Transpositional reactivation of the Dart transposon family in rice lines derived from introgressive hybridization with Zizania latifolia
© Wang et al; licensee BioMed Central Ltd. 2010
Received: 18 March 2010
Accepted: 26 August 2010
Published: 26 August 2010
It is widely recognized that interspecific hybridization may induce "genome shock", and lead to genetic and epigenetic instabilities in the resultant hybrids and/or backcrossed introgressants. A prominent component involved in the genome shock is reactivation of cryptic transposable elements (TEs) in the hybrid genome, which is often associated with alteration in the elements' epigenetic modifications like cytosine DNA methylation. We have previously reported that introgressants derived from hybridization between Oryza sativa (rice) and Zizania latifolia manifested substantial methylation re-patterning and rampant mobilization of two TEs, a copia retrotransposon Tos17 and a MITE mPing. It was not known however whether other types of TEs had also been transpositionally reactivated in these introgressants, their relevance to alteration in cytosine methylation, and their impact on expression of adjacent cellular genes.
We document in this study that the Dart TE family was transpositionally reactivated followed by stabilization in all three studied introgressants (RZ1, RZ2 and RZ35) derived from introgressive hybridization between rice (cv. Matsumae) and Z. latifolia, while the TEs remained quiescent in the recipient rice genome. Transposon-display (TD) and sequencing verified the element's mobility and mapped the excisions and re-insertions to the rice chromosomes. Methylation-sensitive Southern blotting showed that the Dart TEs were heavily methylated along their entire length, and moderate alteration in cytosine methylation patterns occurred in the introgressants relative to their rice parental line. Real-time qRT-PCR quantification on the relative transcript abundance of six single-copy genes flanking the newly excised or inserted Dart-related TE copies indicated that whereas marked difference in the expression of all four genes in both tissues (leaf and root) were detected between the introgressants and their rice parental line under both normal and various stress conditions, the difference showed little association with the presence or absence of the newly mobilized Dart-related TEs.
Introgressive hybridization has induced transpositional reactivation of the otherwise immobile Dart-related TEs in the parental rice line (cv. Matsumae), which was accompanied with a moderate alteration in the element's cytosine methylation. Significant difference in expression of the Dart-adjacent genes occurred between the introgressants and their rice parental line under both normal and various abiotic stress conditions, but the alteration in gene expression was not coupled with the TEs.
It is widely recognized that hybridization between genetically differentiated natural plant populations may cause structural genomic changes (e.g., via homoeologous or ectopic recombination) as well as perturbation of epigenetic state of the recipient genome (e.g., DNA methylation), and both may result in heritable phenotypic novelties [1–7]. These findings are consistent with Barbara McClintock's insight of "genome shock", which proposed that crossing of different organismal species may cause restructuring of the resultant hybrid genome, and which may represent a facet of adaptive response by plants under specific circumstances . A major cause underlying the genomic shock symptom is transcriptional and transpositional reactivation of otherwise cryptic transposable elements (TEs) in the hybrid genome. The reactivation of TEs is often coupled with disruption of chromatin-based epigenetic controlling mechanisms in the hybrid genome, like loss or re-patterning of cytosine methylation and compromised targeting by small interference (si) RNAs [9–11]. Indeed, several studies in both animals and plants have provided compelling empirical evidence in support of the "TE-epigenetic" basis of genome shock [12–16].
At least circumstantial evidence has indicated that for the hybridization- associated genomic shock to occur, a symmetric hybrid genome is not a prerequisite; instead, introgression or integration of "foreign" chromatin or DNA segments via introgressive hybridization or other means (e.g., transgenic) might as well produce the "shocking" effects on the recipient genome . For example, it was shown in cultured animal cells that random integration of pieces of foreign DNA can cause the host genome to undergo extensive and genome-wide alterations in cytosine methylation of both cellular genes and TE-related DNA repeats [17, 18]. We have demonstrated that introgression of small amount of chromatin of Zizania latifolia (a distantly related species to Oryza) into rice has caused an array of genetic and epigenetic instabilities in the recipient rice genome [19, 20], and in particular, rampant mobilization of a copia retrotransposon Tos17 and a MITE (mPing) . Given the recent finding that the cellular controlling mechanisms for TE activity are likely individualized , it is interesting to explore whether TE reactivation in the rice-Zizania introgressants was confined to these two elements or other TEs also experienced reactivation.
The rice Dart transposon family belongs to the hAT superfamily of class II TEs, and which was first characterized by Fujino and colleagues . Dart was found as transcriptionally active in several rice tissues . Moreover, both Dart and its deletion-derivative called nDart can be transpositionally active in certain rice genotypes that harbour active Dart, even under normal growing conditions . In addition, the element's activity was correlated with its cytosine methylation state, and epigenetically silenced Dart copies can be reactivated by 5-azacytidine treatment [25, 26]. Apparently, except for Tos17 and mPing, the Dart/nDart represents another family of highly active TEs endogenous to the rice genome.
The aim of this study was to investigate (1) whether the Dart TE family was transpositionally reactivated in the same set of rice-Zizania introgressants that showed rampant mobilization of Tos17 and mPing ; (2) whether the element's activity was correlated with its cytosine methylation state; and (3) whether excision and reinsertion of the element copies impacted expression of their adjacent genes under normal or various abiotic stress conditions.
The Dart transposon family was transpositionally reactivated in the rice-Zizaniaintrogressants
Excision sites of Dart-related TEs identified by transposons-display (TD) (designated as Dart-TDE) in the rice-Zizania introgressants
Locus-specific primers (5'-3')
De novo insertion sites of Dart-related TEs identified by transposons-display (TD) (designated as Dart-TDI) in the rice-Zizania introgressants
Position of insertion sites
Locus-specific primers (5'-3')
Chr.3; position: 2726981;
Chr.5; position: 29238540;
Validation and chromosomal location of the Dart excisions and insertions by locus-specific PCR amplification and sequencing in the rice-Zizaniaintrogressants
For each of the putative excised and inserted loci, we designed locus-specific primer pairs specific to the flanks of the Dart elements based on the whole genome sequence of Nipponbare http://rgp.dna.affrc.go.jp (Tables 1 and 2). Note that the design of primers targeting the flanks did not entail that Nipponbare contains a copy of the Dart-related TE at each of the loci. PCR amplification by these locus-specific primers (e.g., Figure 2c) and sequencing of the amplicons verified that all the 15 excisions and 21 insertions were authentic, because the immediate contiguous flanks were intact for all the excisions and typical TSDs were identified for all the insertions (Tables 1 and 2). This locus-specific PCR amplification and sequencing results thus validated transpositional reactivation of the Dart-related elements in the rice-Zizania introgressants.
Cytosine methylation states of the Dart-related elements in the rice-Zizaniaintrogressants and their rice parental line
We next performed the second round restriction by adding each of the pair of isoschizomers, HpaII and MspI, to the BamHI-digests, and using probes specific to each of the three regions to assess their cytosine methylation state in the introgressants relative to Matsumae. We obtained the following results: (1) there had been no detectable internal truncations between the two BamHI sites, as no clear, smaller-sized bands than the expected 2232 bp were detected in this enzyme digest (Figure 4b, the body-region probe); (2) the body-region of the conserved, Dart-related elements was heavily methylated particularly by mCG in all the rice lines, introgressants and parental, as evidenced by the very similar hybridization patterns between BamHI-digest and BamHI+HapII-digest (Figure 4b, the body-region probe), albeit there were 11 5'-CCGG sites within this region of Dart-related elements, and hence several smaller-sized bands would have been detected if the relevant 5'-CCGG sites were hypomethylated (Figure 4a); (3) the only clear difference in the methylation state of the introgressants relative to Matsumae was that one introgressant (RZ35) showed hypermethylation as evidenced by the disappearance of several smaller-sized bands (Figure 4b, the body-region probe; marked by arrows); (4) the 5' region of the Dart-related elements was also heavily methylated by both mCG and mCNG in the all the lines because multiple bands were detected (Figure 4b, the 5' probe), as otherwise we would have predominantly detected a band <678 bp in length (restricted by BamHI at position 678 nt together with restriction by HpaII/MspI at one or more of the six 5'-CCGG sites at the 5'-terminus) (Figure 4a); (5) compared with Matsumae, CG demethylation in RZ1 and concomitant CG hypermethylation and CNG hypomethylation in RZ35 occurred in the 5'-region of Dart-related elements (Figure 4b, the 5' probe); (6) similar to the situation of 5'-region, the 3'-region of the Dart-related elements was also heavily methylated by both mCG and mCNG in all the lines (Figure 4b, the 3' probe), as otherwise we would have predominantly detected a band <656 bp in length (being restricted at position 2910 nt by BamHI together with one or more of the seven 5'-CCGG sites by HpaII/MspI at the 3'-terminus) (Figure 4a); (7) compared with Matsumae, CG demethylation in RZ2 and CNG demethylation in RZ35 occurred in the 3'-region of the Dart-related elements (Figure 4b, the 3' probe); (8) with regard to the methylation state of the 5' and 3' flanks of the Dart-related elements, it was deducible that they had a substantially lower methylation level relative to the Dart-related elements per se, as evidenced by the multiple small-sized bands detected by the Dart 5'- and 3'-region-specific probes (Figure 4b). Taken together the Southern blotting data of all three region-specific probes, it can be concluded that (1) the Dart-related TEs are heavily methylated throughout the entire length, but with their 5' and 3' flanks being relatively less methylated compared with the internal body-region, in all the rice lines studied; (2) to a moderate extent, methylation alteration including both hypo- and hypermethylation occurred in the introgressants relative to their rice parental line Matsumae.
Limited impact by mobility of the Dart-related TEs on expression of their adjacent genes under normal and abiotic stress conditions
Hybridization is prevalent in plants, which plays important roles in genome evolution, and may lead to speciation at both the homoploid level and followed by genome doubling (allopolyploid) [6, 7, 33–37]. Apart from direct transfer and recombinatory generation of genetic variations by hybridization, de novo genetic and epigenetic instabilities can be induced by the process per se, including transcriptional activation and mobilization of cryptic transposable elements (TEs) [15, 16, 29, 38–42]. Several lines of circumstantial evidence have indicated that introgression of DNA or chromatin fragments from an alien species into a recipient genome may also produce similar effects in causing genetic and epigenetic instabilities and generate novel phenotypes [11, 17]. We have reported previously that introgressive hybridization between rice (Oryza sativa) and Z. latifolia had induced rampant mobilization of two TEs, a copia-like LTR retrotransposon Tos17 and a MITE mPing [21, 43]. In this study, we extended the earlier findings and found that the Dart-related TEs were also transpositionally reactivated in the introgressants, although the elements were totally quiescent in the parental rice cultivar Matsumae. We validated the excisions and insertions by transposon-display (TEs) and sequencing, which ruled out genomic rearrangements as the major cause for the dramatically altered hybridization patterns detected by Southern blotting in the introgressants.
Although numerous studies have established correlative or causal links between TE activation and alteration in the element's cytosine methylation state [26, 27, 30, 44, 45], we found that the Dart-related TEs were similarly hypermethylated along their entire length in the introgressants and their rice parental line Matsumae. Nonetheless, moderate alteration in the methylation patterns was discernible in the introgressants. Furthermore, given that the introgressants were at the 9th-selfed generation and stabilized in both phenotype and DNA fingerprinting patterns , we could not rule out the possibility that in earlier generations of the introgressants (no longer available for study), more marked methylation remodelling might have occurred in the Dart-related TEs, which however were either largely reverted to the original pattern and/or those individuals with more drastically altered patterns had been purged out during the sexual reproduction, probably due to reduced fitness. Therefore, it remains a formal possibility that alteration in cytosine methylation had been associated with mobility of the Dart-related TEs in the introgressants, a scenario gaining increased empirical support in a vast range of TEs and organisms [9–11, 26, 28, 30, 46].
An array of studies in both plants and animals has established that activity of TEs, particularly LTR retrotransposons, may significantly impact expression and function of their adjacent genes [38, 41]. Nonetheless, other studies have indicated that the majority of newly transposed TEs particularly those with small-sizes like MITEs tended to insert into functionally neutral genomic regions and impose minor effects on their adjacent genes . We found in this study that the six single-copy protein-coding genes adjacent to the newly excised or inserted Dart-related TEs exhibited significantly altered expression in the introgressants relative to their rice parental line under both normal and several abiotic-stress conditions. However, the altered gene expression in the introgressants was not coupled with the TE excisions or insertions, suggesting that other regulatory mechanisms were responsible for the altered gene expression in the introgressants. Because unbiased amplifications between the introgressants and their rice parental line were observed when their genomic DNA was used as templates, it is likely that epigenetic regulation was involved. The observation that for most of the genes, these rice lines exhibited sharply differential response to 5-AC treatment corroborated this possibility, which also accords with our previous results showing that substantial re-patterning of cytosine methylation occurred in the introgressants for amny genomic loci . Further study is required to elucidate the exact molecular basis underlying the dramatically altered gene expression and their phenotypic consequence in these novel rice lines as a result of introgressive hybridization.
Results of this study have extended our previous findings by documenting that introgressive hybridization between rice and Z. latifolia has induced transpositional reactivation of another distinct family of cryptic TEs in the parental rice genome, namely, the Dart-related TEs, suggesting that introgression of chromatin from a realted alien species might have caused a general breakdown of the host cellular machinery responsible for repressive control of TE activity. Transposition of the Dart-related TEs was accompanied with a moderate alteration in the element's cytosine methylation in the introgressants. In addition, results of this study showed that extensive alteration in expression of a set of Dart-adjacent, protein-coding genes occurred in the introgressants relative to their rice parental line, under both normal and various abiotic stress conditions. Nonetheless, the alteration in gene expression was not coupled with excision or insertion of the Dart-related TEs, implicating other regulatory mechanism(s) was underpinning the changes in gene expression in these novel rice introgressants.
Three introgression lines (RZ1, RZ2 and RZ35) derived from a cross between rice (cv. Matsumae) and Zizania latifolia Griseb, were used in this study . The three stabilized introgressants (at the 9th selfed generation) were homogeneous in phenotype and DNA fingerprinting patterns, and exhibited heritable, novel morphological characteristics in multiple traits compared with their rice parental cultivar Matsumae [20, 21]. The introgressants were maintained along with their rice parental line (cv. Matsumae) by strict selfing in our laboratory.
Abiotic stress and 5-azacytidine treatments
Healthy and uniform seeds of three rice-Zizania introgressants (RZ1, RZ2 and RZ35) and their rice parental line cv. Matsumae were disinfected and thoroughly rinsed, and placed on petri-dishes covered with half-strength Murashige and Skoog (MS) medium in darkness at 25°C. For the three kinds of abiotic stress treatments, seedlings were grown to the 3-leaf-stage, and then aqueous solutions respectively containing 5 mM CuSO4 (heavy metal), 5 mM HgCl2 (heavy metal), 10 mM NaCl (salinity) and 10 mM NaHCO3 (alkaline) containing the half-strength MS medium were added, and grown for one more week. For cold stress, the 3-leaf-stage seedlings were grown in the medium at 12°C for one week. The 5-azacytidine (5-AC) treatment was conducted by treating the germinating seeds in the medium containing 50 mM 5-azacytidine (Sigma) for one week and then thoroughly rinsed with ddH2O and allowed the seedlings to grow in the medium up to the same stage as the other treatments. In all cases mock-control seedlings grown in the half-strength MS medium alone was included.
Southern blot analysis
Genomic DNA was isolated from leaf tissue of young seedlings at the same developmental stage from the various treatments and mock of the three rice-Zizania introgressants (RZ1, RZ2 and RZ35) and their rice parental line Matsumae by a modified CTAB method. To assess possible genetic changes in the patterns of the Dart-related TEs, the genomic DNA (~3 μg, per lane) of each line (the mock-control) was digested by HindIII. To test for possible alteration in cytosine methylation of the Dart-related TEs, the genomic DNA of each line (the mock-control) was first digested with BamHI (to delineate the Dart-related TEs into three regions, 5'-, 3'-, and body-regions; see Results), followed by a second round of digestion with a pair of isoschizomers, HpaII and MspI, that recognize the same sequence 5'-CCGG but with differential sensitivity to methylation of the two cytosine residues. Digested DNA were run on 1% agarose gel and transferred onto Hybond N+ nylon membrane (RPN 303B, Amersham-Pharmacia Biotech, Piscataway, New Jersey) by the alkaline transfer method recommended by the manufacturer.
In total, three pairs of primers specific respectively to the 5'-, 3'- and the body-region of the Dart-related TEs were designed to amplify the fragments to be used as hybridization probes. The primers are: (1) for the 5'-region of Dart-related TEs: Dart5'-forward: 5'- aaatagggcatgaaccccagc, Dart5'-reverse: 5'-ggtcgaaatcacccaaggtg; (2) for the 3'-region of Dart-related TEs: Dart3'-forward: 5'-tccagaccaaccccagtagaa, Dart3'-reverse: 5'-aaaaaaagcaaaggaaatgtataagg; (3) for the body-region of Dart-related TEs: Dart-body-forward: 5'-ctagagaggattatcttagcgtagttgtt, Dart-body-reverse: 5'-cttcttcttacctgtagtggggatag. Authenticity of the amplified fragments was verified by sequencing. The fragments were then agarose gel-purified and labelled with fluorescein-11-dUTP by the Gene Images random prime-labelling module (Amersham-Pharmacia Biotech). Hybridizations were done with the Gene Images CDP-Star detection module (Amersham-Pharmacia Biotech). After washing twice with 0.2×SSC, 0.1% SDS for 50 min. The filters were exposed to X-ray films for chemiluminescence signal detection.
Transposon display (TD), locus-specific PCR amplification and sequencing
The genomic DNA (approximately 300 ng per sample) was cut with MseI and subject to transposons display (TD) following the protocol essentially as reported . Three consecutively nested, sequence-specific primers targeting to the 3' end of Dart-related TEs were designed. Two specific primers (TDPrm1/TDPrm2 and MseI+C/G) were respectively combined with the selective-amplification primers targeting the adapters, while the most external primer (TIR+N/MseI+3) was used for further validation of the isolated TD bands. Detailed information concerning adapters and primers are listed in Additional files 1. The PCR amplification conditions and TD amplification products were resolved by PAGE and visualized by silver-staining . Only clear and reproducible variant bands between two technical replications were considered as putative new insertions by the Dart-related TEs, and recovered for sequencing.
Based on the sequencing results by identifying the expected 3'-terminus of the Dart-related TEs, the contiguous flanking regions were extracted and used to query the Nipponbare genome sequence http://rgp.dna.affrc.go.jp by BlastN, and a set of locus-specific primers each being downstream of the Dart but compatible with the Dart-specific TD primers were designed with Primer 3 http://biocore.unl.edu/cgi-bin/primer3/primer3_www.cgi and those produced the expected results were listed in Tables 1 and 2. Each of these primers were then sequentially combined with the nested Dart-specific TD primers to reproduce the putative excisions and insertions identified by TD in the introgressant(s), and the amplicons were then sequenced for validation.
RNA isolation and quantitative real-time-reverse transcriptase (RT)-PCR analysis
Total RNA was isolated from the same young leaf tissue as used for DNA isolation and also from the root tissue of the same seedlings of the various treated and mock lines, with the Trizol Reagent (Invitrogen) according to the manufacturer's protocol. The RNA was then treated with DNaseI (Invitrogen) to eliminate possible genomic DNA contamination before being reverse transcribed with the SuperScript RNase H- Reverse Transcriptase (Invitrogen).
The expression of genes adjacent to the newly excised or inserted Dart-related TEs in the introgressant(s) was studied by quantitative real-time-RT-PCR using gene-specific primers (see Additional file 2). The q-RT-PCR experiments were performed using a Roche LightCycler480 apparatus (Roche Inc.) according to the manufacturer's instruction and SYBR Premix Ex Taq (TOYOBO) as a DNA-specific fluorescent dye. The primers for the six studied genes were designed by the Primer 5 software (see Additional file 2). Expression of a rice β-actin gene (Genbank accession X79378) was used as internal control with the primer pairs 5'-atgccattctccgtctt and 5'-gctcctgctcgtagtc. The choice of the β-actin gene as the internal control was based on previous investigation showing that expression of this house-keeping gene between the tissues and under the various stress conditions was constant . Conditions of q-RT-PCR were as reported .
This study was supported by the State Key Basic Research and Development Plan of China (2005CB120805), and the Programme for Introducing Talents to Universities (B07017). We are grateful to two anonymous referees for constructive comments to improve the manuscript.
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