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Production and characterization of a novel interspecific somatic hybrid combining drought tolerance and high quality of sweet potato and Ipomoea triloba L.

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Abstract

Key message

A novel interspecific somatic hybrid combining drought tolerance and high quality of sweet potato and Ipomoea triloba L. was obtained and its genetic and epigenetic variations were studied.

Abstract

Somatic hybridization can be used to overcome the cross-incompatibility between sweet potato (Ipomoea batatas (L.) Lam.) and its wild relatives and transfer useful and desirable genes from wild relatives to cultivated plants. However, most of the interspecific somatic hybrids obtained to date cannot produce storage roots and do not exhibit agronomic characters. In the present study, a novel interspecific somatic hybrid, named XT1, was obtained through protoplast fusion between sweet potato cv. Xushu 18 and its wild relative I. triloba. This somatic hybrid produced storage roots and exhibited significantly higher drought tolerance and quality compared with its cultivated parent Xushu 18. Transcriptome and real-time quantitative PCR (qRT-PCR) analyses revealed that the well-known drought stress-responsive genes in XT1 and I. triloba were significantly up-regulated under drought stress. The genomic structural reconstructions between the two genomes of the fusion parents in XT1 were confirmed using genomic in situ hybridization (GISH) and specific nuclear and cytoplasmic DNA markers. The DNA methylation variations were characterized by methylation-sensitive amplified polymorphism (MSAP). This study not only reveals the significance of somatic hybridization in the genetic improvement of sweet potato but also provides valuable materials and knowledge for further investigating the mechanism of storage root formation in sweet potato.

Highlights

  • A novel interspecific somatic hybrid XT1 with high drought tolerance and quality was obtained between sweetpotato and I. triloba.

  • Genetic and epigenetic variations of XT1 were clarified.

  • This study provides valuable materials and knowledge for investigating the mechanism of storage root formation in sweetpotato.

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References

  • Cai YF, Xiang FN, Zhi DY, Liu H, Xia GM (2007) Genotyping of somatic hybrids between Festuca arundinacea Schreb. and Triticum aestivum L. Plant Cell Rep 26:1809–1819

    Article  CAS  PubMed  Google Scholar 

  • Cao QH, Zhang A, Ma DF, Li HM, Li Q, Li P (2009) Novel interspecific hybridization between sweet potato (Ipomoea batatas (L.) Lam.) and its two diploid wild relatives. Euphytica 169:345–352

    Article  CAS  Google Scholar 

  • Cardi T, Bastia T, Monti L, Earle ED (1999) Organelle DNA and male fertility variation in Solanum sp. and interspecific somatic hybrids. Theor Appl Genet 99:819–828

    Article  CAS  Google Scholar 

  • Cervantes-Flores JC, Sosinski B, Pecota KV, Mwanga ROM, Catignani GL, Truong VD, Watkins RH, Ulmer MR, Yencho GC (2011) Identification of quantitative trait loci for dry matter, starch, and β-carotene content in sweet potato. Mol Breed 28:201–216

    Article  CAS  Google Scholar 

  • Chen CL, Guo WW, Yi HL, Deng XX (2004) Cytogenetic analysis of two interspecific Citrus allotetraploid somatic hybrids and their diploid fusion parents. Plant Breed 123:332–337

    Article  Google Scholar 

  • Chen L, Guo XP, Xie CH, He L, Cai XK, Tian LL, Song BT, Liu J (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

    Article  CAS  PubMed  Google Scholar 

  • CIP, AVRDC, IBPGR (1991) Descriptors for sweet potato. In: Huamán Z (ed) International Board for Plant Genetic Resources, Rome

  • Collonnier C, Mulya K, Fock I, Mariska I, Servaes A, Vedel F, Siljak-Yakovlev S, Souvannavong V, Ducreux G, Sihachakr D (2001) Source of resistance against Ralstonia solanacearum in fertile somatic hybrids of eggplant (Solanum melongena L.) with Solanum aethiopicum L. Plant Sci 160:301–313

    Article  CAS  PubMed  Google Scholar 

  • Gao S, Yuan L, Zhai H, Liu CL, He SZ, Liu QC (2011) Transgenic sweet potato plants expressing an LOS5 gene are tolerant to salt stress. Plant Cell Tissue Organ Cult 107:205–213

    Article  CAS  Google Scholar 

  • Guo JM, Liu QC, Zhai H, Wang YP (2006) Regeneration of plants from Ipomoea cairica L. protoplasts and production of somatic hybrids between I. cairica L. and sweet potato, I. batatas (L.) Lam. Plant Cell Tissue Organ Cult 87:321–327

    Article  CAS  Google Scholar 

  • Gupta V, Bijo AJ, Kumar M, Reddy CRK, Jha B (2012) Detection of epigenetic variations in the protoplast-derived germlings of Ulva reticulata using methylation sensitive amplification polymorphism (MSAP). Mar Biotechnol 14:692–700

    Article  CAS  Google Scholar 

  • Gupta V, Kumari P, Reddy CRK (2015) Development and characterization of somatic hybrids of Ulva reticulata Forsskål (×) Monostromaoxyspermum (Kutz.) Doty. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00003

    Article  PubMed  PubMed Central  Google Scholar 

  • He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi YJ, Chen RS, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang JC, Sun M (2000) Genetic diversity and relationships of sweet potato and its wild relatives in Ipomoea series Batatas (Convolvulaceae) as revealed by inter-simple sequence repeat (ISSR) and restriction analysis of chloroplast DNA. Theor Appl Genet 100:1050–1060

    Article  CAS  Google Scholar 

  • Iovene M, Savarese S, Cardi T, Frusciante L, Scotti N, Simon PW, Carputo D (2007) Nuclear and cytoplasmic genome composition of Solanum bulbocastanum (+) S. tuberosum somatic hybrids. Genome 50:443–450

    Article  CAS  PubMed  Google Scholar 

  • Ji H, Zhang HX, Li HT, Li YC (2015) Analysis on the nutrition composition and antioxidant activity of different types of sweet potato cultivars. Food Nutr Sci 6:161–167

    CAS  Google Scholar 

  • Jia LC, Zhai H, He SZ, Yang YF, Liu QC (2017) Analysis of drought tolerance and genetic and epigenetic variations in a somatic hybrid between Ipomoea batatas (L.) Lam. and I. triloba L. J Integr Agric 16:36–46

    Article  CAS  Google Scholar 

  • Joyce SM, Cassells AC (2002) Variation in potato microplant morphology in vitro and DNA methylation. Plant Cell Tissue Organ Cult 70:125–137

    Article  CAS  Google Scholar 

  • Kanchanaketu T, Sangduen N, Toojinda T, Hongtrakul V (2012) Genetic diversity analysis of Jatropha curcas L. (Euphorbiaceae) based on methylation-sensitive amplification polymorphism. Genet Mol Res 11:944–955

    Article  CAS  PubMed  Google Scholar 

  • Kasha KJ, Kao KN (1970) High frequency haploid production in barley (Hordeum vulgare L.). Nature 225:874–876

    Article  CAS  PubMed  Google Scholar 

  • Kumari P, Singh KP, Bisht D, Kumar S (2020) Somatic hybrids of Sinapis alba + Brassica juncea: study of backcross progenies for morphological variations, chromosome constitution and reaction to Alternaria brassicae. Euphytica 216:1–14

    Article  Google Scholar 

  • Li Y, Sink C (1992) Cell type determines plastid transmission in tomato intergeneric somatic hybrids. Curr Genet 22:167–171

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Liu QC, Zhai H, Ma DF, Wang X, Li XQ, Wang YP (2008) Genetic diversity in main parents of sweet potato in China as revealed by ISSR markers. Acta Agr Sin 34:972–977

    CAS  Google Scholar 

  • Liu QC (2011) Sweetpotato omics and biotechnology in China. Plant Omics J 4:295–301

  • Liu QC (2017) Improvement for agronomically important traits by gene engineering in sweet potato. Breed Sci 67:15–26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SW, Xia GM (2014) The place of asymmetric somatic hybridization in wheat breeding. Plant Cell Rep 33:595–603

    Article  CAS  PubMed  Google Scholar 

  • Liu QC, Kokubu T, Sato M (1991) Plant regeneration from Ipomoea triloba L. protoplasts. Jpn J Breed 41:103–108

    Article  CAS  Google Scholar 

  • Liu QC, Mi KX, Zhou HY, Ma B, Zhai H (1998) Regeneration and identification of interspecific somatic hybrid plants between sweet potato and Ipomoea lacunosa. Acta Agron Sin 24:529–535

    Google Scholar 

  • Liu QC, Zhai H, Wang Y, Zhang DP (2001) Efficient plant regeneration from embryogenic suspension cultures of sweet potato. In Vitro Cell Dev Biol-Plant 37:564–567

    Article  Google Scholar 

  • Liu H, Liu SW, Xia GM (2009) Generation of high frequency of novel alleles of the high molecular weight glutenin in somatic hybridization between bread wheat and tall wheatgrass. Theor Appl Genet 118:1193–1198

    Article  CAS  PubMed  Google Scholar 

  • Liu DG, He SZ, Zhai H, Wang LJ, Zhao Y, Wang B, Li RJ, Liu QC (2014) Overexpression of IbP5CR enhances salt tolerance in transgenic sweet potato. Plant Cell Tissue Organ Cult 117:1–16

    Article  Google Scholar 

  • Liu SW, Li F, Kong LN, Sun Y, Qin LM, Chen SY, Cui HF, Huang YH, Xia GM (2015) Genetic and epigenetic changes in somatic hybrid introgression lines between wheat and tall wheatgrass. Genetics 199:1035–1045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin FW, Jones A (1973) The species of Ipomoea closely related to the sweet potato. Econ Bot 26:201–215

    Article  Google Scholar 

  • Negrutiu I, Brouwer D, Watts JW, Sidorov VI, Dirks R, Jacobs M (1986) Fusion of plant protoplasts: a study using auxotrophic mutants of Nicotiana plumbaginifolia, Viviani. Theor Appl Genet 72:279–286

    Article  CAS  PubMed  Google Scholar 

  • Parokonny AS, Kenton AY, Meredith L, Owens SJ, Bennett MD (1992) Genomic divergence of allopatric sibling species studied by molecular cytogenetics of their F1 hybrids. Plant J 2:695–704

    Article  Google Scholar 

  • Rangwala SH, Richards EJ (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr Opin Genet Dev 14:686–691

    Article  CAS  PubMed  Google Scholar 

  • Ruiz M, Pensabene-Bellavia G, Quiñones A, García-Lor A, Morillon R, Ollitrault P, Primo-Millo E, Navarro L, Aleza P (2018) Molecular characterization and stress tolerance evaluation of new allotetraploid somatic hybrids between Carrizo citrange and Citrus macrophylla W. rootstocks. Front Plant Sci 9:901

    Article  PubMed  PubMed Central  Google Scholar 

  • Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159

    Article  CAS  PubMed  Google Scholar 

  • Sarilar V, Palacios PM, Rousselet A, Ridel C, Falque M, Eber F, Chèvre AM, Joets J, Brabant P, Alix K (2013) Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. New Phytol 198:593–604

    Article  CAS  PubMed  Google Scholar 

  • Scotti N, Monti L, Cardi T (2003) Organelle DNA variation in parental Solanum spp. genotypes and nuclear-cytoplasmic interactions in Solanum tuberosum (+) S. commersonii somatic hybrid backcross progeny. Theor Appl Genet 108:87–94

    Article  CAS  PubMed  Google Scholar 

  • Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13:1749–1759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen HS, He H, Li JG, Chen W, Wang XC, Guo L, Peng ZY, He GM, Zhong SW, Qi YJ, Terzaghi W, Deng XW (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24:875–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng XG, Zhao ZQ, Yu HF, Wang JS, Gu HH (2013) Rapid alterations of DNA sequence and cytosine methylation induced by somatic hybridization between Brassica oleracea L. var. italica and Brassica nigra (L.) Koch. Plant Cell Tissue Organ Cult 115:395–405

    Article  CAS  Google Scholar 

  • Smyda-Dajmund P, Śliwka J, Villano C, Janiszewska M, Aversano R, Bednarek PT, Carputo D, Zimnoch-Guzowska E (2021) Analysis of cytosine methylation in genomic DNA of Solanum × michoacanum (+) S. tuberosum somatic hybrids. Agronomy 11:845

    Article  CAS  Google Scholar 

  • Sun YQ, Zhang XL, Nie YC, Guo XP, Jin SX, Liang SG (2004) Production and characterization of somatic hybridization between upland cotton (Gossypium hirsutum) and wild cotton (G. klotzschianum Anderss) via electrofusion. Theor Appl Genet 109:472–479

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Xu CH, Wang MQ, Zhi DY, Xia GM (2014) Genomic changes at the early stage of somatic hybridization. Genet Mol Res 13:1938–1948

    Article  CAS  PubMed  Google Scholar 

  • Tu YQ, Sun J, Ge XH, Li ZY (2009) Chromosome elimination, addition and introgression in intertribal partial hybrids between Brassica rapa and Isatis indigotica. Ann Bot 103:1039–1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tu W, Dong JK, Zou Y, Zhao QH, Wang HB, Ying JW, Wu JH, Du J, Cai XK, Song BT (2021) Interspecific potato somatic hybrids between Solanum malmeanum and S. tuberosum provide valuable resources for freezing-tolerance breeding. Plant Cell Tissue Organ Cult 147:73–83

    Article  CAS  Google Scholar 

  • Wang YP, Sonntag K, Rudloff E (2003) Development of rapeseed with high erucic acid content by asymmetric somatic hybridization between Brassica napus and Crambe abyssinica. Theor Appl Genet 106:1147–1155

    Article  CAS  PubMed  Google Scholar 

  • Wang JF, Zhao CZ, Liu C, Xia GM, Xiang FN (2011) Introgression of Swertia mussotii gene into Bupleurum scorzonerifolium via somatic hybridization. BMC Plant Biol 11:71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia GM (2009) Progress of chromosome engineering mediated by asymmetric somatic hybridization. J Genet Genomics 36:547–556

    Article  CAS  PubMed  Google Scholar 

  • Xia GM, Xiang FN, Zhou AF, Wang H, Chen HM (2003) Asymmetric somatic hybridization between wheat (Triticum aestivum L.) and Agropyron elongatum (Host) Nevishi. Theor Appl Genet 107:299–305

    Article  CAS  PubMed  Google Scholar 

  • Xiang FN, Xia GM, Zhi DY, Wang J, Nie H, Chen HM (2004) Regeneration of somatic hybrids in relation to the nuclear and cytoplasmic genomes of wheat and Setaria italica. Genome 47:680–688

    Article  CAS  PubMed  Google Scholar 

  • Xiao SX, Biswas MK, Li MY, Deng XX, Xu Q, Guo WW (2014) Production and molecular characterization of diploid and tetraploid somatic hybrid plants between male sterile Satsuma mandarin and seedy sweet orange cultivars. Plant Cell Tissue Organ Cult 116:81–88

    Article  CAS  Google Scholar 

  • Xu XY, Liu JH, Deng XX (2004) Production and characterization of intergeneric diploid cybrids derived from symmetric fusion between Microcitrus papuana Swingle and sour orange (Citrus aurantium). Euphytica 136:115–123

    Article  Google Scholar 

  • Xu YH, Zhong L, Wu XM, Fang XP, Wang JB (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:471–483

    Article  CAS  PubMed  Google Scholar 

  • Xu SX, Cai DF, Tan FQ, Fang YN, Xie KD, Grosser JW, Guo WW (2014) Citrus somatic hybrid: an alternative system to study rapid structural and epigenetic reorganization in allotetraploid genomes. Plant Cell Tissue Organ Cult 119:511–522

    Article  CAS  Google Scholar 

  • Yang YF, Guan SK, Zhai H, He SZ, Liu QC (2009) Development and evaluation of a storage root-bearing sweet potato somatic hybrid between Ipomoea batatas (L.) Lam. and I. triloba L. Plant Cell Tissue Organ Cult 99:83–89

    Article  Google Scholar 

  • Yu XS, Yu XS, Chu BJ, Liu RE, Sun J, Brian JJ, Wang HZ, Zhu S, Sun YQ (2012) Characteristics of fertile somatic hybrids of G. hirsutum L. and G. trilobum generated via protoplast fusion. Theor Appl Genet 125:1503–1516

    Article  CAS  PubMed  Google Scholar 

  • Zhai H, Wang FB, Si ZZ, Huo JX, Xing L, An YY, He SZ, Liu QC (2016) A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnol J 14:592–602

    Article  CAS  PubMed  Google Scholar 

  • Zhang BY, Liu QC, Zhai H, Zhou HY, Zhang DP, Wang YP (2002) Production of fertile interspecific somatic hybrid plants between sweet potato and its wild relative, Ipomoea lacunosa. Acta Hortic 583:81–85

    Article  CAS  Google Scholar 

  • Zhao N, Yu XX, Jie Q, Li H, Hu J, Zhai H, He SZ, Liu QC (2013) A genetic linkage map based on AFLP and SSR markers and mapping of QTL for dry-matter content in sweet potato. Mol Breed 32:807–820

    Article  CAS  Google Scholar 

  • Zhou AF, Xia GM, Chen HM (2001) Hu H, Analysis of chromosomal and organellar DNA of somatic hybrids between Triticum aestiuvm and Haynaldia villosa Schur. Mol Genet Genomics 265:387–393

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2006) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  PubMed  Google Scholar 

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Funding

This work was supported by the National Key R&D Program of China (2019YFD1001302/2019YFD1001300) and the earmarked fund for CARS-10-Sweet potato.

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QL, LJ and HZhai conceived and designed the experiments. LJ and YY performed the experiments. LJ, YY, SH, GX, NZ, HZhang and SG analyzed the data. QL, LJ and YY wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Qingchang Liu.

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Communicated by Teodoro Cardi.

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Jia, L., Yang, Y., Zhai, H. et al. Production and characterization of a novel interspecific somatic hybrid combining drought tolerance and high quality of sweet potato and Ipomoea triloba L.. Plant Cell Rep 41, 2159–2171 (2022). https://doi.org/10.1007/s00299-022-02912-8

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