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Long non-coding RNAs are major contributors to transcriptome changes in sunflower meiocytes with different recombination rates.

Flórez-Zapata NM, Reyes-Valdés MH, Martínez O - BMC Genomics (2016)

Bottom Line: Experimental data indicates that, relative to their wild ancestors, cultivated sunflower varieties show a higher recombination rate during meiosis.To better understand the molecular basis for this difference, we compared gene expression in male sunflower meiocytes in prophase I isolated from a domesticated line, a wild relative, and a F1 hybrid of the two.We identified 6895 lncRNAs that are exclusively expressed in meiocytes, these lncRNAs appear to have higher conservation, a greater degree of differential expression, a higher proportion of sRNA similarity, and higher TE content relative to lncRNAs that are also expressed in the somatic transcriptome. lncRNAs play important roles in plant meiosis and may participate in chromatin modification processes, although other regulatory functions cannot be excluded. lncRNAs could also be related to the different recombination rates seen for domesticated and wild sunflowers.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad (LANGEBIO)/Unidad de Genómica Avanzada, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), 36821, Irapuato, Guanajuato, México.

ABSTRACT

Background: Meiosis is a form of specialized cell division that marks the transition from diploid meiocyte to haploid gamete, and provides an opportunity for genetic reassortment through recombination. Experimental data indicates that, relative to their wild ancestors, cultivated sunflower varieties show a higher recombination rate during meiosis. To better understand the molecular basis for this difference, we compared gene expression in male sunflower meiocytes in prophase I isolated from a domesticated line, a wild relative, and a F1 hybrid of the two.

Results: Of the genes that showed differential expression between the wild and domesticated genotypes, 63.62 % could not be identified as protein-coding genes, and of these genes, 70.98 % passed stringent filters to be classified as long non-coding RNAs (lncRNAs). Compared to the sunflower somatic transcriptome, meiocytes express a higher proportion of lncRNAs, and the majority of genes with exclusive expression in meiocytes were lncRNAs. Around 40 % of the lncRNAs showed sequence similarity with small RNAs (sRNA), while 1.53 % were predicted to be sunflower natural antisense transcripts (NATs), and 9.18 % contained transposable elements (TE). We identified 6895 lncRNAs that are exclusively expressed in meiocytes, these lncRNAs appear to have higher conservation, a greater degree of differential expression, a higher proportion of sRNA similarity, and higher TE content relative to lncRNAs that are also expressed in the somatic transcriptome.

Conclusions: lncRNAs play important roles in plant meiosis and may participate in chromatin modification processes, although other regulatory functions cannot be excluded. lncRNAs could also be related to the different recombination rates seen for domesticated and wild sunflowers.

No MeSH data available.


Related in: MedlinePlus

Transposable elements (TEs) in sunflower lncRNAs. a Relative percentages of DNA Transposons and Retrotransposons found within 2326 (9.18 %) sunflower lncRNA. b Bar chart for the number of lncRNA containing TEs per TEs family. DNA Transposons: DH = Helitron, DT = Unknown DNA transposon, DTA = hAT, DTC = CACTA, DTH = Harbinger, DTM = Mutator, DXX = MITE. Retrotransposons: RI = unknown non-LTR retrotransposons, RIL = LINEs, RLC = Copia retrotransposons, RLG = Gypsy retrotransposons, RLR = retroviruses, RLX = Unknown LTR retrotransposons, RX = Unknown retrotransposons
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Fig6: Transposable elements (TEs) in sunflower lncRNAs. a Relative percentages of DNA Transposons and Retrotransposons found within 2326 (9.18 %) sunflower lncRNA. b Bar chart for the number of lncRNA containing TEs per TEs family. DNA Transposons: DH = Helitron, DT = Unknown DNA transposon, DTA = hAT, DTC = CACTA, DTH = Harbinger, DTM = Mutator, DXX = MITE. Retrotransposons: RI = unknown non-LTR retrotransposons, RIL = LINEs, RLC = Copia retrotransposons, RLG = Gypsy retrotransposons, RLR = retroviruses, RLX = Unknown LTR retrotransposons, RX = Unknown retrotransposons

Mentions: We found that 2326 (9.18 %) of all lncRNAs identified here contained TEs (Fig. 6). Of these, 91.01 % also carried retrotransposons, while the remaining 8.99 % had DNA transposons (Fig. 6a). The most common TE belonged to the long terminal repeat (LTR) retrotransposons from the Gypsy and Copia families (Fig. 6b). These results are consistent with previous studies showing that these two retrotransposon families are also the more abundant in the sunflower genome [71, 72]. Other repetitive elements, such as tandem repeats and unknown repeats, were also identified (Figure AF1-6 in Additional file 1). The percentage of lncRNAs that contained transposable or repetitive elements was 14.31 %, which was lower than that for maize [46]. Although the different lncRNA TE content in maize and sunflower could be due to methodological strategy, they may also be related to differences in genomic TE contents of the tissues from which the lncRNAs were sampled (i.e., meiotic expressed lncRNAs in sunflower vs. whole-plant expressed lncRNAs in maize), or intrinsic characteristics of lncRNAs. Even in maize, the majority of so-called HC-lnRNAs (those that are not sRNA precursors) do not contain repetitive sequences [46], which suggests that lncRNA diversity occurs at both functional and evolutionary levels, even within the same species. As such, inter-species differences in lncRNA characteristics would certainly be expected.Fig. 6


Long non-coding RNAs are major contributors to transcriptome changes in sunflower meiocytes with different recombination rates.

Flórez-Zapata NM, Reyes-Valdés MH, Martínez O - BMC Genomics (2016)

Transposable elements (TEs) in sunflower lncRNAs. a Relative percentages of DNA Transposons and Retrotransposons found within 2326 (9.18 %) sunflower lncRNA. b Bar chart for the number of lncRNA containing TEs per TEs family. DNA Transposons: DH = Helitron, DT = Unknown DNA transposon, DTA = hAT, DTC = CACTA, DTH = Harbinger, DTM = Mutator, DXX = MITE. Retrotransposons: RI = unknown non-LTR retrotransposons, RIL = LINEs, RLC = Copia retrotransposons, RLG = Gypsy retrotransposons, RLR = retroviruses, RLX = Unknown LTR retrotransposons, RX = Unknown retrotransposons
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4940957&req=5

Fig6: Transposable elements (TEs) in sunflower lncRNAs. a Relative percentages of DNA Transposons and Retrotransposons found within 2326 (9.18 %) sunflower lncRNA. b Bar chart for the number of lncRNA containing TEs per TEs family. DNA Transposons: DH = Helitron, DT = Unknown DNA transposon, DTA = hAT, DTC = CACTA, DTH = Harbinger, DTM = Mutator, DXX = MITE. Retrotransposons: RI = unknown non-LTR retrotransposons, RIL = LINEs, RLC = Copia retrotransposons, RLG = Gypsy retrotransposons, RLR = retroviruses, RLX = Unknown LTR retrotransposons, RX = Unknown retrotransposons
Mentions: We found that 2326 (9.18 %) of all lncRNAs identified here contained TEs (Fig. 6). Of these, 91.01 % also carried retrotransposons, while the remaining 8.99 % had DNA transposons (Fig. 6a). The most common TE belonged to the long terminal repeat (LTR) retrotransposons from the Gypsy and Copia families (Fig. 6b). These results are consistent with previous studies showing that these two retrotransposon families are also the more abundant in the sunflower genome [71, 72]. Other repetitive elements, such as tandem repeats and unknown repeats, were also identified (Figure AF1-6 in Additional file 1). The percentage of lncRNAs that contained transposable or repetitive elements was 14.31 %, which was lower than that for maize [46]. Although the different lncRNA TE content in maize and sunflower could be due to methodological strategy, they may also be related to differences in genomic TE contents of the tissues from which the lncRNAs were sampled (i.e., meiotic expressed lncRNAs in sunflower vs. whole-plant expressed lncRNAs in maize), or intrinsic characteristics of lncRNAs. Even in maize, the majority of so-called HC-lnRNAs (those that are not sRNA precursors) do not contain repetitive sequences [46], which suggests that lncRNA diversity occurs at both functional and evolutionary levels, even within the same species. As such, inter-species differences in lncRNA characteristics would certainly be expected.Fig. 6

Bottom Line: Experimental data indicates that, relative to their wild ancestors, cultivated sunflower varieties show a higher recombination rate during meiosis.To better understand the molecular basis for this difference, we compared gene expression in male sunflower meiocytes in prophase I isolated from a domesticated line, a wild relative, and a F1 hybrid of the two.We identified 6895 lncRNAs that are exclusively expressed in meiocytes, these lncRNAs appear to have higher conservation, a greater degree of differential expression, a higher proportion of sRNA similarity, and higher TE content relative to lncRNAs that are also expressed in the somatic transcriptome. lncRNAs play important roles in plant meiosis and may participate in chromatin modification processes, although other regulatory functions cannot be excluded. lncRNAs could also be related to the different recombination rates seen for domesticated and wild sunflowers.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad (LANGEBIO)/Unidad de Genómica Avanzada, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), 36821, Irapuato, Guanajuato, México.

ABSTRACT

Background: Meiosis is a form of specialized cell division that marks the transition from diploid meiocyte to haploid gamete, and provides an opportunity for genetic reassortment through recombination. Experimental data indicates that, relative to their wild ancestors, cultivated sunflower varieties show a higher recombination rate during meiosis. To better understand the molecular basis for this difference, we compared gene expression in male sunflower meiocytes in prophase I isolated from a domesticated line, a wild relative, and a F1 hybrid of the two.

Results: Of the genes that showed differential expression between the wild and domesticated genotypes, 63.62 % could not be identified as protein-coding genes, and of these genes, 70.98 % passed stringent filters to be classified as long non-coding RNAs (lncRNAs). Compared to the sunflower somatic transcriptome, meiocytes express a higher proportion of lncRNAs, and the majority of genes with exclusive expression in meiocytes were lncRNAs. Around 40 % of the lncRNAs showed sequence similarity with small RNAs (sRNA), while 1.53 % were predicted to be sunflower natural antisense transcripts (NATs), and 9.18 % contained transposable elements (TE). We identified 6895 lncRNAs that are exclusively expressed in meiocytes, these lncRNAs appear to have higher conservation, a greater degree of differential expression, a higher proportion of sRNA similarity, and higher TE content relative to lncRNAs that are also expressed in the somatic transcriptome.

Conclusions: lncRNAs play important roles in plant meiosis and may participate in chromatin modification processes, although other regulatory functions cannot be excluded. lncRNAs could also be related to the different recombination rates seen for domesticated and wild sunflowers.

No MeSH data available.


Related in: MedlinePlus