Log in

Genome-wide genetic variation and comparative transcriptome analyses of citrus mutant Jedae-unshiu and wild-type Citrus unshiu

  • Original Article
  • Published:
Plant Biotechnology Reports Aims and scope Submit manuscript

Abstract

‘Miyagawa-wase’ mandarin (Citrus. unshiu Marc. cv. Miyagawa-wase) is one of the most widely cultivated citrus varieties in Korea. Previously, we used γ-irradiation to develop new citrus varieties by mutation breeding, a useful tool for increasing genetic diversity in a short time. One of the new citrus varieties we generated, Jedae-unshiu, produces uniquely shaped fruit with vertical troughs on the flavedo. Although comparative analyses of genome-wide variation and transcriptomics have been reported for seedless or color-change citrus variants, little is known regarding genetic variants linked to morphological variation in citrus fruits. In this study, genome-wide single nucleotide polymorphisms (SNPs) and insertion/deletion (InDel) variants were identified in Jedae-unshiu by whole-genome re-sequencing and subjected to functional annotation by gene ontology (GO) analysis. The results show that InDel-containing genes are more highly represented in the GO database than SNP-containing genes. In addition, we compared Jedae-unshiu and wild-type control transcriptomes to identify candidate genetic determinants of the unique fruit phenotype of Jedae-unshiu. A total of 641 unique, differentially expressed genes (DEGs) were identified in Jedae-unshiu relative to wild-type control, including 388 up-regulated and 253 down-regulated genes. The DEGs were mapped to GO terms and subjected to Kyoto Encyclopedia of Genes and Genomes pathway analysis to identify DEGs involved in cellular processes potentially linked to the unique phenotype of Jedae-unshiu fruit. The expression of 10 DEGs (5 up- and 5 down-regulated) was quantified by reverse transcriptase-polymerase chain reaction (RT-PCR). Our findings provide insight into putative genetic determinants of fruit morphology in citrus.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data that support the finding of this study are available from the corresponding author upon reasonable requests.

References

  • Agisimanto D, Noor NM, Ibrahim R, Mohamad A (2016) Gamma irradiation effect on embryogenic callus growth of Citrus reticulata cv. Limau Madu Sains Malaysiana 45(3):329–337

    CAS  Google Scholar 

  • Allario T, Brumos J, Colmenero-Flores JM, Iglesias DJ, Pina JA, Navarro L, Talon M, Ollitrault P, Morillon R (2013) Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environ 36(4):856–868

    Article  CAS  PubMed  Google Scholar 

  • Ander S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169

    Article  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashburner M et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi X, Liao L, Deng L, ** Z, Huang Z, Sun G, **ong B, Wang Z (2022) Combined transcriptome and metabolome analyses reveal candidate genes involved in tangor (Citrus reticulata × Citrus sinensis) fruit development and quality formation. Int J Mol Sci 23:5457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of illumina second-generation sequencing data. BMC Bioinform 11:485

    Article  Google Scholar 

  • Donkersley P, Silva FWS, Carvalho CM, Al-Sadi AM, Elliot SL (2018) Biological, environmental and socioeconomic threats to citrus lime production. J Plant Dis Protect 125(4):339–356

    Article  Google Scholar 

  • Eun CH, Kim IJ (2021) Genome-wide DNA polymorphisms of Citrus unshiu Marc. cv. Miyagawa-wase cultivated in different regions based on whole-genome re-sequencing. Plant Biotech Rep 15:551–559

    Article  CAS  Google Scholar 

  • Eun CH, Kim IJ (2022) The citrus mutant Jedae-unshiu induced by gamma irradiation exhibits a unique fruit shape and increased flavonoid content. Plants 11:1337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge H, Li Y, Fu H, Long G, Luo L, Li R, Deng Z (2015) Production of sweet orange somaclones tolerant to citrus canker disease by in vitro mutagenesis with EMS. Plant Cell Tiss Organ Cult 123:29–38

    Article  CAS  Google Scholar 

  • Gulsen O, Uzun A, Pala H, Canilhos E, Kafa G (2007) Development of seedless and Mal seco tolerant mutant lemons through budwood irradiation. Sci Hort 112:184–190

    Article  Google Scholar 

  • Guo X, Zhang Y, Tu Y, Wang Y, Cheng W, Yang Y (2018) Overexpression of an EIN3-binding F-box protein2-like gene caused elongated fruit shape and delayed fruit development and ripening in tomato. Plant Sci 272:131–141

    Article  CAS  PubMed  Google Scholar 

  • Healey A, Furtado A, Cooper T, Henry RJ (2014) Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species. Plant Meth 10:21

    Article  Google Scholar 

  • Hui W, Zheng H, Fan J et al (2022) Genome-wide characterization of the MBF1 gene family and its expression pattern in different tissues and stresses in Zanthoxylum armatum. BMC Genom 23:652

    Article  CAS  Google Scholar 

  • Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao SJ (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants 9(4):491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang F, Lopez A, Jeon S et al (2019) Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Hortic Res 6:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Meth 12:357–360

    Article  CAS  Google Scholar 

  • Kim JH, Handayani E, Wakana A, Sato M, Miyamoto M, Miyazaki R, Zhou X, Sakai K, Mizunoe Y, Shigyo M et al (2020) Distribution and evolution of Citrus accessions with S3 and/or S11 alleles for self-incompatibility with an emphasis on sweet orange [Citrus sinensis (L.) Osbeck; SfS3 or SfS3sm]. Genet Resour Crop Evol 67:2101–2117

    Article  CAS  Google Scholar 

  • Lai X, Chahtane H, Martin-Arevalillo R, Zubieta C, Parcy F (2020) Contrasted evolutionary trajectories of plant transcription factors. Curr Opin Plant Biol 54:101–107

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Wang C, Long D, Jiang Y, He L, Wang Z, Ma X, Bai F, Liu J, Wu L, Song F (2022) Genome-wide identification, bioinformatics characterization and functional analysis of pectin methylesterase inhibitors related to low temperature-induced juice sac granulation in navel orange (Citrus sinensis Osbeck). Sci Hort 298:110983

    Article  CAS  Google Scholar 

  • Liu Y, You S, Taylor-Teeples M, Li WL, Schuetz M, Brady SM, Douglasa CJ (2014) BEL1-LIKE HOMEODOMAIN6 and KNOTTED Arabidopsis Thaliana7 interact and regulate secondary cell wall formation via repression of REVOLUTA. Plant Cell 26:4843–4861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Zhang W, Long S, Zhao C (2021) Maintenance of cell wall integrity under high salinity. Int J Mol Sci 22:3260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu N, Yang W, Li X, Zhao P, Liu Y, Guo L, Huang L, Gao W (2022a) Comparison of characterization and antioxidant activity of different citrus peel pectins. Food Chem 386:132683

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Li Y, Fang H, Huang B, Zhao C, Sun C, Li S, Chen K (2022b) Genome-wide identification and expression analysis of MATE gene family in citrus fruit (Citrus clementina). Genomics 114(5):110446

    Article  CAS  PubMed  Google Scholar 

  • Liu DH, Luo Y, Han H, Liu YZ, Alam SM, Zhao HX, Li YT (2022c) Genome-wide analysis of citrus TCP transcription factors and their responses to abiotic stresses. BMC Plant Biol 22:325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahmoud GA, El-Tobgy KMK, Abo-El-Seoud M (2010) Application of combined biocides and gamma radiation for kee** good quality stored grapefruits. Archiv Phytopath Plant Protec 43:712–721

    Article  CAS  Google Scholar 

  • Maluszynski M, Nichterlein K, Van Zanten L, Ahloowalia BS (2000) Officially released mutant varieties—the FAO/IAEA database. Mut Breed Rev 12(1):1–84

    Google Scholar 

  • Mariana BD, Arisah H, Yenni Y, Selvawajayant M (2018) Seedless fruit pummelo induced by gamma ray irradiation: fruit morphological characters and stability evaluation. Biodiversitas 19:706–711

    Article  Google Scholar 

  • Medina-Puche L, Martínez-Rivas FJ, Molina-Hidalgo FJ, García-Gago JA, Mercado JA, Caballero JL, Munoz-Blanco J, Blanco-Portales R (2021) Ectopic expression of the atypical HLH FaPRE1 gene determines changes in cell size and morphology. Plant Sci 305:110830

    Article  CAS  PubMed  Google Scholar 

  • Moussa JP (2006) Role of gamma irradiation in regulation of NO3 level in rocket (Eruca vescaria subsp. sativa) plants. Russ J Plant Physiol 53:193–197

    Article  CAS  Google Scholar 

  • Ollitrault P, Ahmed D, Costantino G, Evrard JC, Cardi C, Mournet P, Perdereau A, Froelicher Y (2021) Segregation distortion for male parents in high density genetic maps from reciprocal crosses between two self-incompatible cultivars confirms a gametophytic system for self-incompatibility in citrus. Agriculture 11:379

    Article  CAS  Google Scholar 

  • Peng W, Yang Y, Xu J, Peng E, Dai S, Dai L, Wang Y, Yi T, Wang B, Li D, Song N (2022) TALE transcription factors in sweet orange (Citrus sinensis): genomewide identifcation, characterization, and expression in response to biotic and abiotic stresses. Front Plant Sci 12:814252

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiao S, Xu Y, Hu Q, Dong W, He S, Qi X, Sun Y (2022) Transcriptome analysis of sponge gourd (Luffa cylindrica) reveals candidate genes associated with fruit size. Agronomy 12:1810

    Article  CAS  Google Scholar 

  • Raveh E, Goldenberg L, Porat R, Carmi N, Gentile A, La Malfa S (2020) Conventional breeding of cultivated citrus varieties. In: Gentile A, La Malfa S, Deng Z (eds) The citrus genome. Compendium of plant genomes. Springer, Cham, pp 33–48

    Google Scholar 

  • Rhodes J, Yang H, Moussu S, Boutrot F, Santiago J, Zipfel C (2021) Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2. Nat Commun 12:705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saadati S, Borzouei A, Rahemi MR, Khiabani BN (2022) Alteration of physiological and biochemical properties in leaves and fruits of pomegranate in response to gamma irradiation. Sci Rep 12:4312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Tanizawa Y, Mochizuki T, Nagasaki H, Yoshioka T, Toyoda A, Fujiyama A, Kaminuma E, Nakamura Y (2017) Draft sequencing of the heterozygous diploid genome of satsuma (Citrus unshiu Marc.) using a hybrid assembly approach. Front Genet 8:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Snoussi H, Askri H, Nacouzi D, Ouerghui I, Ananga A, Najar A, Kayal WE (2022) Comparative transcriptome profiling of salinity-induced genes in citrus rootstocks with contrasted salt tolerance. Agriculture 12:350

    Article  CAS  Google Scholar 

  • Song N, Cheng Y, Peng W, Peng E, Zhao Z, Liu T, Yi T, Dai L, Wang B, Hong Y (2021) Genome-wide characterization and expression analysis of the sbpbox gene family in sweet orange (Citrus sinensis). Int J Mol Sci 22(16):8918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starrantino A, Russo F, Donini B, Spina P (1988) Lemon mutants obtained by gamma irradiation of the nucellus cultured in vitro. Proc Int Soc Citric 2:231–235

    Google Scholar 

  • Sun L, Nasrullah KF, Nie Z, Xu J, Huang X, Sun J, Wang P (2022) Genome-wide identification and transcript analysis during fruit ripening of ACS gene family in sweet orange (Citrus sinensis). Sci Hort 294:110786

    Article  CAS  Google Scholar 

  • Sutarto I, Agisimanto D, Supriyanto A (2009) Development of promising seedless citrus mutants through gamma irradiation. In: Shu QY (ed) Induced Plant Mutations in the Genomics Era. Food and Agriculture Organization of the United Nations, Rome, p 306–308

  • Swingle WT, Reece PC (1967) The botany of citrus and its wild relatives. In: Reuther W, Webber HJ, Batchelor DL (eds) The Citrus Industry. University of California Press, Berkeley, CA, USA, pp 190–430

    Google Scholar 

  • Tanaka T (1977) Fundamental discussion of citrus classification. Studia Citrologia 14:1–6

    Google Scholar 

  • Torkamaneh D, Boyle B, Belzile F (2018) Efficient genome-wide genoty** strategies and data integration in crop plants. Theor Appl Genet 131:499–511

    Article  CAS  PubMed  Google Scholar 

  • Verger S, Chabout S, Gineau E, Mouille G (2016) Cell adhesion in plants is under the control of putative O-fucosyltransferases. Development 143:2536–2540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner TA, Kohorn BD (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13:303–318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U et al (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotech 32:656–662

    Article  CAS  Google Scholar 

  • Yan F, Gao Y, Pang X et al (2020) BEL1-LIKE HOMEODOMAIN4 regulates chlorophyll accumulation, chloroplast development, and cell wall metabolism in tomato fruit. J Exp Bot 71(18):5549–5561

    Article  CAS  PubMed  Google Scholar 

  • Ye LX, Gan ZM, Wang WF, Ai XY, **e ZZ, Hu CG, Zhang JZ (2020) Comparative analysis of the transcriptome, methylome, and metabolome during pollen abortion of a seedless citrus mutant. Plant Mol Biol 104:151–171

    Article  CAS  PubMed  Google Scholar 

  • Yue ZL, Liu N, Deng ZP, Zhang Y, Wu ZM, Zhao JL, Sun Y, Wang ZY, Zhan SW (2022) The receptor kinase OsWAK11 monitors cell wall pectin changes to fine-tune brassinosteroid signaling and regulate cell elongation in rice. Cur Biol 32(11):2454–2466

    Article  CAS  Google Scholar 

  • Yuning L, **anmei Y, **g**g Z, **ghua D, Luyang L, **tian L, Benshui S (2022) Transcriptome analyses reveal the potential mechanisms for color changes of a sweet orange peel induced by Candidatus Liberibacter asiaticus. Gene 839:146736

    Article  PubMed  Google Scholar 

  • Zhu Z, Chen G, Guo X, Yin W, Yu X, Hu J, Hu Z (2017) Overexpression of SlPRE2, an atypical bHLH transcription factor, affects plant morphology and fruit pigment accumulation in tomato. Sci Rep 7:5786

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by the Basic Science Research Program through the National Research Foundation of Korea [grant numbers: 2019R1A6A1A11052070, 2017R1D1A1B06034883, and 2020R1I1A1A01063379].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to In-Jung Kim.

Additional information

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.

Supplementary file1 (DOCX 155 KB)

Supplementary file2 (XLSX 146 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eun, CH., Kim, IJ. Genome-wide genetic variation and comparative transcriptome analyses of citrus mutant Jedae-unshiu and wild-type Citrus unshiu. Plant Biotechnol Rep 17, 111–121 (2023). https://doi.org/10.1007/s11816-022-00814-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11816-022-00814-5

Keywords

Navigation