http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–3 ! 2014 Informa UK Ltd. DOI: 10.3109/19401736.2014.919475
MITOGENOME ANNOUNCEMENT
Rearrangement of trnQ-trnM in the mitochondrial genome of Allantus luctifer (Smith) (Hymenoptera: Tenthredinidae) Shu-Jun Wei1, Fang-Fang Niu1,2, and Bao-Zhen Du1,3 Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China, 2College of Agronomy and Plant Protection, Qingdao Agricultural University, Qingdao, China, and 3Department of Plant Protection, Shandong Agricultural University, Tai’an, Shandong, China
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
1
Abstract
Keywords
The complete mitochondrial genome of the Allantus luctifer (Smith) (Hymenoptera: Tenthredinidae: Allantinae) is reported in this study (GenBank accession No. KJ713152). This is the first mitochondrial genome from the subfamily Allantinae and the first completely sequenced mitochondrial genome from the Tenthredinoidea. The length of this mitochondrial genome is 15,418 bp with an A+T content of 81.13%, including 13 protein-coding, 2 rRNA and 22 tRNA gene, and an A+T-rich region (Table 1). Gene arrangement is identical to the other two mitochondrial genomes of tenthredinoid species in nearly all region as in the pupative ancestral arrangement of insects. The ancestral pattern of ‘‘A+T-rich region-trnI(+)-trnQ()-trnM(+)’’ was rearranged to ‘‘trnM(-)-trnQ(+)-A+T-rich region-trnI(+)’’, which is novel to the Hymenoptera. All protein-coding genes start with ATN start codon. Eleven protein-coding genes stop with termination codon TAA, whereas one protein-coding gene uses incomplete stop codon TA and one uses T. The A+T-region is 463 bp long with an A+T content of 86.6%.
Allantus luctifer, gene rearrangement, mitochondrial genome, Sawfly
In mitochondrial genomes of Hymenoptera, gene rearrangement rate was relatively conserved in ‘‘Symphyta’’, but usually accelerated in suborder Apocrita (Dowton et al., 2003, 2009; Dowton & Austin, 1999). Presently, four mitochondrial genomes were completely or partially sequenced from the ‘‘Symphyta’’, representing the Pergidae (Castro & Dowton, 2005) and Tenthredinidae (Wei et al., 2013) of Tenthredinoidea, Cephidae
History Received 17 April 2014 Accepted 26 April 2014 Published online 27 May 2014
of Cephoidea and Orussidae of Orussoidea (Dowton et al., 2009). Here, we sequenced the complete mitochondrial genome of Allantus luctifer (Smith, 1874) from the subfamily Allantinae of Tenthredinidae (GenBank accession No. KJ713152). The length of this mitochondrial genome was 15,418 bp long with an A+T content of 81.13%, including 13 protein-coding, 2 rRNA and 22 tRNA gene, and an A+T-rich region (Table 1). There were totally
Table 1. Annotation of the complete mitochondrial genome of A. luctifer. Gene trnM trnQ A+T-rich region trnI nad2 trnW trnC trnY cox1 trnL2 cox2 trnK trnD atp8
Strand
Position
Length (bp)
Anti/Start codon
– +
1–70 70–138 139–601 602–671 671–1714 1723–1786 1795–1864 1867–1935 1933–3474 3487–3554 3556–4236 4242–4312 4312–4378 4379–4543
70 69 463 70 1044 64 70 69 1542 68 681 71 67 165
CAT TTG
+ + + – – + + + + + +
GAT ATA TCA GCA GTA ATT TAA ATG CTT GTC ATT
Stop codon
TAA
TAA TAA TAA
Intergenic nucleotides (bp) –1 0 0 –1 8 8 2 –3 12 1 5 –1 0 –4 (continued )
Correspondence: Shu-Jun Wei, Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, 9 Shuguanghuayuan Middle Road, Haidian District, Beijing, China. Tel: +86 01051503439. Fax: +86 01051503899. E-mail: [email protected]
2
S.-J. Wei et al.
Mitochondrial DNA, Early Online: 1–3
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
Table 1. Continued
Gene
Strand
Position
Length (bp)
Anti/Start codon
Stop codon
Intergenic nucleotides (bp)
atp6 cox3 trnG nad3 trnA trnR trnN trnS1 trnE trnF nad5 trnH nad4 nad4L trnT trnP nad6 cob trnS2 nad1 trnL1 rrnL trnV rrnS
+ + + + + + + + + – – – – – + – + + + – – – – –
4540–5208 5208–5996 6008–6070 6068–6424 6424–6490 6509–6576 6585–6651 6652–6719 6735–6799 6804–6869 6878–8605 8603–8668 8669–10,010 10,012–10,299 10,302–10,366 10,367–10,432 10,425–10,943 10,943–12,079 12,094–12,161 12,183–13,132 13,133–13,200 13,201–14,540 14,541–14,611 14,612–15,418
669 789 63 357 67 68 67 68 65 66 1728 66 1342 288 65 66 519 1137 68 950 68 1340 71 807
ATA ATG TCC ATA TGC TCG GTT TCT TTC GAA ATA GTG ATG ATA TGT TGG ATT ATG TGA ATA TAG
TAA TAA
–1 11 –3 –1 18 8 0 15 4 8 –3 0 1 2 0 –8 –1 14 21 0 0 0 0 0
TAC
TAA
TAA T TAA TAA TAA TA
+ Indicates that the gene was coded on the majority strand, while – indicates that the gene is coded on the minority strand; AT indicates the A+T-rich region.
27 overlapped nucleotides between neighboring genes in eleven locations and the length of overlapped sequence is 1–8 bp, while there were totally 138 bp intergenic nucleotides in 16 locations and the length of intergenic spacer is 1–21 bp. Eleven pairs of genes were directly adjacent without intergenetic or overlapping nucleotides. In the other two reported mitochondrial genomes of Perga condei (Pergidae) (Castro & Dowton, 2005) and Monocellicampa pruni (Tenthredinidae: Nematinae) (Wei et al., 2013) from Tenthredinoidea, a region from A+T-rich region to trnM and A+T-rich region to nad2 was failed to sequence, respectively. However, the comparable region of the three tenthredinoid mitochondrial genomes show identical gene orders and directions as in the pupative ancestral arrangement of insects (Clary & Wolstenholme, 1985). In mitochondrial genome of A. luctifer, the arrangement of ‘‘A+T-rich region-trnI(+)-trnQ(-)-trnM(+)’’ in the pupative ancestral arrangement of insects was rearranged into a new pattern of ‘‘trnM(-)-trnQ(+)-A+T-rich region-trnI(+)’’. Reversal of one of the trnQ and trnM gene has been reported in other species of Hymenoptera (Castro et al., 2006; Mao et al., 2012; Wei et al., 2010). However, reversal of both adjacent genes of trnQ and trnM in the A. luctifer mitochondrial genome is novel to the Hymenoptera. More species should be examined to verify the universality of trnQ-trnM rearrangement in Tenthredinoidea. In the protein-coding genes, the lowest A+T content was 72.5% in the cox1, while the highest is 88.5% in atp8. All proteincoding genes start with ATN codons (3 with ATA, 4 with ATG and 6 with ATT). Eleven protein-coding genes stoped with termination codon TAA. One protein-coding gene used incomplete stop codon TA and one used T, which was commonly reported in other invertebrates (Masta & Boore, 2004). All of the 22 tRNA genes were present in the range of 63 to 71 bp. The rrnL was 1340 bp long with an A+T content of 84.1% while the rrnS was 807 bp long with an A+T content of 83.5%. The A+T-region was 463 bp long with an A+T content of 86.6%. This region was
believed to be involved in the regulation of transcription and control of DNA replication (Zhang & Hewitt, 1997).
Acknowledgements Authors thank Prof. Mei-Cai Wei from Central South University of Forestry and Technology for his help on the species identification.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Funding for this study was provided jointly by the National Science Foundation of China (31101661) and the State Key Program of National Natural Science Foundation of China (31230068).
References Castro L, Dowton M. (2005). The position of the Hymenoptera within the Holometabola as inferred from the mitochondrial genome of Perga condei (Hymenoptera: Symphyta: Pergidae). Mol Phylogenet Evol 34: 469–79. Castro LR, Ruberu K, Dowton M. (2006). Mitochondrial genomes of Vanhornia eucnemidarum (Apocrita: Vanhorniidae) and Primeuchroeus spp. (Aculeata: Chrysididae): Evidence of rearranged mitochondrial genomes within the Apocrita (Insecta: Hymenoptera). Genome 49:752–66. Clary DO, Wolstenholme DR. (1985). The mitochondrial DNA molecule of Drosophila yakuba: Nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–71. Dowton M, Austin AD. (1999). Evolutionary dynamics of a mitochondrial rearrangement ‘‘hot spot’’ in the Hymenoptera. Mol Biol Evol 16: 298–309. Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF. (2009). Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol 26:1607–17. Dowton M, Castro LR, Campbell SL, Bargon SD, Austin AD. (2003). Frequent mitochondrial gene rearrangements at the Hymenopteran nad3-nad5 junction. J Mol Evol 56:517–26.
DOI: 10.3109/19401736.2014.919475
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
Mao M, Valerio A, Austin AD, Dowton M, Johnson NF. (2012). The first mitochondrial genome for the wasp superfamily Platygastroidea: The egg parasitoid Trissolcus basalis. Genome 55: 194–204. Masta SE, Boore JL. (2004). The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21:893–902. Wei SJ, Shi M, Sharkey MJ, Van Achterberg C, Chen XX. (2010). Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and
Mitogenome of A. luctifer
3
the phylogenetic utility of mitochondrial genomes with special reference to holometabolous insects. BMC Genomics 11:371. Wei SJ, Wu QL, Liu W. (2013). Sequencing and characterization of the Monocellicampa pruni (Hymenoptera: Tenthredinidae) mitochondrial genome. Mitochondrial DNA. [Epub ahead of print]. doi:10.3109/19401736.2013.819501. Zhang DX, Hewitt GM. (1997). Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol 25:99–120.
MITOGENOME ANNOUNCEMENT
Rearrangement of trnQ-trnM in the mitochondrial genome of Allantus luctifer (Smith) (Hymenoptera: Tenthredinidae) Shu-Jun Wei1, Fang-Fang Niu1,2, and Bao-Zhen Du1,3 Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China, 2College of Agronomy and Plant Protection, Qingdao Agricultural University, Qingdao, China, and 3Department of Plant Protection, Shandong Agricultural University, Tai’an, Shandong, China
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
1
Abstract
Keywords
The complete mitochondrial genome of the Allantus luctifer (Smith) (Hymenoptera: Tenthredinidae: Allantinae) is reported in this study (GenBank accession No. KJ713152). This is the first mitochondrial genome from the subfamily Allantinae and the first completely sequenced mitochondrial genome from the Tenthredinoidea. The length of this mitochondrial genome is 15,418 bp with an A+T content of 81.13%, including 13 protein-coding, 2 rRNA and 22 tRNA gene, and an A+T-rich region (Table 1). Gene arrangement is identical to the other two mitochondrial genomes of tenthredinoid species in nearly all region as in the pupative ancestral arrangement of insects. The ancestral pattern of ‘‘A+T-rich region-trnI(+)-trnQ()-trnM(+)’’ was rearranged to ‘‘trnM(-)-trnQ(+)-A+T-rich region-trnI(+)’’, which is novel to the Hymenoptera. All protein-coding genes start with ATN start codon. Eleven protein-coding genes stop with termination codon TAA, whereas one protein-coding gene uses incomplete stop codon TA and one uses T. The A+T-region is 463 bp long with an A+T content of 86.6%.
Allantus luctifer, gene rearrangement, mitochondrial genome, Sawfly
In mitochondrial genomes of Hymenoptera, gene rearrangement rate was relatively conserved in ‘‘Symphyta’’, but usually accelerated in suborder Apocrita (Dowton et al., 2003, 2009; Dowton & Austin, 1999). Presently, four mitochondrial genomes were completely or partially sequenced from the ‘‘Symphyta’’, representing the Pergidae (Castro & Dowton, 2005) and Tenthredinidae (Wei et al., 2013) of Tenthredinoidea, Cephidae
History Received 17 April 2014 Accepted 26 April 2014 Published online 27 May 2014
of Cephoidea and Orussidae of Orussoidea (Dowton et al., 2009). Here, we sequenced the complete mitochondrial genome of Allantus luctifer (Smith, 1874) from the subfamily Allantinae of Tenthredinidae (GenBank accession No. KJ713152). The length of this mitochondrial genome was 15,418 bp long with an A+T content of 81.13%, including 13 protein-coding, 2 rRNA and 22 tRNA gene, and an A+T-rich region (Table 1). There were totally
Table 1. Annotation of the complete mitochondrial genome of A. luctifer. Gene trnM trnQ A+T-rich region trnI nad2 trnW trnC trnY cox1 trnL2 cox2 trnK trnD atp8
Strand
Position
Length (bp)
Anti/Start codon
– +
1–70 70–138 139–601 602–671 671–1714 1723–1786 1795–1864 1867–1935 1933–3474 3487–3554 3556–4236 4242–4312 4312–4378 4379–4543
70 69 463 70 1044 64 70 69 1542 68 681 71 67 165
CAT TTG
+ + + – – + + + + + +
GAT ATA TCA GCA GTA ATT TAA ATG CTT GTC ATT
Stop codon
TAA
TAA TAA TAA
Intergenic nucleotides (bp) –1 0 0 –1 8 8 2 –3 12 1 5 –1 0 –4 (continued )
Correspondence: Shu-Jun Wei, Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, 9 Shuguanghuayuan Middle Road, Haidian District, Beijing, China. Tel: +86 01051503439. Fax: +86 01051503899. E-mail: [email protected]
2
S.-J. Wei et al.
Mitochondrial DNA, Early Online: 1–3
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
Table 1. Continued
Gene
Strand
Position
Length (bp)
Anti/Start codon
Stop codon
Intergenic nucleotides (bp)
atp6 cox3 trnG nad3 trnA trnR trnN trnS1 trnE trnF nad5 trnH nad4 nad4L trnT trnP nad6 cob trnS2 nad1 trnL1 rrnL trnV rrnS
+ + + + + + + + + – – – – – + – + + + – – – – –
4540–5208 5208–5996 6008–6070 6068–6424 6424–6490 6509–6576 6585–6651 6652–6719 6735–6799 6804–6869 6878–8605 8603–8668 8669–10,010 10,012–10,299 10,302–10,366 10,367–10,432 10,425–10,943 10,943–12,079 12,094–12,161 12,183–13,132 13,133–13,200 13,201–14,540 14,541–14,611 14,612–15,418
669 789 63 357 67 68 67 68 65 66 1728 66 1342 288 65 66 519 1137 68 950 68 1340 71 807
ATA ATG TCC ATA TGC TCG GTT TCT TTC GAA ATA GTG ATG ATA TGT TGG ATT ATG TGA ATA TAG
TAA TAA
–1 11 –3 –1 18 8 0 15 4 8 –3 0 1 2 0 –8 –1 14 21 0 0 0 0 0
TAC
TAA
TAA T TAA TAA TAA TA
+ Indicates that the gene was coded on the majority strand, while – indicates that the gene is coded on the minority strand; AT indicates the A+T-rich region.
27 overlapped nucleotides between neighboring genes in eleven locations and the length of overlapped sequence is 1–8 bp, while there were totally 138 bp intergenic nucleotides in 16 locations and the length of intergenic spacer is 1–21 bp. Eleven pairs of genes were directly adjacent without intergenetic or overlapping nucleotides. In the other two reported mitochondrial genomes of Perga condei (Pergidae) (Castro & Dowton, 2005) and Monocellicampa pruni (Tenthredinidae: Nematinae) (Wei et al., 2013) from Tenthredinoidea, a region from A+T-rich region to trnM and A+T-rich region to nad2 was failed to sequence, respectively. However, the comparable region of the three tenthredinoid mitochondrial genomes show identical gene orders and directions as in the pupative ancestral arrangement of insects (Clary & Wolstenholme, 1985). In mitochondrial genome of A. luctifer, the arrangement of ‘‘A+T-rich region-trnI(+)-trnQ(-)-trnM(+)’’ in the pupative ancestral arrangement of insects was rearranged into a new pattern of ‘‘trnM(-)-trnQ(+)-A+T-rich region-trnI(+)’’. Reversal of one of the trnQ and trnM gene has been reported in other species of Hymenoptera (Castro et al., 2006; Mao et al., 2012; Wei et al., 2010). However, reversal of both adjacent genes of trnQ and trnM in the A. luctifer mitochondrial genome is novel to the Hymenoptera. More species should be examined to verify the universality of trnQ-trnM rearrangement in Tenthredinoidea. In the protein-coding genes, the lowest A+T content was 72.5% in the cox1, while the highest is 88.5% in atp8. All proteincoding genes start with ATN codons (3 with ATA, 4 with ATG and 6 with ATT). Eleven protein-coding genes stoped with termination codon TAA. One protein-coding gene used incomplete stop codon TA and one used T, which was commonly reported in other invertebrates (Masta & Boore, 2004). All of the 22 tRNA genes were present in the range of 63 to 71 bp. The rrnL was 1340 bp long with an A+T content of 84.1% while the rrnS was 807 bp long with an A+T content of 83.5%. The A+T-region was 463 bp long with an A+T content of 86.6%. This region was
believed to be involved in the regulation of transcription and control of DNA replication (Zhang & Hewitt, 1997).
Acknowledgements Authors thank Prof. Mei-Cai Wei from Central South University of Forestry and Technology for his help on the species identification.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. Funding for this study was provided jointly by the National Science Foundation of China (31101661) and the State Key Program of National Natural Science Foundation of China (31230068).
References Castro L, Dowton M. (2005). The position of the Hymenoptera within the Holometabola as inferred from the mitochondrial genome of Perga condei (Hymenoptera: Symphyta: Pergidae). Mol Phylogenet Evol 34: 469–79. Castro LR, Ruberu K, Dowton M. (2006). Mitochondrial genomes of Vanhornia eucnemidarum (Apocrita: Vanhorniidae) and Primeuchroeus spp. (Aculeata: Chrysididae): Evidence of rearranged mitochondrial genomes within the Apocrita (Insecta: Hymenoptera). Genome 49:752–66. Clary DO, Wolstenholme DR. (1985). The mitochondrial DNA molecule of Drosophila yakuba: Nucleotide sequence, gene organization, and genetic code. J Mol Evol 22:252–71. Dowton M, Austin AD. (1999). Evolutionary dynamics of a mitochondrial rearrangement ‘‘hot spot’’ in the Hymenoptera. Mol Biol Evol 16: 298–309. Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF. (2009). Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol 26:1607–17. Dowton M, Castro LR, Campbell SL, Bargon SD, Austin AD. (2003). Frequent mitochondrial gene rearrangements at the Hymenopteran nad3-nad5 junction. J Mol Evol 56:517–26.
DOI: 10.3109/19401736.2014.919475
Mitochondrial DNA Downloaded from informahealthcare.com by McMaster University on 03/31/15 For personal use only.
Mao M, Valerio A, Austin AD, Dowton M, Johnson NF. (2012). The first mitochondrial genome for the wasp superfamily Platygastroidea: The egg parasitoid Trissolcus basalis. Genome 55: 194–204. Masta SE, Boore JL. (2004). The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21:893–902. Wei SJ, Shi M, Sharkey MJ, Van Achterberg C, Chen XX. (2010). Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and
Mitogenome of A. luctifer
3
the phylogenetic utility of mitochondrial genomes with special reference to holometabolous insects. BMC Genomics 11:371. Wei SJ, Wu QL, Liu W. (2013). Sequencing and characterization of the Monocellicampa pruni (Hymenoptera: Tenthredinidae) mitochondrial genome. Mitochondrial DNA. [Epub ahead of print]. doi:10.3109/19401736.2013.819501. Zhang DX, Hewitt GM. (1997). Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem Syst Ecol 25:99–120.
