Skip to main content
Log in

Cis-regulated additively expressed genes play a fundamental role in the formation of triploid loquat (Eriobotrya japonica (Thunb.) Lindl.) Heterosis

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

Triploid loquat (Eriobotrya japonica (Thunb.) Lindl.) has greater vigor than their respective diploid and tetraploid parents, but the molecular basis of this triploid heterosis remains unclear. Recent studies have suggested that DNA methylation is involved in heterosis, which is a recognized method of suppressing gene expression. However, our previous studies revealed a trend of increased DNA methylation in triploid loquat hybrids compared to their parents. To elucidate the mechanism of triploid loquat heterosis, we investigated the levels and regulation of relative gene expression between hybrid and parental lines using RNA-Seq technology. We found that gene expression in the hybrid lines was down-regulated and gene expression analysis revealed that approximately 94.56 and 86.97% were expressed additively in triploid-A and triploid-B, respectively. Analyses of the allele-specific gene expression in the hybrids revealed significantly more Longquan-1 alleles were preferentially expressed in the two hybrid lines. Further analysis of cis- and trans-regulatory effects showed that gene expression variation between parental alleles is largely attributable to cis-regulatory variation in triploid loquat and analyses of genes belonging to cis-regulatory variation showed that 88–90% of cis genes contributed to an additive expression pattern. Taken together, our results suggest that gene expression variation in triploid loquat fundamentally cis-regulated may play a dominant role in triploid loquat heterosis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  PubMed  CAS  Google Scholar 

  • Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing or duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Auger DL, Gray AD, Ream TS, Kato A, Coe EH, Birchler JA (2005) Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics 169:389–97

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bell GDM, Kane NC, Rieseberg LH, Adams KL (2013) RNA-Seq analysis of allele-specific expression, hybrid effects, and regulatory divergence in hybrids compared with their parents from natural populations. Genom Biol Evol 5(7):1309–1323

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57(1):289–300

    Google Scholar 

  • Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bruce AB (1910) The mendelian theory of heredity and the augmentation of vigor. Science 32:627–628

    Article  PubMed  CAS  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15(2):57–71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482

    Article  PubMed  CAS  Google Scholar 

  • Coors JG, Pandey S (1999) The genetics and exploitation of heterosis in crops. American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America, Madison

    Google Scholar 

  • Crow JF (1999) Dominance and overdominance. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. American Society of Agronomy, Madison, pp 49–58

    Google Scholar 

  • Cubillos FA, Stegle O, Grondin C, Canut M, Tisné S, Gy I, Loudet O (2014) Extensive cis-regulatory variation robust to environmental perturbation in Arabidopsis. Plant Cell 26:4298–310

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • East EM (1909) The distinction between development and heredity in inbreeding. Am Nat 43:173–181

    Article  Google Scholar 

  • Feng SQ, Chen XL, Wu SJ, Chen XS (2015) Recent advances in understanding plant heterosis. Agric Sci 6:1033–1038

    CAS  Google Scholar 

  • Fujimoto R, Taylor JM, Shirasawa S, Peacock WJ, Dennis ES (2012) Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci USA 109:7109–7114

    Article  PubMed  PubMed Central  Google Scholar 

  • Ge X, Chen W, Song S, Wang W, Hu S, Yu J (2008) Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biol 8:114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gibney ER, Nolan CM (2010) Epigenetics and gene expression. Heredity 105:4–13

    Article  PubMed  CAS  Google Scholar 

  • Groszmann M, Greaves IK, Albertyn ZI, Scofield GN, Peacock WJ, Dennis ES (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci USA 108:2617–2622

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo M, Rafalski JA (2013) Gene expression and heterosis in maize hybrids. In: Chen ZJ, Birchler JA (eds) Polyploid and hybrid genomics. Wiley, New York, pp 59–84

    Chapter  Google Scholar 

  • Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant cell 16:1707–1716

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  PubMed  CAS  Google Scholar 

  • Guo H, Mendrikahy JN, Xie L, Deng J, Lu Z, Wu J, Li X, Shahid MQ, Liu X (2017) Transcriptome analysis of neo-tetraploid rice reveals specific differential gene expressions associated with fertility and heterosis. Sci Rep 7:40139

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Article  PubMed  CAS  Google Scholar 

  • Hofmann NR (2012) A global view of hybrid vigor: DNA methylation, small RNAs, and gene expression. Plant Cell 24:841

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu X, Wang H, Diao X, Liu Z, Li K, Wu Y, Liang Q, Wang H, Huang C (2016) Transcriptome profiling and comparison of maize ear heterosis during the spikelet and floret differentiation stages. BMC Genom 17:959

    Article  CAS  Google Scholar 

  • Huang Y, Zhang L, Zhang J, Yuan D, Xu C, Li X, Zhou D, Wang S, Zhang Q (2006) Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol 62:579–591

    Article  PubMed  CAS  Google Scholar 

  • Huang W, Ye J, Zhang J, Lin Y, He M, Huang J (2016) Transcriptome analysis of Chlorella zofingiensis to identify genes and their expressions involved in astaxanthin and triacylglycerol biosynthesis. Algal Res 17:236–243

    Article  Google Scholar 

  • Jackson S, Chen ZJ (2010) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13(2):153–159

    Article  PubMed  CAS  Google Scholar 

  • Khatib H (2007) Is it genomic imprinting or preferential expression? Bioessays 29(10):1022–1028

    Article  PubMed  CAS  Google Scholar 

  • Kyndt T, Denil S, Haegeman A, Trooskens G, De Meyer T, Van Criekinge W, Gheysen G (2012) Transcriptome analysis of rice mature root tissue and root tips in early development by massive parallel sequencing. J Exp Bot 63:2141–2157

    Article  PubMed  CAS  Google Scholar 

  • Leitch IJ, Bennett MD (1997) Polyploidy in angiosperms. Trends Plant Sci 2:470–476

    Article  Google Scholar 

  • Lemos B, Araripe LO, Fontanillas P, Hartl DL (2008) Dominance and the evolutionary accumulation of cis- and trans-effects on gene expression. Proc Natl Acad Sci USA 105:14471–14476

    Article  PubMed  PubMed Central  Google Scholar 

  • Li W, Zhu H, Challa GS, Zhang Z (2013) A non-additive interaction in a single locus causes a very short root phenotype in wheat. Theor Appl Genet 126:1189–1200

    Article  PubMed  CAS  Google Scholar 

  • Li X, Shahid MQ, Wu J, Wang L, Liu X, Lu Y (2016) Comparative small RNA analysis of pollen development in autotetraploid and diploid rice. Int J Mol Sci 17:499

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li X, Shahid MQ, Xia J, Lu Z, Fang N, Wang L, Wu J, Chen Z, Liu X (2017) Analysis of small RNAs revealed differential expressions during pollen and embryo sac development in autotetraploid rice. BMC Genom 18:129

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆Ct method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104

    Article  PubMed  CAS  Google Scholar 

  • McManus CJ, Coolon JD, Duff MO, Eipper-Mains J, Graveley BR, Wittkopp PJ (2010) Regulatory divergence in Drosophila revealed by mRNA-sEq. Genom Res 20:816–25

    Article  CAS  Google Scholar 

  • Meyer S, Pospisil H, Scholten S (2007) Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol Biol 63:381–391

    Article  PubMed  CAS  Google Scholar 

  • Meyer RC, Witucka-Wall H, Becher M, Blacha A, Boudichevskaia A, Dörmann P, Fiehn O, Friedel S, von Korff M, Lisec J, Melzer M, Repsilber D, Schmidt R, Scholz M, Selbig J, Willmitzer L, Altmann T (2012) Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. Plant J 71:669–683

    Article  PubMed  CAS  Google Scholar 

  • Mori A, Romero-Severson J, Severson DW (2007) Genetic basis for reproductive diapause is correlated with life history traits within the Culex pipiens complex. Insect Mol Biol 16(5):515–524

    PubMed  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Method 5:621–628

    Article  CAS  Google Scholar 

  • Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  PubMed  CAS  Google Scholar 

  • Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–37

    Article  PubMed  CAS  Google Scholar 

  • Paschold A, Jia Y, Marcon C, Lund S, Larson NB, Yeh CT, Ossowski S, Lanz C, Nettleton D, Schnable PS, Hochholdinger F (2012) Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents. Genom Res 22(12):2445–2454

    Article  CAS  Google Scholar 

  • Paun O, Fay MF, Soltis DE, Chase MW (2007) Genetic and epigenetic alterations after hybridization and genome doubling. Taxon 56:649–656

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronald J, Akey JM, Whittle J, Smith EN, Yvert G, Kruglyak L (2005) Simultaneous genotyping, gene-expression measurement, and detection of allele-specific expression with oligonucleotide arrays. Genom Res 15:284–291

    Article  CAS  Google Scholar 

  • Shi X, Ng DWK, Zhang C, Comai L, Ye W, Chen ZJ (2012) Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat Commun 3:950

    Article  PubMed  CAS  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Am Breeders Assoc Rep 4:296–301

    Google Scholar 

  • Soltis DE, Soltis PS (1999) Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol 14(9):348–352

    Article  PubMed  CAS  Google Scholar 

  • Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Song GS, Zhai HL, Peng YG, Zhang L, Wei G, Chen XY, Xiao YG, Wang L, Chen YJ, Wu B, Chen B, Zhang Y, Chen H, Feng XJ, Gong WK, Liu Y, Yin ZJ, Wang F, Liu GZ, Xu HL, Wei XL, Zhao XL, Ouwerkerk PBF, Hankemeier T, Reijmers T, Heijden RH, Lu CM, Wang M, Greef J, Zhu Z (2010) Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol Plant 3:1012–1025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Springer NM. Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genom Res 17:264–275

    Article  CAS  Google Scholar 

  • Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173:2199–2210

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM (2008) Gene expression analyses in maize in breeds and hybrids with varying levels of heterosis. BMC Plant Biol 8:33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Thiemann A, Fu J, Schrag TA, Melchinger AE, Frisch M, Scholten S (2010) Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L. Theor Appl Genet 120(2):401–13

    Article  PubMed  CAS  Google Scholar 

  • Thiemann A, Fu J, Seifert F, Grant-Dwonton RT, Schrag TA, Pospisil H, Frisch M, Melchinger AE, Scholten S (2014) Genome-wide meta-analysis of maize heterosis reveals the potential role of additive gene expression at pericentromeric loci. BMC Plant Biol 14:88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tirosh I, Reikhav S, Levy AA, Barkai N (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324:659–662

    Article  PubMed  CAS  Google Scholar 

  • Wang WX (2008) Genome variation and DNA methylation analysis of natural and artificial triploid loquats. Southwest University, Chongqing

    Google Scholar 

  • Wang J, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang J, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L, Chen ZJ (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang H, Fang Y, Wang L, Zhu W, Ji H, Wang H, Xu S, Sima Y (2015) Heterosis and differential gene expression in hybrids and parents in Bombyx mori by digital gene expression profiling. Sci Rep 5:8750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Shahid MQ, Lin S, Chen C, Hu C (2017) Footprints of domestication revealed by RAD-tag resequencing in loquat: SNP data reveals a non-significant domestication bottleneck and a single domestication event. BMC Genom 18:354

    Article  Google Scholar 

  • Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G, Zhai H, Peng Y, Li D, Xu H, Wei X, Cao M, Deng H, Xin Y, Yuan L, Yu J, Zhu Z, Zhu L (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci 106:7695–7701

    Article  PubMed  PubMed Central  Google Scholar 

  • Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13:59–69

    Article  CAS  Google Scholar 

  • Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430:85–88

    Article  PubMed  CAS  Google Scholar 

  • Wu D, Fan W, He Q, Guo Q, Spano AJ, Wang Y, Timko MP, Liang G (2015) Genetic diversity of loquat (Eriobotrya japonica (Thunb.) Lindl.) native to Guizhou Province (China) and its potential in the genetic improvement of domesticated cultivars. Plant Mol Biol Rep 33:952–961

    Article  CAS  Google Scholar 

  • Yoo M, Szadkowski E, Wendel J (2013) Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity 110:171–80

    Article  PubMed  CAS  Google Scholar 

  • Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang Q, Saghai Maroof MA (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhai R, Feng Y, Wang H, Zhan X, Shen X, Wu W, Zhang Y, Chen D, Dai G, Yang Z, Cao L, Cheng S (2013a) Transcriptome analysis of rice root heterosis by RNA-SEq. BMC Genom 14:19

    Article  CAS  Google Scholar 

  • Zhai R, Feng Y, Zhan X, Shen X, Wu W, Yu P, Zhang Y, Chen D, Wang H, Lin Z, Cao L, Cheng S (2013b) Identification of transcriptome SNPs for assessing allele-specific gene expression in a superhybrid rice Xieyou9308. PLoS One 8:e60668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Borevitz JO (2009) Global analysis of allele-specific expression in Arabidopsis thaliana. Genetics 182:943–954

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang HY, He H, Chen LB, Li L, Liang MZ, Wang XF, Liu XG, He GM, Chen RS, Ma LG, Deng XW (2008) A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant 1(5):720–731

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Liu Y, Xia EH, Yao QY, Liu XD, Gao LZ (2015) Autotetraploid rice methylome analysis reveals methylation variation of transposable elements and their effects on gene expression. Proc Natl Acad Sci USA 112:E7022–9

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Biomarker Technologies, Beijing, China for providing technical support.

Funding

This work was supported by National Science and Technology Support Projects (2013BAD02B02-1), State Spark-Program (2015GA811003), Central Fiscal for Forestry Science and Technology Extension and Demonstration Project (Chongqing forest research extension 2016-03) and the program of Chongqing forestry key scientific and technological projects (Chongqing forest research 2016-10), Basic and frontier research project of Chongqing (cstc2014jcyjA80006).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qigao Guo or Guolu Liang.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Wu, D., Wang, L. et al. Cis-regulated additively expressed genes play a fundamental role in the formation of triploid loquat (Eriobotrya japonica (Thunb.) Lindl.) Heterosis. Mol Genet Genomics 293, 967–981 (2018). https://doi.org/10.1007/s00438-018-1433-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-018-1433-6

Keywords

Navigation