Absence of major epigenetic and transcriptomic changes accompanying an interspecific cross between peach and almond

Abstract

Hybridization has been widely used in breeding of cultivated species showing low genetic variability, such as peach (Prunus persica). The merging of two different genomes in a hybrid often triggers a so-called “genomic shock” with changes in DNA methylation and in the induction of transposable element expression and mobilization. Here, we analysed the DNA methylation and transcription levels of transposable elements and genes in leaves of Prunus persica and Prunus dulcis and in an F1 hybrid using high-throughput sequencing technologies. Contrary to the “genomic shock” expectations, we found that the overall levels of DNA methylation in the transposable elements in the hybrid are not significantly altered compared with those of the parental genomes. We also observed that the levels of transcription of the transposable elements in the hybrid are in most cases intermediate as compared with that of the parental species and we have not detected cases of higher transcription in the hybrid. We also found that the proportion of genes whose expression is altered in the hybrid compared with the parental species is low. The expression of genes potentially involved in the regulation of the activity of the transposable elements is not altered. We can conclude that the merging of the two parental genomes in this Prunus persica x Prunus dulcis hybrid does not result in a “genomic shock” with significant changes in the DNA methylation or in the transcription. The absence of major changes may facilitate using interspecific peach x almond crosses for peach improvement.

References

[1] Mason AS, Batley J . Creating new interspecific hybrid and polyploid crops. Trends Biotechnol. 2015; 33: 436-41.

[2] Nieto Feliner G, Casacuberta J, Wendel JF . Genomics of evolutionary novelty in hybrids and Polyploids. Front Genet. 2020; 11: 792.

[3] Comai L, Madlung A, Josefsson C et al. Do the different parental ‘heteromes’ cause genomic shock in newly formed allopolyploids? Philos Trans R Soc Lond Ser B Biol Sci . 2003; 358: 1149-55.

[4] Buggs RJ, Doust AN, Tate JA et al. Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity. 2009; 103: 73-81.

[5] Hegarty MJ, Barker GL, Wilson ID et al. Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. Curr Biol. 2006; 16: 1652-9.

[6] Yoo MJ, Szadkowski E, Wendel JF . Homoeolog expression bias and expression level dominance in allopolyploid cotton. Heredity. 2013; 110: 171-80.

[7] Mhiri C, Parisod C, Daniel J et al. Parental transposable element loads influence their dynamics in young Nicotiana hybrids and allotetraploids. New Phytol. 2019; 221: 1619-33.

[8] Parisod C, Salmon A, Zerjal T et al. Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina . New Phytol. 2009; 184: 1003-15.

[9] Paz RC, Rendina González AP, Ferrer MS et al. Short-term hybridisation activates Tnt1 and Tto1 Copia retrotransposons in wild tuber-bearing Solanum species. Plant Biol. 2015; 17: 860-9.

[10] Wang HY, Tian Q, Ma YQ et al. Transpositional reactivation of two LTR retrotransposons in rice-Zizania recombinant inbred lines (RILs). Hereditas. 2010; 147: 264-77.

[11] Senerchia N, Felber F, Parisod C . Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation. Proc R Soc B Biol Sci. 2015; 282: 20142874.

[12] Ungerer MC, Strakosh SC, Zhen Y . Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol. 2006; 16: R872.

[13] McClintock B. The significance of responses of the genome to challenge. Science. 1984; 226: 792-801.

[14] Fultz D, Slotkin RK . Exogenous transposable elements circumvent identity-based silencing, permitting the dissection of expression-dependent silencing. Plant Cell. 2017; 29: 360-76.

[15] Deniz Ö, Frost JM, Branco MR . Regulation of transposable elements by DNA modifications. Nat Rev Genet. 2019; 20: 417-31.

[16] Gutzat R, Mittelsten Scheid O . Epigenetic responses to stress: triple defense? Curr Opin Plant Biol. 2012; 15: 568-73.

[17] Ding M, Chen ZJ. Epigenetic perspectives on the evolution and domestication of polyploid plant and crops. Curr Opin Plant Biol. 2018;42:37-48.

[18] Song Q, Zhang T, Stelly DM et al. Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol. 2017; 18: 99.

[19] Ni Z, Kim ED, Ha M et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature. 2009; 457: 327-31.

[20] Yaakov B, Kashkush K . Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome. 2011; 54: 42-9.

[21] Groszmann M, Greaves IK, Albertyn ZI et al. Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci U S A. 2011; 108: 2617-22.

[22] Ha M, Lu J, Tian L et al. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci U S A. 2009; 106: 17835-40.

[23] Göbel U, Arce A, He F et al. Robustness of transposable element regulation but no genomic shock observed in interspecific Arabidopsis hybrids. Genome Biol Evol. 2018; 10: 1403-15.

[24] Kawakami T, Dhakal P, Katterhenry AN et al. Transposable element proliferation and genome expansion are rare in contemporary sunflower hybrid populations despite widespread transcriptional activity of LTR retrotransposons. Genome Biol Evol. 2011; 3: 156-67.

[25] Arús P, Verde I, Sosinski B et al. The peach genome. Tree Genet Genomes. 2012; 8: 531-47.

[26] Donoso JM, Eduardo I, Picañol R et al. High-density mapping suggests cytoplasmic male sterility with two restorer genes in almond × peach progenies. Hortic Res. 2015; 2: 15016.

[27] Donoso JM, Picañol R, Serra O et al. Exploring almond genetic variability useful for peach improvement: mapping major genes and QTLs in two inter-specific almond • peach populations. Mol Breed. 2016; 36: 16.

[28] Hodel RGJ, Zimmer E, Wen J . A phylogenomic approach resolves the backbone of Prunus (Rosaceae) and identifies signals of hybridization and allopolyploidy. Mol Phylogenet Evol. 2021; 160: 107118.

[29] Alioto T, Alexiou KG, Bardil A et al. Transposons played a major role in the diversification between the closely related almond and peach genomes: results from the almond genome sequence. Plant J. 2020; 101: 455-72.

[30] Velasco D, Hough J, Aradhya M et al. Evolutionary genomics of peach and almond domestication. G3 (Bethesda). 2016; 6: 3985-93.

[31] Marimon N, Luque J, Arús P et al. Fine mapping and identification of candidate genes for the peach powdery mildew resistance gene Vr3. Hortic Res. 2020; 7: 175.

[32] Zakrzewski F, Schmidt M, Van Lijsebettens M et al. DNA methylation of retrotransposons, DNA transposons and genes in sugar beet (Beta vulgaris L.) . Plant J. 2017; 90: 1156-75.

[33] Zemach A, Kim MY, Silva P et al. Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci U S A. 2010; 107: 18729-34.

[34] Verde I, Jenkins J, Dondini L et al. The peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics. 2017; 18: 225.

[35] Leibman D, Kravchik M, Wolf D et al. Differential expression of cucumber RNA-dependent RNA polymerase 1 genes during antiviral defence and resistance. Mol Plant Pathol. 2018; 19: 300-12.

[36] Wang N, Zhang D, Wang Z et al. Mutation of the RDR1 gene caused genome-wide changes in gene expression, regional variation in small RNA clusters and localized alteration in DNA methylation in rice. BMC Plant Biol. 2014; 14: 177.

[37] Rajendrakumar P, Hariprasanna K, Seetharama N . Prediction of Heterosis in crop plants-status and prospects. Am J Exp Agric. 2015; 9: 1-16.

[38] Warschefsky E, Penmetsa RV, Cook DR et al. Back to the wilds: tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am J Bot. 2014; 101: 1791-800.

[39] Micheletti D, Dettori MT, Micali S et al. Whole-genome analysis of diversity and SNP-major gene association in peach Germplasm. PLoS One. 2015; 10: e0136803.

[40] Martínez-Gómez P, Rubio M, Dicenta F et al. Resistance to plum pox virus (RB3.30 isolate) in a group of California almonds and transfer of resistance to peach. J Am Soc Hortic Sci. 2004; 129: 544-8.

[41] Rothkegel K, Espinoza A, Sanhueza D et al. Identification of DNA methylation and Transcriptomic profiles associated with fruit Mealiness in Prunus persica (L.) Batsch. Front Plant Sci. 2021; 12: 684130.

[42] Inglis PW, Pappas MCR, Resende LV et al. Fast and inexpensive protocols for consistent extraction of high quality DNA and RNA from challenging plant and fungal samples for high-throughput SNP genotyping and sequencing applications. PLoS One. 2018; 13: e0206085.

[43] Doyle JJ, Doyle JL . Isolation of plant DNA from fresh tissue. Focus. 1990; 12: 13-5.

[44] Krueger F, Andrews SR. Bismark: a flexible aligner and methylation caller for bisulfite-Seq applications. Bioinformatics. 2011;27:1571-2.

[45] Catoni M, Tsang JM, Greco AP et al. DMRcaller: a versatile R/Bioconductor package for detection and visualization of differentially methylated regions in CpG and non-CpG contexts. Nucleic Acids Res. 2018; 46: e114.

[46] Benjamini Y, Hochberg Y . Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol. 1995; 57: 289-300.

[47] Vendrell-Mir P, López-Obando M, Nogué F et al. Different families of Retrotransposons and DNA transposons are actively transcribed and may have transposed recently in Physcomitrium (Physcomitrella) patens. Front Plant Sci. 2020; 11: 1274.

[48] Langmead B, Salzberg SL . Fast gapped-read alignment with bowtie 2. Nat Methods. 2012; 9: 357-9.