic acid pathway in leaflets of Solanum lines during early stage of infection. Eur J Plant Pathol 147:615–625. https://doi.org/10.1007/s10658-016-1030-7
Barone A, Sebastiano A, Carputo D, Della Rocca F, Frusciante L (2001) Molecular marker-assisted introgression of the wild Solanum commersonii genome into the cultivated S. tuberosum gene pool. Theor App Genet 102:902–907. https://doi.org/10.1007/s001220000498
Bethke P, Halterman DA, Jansky S (2017) Are we getting better at using wild potato species in light of new tools? Crop Sci 57:1241–1258. https://doi.org/10.2135/cropsci2016.10.0889
Birch P, Bryan G, Fenton B, Gilory E (2012) Crops that feed the world: 8: Potato are the trends of increased global production sustainable? Food Sec 4(4):477–508. https://doi.org/10.1007/s12571-012-0220-1
Bradshaw JE (2009) A genetic perspective on yield plateau in potato. Indian Potato Assoc 36(3-4):79–94
Bradshaw J, Bryan GJ, Ramsay G (2006) Genetic resources (including wild and cultivated Solanum species) and progress in their utilization in potato breeding. Potato Res 49:49–65. https://doi.org/10.1007/s11540-006-9002-5
Carputo D (1999) Post-zygotic gametic selection due to endosperm balance number explains unusual chromosome number of 3x x 2x progeny in Solanum. Sex Plant Reprod 12:27–31. https://doi.org/10.1007/s004970050168
Carputo D, Barone A (2005) Ploidy level manipulations in potato through sexual hybridisation. Ann Appl Biol 146:71–79
Carputo D, Barone A, Cardi T, Sebastiano A, Frusciante L, Peloquin S (1997) Endosperm balance number manipulation for direct in vivo germplasm introgression to potato from a sexually isolated relative (Solanum commersonii Dun.). Proc Natl Acad Sci U S A 94(22):12013–12017
Carputo D, Frusciante L, Monti L, Parisi M, Barone A (2002) Tuber quality and soft rot resistance of hybrids between Solanum tuberosum and the incongruent wild relative S. commersonii. Am J Potato Res 79:345–352. https://doi.org/10.1007/BF02870172
Carputo D, Parisi M, Consiglio F, Iovene M, Caruso G, Monti L, Frusciante L (2003) Aneuploid hybrids from 5x − 4x crosses in potato: chromosome number, fertility, morphology and yield. Am J Potato Res 80:93–101. https://doi.org/10.1007/BF02870208
Carputo D, Aversano R, Barone A, Matteo A, Iorizzo M, Sigillo L, Zoina A, Frusciante L (2009) Resistance to Ralstonia solanacearum of sexual hybrids between Solanum commersonii and S. tuberosum. Am J Potato Res 86:196–202. https://doi.org/10.1007/s12230-009-9072-4
Carputo D, Alioto D, Aversano R, Garramone R, Miraglia V, Villano C, Frusciante L (2013) Genetic diversity among potato species as revealed by phenotypic resistances and SSR markers. Plant Genet Resour 1–9. https://doi.org/10.1017/S1479262112000500
Caruso I, Castaldi L, Caruso G, Frusciante L, Carputo D (2008) Breeding potential of Solanum tuberosum–S. commersonii pentaploid hybrids: fertility studies and tuber evaluation. Euphytica 164:357–363
Champoiseau PG, Jones JB, Allen C (2009) Ralstonia solanacearum race 3 biovar 2 causes tropical losses and temperate anxieties [Online]. American Phytopathological Society, Madison. https://doi.org/10.1094/PHP-2009-0313-01-RV
Charkowski A, Sharma K, Parker ML, Secor GA, Elphinstone J (2020) Bacterial diseases of potato. In: Campos H, Ortiz O (eds) Potato crop. Its Agric. Nutr. Soc. Contrib. to Humankind. Springer, pp 351–388
Chen Y-KH, Palta JP, Bamberg JB (1999) Freezing tolerance and tuber production in selfed and backcross progenies derived from somatic hybrids between Solanum tuberosum L. and S. commersonii Dun. Theor Appl Genet 99:100–107. https://doi.org/10.1007/s001220051213
Chen L, Guo X, Xie C, He L, Cai X, Tian L, Song B, Liu J (2013) Nuclear and cytoplasmic genome componets of Solanum tuberosum + S. chacoense somatic hybrids and three SSR alleles related to bacterial wilt resistance. Theor Appl Genet 126:1861–1872. https://doi.org/10.1007/s00122-013-2098-5
Clulow S, Wilkinson M, Waugh R, Baird E, De Maine M, Powell W (1991) Cytological and molecular observations on Solanum phureja –induced dihaploid potatoes. Theor Appl Genet 82:545–551. https://doi.org/10.1007/BF00226789
Correll D (1962) The potato and its wild relatives. Texas Research foundation. Renner
Da Silva G, Pereira A, Castro C, Souza V, Carvalho F (2009) Repetibilidade e importancia de caracteres para avalidacao de colecao ativa de germoplasma de batata. Hortic Bras 27(3):290–293
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry 19:11–15
Elphinstone JG (2005) The current bacterial wilt situation: a global overview. In: Allen C, Prior P, Hayward A (eds) Bacterial wilt disease and the Ralstonia solanacearum species complex. APS Press, St. Paul, pp 9–28
Fegan M, Prior P (2005) How Complex is the “Ralstonia solanacearum Species Complex”. In: Allen C, Prior P, Hayward A (eds) Bacterial wilt disease and the Ralstonia solanacearum species complex. APS Press, St. Paul, pp 449–462
Fernández E, Gutarra L, Kreuze J (2015) Evaluación del gen que codifica la enzima βHPMEH para la inhibición de la marchitez bacteriana causada por Ralstonia solanacearum. Rev Peru Biol 22(2):193–198. https://doi.org/10.15381/rpb.v22i2.11353
Ferreira V (2019) Estudio de la interacción entre Ralstonia solanacearum y Solanum commersonii. Doctorate Dissertation, Universidad de la República, Uruguay
Ferreira V, Pianzola M, Vilaró F, Glaván G, Rodríguez M, Orellano E, Valls M, Siri M (2017) Interspecific potato breeding lines display differential colonization patterns and induced defense responses after Ralstonia solanacearum infection. Front Plant Sci 8:1424. https://doi.org/10.3389/fpls.2017.01424
Gaiero P, Mazzella C, Vilaró F, Speranza P, de Jong H (2017) Pairing analysis and in situ hybridisation reveal autopolyploid-like behaviour in Solanum commersonii x S. tuberosum (potato) interspecific hybrids. Euphytica 213:137–142. https://doi.org/10.1007/s10681-017-1922-4
Galván G, Fraguas F, Quirici L, Santos L, Silvera E, Siri M, Villanueva P, Rauduviniche L, González M, Torres D, Castillo A, Dalla Rizza M, Vilaró F, Gepp V, Ferreira F, Pianzola (2006) Solanum commersonii: una especie con gran potencial para el mejoramiento genético de para por resistencia a Ralstonia solanacearum. Red de Recursos Genéticos del Cono Sur II 87–101
Gao G, Qu D, Lian Y, Jin L, Feng L (2000) Identification molecular markers linked with resistance to bacterial wilt (Ralstonia solanacearum) in diploid potato. Acta Horticulturae Sinica 27:37–41
Ghislain M, Núñez J, Del Rosario HM, Pignataro J, Guzman F, Bonierbale M, Spooner DM (2009) Robust and highly informative microsatellite-based genetic identity kit for potato. Mol Breed 23:377–388. https://doi.org/10.1007/s11032-008-9240-0
González M (2010) Análisis de la resistencia a Ralstonia solanacearum en una progenie segregante de Solanum commersonii. MSc Dissertation, Universidad de la República, Uruguay
González M, Galván G, Siri MI, Borges A, Vilaró F (2013) Resistencia a la marchitez bacteriana de la papa en Solanum commersonii. Agrociencia Uruguay 17:45–54. https://doi.org/10.2477/vol17iss1pp45-54
Grun P, Aubertin M (1965) Evolutionary pathways of cytoplasmic male sterility in Solanum. Genetics 51:399–409
Gutarra L, Kreuze J, Lindqvist-Kreuze H, De Mendiburu F (2015) Variation of resistance to different strains of Ralstonia solanacearum in highland tropics adapted potato genotypes. Am J Potato Res 92:258–265
Hawkes J (1994) Origin of the cultivated potato and species relationship. In: Bradshaw JE, Mackay GR (eds) Potato genetics. Cambridge University Press, Wallingford, pp 3–42
Haynes FL (1980) Progress and future plans for the use of Phureja-Stenotomun populations. In: Report of the Planning Conference: Utilization of the genetic resources of the Potato III. Centro Internacional de la Papa (CIP), Lima, Perú, pp 80–88
Hayward A (1991) Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. En: Ann Rev Phytopatol 29:65–87. https://doi.org/10.1146/annurev.py.29.090191.000433
Henry I, Dilkes B, Tyagi A, Lin H-Y, Comai L (2009) Dosage and parent-of-origin effects shaping aneuploidy swarms in A. thaliana. Heredity 103:458–468. https://doi.org/10.1038/hdy.2009.81
Huamán Z (2008) Descriptores morfológicos de la papa (Solanum tuberosum L.). CCBAT, Tenerife
Huet G (2014) Breeding for resistances to Ralstonia solanacearum. Front Plant Sci 12. https://doi.org/10.3389/fpls.2014.00715
Iovene M, Barone A, Frusciante L, Monti L, Carputo D (2004) Selection for aneuploid potato hybrids combining a low wild genome and resistance traits from Solanum commersonii. Theor Appl Genet 109:1139–1146. https://doi.org/10.1007/s00122-004-1741-6
Jansky S (2006) Overcoming hybridisation barriers in potato. Plant Breed 125:1–12. https://doi.org/10.1111/j.1439-0523.2006.01178.x
Jansky SH, Peloquin SJ (2005) Advantages of wild diploid Solanum species over cultivated diploid relatives in potato breeding programs. Genet Resour Crop Evol 53:669–674
Johnston S, den Nijs T, Peloquin S, Hanneman R (1980) The significance of genic balance to endosperm development in interspecific crosses. Theor Appl Genet 57(1):5–9. https://doi.org/10.1007/BF00276002
Khush G (1973) Cytogenetics of aneuploids. Academic Press, London
Kim-Lee H, Moon JS, Hong YJ, Kim MS, Cho HM (2005) Bacterial wilt resistance in the progenies of the fusion hybrids between haploid of potato and Solanum commersonii. Am J Potato Res 82:129–137
Laferriere LT, Helgeson JP, Allen C (1999) Fertile Solanum tuberosum + S. commersonii somatic hybrids as sources of resistance to bacterial wilt caused by Ralstonia solanacearum. Theor Appl Genet 98:1272–1278. https://doi.org/10.1007/s001220051193
Lopes CA, de Melo PE, Rossato M, da Silva Pereira A (2018) Breeding potatoes for resistance to bacterial blight in Brazil: a quick review in face of a more effective screening protocol. Hortic Bras 36(1). https://doi.org/10.1590/s0102-053620180102
Machida-Hirano R (2015) Diversity of potato genetic resources. Breed Sci 65:26–40. https://doi.org/10.1270/jsbbs.65.26
Mendiburu AO, Peloquin SJ (1977) The significance of 2n gametes in potato breeding. Theor Appl Genet 49:53–61
Micheletto S, Boland R, Huarte M (2000) Argentinian wild diploid Solanum species as sources of quantitative late blight resistance. Theor Appl Genet 101(5–6):902–906. https://doi.org/10.1007/s001220051560
Montanelli C, Chiari A, Chiari T, Stefanini F, Nascari G (1995) Evaluation of resistance to Pseudomonas solanacearum in potato under controlled conditions. Euphytica 81:35–43. https://doi.org/10.1007/BF00022457
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plantarum 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Muthoni J, Shimelis H, Melis R (2015) Combining ability analysis of tuber yield and related traits and bacterial wilt (Ralstonia solanacearum) resistance in potato. Austr J Crop Sci 9(5):401–412
Muthoni J, Shimelis H, Melis R (2020) Conventional breeding of potatoes for resistance to bacterial wilt (Ralstonia solanacearum): Any light in the horizon? Austr J Crop Sci 14(03):485–494. https://doi.org/10.21475/ajcs.20.14.03.p2144
Narancio R, Zorrilla P, Robello C, González M, Vilaró F, Pritsch C, Dalla Rissa M (2013) Insights on gene expression response of a characterized resistance genotype of Solanum commersonii Dun. against Ralstonia solanacerum. Eur J Plant Pathol 136:823–835. https://doi.org/10.1007/s10658-013-0210-y
Ono S, Sanetomo R, Hosaka K (2016) Genetic transmission of Solanum demissum (2n = 6x = 72) chromosomes from a pentaploid hybrid of S. tuberosum (2n = 4x = 48) into the aneuploid BC1 progeny. Euphytica 207:149–168. https://doi.org/10.1007/s10681-015-1558-1
Ortiz R, Simon P, Jansky SH, Stelly D (2009) Ploidy manipulation of the gametophyte, endosperm and sporophyte in nature and for crop improvement: a tribute to Professor Stanley J. Peloquin (1921-2008). Ann Bot 104:795–807. https://doi.org/10.1093/aob/mcp207
Patil V, Gopal J, Singh B (2012) Improvement for bacterial wilt resistance in potato by conventional and biotechnological approaches. Agr Res 1(4):299–316. https://doi.org/10.1007/s40003-012-0034-6
Pavek JJ, Corsini DL (2001) Utilization of potato genetic resources in variety development. Am J Potato Res 78:433–441
Pijnacker L, Ferwerda M, Puite K, Roest S (1987) Elimination of Solanum phureja nucleolar chromosomes in S. tuberosum + S. phureja somatic hybrids. Theor Appl Genet 73:878–882. https://doi.org/10.1007/BF00289393
Plaisted R, Hoopes R (1989) The past record and future prospects for the use of exotic potato germplasm. Am Potato J 66:603–626
R Core Team (2018) R: a language and environment for statistical computing. http://www.rstudio.com/
Ross H (1986) Potato breeding problems and perspectives (Advances in Plant Breeding Series 13). Paul Parey Scientific Pub, Berlin
Sheltzer J, Torres E, Dunham M, Amon A (2012) Transcriptional consequence of aneuploidy. PNAS 109(31):12544–12649. https://doi.org/10.1073/pnas.1209227109
Siri M, Galván G, Quirici L, Villanueva P, Ferreira F, Franco L, Pianzola M (2009) Molecular marker diversity and bacterial wilt resistance in wild Solanum commersonii accessions from Uruguay. Euphytica. 165:371–382. https://doi.org/10.1007/s10681-008-9800-8
Siri MI, Sanabria A, Pianzzola MJ (2011) Genetic diversity and aggressiveness of Ralstonia solanacearum strains causing bacterial wilt of potato in Uruguay. Plant Dis 95:1292–1301. https://doi.org/10.1094/PDIS-09-10-0626
Tung P (1992) Genetic variation for bacterial wilt resistance in a population of tetraploid potato. Euphytica 65:73–80. https://doi.org/10.1007/BF00035549
Yuliar, Asi Nion Y, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ 30(1):1–11. https://doi.org/10.1264/jsme2.ME14144
Vilaró F, Plaisted R, Hoopes R (1989) Comparison of cytoplasmic male sterilities in progenies of Tuberosum x Andigena and Tuberosum x Neo-tuberosum crosses. Am Potato J 66:13–24. https://doi.org/10.1007/BF02853485
Watanabe K, El-Nashaar H, Iwanaga M (1992) Transmission of bacterial wilt resistance by first division restitution (FDR) 2n pollen via 4x x 2x crosses in potatoes. Euphytica 60:21–26. https://doi.org/10.1007/BF00022254
Yanping Z, Hui L, Hairui Z, Gao G (2014) Identification and utility of sequence related amplified polymorphism (SRAP) markers linked to bacterial wilt resistance genes in potato. Afr J Biotechnol 13(12):1314–1322. https://doi.org/10.5897/AJB2013.13021
Tung P, Hermsen J, Vander Zaag P, Schmiediche P (1993) Inheritance of resistance to Pseudomonas solanacearum in tetraploid potato. Plant Breed 111:23–30. https://doi.org/10.1111/j.1439-0523.1993.tb00603.x
Acknowledgements
Research was supported by Agencia Nacional de Investigación e Innovación (ANII) and Departamento de Biología Vegetal of Facultad de Agronomía - Universidad de la República (Udelar). We are thankful to Cristina Mazzela, Magdalena Vaio and the staff of Laboratorio de Evolución y Domesticación de Plantas of Facultad de Agonomía - Udelar for the permanent support, patience and valuable suggestions. We wish to thank Pablo Sandro, Matías Antuoni and Julio Sburlatti for their assistance during the development of the experiments. We also wish to thank Gervasio Krismanich, Victoria Dodera, Soraya Silva and Rodrigo Chiruzzo for their assistance with microsatellite markers amplification and genotyping. We are also grateful to Alicia Castillo, Victoria Bonecarrere and the technical staff at INIA and María Ines Siri, Maria Julia Pianzola and the staff at Laboratorio de Microbiología of Facultad de Química - Udelar for kindly providing plant material and for inoculation preparation. We also want to thank Elsa L. Camadro for her useful suggestions.
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This study was funded by the Agencia Nacional de Investigación e Innovación (ANII) grant code FMV_1_2011_ 1_6697 and Departamento de Biología Vegetal of Facultad de Agronomía - Universidad de la República. Mariana Andino was supported by grant ANII POS_NAC_2012_1_8632.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Mariana Andino, Paola Gaiero and Pablo González-Barrios. Francisco Vilaró produced the hybrids and backcrosses through interspecific crosses. Francisco Vilaró and Guillermo Galván supervised the field trial. Pablo Speranza supervised data analyses and interpretation. The first draft of the manuscript was written by Mariana Andino, Paola Gaiero and Pablo Speranza, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Andino, M., Gaiero, P., González-Barrios, P. et al. Potato Introgressive Hybridisation Breeding for Bacterial Wilt Resistance Using Solanum commersonii Dun. as Donor: Genetic and Agronomic Characterisation of a Backcross 3 Progeny. Potato Res. 65, 119–136 (2022). https://doi.org/10.1007/s11540-021-09512-1
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DOI: https://doi.org/10.1007/s11540-021-09512-1