The complete mitochondrial genome of Chilo infuscatellus (Lepidoptera: Pyralidae), and related phylogenetic analysis

doi:10.21203/rs.3.rs-3243773/v1

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The complete mitochondrial genome of Chilo infuscatellus (Lepidoptera: Pyralidae), and related phylogenetic analysis

https://doi.org/10.21203/rs.3.rs-3243773/v1

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published 02 Feb, 2024

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The Chilo infuscatellus (Lepidoptera: Pyralidae) is a significant pest of sugarcane in China. The genome-level characteristics of this pest are important genetic resources for identification, phylogenetic analysis, and even management. In the present study, the complete mitogenome of C. infuscatellus was sequenced and characterized. The complete mitogenome of C. infuscatellus is 15,252 bp in length and comprises 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), 2 ribosomal RNA genes (rRNAs), and an A + T-rich region. Except for the CGA codon for the cox1 gene, the PCGs initiated with ATN codons (ATG, ATT, and ATA). These PCGs terminated with TAA or an incomplete T. Except for the loss of the “DHU” arm for trnS1, the tRNA genes were folded into the typical cloverleaf structure. The A + T-rich region has a high AT content of 96.19% and contains the motifs “ATAGA” and “ATTTA”, as well as a 19 bp poly-T stretch and microsatellite regions. The C. infuscatellus mitogenome exhibits a conserved gene order among lepidopteran insects, with a rearrangement of the trnM gene compared to the ancestral mitogenome. Phylogenetic analysis based on the 13 PCGs using Bayesian inference (BI) and maximum likelihood (ML) methods confirmed the monophyly of Pyralidae and Crambidae within Pyraloidea. The relationships between subfamilies in Pyralidae can be described as (Galleriinae + (Phycitinae + (Pyralinae + Epipaschiinae))). The “PS clade” and “non-PS clade” were formed in the family Crambidae. Our results enrich the genetic resources of sugarcane borers and provide insights into the phylogeny of Pyraloidea insects.

mitochondrial genome

pyralidae

phylogenetic analysis

gene rearrangement

Pyraloidea is the third richest superfamily within the order Lepidoptera and consists of the family Pyralidae and the family Crambidae (Solis, 2007). It is a very large group of lepidopteran insects that contains more than 15,684 species (Regier et al., 2012). Several Pyraloidea insects are notorious pest species, causing great losses in agriculture and forestry, such as sugarcane borers (Wang et al., 2018), Ostrinia furnacalis (Iqbal et al., 2021), and Cnaphalocrocis medinalis (Zheng et al., 2011). Accurate identification and phylogenetic understanding of these pests are crucial for studying and managing them effectively (Regier et al., 2012). However, morphology-based taxonomy of certain pyralids may be a great challenge due to their high species diversity. For instance, the two main sugarcane borers, namely Chilo infuscatellus (Snellen; Lepidoptera: Pyralidae) and Chilo sacchariphagus (Lepidoptera: Crambidae), exhibit similar morphology and cause similar damage to sugarcane (Wang et al., 2018). Furthermore, the phylogenetic relationships among the 21 subfamilies within Pyraloidea have been controversial according to certain groups of investigations on morphological and genetic data (Liu et al., 2021; Wu et al., 2023).

Mitochondria are unique organelles that are found in nearly all eukaryotic cells and have their own genomes (Osellame et al., 2012; Chen et al., 2022). Animal mitogenome is a double-stranded circular DNA molecule that encodes 37 conserved genes, including 13 protein-coding genes (PCGs), 2 ribosomal RNA (rRNA) genes, 22 transfer RNA (tRNA) genes, and a control region (A + T-rich region) that regulate its transcription and replication (Boore, 1999; Taanman, 1999; Cameron, 2014). The mitochondrial genome is an excellent molecular marker for phylogenetic analyses and species identification due to several unique characteristics including conserved gene components, infrequent recombination, maternal inheritance, and a relatively fast evolution rate (Curole et al., 1999; Cameron, 2014). Moreover, the entire mitochondrial genome can also provide genome-level characteristics for phylogenetic research such as gene arrangement and composition (Tyagi et al., 2020; Yi et al., 2022). With the advancements in sequencing techniques, numerous complete mitogenomes have been obtained and applied in a wide range of evolutionary studies in recent years (Chen et al., 2022; Wu et al., 2023).

Chilo infuscatellus (Lepidoptera: Pyralidae) is an economic pest found in sugarcane-producing areas of southern China and undergoes complete metamorphosis insects in the northern millet area in the north (Wang et al., 2018). There are few studies on its biology and physiology, particularly the research on the mitochondrial genome has not been reported. In the present study, the complete mitogenome of C. infuscatellus was obtained by using next-generation sequencing (NGS). The characteristics of the C. infuscatellus mitogenome were described, including its genome structure, nucleotide composition, and codon usage. In addition, the phylogenetic position of C. infuscatellus within Pyraloidea was explored based on the 13 PCGs by using maximum likelihood (ML) and Bayesian inference (BI) analysis. Our study not only enriches the mitogenomic data resources but also offers further evidence for the evolution of species within the superfamily Pyraloidea.

Sample collection and DNA extraction

Specimens of C. infuscatellus were collected from sugarcane orchards in Zhanjiang City, Guangdong Province, China. Fresh samples were preserved in 100% ethanol and stored in a -20°C freezer. Total genomic DNA was isolated from the whole body of C. infuscatellus using a DNeasy tissue kit (Qiagen, Hilden, Germany). The quality of the extracted DNA was assessed by a Qubit fluorometer with a dsDNA high-sensitivity kit (ThermoFisher, Foster City, CA, USA) and 1.0% agarose gel electrophoresis.

Mitochondrial genome sequencing and assembly

The mitogenome of C. infuscatellus was sequenced using next-generation sequencing. The extracted DNA was used to construct the sequencing library with the NEBNext Ultra DNA Library Prep Kit. Sequencing was carried out on the Illumina NovaSeq 6000 platform (BIOZERON Co., Ltd, Shanghai, China). A total of 5.099 Gb of raw data was obtained with 150 bp paired-end read lengths. The Trimmomatic v0.39 was used to remove the adapters and low-quality reads. Finally, a total of 5.08 Gb of clean data with a Q30 of 93.02% was obtained after data trimming and filtering. According to the reference mitogenome of closely related species C. sacchariphagus (GenBank Accession number: NC_029716.1), the Illumina reads of the mitochondrion were de novo assembled using the SPAdes-3.13.1 package (Bankevich et al., 2012).

Mitochondrial genome annotation and analysis

The PCGs, rRNA genes, and tRNA genes were identified using the MITOS Web Server (http://mitos.bioinf.uni-leipzig.de/index.py) (Bernt et al., 2013). ORF software available on the NCBI website (http://www.ncbi.nlm.nih.gov/projects/gorf/) was also used to validate the annotated protein-coding gene. The sequence length, base content, codon usage, and amino acid composition were statistically analyzed using Editseq and MEGA 5.0 (Kumar et al., 2004). The bias of nucleotide composition was measured as AT skewness (AT skewness = (A - T)/ (A + T)) and GC skewness (GC skewness = (G - C)/(G + C)) respectively. The mitogenome sequence data of C. infuscatellus has been deposited in the GenBank database.

Phylogenetic analysis

A total of 13 PCGs from 54 lepidopteran mitogenomes were used for phylogenetic analysis (Table S1). Thitarodes renzhiensis and Pieris rapae were used as the outgroups. The 13 PCGs from each species were extracted and concatenated by PhyloSuite v1.2.2, and subsequently aligned by MAFFT 7.14934 and MACSE v. 2.03. The Gblocks v0.91b36 was employed to obtain the conserved blocks from the aligned sequences. The best evolutionary model was GTR + F + R4 which is selected by using ModelFinder based on the Bayesian Information Criterion (BIC). Phylogenetic trees were conducted using Bayesian inference (BI) and maximum-likelihood (ML) methods, respectively. ML analyses were performed by IQtree with 1,000 replicates of ultrafast likelihood bootstrap. And BI analyses were performed using MrBayes v3.2.2 (Huelsenbeck and Ronquist, 2001), with 3 million generations and sampling every 1000 generations. The first 25% of samples were discarded as burn-in. The phylogenetic trees were visualized using FigTree v1.4.2.

Genome composition and base structure

The complete mitogenome of C. infuscatellus was 15,252 bp in length (GenBank accession number: OR288533), within the range of sequenced lepidopteran mitogenomes from 14,838 to 16,173 bp (Table S1). This mitogenome contained a total of 37 genes, including 13 PCGs (cox1-cox3, cob, nad1-nad6, nad4l, atp6, and atp8), 22 tRNA genes, and 2 rRNA genes (Table 1). Among them, 4 PCGs (nad1, nad4, nad4l, and nad5), 8 tRNA genes (trnF, trnH, trnP, trnL1, trnV, trnQ, trnC, and trnY), and 2 rRNA genes were encoded by the minor strand (N-strand) (Fig. 1). The remaining 23 genes were encoded by the major strand (J-strand). The location and structure of the protein-coding genes, tRNA genes, and rRNA genes were found to be conserved.

Table 1

Characteristics of the mitochondrial genome of *Chilo infuscatellus*
Feature	Strand	Location	Size(bp)	Anticodon	Start/Stop codon	Intergenic nucleotides
trnM	+	1–67	67	CAT		0
trnI	+	68–134	67	GAT		3
trnQ	-	138–206	69	TTG		53
nad2	+	260–1273	1014		ATT/TAA	1
trnW	+	1275–1341	67	TCA		-8
trnC	-	1334–1403	70	GCA		2
trnY	-	1406–1470	65	GTA		6
cox1	+	1477–3007	1531		CGA/T	0
trnL2	+	3008–3074	67	TAA		0
cox2	+	3075–3759	685		ATG/T	-3
trnK	+	3757–3826	70	CTT		0
trnD	+	3827–3896	70	GTC		0
atp8	+	3897–4062	166		ATT/T	-2
atp6	+	4061–4738	678		ATG/TAA	-1
cox3	+	4738–5526	789		ATG/TAA	2
trnG	+	5529–5594	66	TCC		0
nad3	+	5595–5948	354		ATT/TAA	8
trnA	+	5957–6021	65	TGC		3
trnR	+	6025–6090	66	TCG		-1
trnN	+	6090–6154	65	GTT		-1
trnS1	+	6154–6219	66	GCT		3
trnE	+	6223–6289	67	TTC		3
trnF	-	6293–6360	68	GAA		0
nad5	-	6361–8098	1738		ATT/T	0
trnH	-	8099–8163	65	GTG		-1
nad4	-	8163–9503	1341		ATG/TAA	-2
nad4l	-	9502–9793	292		ATG/T	2
trnT	+	9796–9859	64	TGT		0
trnP	-	9860–9924	65	TGG		2
nad6	+	9927-10,454	528		ATA/TAA	13
cob	+	10,468 − 11,613	1146		ATG/TAA	-2
trnS2	+	11,612 − 11,680	69	TGA		12
nad1	-	11,693 − 12,634	942		ATG/TAA	1
trnL1	-	12,636 − 12,702	67	TAG		-21
rrnL	-	12,682 − 14,069	1388			-2
trnV	-	14,068 − 14,133	66	TAC		0
rrnS	-	14,134 − 14,911	778			0
A + T-rich region		14,912 − 15,252	341			0

Note: + represents the major strand; - represents the minor strand.

The mitogenome of C. infuscatellus exhibits 11 gene overlaps, ranging in size from 1 to 21 bp, and 15 intergenic spacers, ranging in length from 1 to 53 bp (Table 1). The largest gene overlap is observed between trnL1 and rrnL, and there is a 2 bp overlapping fragment between atp8 and atp6, which is shorter than that in most lepidopteran mitogenomes (Campbell and Barker, 1999; Cao et al., 2014; Wang et al., 2022). The longest intergenic spacer is located between trnQ and nad2 (Table 1).

The nucleotide composition of the C. infuscatellus mitogenome was as follows: T (40.30%), A (39.83%), C (11.99%), and G (7.88%). The A + T content, which is consistent with the characteristic of a strong A + T bias in insect mitogenome, was 80.13% in the entire mitogenome, 78.38% in PCGs, 81.58% in tRNA genes, and 84.86% in rRNA genes (Table 2). The GC skewness was considerably higher than that of the AT skewness across the entire mitogenome, with values of -0.01 and − 0.21 for AT and GC skewness, respectively. Moreover, the content of the T base was higher than that of A, while the content of the C base was higher than that of G.

Table 2

Nucleotide composition of *C. infuscatellus* mitogenome.
Feature	A%	T%	C%	G%	AT%	GC%	AT Skew	GC Skew
protein-coding genes	33.73	44.65	10.43	11.18	78.38	21.62	-0.14	0.03
1st codon position	36.92	36.60	10.19	16.29	73.52	26.48	0.004	0.23
2nd codon position	21.99	48.49	16.18	13.34	70.48	29.52	-0.38	-0.10
3rd codon position	42.27	48.89	4.93	3.91	91.16	8.84	-0.07	-0.12
tRNAs	40.86	40.72	7.89	10.54	81.58	18.42	0.00	0.14
rRNAs	43.17	41.69	4.85	10.30	84.86	15.14	0.02	0.36
A + T-rich region	45.45	50.73	2.93	0.88	96.19	3.81	-0.05	-0.54
whole mitogenome	39.83	40.30	11.99	7.88	80.13	19.87	-0.01	-0.21

PCGs

The A + T content in the PCGs of the C. infuscatellus mitogenome was measured to be 78.38%, which was significantly higher than the G + C content (21.62%). Notably, the A + T content at the third codon position was the highest (91.16%) (Table 2), which is consistent with other insect mitogenomes (Boore, 1999; Tang et al., 2014; Yang et al., 2021; Kim et al., 2022). GC skewness was lower than AT skewness in 13 PCGs, which was in contrast to the skewness observed in the entire mitogenome. AT skewness was − 0.14, and GC skewness was 0.03. In lepidopteran mitogenomes, the AT skewness values of PCGs are all negative, while the values of GC skewness can be either negative or positive.

Among the 13 PCGs in the C. infuscatellus mitogenome, seven PCGs (cox2, atp6, cox3, nad4, nad4l, cob, and nad1) start with ATG, while four PCGs (nad2, atp8, nad3, and nad5) start with ATT. The remaining two PCGs, e.g. cox1 and nad6, start with CGA and ATA, respectively. The ATN and CGA start codons for PCGs are commonly found in insect mitogenomes (Sun et al., 2016; Zheng et al., 2018). Regarding the termination codons, eight PCGs (nad2, atp6, cox3, nad3, nad4, cob, nad1, and nad6) end with TAA. Five PCGs (cox1, cox2, atp8, nad5, and nad4l) have an incomplete termination codon of a single T. The incomplete termination codon, widely observed in insect mitogenomes, is believed to potentially undergo completion through the process of post-transcriptional polyadenylation (Ojala et al., 1981; Jiang et al., 2009; Donath et al., 2019).

The relative synonymous codon usage was calculated using MEGA5.0. Results showed that amino acids with two synonymous codons exhibited a high usage frequency of A or U in the third codon position. Codon usage analysis showed that the most frequently used codon was UUA (L), followed by AUU (I), UUU (F), AUA (I), AAU (N), and UAU (Y). The biased usage of A and U results in a high A + T content in other insect mitogenomes (Ding et al., 2023; Huang et al., 2022, 2023). Additionally, the analysis of amino acid composition showed that Leu was the highest, followed by Ile, Phe, and Ser (Fig. 2).

rRNA and tRNA genes

Two rRNA genes (rrnL and rrnS) of the C. infuscatellus mitogenome were 1388 and 778 bp in length, respectively. They were located between trnL1 and trnV, and between trnV and the A + T-rich region, respectively. The analysis of base composition showed that the A + T content of rRNA genes was 84.86%. The A + T bias was obvious, and the AT-skew and GC-skew were 0.02 and 0.36, respectively. The length, location, and base composition of two rRNA genes were similar to those of other lepidopteran insects (Table 1) (Boore, 1999; Taanman, 1999; Yang et al., 2021; Kim et al., 2022; Yukuhiro et al., 2002; Qin et al., 2015; Yang et al., 2019).

The total length of the 22 tRNA genes in the C. infuscatellus mitogenome is 1471 bp. Among these tRNAs, trnK, trnC, and trnD were the longest (70 bp), while trnT was the shortest with only 64 bp in size. The “DHU” arm was absent in the trnS1 gene, and trnS2 exhibited two mismatched base pairs in the anticodon stem (Fig. 3). Similarly, trnL1 (CUN) and trnA contain a U-U mismatch in the recipient stem. All tRNA genes, except for trnS1, were folded into the typical cloverleaf structure. This is consistent with the results obtained by other lepidopteran insects (Chai et al., 2012; Bian et al., 2020).

A + T-rich region

The A + T-rich region of the C. infuscatellus mitogenome is 341 bp in length, located between rrnS and trnM (Fig. 4 and Table 1). The content of A + T is high at 96.19%, while the content of G + C is only 3.81%. The AT-skew for the control region was slightly negative (-0.05), indicating a higher occurrence of T nucleotides compared to A nucleotides. The length and A + T content of this region are comparable to those of other insects within the same genus, such as Chilo suppressalis (Chai et al., 2012), Chilo auricilius (Cao and Du, 2014), and C. sacchariphagus. However, the A + T-rich region in the T. renzhiensis mitogenome is 1367 bp in size (Cao et al., 2012), while it is 288 bp in the Cydalima perspectalis mitogenome (Gao et al., 2023), This suggests that the A + T-rich region in lepidopteran mitogenomes is not conserved.

The A + T-rich region of the C. infuscatellus mitogenome contains a motif of “ATAGA” and a 19 bp poly-T stretch, which is similar to most lepidopteran mitogenomes (Chen et al., 2022; Shah et al., 2022). The ten copies of “ATTTA” motif and microsatellite A/T repeat sequences were also found in the A + T-rich region, which are considered common features in insects (Kim et al., 2012; Bian et al., 2020; Riyaz et al., 2021). In addition, a 6 bp poly-T stretch was observed at the end of the A + T-rich region.

Gene rearrangement

Gene rearrangement is an important clue for exploring the evolution of insects. In contrast to the high frequency of rearrangement events found in Hymenoptera, lepidopteran mitogenomes have a relatively conserved gene arrangement (Zhu et al., 2018; Yi et al., 2022). CREx analysis demonstrated that the mitogenome of C. infuscatellus exhibits trnM gene rearrangement events compared to the ancestral mitogenome (Fig. 5). The order of tRNA genes between the A + T-rich region and nad2 has been changed from trnI-trnQ-trnM to trnM-trnI-trnQ. This rearrangement occurred among most lepidopteran species, except for the Hepialoidea species, which maintains the ancestral gene order (Cao et al., 2012). It implies that the rearrangement of trnM occurred during the divergence of Hepialoidea and other lepidopteran lineages. The rearrangement is commonly explained by the tandem duplication-random loss (TDRL) model, which suggests that the trnM gene underwent duplication and subsequent loss in a random manner (Cameron, 2014).

Phylogenetic analysis

The phylogenetic trees were constructed based on 13 PCGS of 54 lepidopteran mitogenomes using ML and BI methods (Fig. 6). The phylogeny of the superfamily Pyraloidea has been extensively discussed in numerous studies, and the phylogenetic relationships within the superfamily Pyraloidea are relatively stable. Although some clades exhibited low support values, the results of the two trees were identical.

In the present study, two phylogenetic trees were divided into two branches. One branch is composed of four subfamilies of the Pyralidae, while the other branch is composed of seven subfamilies of the Crambidae. This strongly supports the monophyly of Pyralidae and Crambidae (Qi et al., 2021; Wu et al., 2023). Except for the absence of the mitogenome in Chrysauginae, there are five subfamilies within Pyralidae. The phylogenetic relationships among these subfamilies were presented as ((Epipaschiae + Pyralinae) + Phylitinae) + Galleriinae) (Fig. 6). These results are consistent with numerous reports in recent years (Zhu et al., 2018; Liu et al., 2021) and do not support the reversion of Phycitinae and Pyralinae based on a unique orientation of the uncus arms, as reported in the early study (Solis and Mitter, 1992). Within the family Crambidae, two lineages were identified, namely the “PS clade” (Pyraustinae and Spilomelinae) and the “non-PS clade” (the other subfamilies) (Regier et al., 2012). Our results confirmed that Spilomelinae and Pyraustinae were grouped together and separated from the other subfamilies. It has been reported that the “non-PS clade” can be further divided into two branches, namely the “OG clade”(including Odontiinae and Glaphyriinae) and the “CAMMSS clade”(including Nymphulinae, Crambinae, Scopariinae, and Schoenobiinae) (Regier et al., 2012). Our BI and ML analyses supported the absence of two clades. However, the phylogenetic relationship of subfamilies in the “CAMMSS clade” is highly controversial in various literature (Yang et al., 2018; Roh et al., 2020). Certain groups of researchers suggested that the phylogenetic relationship can be represented as (Scopariinae + Crambinae) + (Nymphulinae + Schoenobiinae) (Regier et al., 2012; Jeong et al., 2021; Cheng et al., 2022). However, other researchers have reported alternative relationships, including (Scopariinae + (Crambinae + (Schoenobiinae + Nymphulinae))) or (Schoenobiinae + (Scopariinae + (Nymphulinae + Crambinae))) (Gao et al., 2023; Wu et al., 2023). In this article, the relationship among the three taxa appears to be ((Nymphulinae + Scopariinae) + (Crambinae + Schoenobiinae)), but with low bootstrap support. It is also supported by another recent study (Liu et al., 2021). The controversial phylogenetic relationship of these subfamilies may be attributed to the limited availability of mitochondrial data for the subfamily Schoenobiinae. More data is required to validate these findings.

The C. infuscatellus has a typical lepidopteran mitogenome that contains containing 13 PCGs, 2 rRNAs, 22 tRNAs, and a CR. It is 15,252 bp in length and has a high AT content of 76.49%. The PCGs initiated with ATN codons or CGA and terminated with TAA or an incomplete T. The loss of the “DHU” arm was found in trnS1. The control region exhibits the highest AT content and contains a motif of “ATAGA”, a 19 bp of poly-T stretch, and ten copies of ATTTA. The gene order of C. infuscatellus mitogenome is conserved among Lepidoptera. The two phylogenetic trees were identical and the phylogenetic relationships of subfamilies within Pyraloidea are well-supported by recent research. In conclusion, this study enriches the genetic data for the identification and phylogeny of sugarcane borers.

Author Contributions

All authors contributed to the study conception and design. YJ, LJ, MY: methodology, data acquisition and analysis, original draft preparation; CY, LM, XH, AY:data analysis, data interpretation; LJ and WH: supervising, writing, and editing. All the authors have read and approved the manuscript.

Funding

This work was financially supported by the GDAS' Project of Science and Technology Development (Grant No. 2020GDASYL-20200103056 & 2020GDASYL-20200103072), the National Natural Science Foundation of China (Grant No: 32172471) and Qingyuan Municipal Science and Technology Project (2020KJJH033).

Conflicts of Interest

The authors declare no conflict of interest.

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TableS1Listofmitogenomesusedforphylogeneticanalysis.docx
Table S1 List of mitogenomes used for phylogenetic analysis.

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The complete mitochondrial genome of Chilo infuscatellus (Lepidoptera: Pyralidae), and related phylogenetic analysis

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Abstract

Figures

Introduction

Materials and Methods

Sample collection and DNA extraction

Mitochondrial genome sequencing and assembly

Mitochondrial genome annotation and analysis

Phylogenetic analysis

Results

Genome composition and base structure

PCGs

rRNA and tRNA genes

A + T-rich region

Gene rearrangement

Phylogenetic analysis

Conclusions

Declarations

References

Additional Declarations

Supplementary Files

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Journal Publication

Version 1