2urn:lsid:arphahub.com:pub:45048D35-BB1D-5CE8-9668-537E44BD4C7Eurn:lsid:zoobank.org:pub:91BD42D4-90F1-4B45-9350-EEF175B1727AZooKeysZK1313-29891313-2970Pensoft Publishers10.3897/zookeys.1092.8099380993Research ArticleBuprestidaeBuprestoideaColeopteraInsectaInvertebrataMolecular systematicsPhylogenyThe complete mitochondrial genomes of five Agrilinae (Coleoptera, Buprestidae) species and phylogenetic implicationsWeiZhonghuawzh1164@126.comhttps://orcid.org/0000-0001-7349-99391ConceptualizationData curationFormal analysisFunding acquisitionThe Key Laboratory of Southwest China Wildlife Resources Conservation of the Ministry of Education, College of Life Sciences, China West Normal University, 637009, Nanchong, Sichuan Province, ChinaChina West Normal UniversityNanchongChina
2022060420221092195212C7F4D494-95AC-58A0-A4CD-526D67D184DEF8957AFF-24AE-44E5-9577-43E3160A778B64236752101202218032022Zhonghua WeiThis is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.http://zoobank.org/F8957AFF-24AE-44E5-9577-43E3160A778B
Five complete mitochondrial genomes of five species from the subfamily Agrilinae were sequenced and annotated, including Coraebusdiminutus Gebhardt, 1928 (15,499 bp), Coraebuscloueti Théry, 1893 (15,514 bp), Meliboeussinae Obenberger, 1935 (16,108 bp), Agrilussichuanus Jendek, 2011 (16,521 bp), and Sambusfemoralis Kerremans, 1892 (15,367 bp). These mitogenomes ranged from 15,367 to 16,521 bp in length and encoded 37 typical mitochondrial genes: 13 protein-coding genes (13 PCGs), 2 ribosomal RNA genes (2 rRNAs), 22 transfer RNA genes (22 tRNAs), and a control region (CR). Most of PCGs had typical ATN start codons and terminated with TAR or an incomplete stop codon T–. Among these five mitogenomes, Leu2, Ile, Phe, Ser2, Gly, Met, and Val were the seven most frequently encoded amino acids. Interestingly, in A.sichuanus, a 774 bp insertion was present at trnW and trnC junction, which is unusual in Buprestidae. Additionally, phylogenetic analyses were performed based on three kinds of nucleotide matrixes (13 PCGs, 2 rRNAs, and 13 PCGs + 2 rRNAs) using Bayesian inference and maximum-likelihood methods. The results showed that the clade of Buprestidae was well separated from outgroups and all Agrilinae species formed to a single highly supported clade. The tribe Coraebini was polyphyletic, as the genus Meliboeus (Coraebini) clustered with the genus Trachys (Tracheini). The rRNA genes had important impact for the tree topology of Agrilinae. Compared to the tribes Tracheini and Agrilini, the tribe Coraebini is a younger group.
Wei Z (2022) The complete mitochondrial genomes of five Agrilinae (Coleoptera, Buprestidae) species and phylogenetic implications. ZooKeys 1092: 195–212. https://doi.org/10.3897/zookeys.1092.80993
Introduction
The superfamily Buprestoidea, which contains the families Buprestidae and Schizopodidae, differs from other groups of the Elateriformia by their serrate antennae, hypognathous head, transverse suture of metaventrite present, and two connate basal abdominal ventrites (Bellamy and Volkovitsh 2016). The buprestid beetles are a large group containing six subfamilies, 521 genera, and more than 15,000 species widely distributed in the world (Bellamy 2008; Kubáň et al. 2016). The adults exhibit a broad range of host utilization in leaves, flowers, and stems, whereas larvae are mostly internal feeders on roots and stems, or feed on foliage of woody or herbaceous plants (Bellamy and Volkovitsh 2016). Only adults of the Australian Xyrosceliscrocata were reported to feed on the sap of the host plant Macrozamiacommunis (Bellamy 1997).
Although taxonomists have made important contributions to the buprestid classification of subfamilies and tribes based on several morphological characteristics (Cobos 1980, 1986; Tôyama 1987; Hołyński 1988, 1993, 2009; Bellamy 2003), the problems of the overall classification in Buprestoidea remain unsettled.
In the past two decades, molecular systematic approaches have been used to resolve unsettled classification and phylogenetic relationships in Insecta (Short and Fikáček 2013; Cline et al. 2014; Robertson et al. 2015; Kundrata et al. 2017; Gimmel et al. 2019; Lee et al. 2020). As to Buprestidae, Bernhard et al. (2005) first used molecular phylogenetic methods based on three mitochondrial markers (nad1, 12S, and 16S) and confirmed that the Agrilusviridis complex, which is widely distributed across Eurasia, is monophyletic. Pentinsaari et al. (2014) and Pellegrino et al. (2017) used mitochondrial markers to evaluate the diversity of A.viridis complex, their results suggest that different feeding forms of A.viridis represent distinct species. Subsequently, Evans et al. (2015) performed the first large-scale phylogenetic trees combing nuclear and mitochondrial data from 141 species to understand the higher-level relationships in Buprestidae. In that study, the monophyly of the family Schizopodidae and subfamilies Agrilinae, Julodinae, and Galbellinae were strongly supported, while the interrelationships of Chrysochroinae and Buprestinae remained uncertain. Hansen et al. (2016) used molecular systematic methods based on nuclear and mitochondrial data (coi and ak) to investigate the relationships within Chrysobothrisfemorata species group, and their results showed that some morphological species were not well separated. Kelnarova et al. (2019) provided a molecular phylogeny of Agrilus species from the Northern Hemisphere and their results suggest that DNA barcoding is a powerful species identification to Agrilus.
During this time, the mitogenome emerged as a valuable source for higher-level phylogenetic analyses, evolutionary strategies, and genetic diversity analyses (Saccone et al. 1999; Krzywinski et al. 2011; Cameron 2014; Qin et al. 2015; Song et al. 2019; Wang et al. 2019). Several buprestid mitogenomes have been sequenced and reported, such as the mitogenome of Chrysochroafulgidissima (Schönherr, 1817) by Hong et al. (2009); the mitogenome of Agrilusplanipennis Fairmaire, 1888 by Duan et al. (2017), who also performed phylogenetic analyses based on 13 PCGs of 45 mitogenomes of coleopterans; the mitogenome of Trachysvariolaris Saunders, 1873 by Cao and Wang (2019a); and the mitogenome of Coraebuscavifrons Descarpentries & Villiers, 1967 by Cao and Wang (2019b). More detailed information of buprestid mitogenomes is presented in Table 1.
Information on the mitogenomes of Buprestidae and two outgroups used in this study.
No.
Taxa
Accession no.
Genome size (bp)
A%
A+T%
AT skew
GC skew
References
1
Coraebusdiminutus
OK189521
15,499
38.34
68.42
0.12
−0.25
This study
2
Coraebuscloueti
OK189520
15,514
38.53
69.27
0.11
−0.25
This study
3
Meliboeussinae
OK189522
16,108
40.18
72.42
0.11
−0.22
This study
4
Sambusfemoralis
OK349489
15,367
40.98
73.23
0.12
−0.18
This study
5
Agrilussichuanus
OK189519
16,521
40.19
71.73
0.12
−0.21
This study
6
Agrilusplanipennis
KT363854
15,942
40.25
71.90
0.12
−0.24
Duan et al. 2017
7
Agrilusmali
MN894890
16,204
40.34
74.46
0.08
−0.18
Sun et al. 2020
8
Coraebuscavifrons
MK913589
15,686
38.94
69.79
0.12
−0.18
Cao and Wang 2019b
9
Trachysauricollis
MH638286
16,429
38.94
71.05
0.10
−0.20
Xiao et al. 2019
10
Trachystroglodytiformis
KX087357
16,316
41.03
74.62
0.10
−0.19
Unpublished
11
Trachysvariolaris
MN178497
16,771
39.92
72.11
0.11
−0.21
Cao and Wang 2019a
12
Melanophilaacuminata
MW287594
15,853
38.74
75.66
0.02
−0.25
Peng et al. 2021
13
Anthaxiachinensis
MW929326
15,881
40.12
73.61
0.09
−0.29
Chen et al. 2021
14
Chrysochroafulgidissima
EU826485
15,592
40.31
69.92
0.15
−0.24
Hong et al. 2009
15
Acmaeodera sp.
FJ613420
16,217
38.11
68.41
0.11
−0.25
Sheffield et al. 2009
16
Heterocerusparallelus (outgroup)
KX087297
15,845
41.90
74.03
0.13
−0.24
Unpublished
17
Dryopsernesti (outgroup)
KX035147
15,672
39.04
72.98
0.07
−0.23
Unpublished
Currently, the subfamily Agrilinae contains four tribes (Agrilini, Coraebini, Aphanisticini, and Tracheini); however, the phylogenetic placement of several genera of this subfamily remains unstable. The genera in the tribes Coraebini and Agrilini were revised by Kubáň et al. (2000). In that study, the genus Sambus in the tribe Coraebini was transferred to Agrilini based on the female behavior of ovipositing on rather smooth surfaces of living plants. Later, Kubáň (2016) placed the genera Sambus, Parasambus, and Pseudagrilus in incertae sedis. In order to solve these problems, we contribute mitogenomic data of five species of buprestids, Coraebusdiminutus Gebhardt, 1928, Coraebuscloueti Théry, 1893, Meliboeussinae Obenberger, 1935, Agrilussichuanus Jendek, 2011, and Sambusfemoralis Kerremans, 1892, and perform a molecular phylogenetic analysis in this study. The phylogenetic trees of 15 species from nine genera belonging to four subfamilies of Buprestidae were constructed based on the newly sequenced and previously reported mitogenomes (Table 1).
Material and methodsSampling and DNA extraction
Specimens of five species were collected using an entomological net. Among them, C.diminutus, C.cloueti, M.sinae, and A.sichuanus were collected in the Dayaoshan Mountains in Guangxi Zhuang Autonomous Region, and S.femoralis was collected at Yingjiang County in Yunnan Province, China. Specimens were immediately preserved in 95% ethanol in the field after collected and then stored at –24 °C in the laboratory. The specimens were identified based on morphological characteristics under a Leica M205 FA stereomicroscope. Total DNA was extracted from muscle tissues using the Ezup Column Animal Genomic DNA Purification Kit (Shanghai, China) following the manufacturer’s instructions.
Sequencing, sequence assembly, annotation, and heterogeneity
DNA sequencing and de novo assembly of each mitogenome were performed by Beijing Aoweisen Gene Technology Co. Ltd (Beijing, China). 22 tRNA genes were identified using the MITOS webserver, with the parameters of the Invertebrate Mito genetic code (Bernt et al. 2013). Their secondary structures were plotted manually from the MITOS predictions using Adobe Illustrator. Every sequence of tRNA genes was manually checked separately. The PCGs were identified as open reading frames corresponding to the 13 PCGs. The rRNAs and control regions were identified by the boundaries of the tRNA genes. The tRNA secondary structures were identified using tRNAscan-SE (Lowe and Chan 2016). Mitogenome maps (Suppl. material 1: Fig. S1) were produced using Organellar Genome DRAW (OGDRAW) (Greiner et al. 2019). The Base composition and relative synonymous codon usage values were determined using MEGA 6.0 (Kumar et al.2016). Strand asymmetry was calculated using the formulae AT-skew = (A – T) / (A + T), and GC-skew = (G – C) / (G + C) (Perna and Kocher 1995). In the control region (CR), tandem repeat elements were detected by Tandem Repeats Finder (Benson 1999). The heterogeneous analysis of the 13 PCGs and two rRNAs datasets were performed using AliGROOVE 1.06 (Kück et al. 2014), and the nucleotide diversity (Pi) and the ratio of Ka/Ks of PCGS were calculated with DnaSP v. 5 (Librado and Rozas 2009).
Phylogenetic analyses
Phylogenetic trees for A.sichuanus, C.diminutus, C.cloueti, M.sinae, S.femoralis, and 10 other buprestid species belonging to four subfamilies were reconstructed by three separate datasets (13 PCGs, 2 rRNAs, and 13 PCGs + 2 rRNAs) using different best-fit models (Table 4). The mitogenomes of Heterocerusparallelus (Heteroceridae) and Dryopsernesti (Dryopidae) were used as outgroups, as they are phylogenetically distant from Buprestidae in the suborder Polyphaga (Xiao et al. 2019). The phylogenetic analyses were performed using PhyloSuite v. 1.2.2 (Zhang et al. 2020). Nucleotide sequences of the 13 PCGs and 2 rRNAs of all 17 mitogenomes were aligned using ClustalW (Thompson et al. 1994) and trimmed using trimAl v. 1.2 (Capella-Gutiérrez et al. 2009). The best-fit model for three datasets was determined by ModelFinder based on Bayesian information criterion. The maximum-likelihood (ML) and Bayesian inference (BI) methods were used to reconstruct the phylogenetic trees by IQ-tree v. 1.6.8 (Guindon et al. 2010) and MrBayes v. 3.2.6 program respectively (Ronquist et al. 2012). Bayesian analyses were run with two independent chains spanning 2,000,000 generations, four Markov chains, sampling at every 100 generations, and a burn-in period of 0.25 for each chain. The phylogenetic trees were edited and visualized by Figtree v. 1.4.3.
Results and discussionGenome organization and base composition
The complete mitogenomes of the buprestids A.sichuanus, C.diminutus, C.cloueti, M.sinae, and S.femoralis have the following GenBank accession numbers attributed to them: OK189519, OK189521, OK189520, OK189522, OK349489. The mitogenomes of these five species contained the 37 typical mitochondrial genes (13 PCGs, 22 tRNAs, and 2 rRNAs) and a control region (CR) (Table 2). The composition and arrangement of the mitochondrial genes in these species (Table 2) were highly similar as those in most other buprestid species (Duan et al. 2017; Cao and Wang 2019a, 2019b; Xiao et al. 2019; Chen et al. 2021; Peng et al. 2021).
The five newly annotated Buprestidae mitogenomes. The order of these five species in the table is as follows: Agrilussichuanus, Coraebusdiminutus, Coraebuscloueti, Meliboeussinae, and Sambusfemoralis. – not determined.
Gene
Strand
Position From
To
Start codons
Stop condons
Anticodon
Intergenic nucleotides
trnI
J
1/1/1/1/1
65/63/63/64/65
GAT
-3/-3/-3/5-3
trnQ
N
63/61/61/70/63
131/129/129/138/131
AAG
-1/0/0/0/-1
trnM
J
131/129/129/138/131
199/196/196/205/196
CAA
0/0/0/0/0
nad2
J
200/197/197/206/197
1222/1219/1219/1231/1210
ATC/ATT/ATT/ATC/ATT
TAA/TAG/TAA/TAA/TAA
1/1/-2/0/-2
trnW
J
1224/1221/1218/1232/1209
1293/1286/1283/1303/1273
ACA
774/-8/-13/13/-8
trnC
N
2068/1279/1276/1296/1266
2130/1339/1336/1356/1326
GCA
0/2/2/0/0
trnY
N
2131/1342/1339/1357/1327
2195/1404/1401/1419/1387
GAA
9/1/1/1/1
cox1
J
2205/1406/1403/1421/1389
3735/2936/2933/2951/2919
–/–/–/–/–
TAA/TAA/TAA/TAA/TAA
0/0/0/0/0
trnL2
J
3736/2937/2934/2952/2920
3802/3003/3001/3016/2984
AAG
0/0/0/0/0
cox2
J
3803/3004/3002/3017/2985
4484/3670/3668/3698/3666
ATT/ATA/ATA/ATC/ATT
TAA/TAA/TAA/TAA/TAA
0/0/0/0/0
trnK
J
4485/3671/3669/3699/3667
4553/3740/3738/3768/3736
CAA
0/0/0/0/0
trnD
J
4554/3741/3739/3769/3737
4618/3803/3802/3830/3798
GAC
0/0/0/0/0
atp8
J
4619/3804/3803/3831/3799
4777/3962/3961/3989/3954
ATT/ATA/ATC/ATT/ATA
TAG/TAA/TAA/TAA/TAG
0/-7/-7/-7-7
atp6
J
4771/3956/3955/3983/3948
5445/4630/4629/4657/4622
ATG/ATG/ATG/ATG/ATG
TAA/TAA/TAA/TAA/TAA
-1/-1/-1/-1/-1
cox3
J
5445/4630/4629/4657/4622
6233/5416/5415/5443/5405
ATG/ATG/ATG/ATG/ATG
TAG/TAA/TAA/TAA/TAA
8/0/0/0/0
trnG
J
6242/5417/5416/5444/5406
6306/5477/5476/5509/5469
ACC
0/0/0/0/0
nad3
J
6307/5478/5477/5510/5470
6660/5831/5830/5863/5823
ATT/ATT/ATT/ATT/ATT
TAG/TAG/TAG/TAG/TAG
-2/-2/-2/-2/-2
trnA
J
6659/5830/5829/5862/5822
6721/5890/5889/5924/5884
AGC
0/-1/-1/-1/0
trnR
J
6722/5890/5889/5924/5885
6781/5952/5951/5988/5947
ACG
1/-1/-1/-1/1
trnN
J
6783/5952/5951/5988/5949
6849/6017/6016/6051/6013
GAA
0/0/0/0/0
trnS1
J
6850/6018/6017/6052/6014
6916/6075/6074/6117/6080
ACA
1/0/7/-1/0
trnE
J
6918/6076/6082/6117/6081
6982/6139/6143/6179/6143
AAC
-1/-4/-4/-1/-1
trnF
N
6982/6136/6140/6179/6143
7045/6198/6202/6240/6207
GAA
0/0/0/0/0
nad5
N
7046/6199/6203/6241/6208
8768/7915/7919/7960/7915
ATA/ATT/ATT/ATT/ATA
TAA/TAA/TAA/TAA/TAA
0/0/0/0/0
trnH
N
8769/7916/7920/7961/7916
8830/7977/7981/8026/7978
GAG
0/0/0/0/0
nad4
N
8831/7978/7982/8027/7979
10,166/9295/9299/9362/9308
ATG/ATG/ATG/ATG/ATG
TAA/TAA/TAA/TAA/TAA
-7/-7/-7/-7/-7
nad4L
N
10,160/9289/9293/9356/9302
10,444/9576/9580/9640/9589
ATG/ATG/ATG/ATG/ATA
TAA/TAA/TAA/TAA/TAA
4/3/3/2/1
trnT
J
10,449/9580/9584/9643/9591
10,511/9642/9646/9704/9654
AGA
-1/-1/-1/-1/-1
trnP
N
10,511/9642/9646/9704/9654
10,574/9704/9708/9769/9717
AGG
1/1/1/1/1
nad6
J
10,576/9706/9710/9771/9719
11,079/10,185/10,189/10,259/10,192
ATT/ATA/ATA/ATG/ATT
TAA/TAA/TAA/TAA/TAA
-1/-1/-1/-1/-1
cytb
J
11,079/10,185/10,189/10,259/10,192
12,224/11,327/11,331/11,401/11,334
ATG/ATG/ATG/ATG/ATG
TAA/TAG/TAG/TAG/TAG
8/-2/-2/-2/-2
trnS2
J
12,233/11,326/11,330/11,400/11,333
12,298/11,391/11,395/11,465/11,400
ACA
17/9/9/19/14
nad1
N
12,316/11,411/11,415/11,485/11,415
13,266/12,361/12,365/12,432/12,365
TTG/TTG/TTG/TTG/TTG
TAA/TAA/TAA/TAG/TAA
1/1/1/0/1
trnL1
N
13,268/12,363/12,367/12,433/12,367
13,334/12,427/12,431/12,495/12,434
AAG
0/0/0/0/0
rrnL
N
13,335/12,428/12,432/12,496/12,435
14,605/13,693/13,697/13,757/13,692
0/0/0/0/0
trnV
N
14,606/13,694/13,698/13,758/13,693
14,674/13,762/13,766/13,826/13,761
AAC
0/0/0/0/0
rrnS
N
14,675/13,763/13,767/13,827/13,762
15,379/14,480/14,483/14,531/14,457
0/0/0/0/0
A + T rich region
15,380/14,481/14,484/14,532/14,458
16,521/15,499/15,514/16,108/15,367
0/0/0/0/0
Four of the 13 PCGs (nad1, nad4L, nad4, and nad5), eight tRNAs (trnQ, trnV, trnL1, trnP, trnH, trnF, trnY, and trnC), and two rRNAS (rrnL and rrnS) are encoded on the N-strand, whereas the other 23 genes (9 PCGs and 14 tRNAs) are encoded on the J-strand. The mitogenome sequence of these five buprestid species ranged in size from 15,367 to 16,521 bp.
The mean A + T nucleotide contents of five complete mitogenomes were similar: 68.42% in C.diminutus, 69.27% in C.cloueti, 72.42% in M.sinae, 71.73% in A.sichuanus, and 73.23% in S.femoralis. The entire mitogenomes had a higher A + T contents of 68.42–73.23% (66.05–72.50% for PCGs, 70.95–74.03% for tRNA genes, 75.20–77.33% for rRNA genes, and 74.17–78.38% for the CR) than G + C contents, which is consistent with the typical base of buprestid mitogenomes. The overall AT skews in these five complete mitogenomes were 0.12, 0.11, 0.11, 0.12, and 0.12, respectively. These five species showed a positive TA skew, suggesting that a slight AT bias which are similar to those observed in other buprestid species (Duan et al. 2017; Cao and Wang 2019a, 2019b; Xiao et al. 2019; Chen et al. 2021; Peng et al. 2021).
Protein-coding regions, codon usage, and nucleotide diversity
The total lengths of PCGs in these five buprestid species ranged from 11,090 to 11,158 bp, accounting for 67.54–72.17% of the entire mitogenomes. Similar to the other buprestid mitogenomes, nad5 and atp8 were found to be the largest (1708–1723 bp) and smallest (156–159 bp) genes, respectively. The majority of PCGs strictly started with an ATN (ATA/ATT/ATC/ATG) start codon, except for the nad1 starting with TTG. All PCGs strictly terminated with TAR (TAG/TAA) or an incomplete stop codon T–. Similar to most previously sequenced members of Buprestidae, the AT skew (0.11–0.12) of these five PCGs (Table 3) were similar among the 15 buprestid species. Summaries of the numbers of amino acids in the annotated PCGs and relative synonymous codon usage are presented in Figs 1 and 2. Overall codon usage among the sequenced buprestid mitogenomes was found to be similar, with Leu2, Ile, Phe, Ser2, Gly, Met, and Val being the seven most frequently coded amino acids.
Summarized mitogenomic characteristics of the five buprestid species in this study.
Numbers of different amino acids in the mitogenomes of the five buprestid species; the stop codon is not included. AS: Agrilussichuanus, CC: Coraebuscloueti, CD: Coraebusdiminutus, MS: Meliboeussinae, and SF: Sambusfemoralis.
RSCU (relative synonymous codon usage) of the mitogenomes of the five buprestid species; the stop codons are not included.
https://binary.pensoft.net/fig/669394
The nucleotide diversity (Pi) of the 13 PCGs among five species of Agrilinae is provided (Fig. 3), which ranged from 0.202 to 0.375. In these genes, nad2 (Pi = 0.375) presented the highest variability, followed by nad6 (Pi = 0.346), nad4 (Pi = 0.300), and nad5 (Pi = 0.290); cox1 (Pi = 0.20) exhibited the lowest variability. The ratio of Ka/Ks (Fig. 4) for each gene of the 13 PCGs was calculated. The values of nad4 and nad4L are distinctly higher than others, which suggests that the genes nad4 and nad4L have a relatively higher evolutionary rate.
The ratio of Ka/Ks of 13 PCGs among the 15 reported Buprestidae mitogenomes.
https://binary.pensoft.net/fig/669396tRNA, rRNA genes, and heterogeneity
The length of rrnL genes ranged from 1258 bp (S.femoralis) to 1271 bp (A.sichuanus), whereas rrnS ranged from 696 bp (S.femoralis) to 718 bp (C.diminutus). The A + T content of the rRNA genes ranged from 75.20% (C.diminutus) to 77.33% (M.sinae) (Table 3). Compared with those in other sequenced buprestid mitogenomes, the rRNA genes in these five newly sequenced buprestid mitogenomes are highly conserved (Hong et al. 2009; Duan et al. 2017; Cao and Wang 2019a, 2019b; Xiao et al. 2019; Sun et al. 2020; Chen et al. 2021; Peng et al. 2021). These rRNAs were located between the CR and trnL1, and separated by trnV. The total lengths of the 22 tRNA genes ranged from 1414 bp (C.cloueti) to 1444 bp (C.diminutus), whereas individual tRNA genes typically ranged in size from 58 to 70 bp, among which, eight tRNAs were encoded on the N-strand and the remaining 14 encoded on the J-strand. The secondary structures of tRNAs showed a standard clover-leaf structure (Suppl. material 1: Figs S2–S6), except for tRNA-Ser (Fig. 5) which lacks or has an unusual dihydrouridine arm, which forms a loop commonly found in other insects (Xiao et al. 2011; Park et al. 2012; Yu et al. 2016; Yan et al. 2017; Yu and Liang 2018; Li et al. 2019). In A.sichuanus, the longest intergenic nucleotide (774 bp) was located between trnW and trnC, which is an interesting and specific phenomenon in Buprestidae. The degree of heterogeneity of the 13 PCGs dataset was higher than that of the two rRNAs dataset (Suppl. material 1: Fig. S7). Additionally, the heterogeneity in sequence divergences was slightly stronger for Coraebus than for other buprestid genera (Suppl. material 1: Fig. S7).
The predicted secondary structures of the tRNA-Ser in the mitogenomes of the five buprestid species.
https://binary.pensoft.net/fig/669397Control region
The CR, also known as the A + T-rich region (Wolstenholme 1992), was the largest non-coding region and located between trnI and rrnS. The length of CR ranged from 910 bp (S.femoralis) to 1577 bp (M.sinae). The A + T content (74.17–78.38%) of the CR of these five species was found to be higher than that of the whole genome (68.42–73.23%), PCGs (66.05–72.50%), rRNAs (75.20–77.33%), and tRNAs (70.95–73.85%) (Table 3). Moreover, the compositional analysis revealed that the mitogenomes of the five buprestid species had a positive AT skew (0.02–0.18) in the CR. In these five species, only C.cloueti and C.diminutus had no tandem repeat element detected; however, those of A.sichuanus (20 and 40 bp), M.sinae (53 bp), and S.femoralis (265 bp) had different lengths.
Best-fit models of three datasets used for phylogeny.
ML method
BI method
13 PCGs
GTR+F+I+G4
GTR+F+I+G4
2 rRNAs
TVM+F+I+G4
GTR+F+I+G4
13 PCGs +2 rRNAs
GTR+F+I+G4
GTR+F+I+G4
Phylogenetic analyses
Both ML and BI trees using three datasets produced identical topologies (Figs 6–8), (Buprestinae + ((Chrysochroniae + Polycestinae) + Agrilinae)), in terms of subfamily-level relationship. The monophyly of Buprestidae is corroborated again, as all the buprestid species converged together as an independent clade, and two outgroup taxa obviously separated from the buprestid clade. The target species C.diminutus, C.cloueti, Meliboeussinae, Agrilussichuanus, and Sambusfemoralis, as well as other species of Agrilinae, converged together as an independent clade. And the target species, M.sinae, was most closely related to the genus Trachys with high value support (Figs 6–8) which is inconsistent with the previous studies (Kubáň et al. 2000; Evans et al. 2015). The relationship of Agrilinae clades obtained from 2 rRNAs and 13 PCGs + 2 rRNAs datasets are identical but with different topology from the 13 PCGs dataset. In the topology generated from the 13 PCGs dataset, S.femoralis and Agrilus were clustered into a single branch with high support value (Fig. 6, ML: 77, BI: 1) whereas, in the topology generated from the 2 rRNAs and 13 PCGs + 2 rRNAs datasets, S.femoralis split from base of the Agrilinae clades (Figs 7, 8). Based on these results the position of the genus Sambus in the tribe Agrilini was not suitable and suspect. The different tree topologies suggested that the rRNA genes were extremely valuable for the phylogenetic analysis of Agrilinae. Coraebini is the most diverse tribe in Agrilinae, and 10 subtribes are defined (Kubáň et al. 2000). The genus Meliboeus (Meliboeina) and Coraebus (Coraebina) in different clades suggested that the tribe Coraebini was polyphyletic, which is consistent with the previous study of Evans et al. (2015). The samples used in this study might be too limited for a comprehensive phylogeny of Buprestidae which still needs a deep study in the future.
Phylogenetic relationships of 15 selected buprestid species using both BI and ML analyses based on 13 PCGs of mitogenomes. The numbers on the branches show posterior probability (BI tree), whereas the values under branches are bootstrap (ML tree).
Phylogenetic relationships of 15 selected buprestid species using both BI and ML analyses based on 2 rRNAs of mitogenomes. The numbers on the branches show posterior probability (BI tree), whereas the values under branches are bootstrap (ML tree).
https://binary.pensoft.net/fig/669399Conclusions
In this study, five mitogenomes (15,367–16,521 bp) were newly sequenced and annotated, including representatives from the tribes Coraebini and Agrilini in subfamily Agriinae. The mitogenomes of the genera Sambus and Meliboeus are reported for the first time. These five sequences showed a positive AT skew, and the amino acids Leu, Ile, Phe, Ser2, Gly, Met, and Val were most frequently used. The secondary structures of tRNA-Ser are absent the D-arm, which is similar to other orders of Insecta. The rRNA genes are valuable for phylogenetic analyses of Agrilinae as they could affect the tree topologies. The results show that Coraebini is polyphyletic, and the genus Sambus belongs to neither Coraebini nor Agrilini. However, more mitogenome samplings are needed to resolve the phylogeny of the Buprestidae in the future to better understand the phylogenetics of jewel beetles.
Phylogenetic relationships of 15 selected buprestid species using both BI and ML analyses based on 13 PCGs + 2 rRNAs of mitogenomes. The numbers on the branches show posterior probability (BI tree), whereas the values under branches are bootstrap (ML tree).
I am sincerely grateful to Lanrui Wang (Qingyang, Gansu, China) and Yingqi Liu (China Agricultural University, Beijing, China) for their guidance in using the software. I also thank Dr Hui-Feng Zhao (Langfang Normal University, Hebei, China) and Menglin Wang (China West Normal University, Sichuan, China) for revising the manuscript. This work was supported by the Doctoral Scientific Research Foundation of China West Normal University (20E054).
ReferencesBellamyCL (1997) Phylogenetic relationships of Xyroscelis (Coleoptera: Buprestidae).11(4): 569–574. https://doi.org/10.1071/IT94026BellamyCL (2003) An illustrated summary of the higher classification of the superfamily Buprestoidea (Coleoptera). Folia Heyrovskyana (Supplementum 10): 1–197.BellamyCL (2008) A World Catalogue and Bibliography of the Jewel Beetles (Coleoptera: Buprestoidea). Volumes 1–4. Pensoft series faunistica No. 76–79, Sofia/Moscow, [8] + 2684 pp.BellamyCLVolkovitshM (2016) 18 Buprestoidea Crowson, 1955. In: BeutelRGLeschenRAB (Eds) Handbook of Zoology, Arthropoda: Insecta, Volume 1: Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim), 2nd edn., 543–552. https://doi.org/10.1515/9783110373929-021BensonG (1999) Tandem repeats finder: A program to analyze DNA sequences.27(2): 573–580. https://doi.org/10.1093/nar/27.2.573BernhardDFritzschGGlöcknerPWurstC (2005) Molecular insights into speciation in the Agrilusviridis-complex and the genus Trachys (Coleoptera: Buprestidae).102(4): 599–605. https://doi.org/10.14411/eje.2005.083BerntMDonathAJuhlingFExternbrinkFFlorentzCFritzschGStadlerPF (2013) MITOS: Improved de novo metazoan mitochondrial genome annotation.69(2): 313–319. https://doi.org/10.1016/j.ympev.2012.08.023CameronSL (2014) Insect mitochondrial genomics: Implications for evolution and phylogeny.59(1): 95–117. https://doi.org/10.1146/annurev-ento-011613-162007CaoLMWangXY (2019a) The complete mitochondrial genome of the jewel beetle Trachysvariolaris (Coleoptera: Buprestidae).4(2): 3042–3043. https://doi.org/10.1080/23802359.2019.1666053CaoLMWangXY (2019b) The complete mitochondrial genome of the jewel beetle Coraebuscavifrons (Coleoptera: Buprestidae).4(2): 2407–2408. https://doi.org/10.1080/23802359.2019.1636730Capella-GutiérrezSSilla-martínezJMGabaldónT (2009) TrimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses.25(15): 1972–1973. https://doi.org/10.1093/bioinformatics/btp348ChenBWeiZHShiAM (2021) The complete mitochondrial genome of the jewel beetle, Anthaxiachinensis (Coleoptera: Buprestidae).6(10): 2962–2963. https://doi.org/10.1080/23802359.2021.1973920ClineARSmithTRMillerKMoultonMWhitingMAudisioP (2014) Molecular phylogeny of Nitidulidae: assessment of subfamilial and tribal classification and formalization of the family Cybocephalidae (Coleoptera: Cucujoidea).39(4): 758–772. https://doi.org/10.1111/syen.12084CobosA (1980) Ensayo sobre los géneros de la subfamilia Polycestinae (Coleoptera, Buprestidae) (Parte I). EOS.54: 15–94.CobosA (1986) Consejo Superior de Invertigaciones Cientificas, Madrid, 364 pp.DuanJQuanGXMittapalliOCussonMKrellPJDoucetD (2017) The complete mitogenome of the Emerald Ash Borer (EAB), Agrilusplanipennis (Insecta: Coleoptera: Buprestidae).2(1): 134–135. https://doi.org/10.1080/23802359.2017.1292476EvansAMMckennaDDBellamyCLFarrellBD (2015) Large-scale molecular phylogeny of metallic wood-boring beetles (Coleoptera: Buprestoidea) provides new insights into relationships and reveals multiple evolutionary origins of the larval leaf-mining habit.40(2): 385–400. https://doi.org/10.1111/syen.12108GimmelMLBocakovaMGunterNLLeschenmRAB (2019) Comprehensive phylogeny of the Cleroidea (Coleoptera: Cucujiformia).44(3): 527–558. https://doi.org/10.1111/syen.12338GreinerSLehwarkPBockR (2019) OrganellarGenomeDRAW (OGDRAW) version 1.3.1: Expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research 47(W1): W59–W64. https://doi.org/10.1093/nar/gkz238GuindonSDufayardJLefortVAnisimovaMHordijkWGascuelO (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0.59(3): 307–321. https://doi.org/10.1093/sysbio/syq010HansenJAMoultonJKKlingemanWEOliverJBWindhamMTTrigianoRNRedingME (2016) Molecular systematics of the Chrysobothrisfemorata species group (Coleoptera: Buprestidae).108(5): 950–963. https://doi.org/10.1093/aesa/sav080HołyńskiRB (1988) Remarks on the general classification of Buprestidae Leach as applied to Maoraxiina.49(1): 49–54.HołyńskiRB (1993) A reassessment of the internal classification of the Buprestidae Leach (Coleoptera). Crystal.1: 1–42.HołyńskiRB (2009) Gondwana, Warszawa, 391 pp.HongMYJeongHCKimMJJeongHULeeSHKimI (2009) Complete mitogenome sequence of the jewel beetle, Chrysochroafulgidissima (Coleoptera: Buprestidae).20(2–3): 46–60. https://doi.org/10.1080/19401730802644978KelnarovaIJendekEGrebennikovVVBocakL (2019) First molecular phylogeny of Agrilus (Coleoptera: Buprestidae), the largest genus on Earth, with DNA barcode database for forestry pest diagnostics.109(2): 200–211. https://doi.org/10.1017/S0007485318000330KrzywinskiJLiCMorrisMConnJELimaJBPovoaMMWilkersonRC (2011) Analysis of the evolutionary forces shaping mitochondrial genomes of a Neotropical malaria vector complex.58(3): 469–477. https://doi.org/10.1016/j.ympev.2011.01.003KubáňV (2016) Revised and updated edition; Leiden, Boston, 549 pp.KubáňVMajerKKolibáčJ (2000) Classification of the tribe Coraebini Bedel, 1921 (Coleoptera, Buprestidae, Agrilinae). Acta Musei Moraviae.85: 185–287.KubáňVVolkovitshMGKalashianMJJendekE (2016) Family Buprestidae Leach, 1815. In: LöblILöblD (Eds) Catalogue of Palaearctic Coleoptera., 432–574.KückPMeidSAGroßCWägeleJWMisofB (2014) AliGROOVE–visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support. Bioinformatics (Oxford, England) 15: e294. https://doi.org/10.1186/1471-2105-15-294KumarSStecherGTamuraK (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054KundrataRJächMABocakL (2017) Molecular phylogeny of the Byrrhoidea–Buprestoidea complex (Coleoptera, Elateriformia).46(2): 150–164. https://doi.org/10.1111/zsc.12196LeeMHLeeSLeschenRABLeeS (2020) Evolution of feeding habits of sap beetles (Coleoptera: Nitidulidae) and placement of Calonecrinae.45(4): 911–923. https://doi.org/10.1111/syen.12441LiRShuXHLiXDMengLLiBP (2019) Comparative mitogenome analysis of three species and monophyletic inference of Catantopinae (Orthoptera: Acridoidea).111(6): 1728–1735. https://doi.org/10.1016/j.ygeno.2018.11.027LibradoPRozasJ (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data.25(11): 1451–1452. https://doi.org/10.1093/bioinformatics/btp187LoweTMChanPP (2016) tRNAscan-SE On-line: Integrating search and context for analysis of transfer RNA genes. Nucleic Acids Research 33(W1): W686–W689. https://doi.org/10.1093/nar/gkw413ParkJSChoYKimMJNamSHKimI (2012) Description of complete mitochondrial genome of the black-veined white, Aporiacrataegi (Lepidoptera: Papilionoidea), and comparison to papilionoid species.15(3): 331–341. https://doi.org/10.1016/j.aspen.2012.01.002PellegrinoICurlettiGLiberatoreFCuccoM (2017) Cryptic diversity of the jewel beetles Agrilusviridis (Coleoptera: Buprestidae) hosted on hazelnut.84(1): 465–472. https://doi.org/10.1080/24750263.2017.1362050PengXJLiuJWangZZhanQZ (2021) The complete mitochondrial genome of the pyrophilous jewel beetle Melanophilaacuminata (Coleoptera: Buprestidae). Mitochondrial DNA.6(3): 1059–1060. https://doi.org/10.1080/23802359.2021.1899079PentinsaariMMutanenMKailaL (2014) Cryptic diversity and signs of mitochondrial introgression in the Agrilusviridisspecies complex (coleoptera: Buprestidae).111(4): 475–486. https://doi.org/10.14411/eje.2014.072PernaNTKocherTD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes.3(3): 353–358. https://doi.org/10.1007/BF01215182QinJZhangYZZhouXKongXBWeiSJWardRDZhangAB (2015) Mitochondrial phylogenomics and genetic relationships of closely related pine moth (Lasiocampidae: Dendrolimus) species in China, using whole mitochondrial genomes. Genomics 16(1): e428. https://doi.org/10.1186/s12864-015-1566-5RobertsonJAŚlipińskiAMoultonMShockleyFWGorgiALordNPMcKennaDDTomaszewskaWForresterJMillerKBWhitingMFMcHughJV (2015) Phylogeny and classification of Cucujoidea and the recognition of a new superfamily Coccinelloidea (Coleoptera: Cucujiformia).40(4): 745–778. https://doi.org/10.1111/syen.12138RonquistFTeslenkoMDer MarkPVAyresDLDarlingAEHohnaSHuelsenbeckJP (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space.61(3): 539–542. https://doi.org/10.1093/sysbio/sys029SacconeCDe GiorgiCGissiCPesoleGReyesA (1999) Evolutionary genomics in Metazoa: The mitochondrial DNA as a model system.238(1): 195–209. https://doi.org/10.1016/S0378-1119(99)00270-XSheffieldNCSongHCameronSLWhitingMF (2009) Nonstationary evolution and compositional heterogeneity in beetle mitochondrial phylogenomics.58(4): 381–394. https://doi.org/10.1093/sysbio/syp037ShortAEZFikáčekM (2013) Molecular phylogeny, evolution, and classification of the Hydrophilidae (Coleoptera).38(4): 723–752. https://doi.org/10.1111/syen.12024SongFLiHLiuGHWangWJamesPColwellDDTranAGongSCaiWZShaoR (2019) Mitochondrial genome fragmentation unites the parasitic lice of eutherian mammals.68(3): 430–440. https://doi.org/10.1093/sysbio/syy062SunHQZhaoWXLinRZZhouZFHuaiWXYaoYX (2020) The conserved mitochondrial genome of the jewel beetle (Coleoptera: Buprestidae) and its phylogenetic implications for the suborder Polyphaga.112(5): 3713–3721. https://doi.org/10.1016/j.ygeno.2020.04.026ThompsonJDHigginsDGGibsonTJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.22(22): 4673–4680. https://doi.org/10.1093/nar/22.22.4673TôyamaM (1987) The systematic positions of some buprestid genera (Coleoptera, Buprestidae).15: 1–11.WangWQHuangYXBartlettCRZhouFMMengHQinDZ (2019) Characterization of the complete mitochondrial genomes of two species of the genus Aphaena Guérin-Méneville (Hemiptera: Fulgoridae) and its phylogenetic implications.141: 29–40. https://doi.org/10.1016/j.ijbiomac.2019.08.222WolstenholmeDR (1992) Animal mitochondrial DNA: Structure and evolution.141: 173–216. https://doi.org/10.1016/S0074-7696(08)62066-5XiaoJHJiaJGMurphyRWHuangDW (2011) Rapid evolution of the mitochondrial genome in chalcidoid wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. PLoS ONE 6(11): e26645. https://doi.org/10.1371/journal.pone.0026645XiaoLFZhangSDLongCPGuoQYXuJSDaiXHWangJG (2019) Complete mitogenome of a leaf-mining buprestid Beetle, Trachysauricollis, and its phylogenetic implications. Genes 10(12): e992. https://doi.org/10.3390/genes10120992YanLZhangMGaoYPapeTZhangD (2017) First mitogenome for the subfamily Miltogramminae (Diptera: Sarcophagidae) and its phylogenetic implications.114: 422–429. https://doi.org/10.14411/eje.2017.054YuFLiangAP (2018) The complete mitochondrial genome of Ugyops sp. (Hemiptera: Delphacidae). Journal of Insect Science 18(3): e25. https://doi.org/10.1093/jisesa/iey063YuPChengXMaYYuDZhangJ (2016) The complete mitochondrial genome of Brachythemiscontaminata (Odonata: Libellulidae).27: 2272–2273. https://doi.org/10.3109/19401736.2014.984176ZhangDGaoFJakovlićIZouHZhangJLiWXWangGT (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies.20(1): 348–355. https://doi.org/10.1111/1755-0998.13096Supplementary materials10.3897/zookeys.1092.80993.suppl1653210230F62A85-710A-57B4-A1A8-D80168AB38B9
Figures S1–S7
Images (pdf file)
Figure S1. The mitogenome maps of Agrilussichuanus, Coraebuscloueti, Coraebusdiminutus, Meliboeussinae, and Sambusfemoralis. Figure S2. The secondary cloverleaf structure for the tRNAs of Agrilussichuanus. Figure S3. The secondary cloverleaf structure for the tRNAs of Coraebuscloueti. Figure S4. The secondary cloverleaf structure for the tRNAs of Coraebusdiminutus. Figure S5. The secondary cloverleaf structure for the tRNAs of Meliboeussinae. Figure S6. The secondary cloverleaf structure for the tRNAs of Sambusfemoralis. Figure S7. Heterogeneous sequence divergence within datasets 13 PCGs and 2 rRNAs of Buprestidae species.
https://binary.pensoft.net/file/669401This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.Zhonghua Wei