Retrotransposon- and microsatellite sequence-associated genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride

Abstract

Allopolyploidization is considered an essential evolutionary process in plants that could trigger genomic shock in allopolyploid genome through activation of transcription of retrotransposons, which may be important in plant evolution. Two retrotransposon-based markers, inter-retrotransposon amplified polymorphism and retrotransposon-microsatellite amplified polymorphism and a microsatellite-based marker, inter simple sequence repeat were employed to investigate genomic changes in early generations of a newly synthesized allotetraploid Cucumis × hytivus Chen & Kirkbride (2n = 4x = 38) which was derived from crossing between cultivated cucumber C. sativus L. (2n = 2x = 14) and its wild relative C. hystrix Chakr. (2n = 2x = 24). Extensive genomic changes were observed, most of which involved the loss of parental DNA fragments and gain of novel fragments in the allotetraploid. Among the 28 fragments examined, 24 were lost while four were novel, suggesting that DNA sequence elimination is a relatively frequent event during polyploidization in Cucumis. Interestingly, of the 24 lost fragments, 18 were of C. hystrix origin, four were C. sativus-specific, and the remaining two were shared by both species, implying that fragment loss may be correlated with haploid DNA content (genome size) of diploid parents. Most changes were observed in the first generation after polyploidization (S(1)) and stably inherited in the subsequent three generations (S(2)-S(4)), indicating that genomic changes might be a rapid driving force for the stabilization of allotetraploids. Sequence analysis of 11 of the 28 altered DNA fragments showed that genomic changes in the allotetraploid occurred in both coding and non-coding regions, which might suggest that retrotransposons inserted into genome randomly and had a genome-wide effect on the allotetraploid evolution. Fluorescence in situ hybridization (FISH) analysis revealed a unique distribution of retrotransposon and/or microsatellite flanking sequences in mitotic and meiotic chromosomes, where the preferential FISH signals occurred in the centromeric and telomeric regions, implying that these regions were the possible hotspots for genomic changes.

Evolutionary Dynamics of Microsatellite Distribution in Plants: Insight from the Comparison of Sequenced Brassica, Arabidopsis and Other Angiosperm Species

“…This suggested that polyploidy may lead to the significant decrease in the frequency of microsatellites in the whole genome/non-coding sequences, which corresponds to the negative correlation between microsatellite frequency and both genome/non-coding sequences size and TEs content observed in this and other studies [8], [25]. This result is reasonable as polyploidy is often accompanied by the proliferation [28], [29], [30], [31] of TEs (which rarely contain microsatellites [25] and show a tendency to insert into some microsatellites, such as AT-rich repeats [32], [33]), the loss [20], [34], [35], [36], [37], [38] of genes (those are rich in microsatellites [25]), and the direct elimination [39], [40], [41], [42], [43], [44] of some microsatellites; these genomic changes can thus lead to a significant decrease in the frequency of microsatellites.…”

Transcriptome shock in an interspecific F1 triploid hybrid of Oryza revealed by RNA sequencing

“…The combination of divergent genomes within a hybrid can lead to immediate and profound genome modifications in myriad ways, including both structural (chromosomal and molecular) (Shen et al 2005; Doyle et al ; Soltis and Soltis ; Jiang et al ) and epigenetic (Chen et al ), which together may result in heritable changes in gene expression and phenotypic novelties important for species establishment and diversification (Doyle et al ; Hegarty and Hiscock ; Soltis and Soltis ; Tang et al ; Abbott and Rieseberg ; Abbott et al ; Cheng et al ; Xu et al ). Recent studies in both naturally occurring and synthetic (human‐made) homoploid and allopolyploid hybrids have revealed that global transcriptomic change induced by the merge of divergent parental genomes is a general phenomenon, which has been termed “transcriptome shock” (Hegarty et al ; Buggs et al ).…”

Retrotransposons Represent the Most Labile Fraction for Genomic Rearrangements in Polyploid Plant Species

“…A further in-depth analysis of Triticeae polyploids additionally revealed that the larger genome (comparing DNA content per haploid genome) is usually more affected independently of its maternal or paternal status [Bento et al, 2011]. Jiang et al [2011] also corroborated this suggestion through an IRAP and REMAP study of the neosynthesised Cucumis allotetraploid, which revealed that 18% of the rearranged bands corresponded mainly to a loss from the larger parental genome.…”