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.
Similar content being viewed by others
Change history
17 September 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00299-022-02925-3
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Joyce SM, Cassells AC (2002) Variation in potato microplant morphology in vitro and DNA methylation. Plant Cell Tissue Organ Cult 70:125–137
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
Kasha KJ, Kao KN (1970) High frequency haploid production in barley (Hordeum vulgare L.). Nature 225:874–876
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
Li Y, Sink C (1992) Cell type determines plastid transmission in tomato intergeneric somatic hybrids. Curr Genet 22:167–171
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
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
Liu SW, Xia GM (2014) The place of asymmetric somatic hybridization in wheat breeding. Plant Cell Rep 33:595–603
Liu QC, Kokubu T, Sato M (1991) Plant regeneration from Ipomoea triloba L. protoplasts. Jpn J Breed 41:103–108
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
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
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
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
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
Martin FW, Jones A (1973) The species of Ipomoea closely related to the sweet potato. Econ Bot 26:201–215
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
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
Rangwala SH, Richards EJ (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr Opin Genet Dev 14:686–691
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Xia GM (2009) Progress of chromosome engineering mediated by asymmetric somatic hybridization. J Genet Genomics 36:547–556
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Teodoro Cardi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-022-02912-8