Abstract
Key message
Clarification of the genome composition of the potato + eggplant somatic hybrids cooperated with transcriptome analysis efficiently identified the eggplant gene SmPGH1 that contributes to bacterial wilt resistance.
Abstract
The cultivated potato is susceptible and lacks resistance to bacterial wilt (BW), a soil-borne disease caused by Ralstonia solanacearum. It also has interspecies incompatibility within Solanaceae plants. Previously, we have successfully conducted the protoplast fusion of potato and eggplant and regenerated somatic hybrids that showing resistance to eggplant BW. For efficient use of these novel germplasm and improve BW resistance of cultivated potato, it is essential to dissect the genetic basis of the resistance to BW obtained from eggplant. The strategy of combining genome composition and transcriptome analysis was established to explore the gene that confers BW resistance to the hybrids. Genome composition of the 90 somatic hybrids was studied using genomic in situ hybridization coupled with 44 selected eggplant-specific SSRs (smSSRs). The analysis revealed a diverse set of genome combinations among the hybrids and showed a possibility of integration of alien genes along with the detection of 7 smSSRs linked to BW resistance (BW-linked SSRs) in the hybrids. Transcriptome comparison between the resistant and susceptible gene pools identified a BW resistance associated gene, smPGH1, which was significantly induced by R. solanacearum in the resistant pool. Remarkably, smPGH1 was co-localized with the BW-linked SSR emh01E15 on eggplant chromosome 9, which was further confirmed that smPGH1 was activated by R. solanacearum only in the resistant hybrids. Taken together, the identified gene smPGH1 and BW-linked SSRs have provided novel genetic resources that will aid in potato breeding for BW resistance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Austin S, Baer MA, Helgeson JP (1985) Transfer of resistance to potato leaf roll virus from Solanum brevidens into Solanum tuberosum by somatic fusion. Plant Sci 39:75–81. https://doi.org/10.1016/0168-9452(85)90195-5
Barchi L, Pietrella M, Venturini L et al (2019) A chromosome-anchored eggplant genome sequence reveals key events in Solanaceae evolution. Sci Rep 9:11769. https://doi.org/10.1038/s41598-019-47985-w
Bastia T, Carotenuto N, Basile B et al (2000) Induction of novel organelle DNA variation and transfer of resistance to frost and Verticillium wilt in Solanum tuberosum through somatic hybridization with 1EBN S. commersonii. Euphytica 116:1–10. https://doi.org/10.1023/A:1003943704037
Bidani A, Nouri-Ellouz O, Lakhoua L et al (2007) Interspecific potato somatic hybrids between Solanum berthaultii and Solanum tuberosum L. showed recombinant plastome and improved tolerance to salinity. Plant Cell Tiss Organ Cult 91:179–189. https://doi.org/10.1007/s11240-007-9284-6
Cai X, Liu J, Xie C (2004) Mesophyll protoplast fusion of Solanum tuberosum and Solanum chacoense and their somatic hybrid analysis. Acta Hortic Sin 31:623–626. https://doi.org/10.16420/j.issn.0513-353x.2004.05.013
Cardi T, D'Ambrosio E, Consoli D et al (1993) Production of somatic hybrids between frost-tolerant Solanum commersonii and S. tuberosum: characterization of hybrid plants. Theor Appl Genet 87:193–200. https://doi.org/10.1007/bf00223764
Chen L, Guo X, Xie C et al (2013) Nuclear and cytoplasmic genome components 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
Chen S, Zhou Y, Chen Y et al (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Denny TP (2006) Plant pathogenic Ralstonia species. In: Gnanamanickam SS (ed) Plant associated bacteria. Springer, Dordrecht, pp 573–644
Dobin A, Davis CA, Schlesinger F et al (2013) Star: ultrafast universal rna-seq aligner. Bioinformatics 29(1):15–21. https://doi.org/10.1093/bioinformatics/bts635
Dong F, McGrath J, Helgeson J et al (2001) The genetic identity of alien chromosomes in potato breeding lines revealed by sequential GISH and FISH analyses using chromosome-specific cytogenetic DNA markers. Genome 44(4):729–734. https://doi.org/10.1139/gen-44-4-729
Eremina M, Rozhon W, Yang S et al (2015) ENO2 activity is required for the development and reproductive success of plants, and is feedback-repressed by AtMBP-1. Plant J 81(6):895–906. https://doi.org/10.1111/tpj.12775
Feingold S, Lloyd J, Norero N et al (2005) Mapping and characterization of new EST-derived microsatellites for potato (Solanum tuberosum L.). Theor Appl Genet 111:456–466. https://doi.org/10.1007/s00122-005-2028-2
Fernández MB, Pagano MR, Daleo GR et al (2012) Hydrophobic proteins secreted into the apoplast may contribute to resistance against phytophthora infestans in potato. Plant Physiol Biochem 60:59–66. https://doi.org/10.1016/j.plaphy.2012.07.017
Fock I, Collonnier C, Purwito A et al (2000) Resistance to bacterial wilt in somatic hybrids between Solanum tuberosum and Solanum phureja. Plant Sci 160:165–176. https://doi.org/10.1016/s0168-9452(00)00375-7
Fock I, Collonnier C, Luisetti J et al (2001) Use of Solanum stenotomum for introduction of resistance to bacterial wilt in somatic hybrids of potato. Plant Physiol Biochem 39:899–908. https://doi.org/10.1016/s0981-9428(01)01307-9
Ghislain M, Rodriguez F, Villamon F et al (1999) Establishment of microsatellite assays for potato genetic identification. In: CIP program report, pp 167–174
Greplová M, Polzerová H, Vlastníková H (2008) Electrofusion of protoplasts from Solanum tuberosum, S. bulbocastanum and S. pinnatisectum. Acta Physiol Plant 30:787–796. https://doi.org/10.1007/s11738-008-0183-1
Hawkes JG (1994) Origins of cultivated potatoes and species relationships. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxford, pp 3–42
Hermsen JGT (1994) Introgression of genes from wild species, including molecular and cellular approaches. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxford, pp 515–538
Jaspert N, Weckermann K, Piotrowski M et al. (2009) Enolase, a cross-link between glycolysis and stress response. In: The 20th international conference on arabidopsis research.
Kaffarnik FA, Jones AM, Rathjen JP et al (2009) Effector proteins of the bacterial pathogen Pseudomonas syringae alter the extracellular proteome of the host plant, Arabidopsis thaliana. Mol Cell Proteomics 8(1):145–156. https://doi.org/10.1074/mcp.M800043-MCP200
Kim-Lee H, Moon JS, Hong YJ et al (2005) Bacterial wilt resistance in the progenies of the fusion hybrids between haploid of potato and Solanum commersonii. Am J Pot Res 82:129–137. https://doi.org/10.1007/BF02853650
Kulawiec M, Tagashira N, Plader W et al (2003) Chromosome number variation in somatic hybrids between transgenic tomato (Lycopersicon esculentum) and Solanum lycopersicoides. J Appl Genet 44(4):431–447. https://doi.org/10.1016/S0964-8305(03)00041-6
Laferriere L, Helgeson J, 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
Lee H, Guo Y, Ohta M et al (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21(11):2692–2702. https://doi.org/10.1093/emboj/21.11.2692
Leng Y, Ye G, Zeng D (2017) Genetic dissection of leaf senescence in rice. Int J Mol Sci 18(12):2686. https://doi.org/10.3390/ijms18122686
Li C, Cheng A, Wang M et al (2014) Fertile introgression products generated via somatic hybridization between wheat and Thinopyrum intermedium. Plant Cell Rep 33(4):633–641. https://doi.org/10.1007/s00299-013-1553-8
Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general-purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
Liu T, Yu Y, Cai X et al (2016) Introgression of bacterial wilt resistance from Solanum melongena to S. tuberosum through asymmetric protoplast fusion. Plant Cell Tiss Organ Cult 125:433–443. https://doi.org/10.1007/s11240-016-0958-9
Liu Z, Zhang Y, Ma X et al (2020) Biological functions of Arabidopsis thaliana mbpike protein encoded by eno2 in the response to drought and salt stresses. Physiol Plant 168(3):660–674. https://doi.org/10.1111/ppl.13013
Masuelli RW, Camadro EL (1997) Crossability relationships among wild potato species with different ploidies and endosperm balance numbers (EBN). Euphytica 94:227–235. https://doi.org/10.1023/A:1002996131315
McCarthy DJ, Chen YS, Smyth GK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40:10. https://doi.org/10.1093/nar/gks042
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nunome T, Negoro S, Kono L et al (2009) Development of SSR markers derived from SSR-enriched genomic library of eggplant (Solanum melongena L.). Theor Appl Genet 119:1143–1153. https://doi.org/10.1007/s00122-009-1116-0
Pendinen G, Spooner DM, Jiang J et al (2012) Genomic in situ hybridization reveals both auto-and allopolyploid origins of different North and Central American hexaploid potato (Solanum sect.Petota) species. Genome 55(6):407–415. https://doi.org/10.1139/g2012-027
Potato Genome Sequencing Consortium, Xu X, Pan S et al (2011) Genome sequence and analysis of the tuber crop potato. Nature 475(7355):189–195. https://doi.org/10.1038/nature10158
Robinson MD, Mccarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140. https://doi.org/10.1093/bioinformatics/btp616
Skarzhinskaya M, Fahleson J, Glimelius K et al (1998) Genome organization of Brassica napus and Lesquerella fendleri and analysis of their somatic hybrids using genomic in situ hybridization. Genome 41:691–701. https://doi.org/10.1139/g98-056
Tarwacka J, Polkowska-Kowalczyk L, Kolano B et al (2013) Interspecific somatic hybrids Solanum villosum (+) S. tuberosum, resistant to phytophthora infestans. J Plant Physiol 170(17):1541–1548. https://doi.org/10.1016/j.jplph.2013.06.013
Thieme R, Rakosy-Tican E, Gavrilenko T et al (2008) Novel somatic hybrids (Solanum tuberosum L.+ Solanum tarnii) and their fertile BC 1 progenies express extreme resistance to potato virus Y and late blight. Theor Appl Genet 116:691–700. https://doi.org/10.1007/s00122-007-0702-2
Van der Straeten D, Rodrigues-Pousada RA, Goodman HM et al (1991) Plant enolase: gene structure, expression, and evolution. Plant Cell 3(7):719–735. https://doi.org/10.1105/tpc.3.7.719
Wang L, Wang B, Zhao G et al (2017) Genetic and pathogenic diversity of Ralstonia solanacearum causing potato brown rot in China. Am J Potato Res 94:403–416. https://doi.org/10.1007/s12230-017-9576-2
Winstead NN, Kelman A (1952) Inoculation techniques for evaluating resistance to Pseudomonas solanacearum. Phytopathology 42:628–634
Yu Y, Ye W, He L et al (2013) Introgression of bacterial wilt resistance from eggplant to potato via protoplast fusion and genome components of the hybrids. Plant Cell Rep 32:1687–1701. https://doi.org/10.1007/s00299-013-1480-8
Acknowledgements
We greatly appreciate the help of Prof. Conghua Xie for valuable discussion and help on writing this manuscript. This research was supported by the earmarked fund for Modern Agro-industry Technology Research System (CARS-09-P06) and Hubei Technological Innovation Special Fund (2017ABA145).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by Günther Hahne.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, H., Cheng, Z., Wang, B. et al. 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 (2020). https://doi.org/10.1007/s00299-020-02563-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-020-02563-7