Skip to main content
SpringerLink
Log in

Interspecific potato somatic hybrids between Solanum malmeanum and S. tuberosum provide valuable resources for freezing-tolerance breeding

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Freezing stress affects the geographic distribution, growth, and development of potato, resulting in yield loss. Solanum malmeanum, a diploid wild species with strong freezing tolerance, was fused with the freezing sensitive dihaploid S. tuberosum by somatic hybridization. In our study, 980 calli were obtained, and 248 differentiated shoots were obtained from the calli. Parental-specific SSR markers were used to analyse the chromosome composition of the 80 randomly selected regenerated plants, obtaining 51 somatic hybrids. Among them, 44 somatic hybrids were tested with ploidy analysis in the years 2016 and 2020. During subculture, the genomic ploidy levels changed due to the composition of the unstable chromosome in 56.82% of the somatic hybrids. The somatic hybrids showed better freezing tolerance than the cultivated parent. Then, freezing-tolerant somatic hybrids were selected to backcross with cultivars, and we obtained valuable breeding resources with enhanced freezing tolerance and tuberization capacity similar to that of cultivars. The correlation analysis showed that freezing tolerance has no relation with tuberization capacity, which indicates that they are controlled by independent genetic loci.

Key message

Freezing tolerance was transferred to cultivated potato from S. malmeanum by protoplast fusion for the first time, and valuable resources for freezing tolerance breeding were obtained.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abid G, Muhoviski Y, Jacquemin J-M, Mingeot D, Sassi K, Toussaint A, Baudoin J-P (2011) Changes in DNA-methylation during zygotic embryogenesis in interspecific hybrids of beans (Phaseolus ssp.). Plant Cell Tiss Organ Cult 105:383–393

    Article  CAS  Google Scholar 

  • Aversano R, Savarese S, Nova JMD, Frusciante L, Punzo M, Carputo D (2009) Genetic stability at nuclear and plastid DNA level in regenerated plants of Solanum species and hybrids. Euphytica 165:353–361

    Article  CAS  Google Scholar 

  • Bradeen JM, Kole C (2016) Genetics, genomics and breeding of potato. CRC Press, Boca Raton

    Book  Google Scholar 

  • Bryan GJ, Karen ML, Robbie W, Spooner DM (2017) Levels of intra-specific AFLP diversity in tuber-bearing potato species with different breeding systems and ploidy levels. Front Genet 8:119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Camadro EL, Carputo D, Peloquin SJ (2004) Substitutes for genome differentiation in tuber-bearing Solanum: interspecific pollen-pistil incompatibility, nuclear-cytoplasmic male sterility, and endosperm. Theor Appl Genet 109:1369–1376

    Article  CAS  PubMed  Google Scholar 

  • Cardi T, D’Ambrosio E, Consoli D, Puite K, Ramulu KJ, Ramulu KS (1993) Production of somatic hybrids between frost-tolerant Solanum commersonii and S. tuberosum: characterization of hybrid plants. Theor Appl Genet 87:193–200

    Article  CAS  PubMed  Google Scholar 

  • Chandel P, Tiwari JK, Ali N, Devi S, Sharma SH, Sharma SA, Luthra SK, Singh BP (2015) Interspecific potato somatic hybrids between Solanum tuberosum and S. cardiophyllum, potential sources of late blight resistance breeding. Plant Cell Tiss Organ Cult 123:579–589

    Article  Google Scholar 

  • Chang DC, Sohn HB, Cho JH, Im JS, Jin YI, Do GR, Kim SJ, Cho HM, Lee YB (2014) Freezing and frost damage of potato plants: a case study on growth recovery, yield response, and quality changes. Potato Res 57:99–110

    Article  CAS  Google Scholar 

  • Chen HH, Li PH (1980) Characteristics of cold acclimation and deacclimation in tuber-bearing Solanum species. Plant Physiol 65:1146–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YKH, 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

    Article  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin

    Book  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21

    Article  CAS  Google Scholar 

  • Gomez KA, Gomez AA (1984) Statistical procedures for agricultural research. Wiley, New York

    Google Scholar 

  • Guo X, Xie C, Cai X, Song B, He L, Liu J (2010) Meiotic behavior of pollen mother cells in relation to ploidy level of somatic hybrids between Solanum tuberosum and S. chacoense. Plant Cell Rep 29:1277–1285

    Article  CAS  PubMed  Google Scholar 

  • Haan SD, Rodriguez F (2016) Potato origin and production. In: Singh J (ed) Advances in potato chemistry and technology, 2nd edn. Acedemic press, Cambridge, pp 1–32

    Google Scholar 

  • Hawkes JG (1990) The potato: evolution, biodiversity and genetic resources. Belhaven, London

    Google Scholar 

  • Hayes RJ, Dinu II, Thill CA (2005) Unilateral and bilateral hybridization barriers in inter-series crosses of 4x 2EBN Solanum stoloniferum, S. pinnatisectum, S. cardiophyllum, and 2x 2EBN S. tuberosum haploids and haploid-species hybrids. Sex Plant Reprod 17:303–311

    Article  Google Scholar 

  • Jacobs MM, Van Den Berg RG, Vleeshouwers VG, Visser M, Mank R, Sengers M, Hoekstra R, Vosman B (2008) AFLP analysis reveals a lack of phylogenetic structure within Solanum section Petota. BMC Evol Biol 8:1–12

    Article  CAS  Google Scholar 

  • Jacobs MM, Smulders MJ, Van Den Berg RG, Vosman B (2011) What’s in a name; genetic structure in Solanum section Petota studied using population-genetic tools. BMC Evol Biol 11:42–62

    Article  PubMed  PubMed Central  Google Scholar 

  • Kou S, Chen L, Tu W, Scossa F, Wang Y, Liu J, Femie AR, Song B, Xie C (2018) The arginine decarboxylase gene ADC1, associated to the putrescine pathway, plays an important role in potato cold-acclimated freezing tolerance as revealed by transcriptome and metabolome analyses. Plant J 96:1283–1298

    Article  CAS  PubMed  Google Scholar 

  • Liu T, Yu Y, Cai X, Tu W, Xie C, Liu J (2016) Introgression of bacterial wilt resistance from Solanum melongena to S. tuberosum through asymmetric protoplast fusion. Plant Cell Tiss Organ Cult 125:433–443

    Article  CAS  Google Scholar 

  • Luthra SK, Gopal J, Manivel P, Kumar V, Singh BP, Pandey SK (2007) Screening of wild and cultivated species of potato for frost tolerance in north-central plains of India. Potato Journal 34:1–2

    Google Scholar 

  • Luthra SK, Tiwari JK, Lal M, Chandel P, Kumar V (2016) Breeding potential of potato somatic hybrids: evaluations for adaptability, tuber traits, late blight resistance, keeping quality and backcross (BC1) progenies. Potato Res 59:375–391

    Article  Google Scholar 

  • Maune JF, Camadro EL, Erazzú LE (2018) Cross-incompatibility and self-incompatibility: unrelated phenomena in wild and cultivated potatoes? Botany 96:33–45

    Article  CAS  Google Scholar 

  • Menke U, Schilde-Rentschler L, Ruoss B, Zanke C, Hemleben V, Ninnemann H (1996) Somatic hybrids between the cultivated potato Solanum tuberosum L. and the 1EBN wild species Solanum pinnatisectum Dun.: morphological and molecular characterization. Theor Appl Genet 92:617–626

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Naz RMM, Li M, Ramzan S, Li G, Liu J, Cai X, Xie C (2018) QTL mapping for microtuber dormancy and GA3 content in a diploid potato population. Biol Open. https://doi.org/10.1242/bio.027375

    Article  PubMed  Google Scholar 

  • Nyman M, Waara S (1997) Characterization of somatic hybrids between S. tuberosum and its frost-tolerant relative S. commersonii. Theor Appl Genet 95:1127–1132

    Article  Google Scholar 

  • Palta JP, Simon G (1993) Breeding potential for improvement of freezing stress resistance: genetic separation of freezing tolerance, freezing avoidance, and capacity to cold acclimate. In: Li PH, Christersson L (eds) Advances in plant cold hardiness. CRC Press, Boca Raton, pp 299–310

    Google Scholar 

  • Polzerová H, Patzak J, Greplová M (2011) Early characterization of somatic hybrids from symmetric protoplast electrofusion of Solanum pinnatisectum Dun. and Solanum tuberosum L. Plant Cell Tissue Org Cult 104:163–170

    Article  Google Scholar 

  • Preiszner J, Fehér A, Veisz O, Sutka J, Dudits D (1991) Characterization of morphological variation and cold resistance in interspecific somatic hybrids between potato (Solanum tuberosum L.) and S. brevidens Phil. Euphytica 57:37–49

    Article  Google Scholar 

  • Sarkar D, Tiwari JK, Sharma SU, Poonam Sharma SA, Gopal J, Singh BP, Luthra SK, Pandey SK, Pattanayak D (2011) Production and characterization of somatic hybrids between Solanum tuberosum L. and S. pinnatisectum Dun. Plant Cell Tissue Organ Cult 107:427–440

    Article  Google Scholar 

  • Seppänen M, Nissinen O, Perälä S (2001) Freezing and low temperature photoinhibition tolerance in cultivated potato and potato hybrids. Agr Food Sci 10:153–163

    Article  Google Scholar 

  • Seppänen M, Majaharju M, Somersalo S, Pehu E (1998) Freezing tolerance, cold acclimation and oxidative stress in potato. Paraquat tolerance is related to acclimation but is a poor indicator of freezing tolerance. Physiol Plant 102:454–460

    Article  Google Scholar 

  • Sharma S, Sarkar D, Pandey SK, Chandel P, Tiwari JK (2011) Stoloniferous shoot protoplast, an efficient cell system in potato for somatic cell genetic manipulations. Scientia Horticulturae 128:84–91

    Article  CAS  Google Scholar 

  • Shepard JF, Totten RE (1977) Mesophyll cell protoplasts of potato: Isolation, proliferation and plant regeneration. Plant Physiol 60:313–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siri MI, Galván GA, Quirici L, Silvera E, Villanueva P, Ferreira F, Fraguas LF, Pianzzola MJ (2009) Molecular marker diversity and bacterial wilt resistance in wild Solanum commersonii accessions from Uruguay. Euphytica 65:371–382

    Article  CAS  Google Scholar 

  • Spooner DM, Ghislain M, Simon R, Jansky SH, Gavrilenko T (2014) Systematics, diversity, genetics, and evolution of wild and cultivated potatoes. Bot Rev 80:283–383

    Article  Google Scholar 

  • Sree Ramulu K (1986) Case histories of genetic variability in vitro: potato. In: Vasil IK (ed) Cell, culture and somatic cell genetics of plants. Academic Press, Minnesota, pp 449–473

    Google Scholar 

  • Szczerbakowa A, Tarwacka J, Sliwinska E, Wielgat B (2011) Nuclear DNA content and chromosomal number in somatic hybrid allopolyploid of Solanum. Plant Cell Tissue Organ Cult 106:373–380

    Article  CAS  Google Scholar 

  • Thieme R, Darsow U, Gavrilenko T, Dorokhov D, Tiemann H (1997) Production of somatic hybrids between S. tuberosum L. and late blight resistant Mexican wild potato species. Euphytica 97:189–200

    Article  Google Scholar 

  • Tiwari JK, Poonam Sarkar D, Pandey SK, Gopal J, Kumar SR (2010) Molecular and morphological characterization of somatic hybrids between Solanum tuberosum L. and S. etuberosum Lindl. Plant Cell Tissue Organ Cult 103:175–187

    Article  CAS  Google Scholar 

  • Tiwari JK, Devi S, Ali N, Luthra SK, Kumar V, Bhardwaj V, Singh RK, Rawat S, Chakrabarti SK (2018) Progress in somatic hybridization research in potato during the past 40 years. Plant Cell Tiss Organ Cult 132:225–238

    Article  CAS  Google Scholar 

  • Tiwari JK, Rawat S, Luthra SK et al (2021) Genome sequence analysis provides insights on genomic variation and late blight resistance genes in potato somatic hybrid (parents and progeny). Mol Biol Rep 48:623–635

    Article  CAS  PubMed  Google Scholar 

  • Vega SE, Bamberg JB (1995) Screening the US potato collection for frost hardiness. Am Potato J 72:13–21

    Article  Google Scholar 

  • Wang MQ, Zhao JS, Peng ZY, Guo W, Wang Y, Wang L, Xia GM (2007) Chromosomes are eliminated in the symmetric fusion between Arabidopsis thaliana L. and Bupleurum scorzonerifolium Willd. Plant Cell Tissue Organ Cult 92:121–130

    Google Scholar 

  • Wang H, Cheng Z, Wang B, Dong J, Ye W, Yu Y, Liu T, Cai X, Song B, Liu J (2020) Combining genome composition and differential gene expression analyses reveals that SmPGH1 contributes to bacterial wilt resistance in somatic hybrids. Plant Cell Rep 39:1235–1248

    Article  CAS  PubMed  Google Scholar 

  • Xu YS, Murto M, Dunckley R, Jones MGK, Pehu E (1993) Production of asymmetric hybrids between Solanum tuberosum and irradiated S. brevidens. Theor Appl Genet 85:729–734

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Ye W, He L, Cai X, Liu T, Liu J (2013) Introgression of bacterial wilt resistance from eggplant to potato via protoplast fusion and genome components of the hybrids. Plant Cell Rep 32:1687–701

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We greatly appreciate the help of Vice Prof. Yuhong Yao and Ting Liu in revising the manuscript. This research was funded by the Earmarked Fund for Modern Agro-Industry Technology Research System of China (Grant No CARS-09-P07) and the National Natural Science Foundation of China (grant No 31871685).

Author information

Author notes

  1. Wei Tu and Jianke Dong have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, 430070, China

    Wei Tu, Jianke Dong, Ying Zou, Qinghao Zhao, Jingwen Ying, Jianghai Wu, Juan Du, Xingkui Cai & Botao Song

  2. Key Laboratory of Potato Biology and Biotechnology, Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University, Wuhan, 430070, China

    Wei Tu, Jianke Dong, Qinghao Zhao, Haibo Wang, Jingwen Ying, Jianghai Wu, Juan Du, Xingkui Cai & Botao Song

  3. Enshi Academy of Agricultural Sciences, Enshi, 445000, China

    Ying Zou

  4. College of Biological Science and Technology, Hubei Minzu University, Enshi, 445000, China

    Haibo Wang

Authors
  1. Wei Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jianke Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ying Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qinghao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haibo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jingwen Ying
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianghai Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Juan Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xingkui Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Botao Song
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

BS and XC conceived and supervised the study. YZ, QZ, JY, and JW performed the experiments. WT and JD wrote the manuscript; JD revised the manuscript. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Xingkui Cai or Botao Song.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Ewa Grzebelus.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tu, W., Dong, J., Zou, Y. et al. Interspecific potato somatic hybrids between Solanum malmeanum and S. tuberosum provide valuable resources for freezing-tolerance breeding. Plant Cell Tiss Organ Cult 147, 73–83 (2021). https://doi.org/10.1007/s11240-021-02106-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-021-02106-2

Keywords

Search

Navigation