http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–2 ! 2015 Informa UK Ltd. DOI: 10.3109/19401736.2015.1022740
MITOGENOME ANNOUNCEMENT
First complete mitochondrial genome sequence from the tribelocephaline assassin bugs (Hemiptera: Reduviidae) Lijuan Zhang, Fan Song, Hu Li, and Wanzhi Cai
Mitochondrial DNA Downloaded from informahealthcare.com by Nyu Medical Center on 05/27/15 For personal use only.
Department of Entomology, China Agricultural University, Beijing, China
Abstract
Keywords
The complete mitochondrial genome (mitogenome) of Opistoplatys sp. was determined, which was the first representation from the assassin bug subfamily Tribelocephalinae. The mitogenome is a typical circular DNA molecule of 15,615 bp and contains 37 genes and a putative control region. All the 13 protein-coding genes initiate with ATN codons and mostly terminate with TAA or TAG codons except for COII, COIII, and ND5 genes use a single T residue as the termination codon. All the 22 tRNAs have the clover-leaf structure except for the tRNASer(AGN) with the length ranging from 60 to 72 bp. The control region is 1068 bp in length and includes 456 bp tandem repeat sequence with four 94-bp tandem repeat units and a partial fifth (80 bp). In the sampled subfamilies of Reduviidae, Peiratinae + the remaining subfamilies, Triatominae + Stenopodainae, Tribelocephalinae + Ectrichodiinae, are recovered in phylogenetic analyses with high supports.
Assassin bug, Hemiptera, mitochondrial genome, Reduviidae, tribelocephalinae History Received 29 January 2015 Revised 2 February 2015 Accepted 15 February 2015 Published online 21 May 2015
Tribelocephalinae is an exclusively palaeotropical, moderately species-rich subfamily within Reduviidae and contains 15 genera with nearly 130 described species (Re´dei, 2007). Most of the species in this subfamily are nocturnal, feed on other arthropods and probably live on the ground, among debris or under boulders (Re´dei, 2007; Schuh & Slater, 1995; Villiers, 1943). To date, seven mitogenomes have been sequenced from six assassin bug subfamilies, including Triatominae (Dotson & Beard, 2001), Salyavatinae (Hua et al., 2008), Harpactorinae (Li et al., 2011), Peiratinae (Gao et al., 2013; Zhao et al., 2014), Stenopodainae (Li et al., 2013), and Ectrichodiinae (Kocher et al., 2014). Here, we present the complete mitogenome of Opistoplatys sp., the first representation from Tribelocephalinae. Voucher specimen (No. Vhem-00205) was deposited at the Entomological Museum of China Agricultural University (CAU) and the sequence was deposited in GenBank under the accession number KC887533. This mitogenome is 15,615 bp long, including the entire set of 37 genes (13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes) and a control region. Gene order is identical to that of the putative ancestral arrangement of insects and other assassin bugs (Cameron 2014; Gao et al., 2013; Kocher et al., 2014; Li et al., 2011, 2013; Zhao et al., 2014). The A + T content is 75.6% with obvious positive AT-skew (0.09) and negative GC-skew (0.20). The codon usage also exhibits a strong A + T-bias in the third codon positions and the five most abundant codons are ATT (Ile),
TTA (Leu), TTT (Phe), ATA (Met), and AAT (Asn). Such pattern is very common among true bugs, with a similar frequency of occurrences of various codons within a single codon family (Li et al., 2011, 2012a,b; Wang et al., 2014). All protein-coding genes initiate with ATN as the start codon (five with ATG, four with ATT, four with ATA). Conventional stop codons (TAA or TAG) have been assigned to majority of the protein-coding genes. COII, COIII, and ND5, however, terminate with a single T residue. This mitogenome has the complete set of 22 tRNA genes, ranging from 60 to 72 bp, that are present in most metazoan mitogenomes. Among all tRNA genes, only tRNASer(AGN) cannot exhibit the classic cloverleaf secondary structure, due to the deficiency of the dihydrouridine (DHU) arm which is typical feature of true bug mitogenomes (Hua et al., 2008; Li et al., 2011, 2012c; Wang et al., 2014). The lrRNA is 1256 bp long with an A + T content of 79.1%, and the srRNA is 778 bp long with an A + T content of 74.8%. The control region is located between srRNA and trnI and is 1068 bp long with 73.5% A + T content. Tandem repeats (five copies) are detected in this region: a 90-bp sequence tandemly repeated four times, with a partial fifth (80 bp). Phylogenetic analyses showed the similar relationships among sampled subfamilies as Weirauch & Munro (2009) and the following clades were highly supported in both maximum likelihood and Bayesian analyses (Figure 1): (1) Peiratinae + the remaining sampled subfamilies; (2) Triatominae + Stenopodainae; and (3) Tribelocephalinae + Ectrichodiinae.
Correspondence: Dr Wanzhi Cai, Department of Entomology, China Agricultural University, No. 2 Yuanmingyuan West Road, Beijing 100193, China. Tel: +86 10 62732885. Fax: +86 10 62732885. E-mail: [email protected]
Declaration of interest Funding for this study was supported by grants from the National Natural Science Foundation of China (Nos. 31372229, 31420103902, and
Mitochondrial DNA Downloaded from informahealthcare.com by Nyu Medical Center on 05/27/15 For personal use only.
2
L. Zhang et al.
Mitochondrial DNA, Early Online: 1–2
Figure 1. Phylogenetic relationships of seven assassin bug subfamilies inferred from analyses of the 13 protein-coding genes (10,638 bp). Phylogenetic trees were generated from Bayesian inference (MrBayes) under the GTR + I + G model and maximum likelihood analysis (RAxML) under the GTR + G model. Dataset was partitioned by gene. The nodal values indicate the Bayesian posterior probabilities (in left) estimated by 2,000,000 generations (nruns ¼ 2, nchians ¼ 4, samplefreq ¼ 1000) with the initial 25% trees discarded as burn-in and RAxML bootstrap percentages (in right) obtained with 1000 replicates. Dashes indicate nodal values 550%.
31401991), the Beijing Natural Science Foundation (Nos. 6144027 and 6152016), and the China Postdoctoral Science Foundation (Nos. 2013M540167 and 2014T70145). All authors have read and approved the final manuscript. The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References Cameron SL. (2014). Insect mitochondrial genomics: Implications for evolution and phylogeny. Annu Rev Entomol 59:95–117. Dotson EM, Beard CB. (2001). Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Mol Biol 10:205–15. Gao JY, Li H, Truong XL, Dai X, Chang J, Cai W. (2013). Complete nucleotide sequence and organization of the mitochondrial genome of Sirthenea flavipes (Hemiptera: Reduviidae: Peiratinae) and comparison with other assassin bugs. Zootaxa 3669:1–16. Hua JM, Li M, Dong PZ, Cui Y, Xie Q, Bu WJ. (2008). Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics 9:610. Kocher A, Kamilari M, Lhuillier E, Coissac E, Peneau J, Chave J, Murienne J. (2014). Shotgun assembly of the assassin bug Brontostoma colossus mitochondrial genome (Heteroptera, Reduviidae). Gene 552: 184–94. Li H, Gao JY, Cai W. (2013). Complete mitochondrial genome of the assassin bug Oncocephalus breviscutum (Hemiptera: Reduviidae). Mitochondrial DNA. [Epub ahead of print]. DOI: 10.3109/19401736. 2013.840602. Li H, Gao JY, Liu HY, Liu H, Liang AP, Zhou XG, Cai W. (2011). The architecture and complete sequence of mitochondrial genome of
an assassin bug Agriosphodrus dohrni (Hemiptera: Reduviidae). Int J Biol Sci 7:792–804. Li H, Liu H, Shi AM, Sˇtys P, Zhou XG, Cai W. (2012a). The complete mitochondrial genome and novel gene arrangement of the uniqueheaded bug Stenopirates sp. (Hemiptera: Enicocephalidae). PLoS One 7:e29419. Li H, Liu HY, Cao LM, Shi AM, Yang HL, Cai W. (2012b). The complete mitochondrial genome of the damsel bug Alloeorhynchus bakeri (Hemiptera: Nabidae). Int J Bio Sci 8:93–107. Li H, Liu HY, Song F, Shi AM, Zhou XG, Cai W. (2012c). Comparative mitogenomic analysis of damsel bugs representing three tribes in the family Nabidae (Insecta: Hemiptera). PLoS One 7:e45925. Re´dei D. (2007). A new genus of tribelocephaline assassin bugs from Borneo (Hemiptera: Heteroptera: Reduviidae). Zootaxa 1465: 47–53. Schuh RT, Slater JA. (1995). True bugs of the world (Hemiptera: Heteroptera): Classification and natural history. Ithaca: Cornell University Press. Villiers A. (1943). Morphologie et systematic des Tribelocephalitae Africains. Rev Fr Entomol 10:1–28. Wang Y, Li H, Wang P, Song F, Cai WZ. (2014). Comparative mitogenomics of plant bugs (Hemiptera: Miridae): Identifying the AGG codon reassignments between serine and lysine. PLoS One 9:e101375. Weirauch C, Munro JB. (2009). Molecular phylogeny of the assassin bugs (Hemiptera: Reduviidae), based on mitochondrial and nuclear ribosomal genes. Mol Phylogenet Evol 53:287–99. Zhao GY, Li H, Song F, Cai WZ. (2014). The complete mitochondrial genome of an assassin bug Peirates arcuatus (Hemiptera: Reduviidae). Mitochondrial DNA. [Epub ahead of print]. DOI: 10.3109/19401736. 2013.867438.
MITOGENOME ANNOUNCEMENT
First complete mitochondrial genome sequence from the tribelocephaline assassin bugs (Hemiptera: Reduviidae) Lijuan Zhang, Fan Song, Hu Li, and Wanzhi Cai
Mitochondrial DNA Downloaded from informahealthcare.com by Nyu Medical Center on 05/27/15 For personal use only.
Department of Entomology, China Agricultural University, Beijing, China
Abstract
Keywords
The complete mitochondrial genome (mitogenome) of Opistoplatys sp. was determined, which was the first representation from the assassin bug subfamily Tribelocephalinae. The mitogenome is a typical circular DNA molecule of 15,615 bp and contains 37 genes and a putative control region. All the 13 protein-coding genes initiate with ATN codons and mostly terminate with TAA or TAG codons except for COII, COIII, and ND5 genes use a single T residue as the termination codon. All the 22 tRNAs have the clover-leaf structure except for the tRNASer(AGN) with the length ranging from 60 to 72 bp. The control region is 1068 bp in length and includes 456 bp tandem repeat sequence with four 94-bp tandem repeat units and a partial fifth (80 bp). In the sampled subfamilies of Reduviidae, Peiratinae + the remaining subfamilies, Triatominae + Stenopodainae, Tribelocephalinae + Ectrichodiinae, are recovered in phylogenetic analyses with high supports.
Assassin bug, Hemiptera, mitochondrial genome, Reduviidae, tribelocephalinae History Received 29 January 2015 Revised 2 February 2015 Accepted 15 February 2015 Published online 21 May 2015
Tribelocephalinae is an exclusively palaeotropical, moderately species-rich subfamily within Reduviidae and contains 15 genera with nearly 130 described species (Re´dei, 2007). Most of the species in this subfamily are nocturnal, feed on other arthropods and probably live on the ground, among debris or under boulders (Re´dei, 2007; Schuh & Slater, 1995; Villiers, 1943). To date, seven mitogenomes have been sequenced from six assassin bug subfamilies, including Triatominae (Dotson & Beard, 2001), Salyavatinae (Hua et al., 2008), Harpactorinae (Li et al., 2011), Peiratinae (Gao et al., 2013; Zhao et al., 2014), Stenopodainae (Li et al., 2013), and Ectrichodiinae (Kocher et al., 2014). Here, we present the complete mitogenome of Opistoplatys sp., the first representation from Tribelocephalinae. Voucher specimen (No. Vhem-00205) was deposited at the Entomological Museum of China Agricultural University (CAU) and the sequence was deposited in GenBank under the accession number KC887533. This mitogenome is 15,615 bp long, including the entire set of 37 genes (13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes) and a control region. Gene order is identical to that of the putative ancestral arrangement of insects and other assassin bugs (Cameron 2014; Gao et al., 2013; Kocher et al., 2014; Li et al., 2011, 2013; Zhao et al., 2014). The A + T content is 75.6% with obvious positive AT-skew (0.09) and negative GC-skew (0.20). The codon usage also exhibits a strong A + T-bias in the third codon positions and the five most abundant codons are ATT (Ile),
TTA (Leu), TTT (Phe), ATA (Met), and AAT (Asn). Such pattern is very common among true bugs, with a similar frequency of occurrences of various codons within a single codon family (Li et al., 2011, 2012a,b; Wang et al., 2014). All protein-coding genes initiate with ATN as the start codon (five with ATG, four with ATT, four with ATA). Conventional stop codons (TAA or TAG) have been assigned to majority of the protein-coding genes. COII, COIII, and ND5, however, terminate with a single T residue. This mitogenome has the complete set of 22 tRNA genes, ranging from 60 to 72 bp, that are present in most metazoan mitogenomes. Among all tRNA genes, only tRNASer(AGN) cannot exhibit the classic cloverleaf secondary structure, due to the deficiency of the dihydrouridine (DHU) arm which is typical feature of true bug mitogenomes (Hua et al., 2008; Li et al., 2011, 2012c; Wang et al., 2014). The lrRNA is 1256 bp long with an A + T content of 79.1%, and the srRNA is 778 bp long with an A + T content of 74.8%. The control region is located between srRNA and trnI and is 1068 bp long with 73.5% A + T content. Tandem repeats (five copies) are detected in this region: a 90-bp sequence tandemly repeated four times, with a partial fifth (80 bp). Phylogenetic analyses showed the similar relationships among sampled subfamilies as Weirauch & Munro (2009) and the following clades were highly supported in both maximum likelihood and Bayesian analyses (Figure 1): (1) Peiratinae + the remaining sampled subfamilies; (2) Triatominae + Stenopodainae; and (3) Tribelocephalinae + Ectrichodiinae.
Correspondence: Dr Wanzhi Cai, Department of Entomology, China Agricultural University, No. 2 Yuanmingyuan West Road, Beijing 100193, China. Tel: +86 10 62732885. Fax: +86 10 62732885. E-mail: [email protected]
Declaration of interest Funding for this study was supported by grants from the National Natural Science Foundation of China (Nos. 31372229, 31420103902, and
Mitochondrial DNA Downloaded from informahealthcare.com by Nyu Medical Center on 05/27/15 For personal use only.
2
L. Zhang et al.
Mitochondrial DNA, Early Online: 1–2
Figure 1. Phylogenetic relationships of seven assassin bug subfamilies inferred from analyses of the 13 protein-coding genes (10,638 bp). Phylogenetic trees were generated from Bayesian inference (MrBayes) under the GTR + I + G model and maximum likelihood analysis (RAxML) under the GTR + G model. Dataset was partitioned by gene. The nodal values indicate the Bayesian posterior probabilities (in left) estimated by 2,000,000 generations (nruns ¼ 2, nchians ¼ 4, samplefreq ¼ 1000) with the initial 25% trees discarded as burn-in and RAxML bootstrap percentages (in right) obtained with 1000 replicates. Dashes indicate nodal values 550%.
31401991), the Beijing Natural Science Foundation (Nos. 6144027 and 6152016), and the China Postdoctoral Science Foundation (Nos. 2013M540167 and 2014T70145). All authors have read and approved the final manuscript. The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References Cameron SL. (2014). Insect mitochondrial genomics: Implications for evolution and phylogeny. Annu Rev Entomol 59:95–117. Dotson EM, Beard CB. (2001). Sequence and organization of the mitochondrial genome of the Chagas disease vector, Triatoma dimidiata. Insect Mol Biol 10:205–15. Gao JY, Li H, Truong XL, Dai X, Chang J, Cai W. (2013). Complete nucleotide sequence and organization of the mitochondrial genome of Sirthenea flavipes (Hemiptera: Reduviidae: Peiratinae) and comparison with other assassin bugs. Zootaxa 3669:1–16. Hua JM, Li M, Dong PZ, Cui Y, Xie Q, Bu WJ. (2008). Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics 9:610. Kocher A, Kamilari M, Lhuillier E, Coissac E, Peneau J, Chave J, Murienne J. (2014). Shotgun assembly of the assassin bug Brontostoma colossus mitochondrial genome (Heteroptera, Reduviidae). Gene 552: 184–94. Li H, Gao JY, Cai W. (2013). Complete mitochondrial genome of the assassin bug Oncocephalus breviscutum (Hemiptera: Reduviidae). Mitochondrial DNA. [Epub ahead of print]. DOI: 10.3109/19401736. 2013.840602. Li H, Gao JY, Liu HY, Liu H, Liang AP, Zhou XG, Cai W. (2011). The architecture and complete sequence of mitochondrial genome of
an assassin bug Agriosphodrus dohrni (Hemiptera: Reduviidae). Int J Biol Sci 7:792–804. Li H, Liu H, Shi AM, Sˇtys P, Zhou XG, Cai W. (2012a). The complete mitochondrial genome and novel gene arrangement of the uniqueheaded bug Stenopirates sp. (Hemiptera: Enicocephalidae). PLoS One 7:e29419. Li H, Liu HY, Cao LM, Shi AM, Yang HL, Cai W. (2012b). The complete mitochondrial genome of the damsel bug Alloeorhynchus bakeri (Hemiptera: Nabidae). Int J Bio Sci 8:93–107. Li H, Liu HY, Song F, Shi AM, Zhou XG, Cai W. (2012c). Comparative mitogenomic analysis of damsel bugs representing three tribes in the family Nabidae (Insecta: Hemiptera). PLoS One 7:e45925. Re´dei D. (2007). A new genus of tribelocephaline assassin bugs from Borneo (Hemiptera: Heteroptera: Reduviidae). Zootaxa 1465: 47–53. Schuh RT, Slater JA. (1995). True bugs of the world (Hemiptera: Heteroptera): Classification and natural history. Ithaca: Cornell University Press. Villiers A. (1943). Morphologie et systematic des Tribelocephalitae Africains. Rev Fr Entomol 10:1–28. Wang Y, Li H, Wang P, Song F, Cai WZ. (2014). Comparative mitogenomics of plant bugs (Hemiptera: Miridae): Identifying the AGG codon reassignments between serine and lysine. PLoS One 9:e101375. Weirauch C, Munro JB. (2009). Molecular phylogeny of the assassin bugs (Hemiptera: Reduviidae), based on mitochondrial and nuclear ribosomal genes. Mol Phylogenet Evol 53:287–99. Zhao GY, Li H, Song F, Cai WZ. (2014). The complete mitochondrial genome of an assassin bug Peirates arcuatus (Hemiptera: Reduviidae). Mitochondrial DNA. [Epub ahead of print]. DOI: 10.3109/19401736. 2013.867438.
