Abstract
The coffee leaf miner (Leucoptera coffeella) is one of the major pests of coffee crops in the neotropical regions, and causes major economic losses. Few molecular data are available to identify this pest and advances in the knowledge of the genome of L. coffeella will contribute to improving pest identification and also clarify taxonomy of this microlepidoptera. L. coffeella DNA was extracted and sequenced using PacBio HiFi technology. Here we report the complete L. coffeella circular mitochondrial genome (16,407 bp) assembled using Aladin software. We found a total of 37 genes, including 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), 2 ribosomal RNA genes (rRNAs) and an A + T rich-region and a D-loop. The L. coffeella mitochondrial gene organization is highly conserved with similarities to lepidopteran mitochondrial gene rearrangements (trnM-trnI-trnQ). We concatenated the 13 PCG to construct a phylogenetic tree and inferred the relationship between L. coffeella and other lepidopteran species. L. coffeella is found in the Lyonetiidae clade together with L. malifoliella and Lyonetia clerkella, both leaf miners. Interestingly, this clade is assigned in the Yponomeutoidea superfamily together with Gracillariidae, and both superfamilies displayed species with leaf-mining feeding habits.
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Introduction
Leucoptera coffeella (Guèrin-Meneville & Perrotet 1842) (Lepidoptera: Lyonetiidae) is a monophagous pest in coffee crops of Neotropical America where it causes important economic losses1. In Brazil, the world’s largest coffee producer, the negative impact corresponds to more than 50% of the production costs. However, in cases of severe infestations, the damage can compromise up to 70% of the costs2,3.
The coffee leaf miner is a microlepidoptera that consumes the palisade parenchyma during the larval stages. The mines reduce the photosynthetic area and induce premature leaf senescence, leading to leaf abscission and, consequently, decreasing the coffee grain yields4,5. Despite of the extensive occurrence of this pest and its agronomic importance in coffee growing areas, only a few DNA markers are currently available to monitor the presence of L. coffeella in coffee plantations and to characterize its phylogeographic and phylogenetic origins6.
Mitochondrial genomes (mitogenomes) are extensively used in differentiation studies to infer phylogenetic relationships7 and to develop species-specific molecular markers. However, data from families with large body size species are more abundant than small species, and species-rich tropical ecosystems are usually poorly investigated compared to temperate region faunas8. Among the 109 families in Lepidoptera, mitogenomes of Yponomeutoidea superfamily and Lyonetiidae family are poorly represented9,10. There are 11 families in Yponomeutoidea (Argyresthiidae, Attevidae, Bedelliidae, Glyphipterigidae, Heliodinidae, Lyonetiidae, Plutellidae, Praydidae, Scythropiidae, Yponomeutidae, Ypsolophidae) with 269 out of the 452 species found in NCBI classified in these families. Only nine families of Yponomeutoidea have complete mitochondrial genome data.
The mitochondrial DNA (mtDNA) has a higher mutation rate than the nuclear one and, as a result of its high copy number, large amounts of mtDNA can be assembled from genomic sequencing11,12,13,14. Bioinformatics analysis of the mitogenome features allows the determination of its gene size and arrangement, base composition, codon usage, and tRNA secondary structure, which are used to classify insects taxonomically and to assess their evolutionary history.
Insect mitogenomes are relatively small, with highly conserved structures, rapid evolution rates, low levels of recombination, and maternal inheritance. These 14-19kb length double-stranded circular molecules encode 13 Protein-Coding Genes (PCGs): two ATPase (ATP6 and ATP8), three cytochrome c oxidase genes (COI, COII, COIII), one cytochrome b (CYTB), seven NADH dehydrogenase genes (NADH1-6 and NADH4L), 22 transfer RNAs (tRNA), two ribosomal RNA genes (rrnS and rrnL) and a non-coding A + T-rich region9,11, 15,16,17,18,19,20.
In order to fulfill the knowledge gap of mitogenome data of the coffee leaf miner and other leaf-mining insects from the Yponomeutoidea group, we assembled and analyzed the L. coffeella mitogenome for sequencing data recently obtained by Martins et al.21.
Results and discussion
Mitochondrial genome organization and base composition
We assembled the complete mitochondrial genome of L. coffeella which consisted in a 16,407 bp circular DNA. Our genome contains 13 PCGs, two rRNA, 22 tRNA genes, and an A + T-rich region. Four of the 13 PCGs (NADH1, NADH4L, NADH4, and NADH5), 8 tRNAs (trnY, trnC, trnQ, trnV, trnL1, trnP, trnH and trnF) and the two rRNAs (rrnS and rrnL) are encoded by the minority-strand while the remaining 23 genes are encoded by the majority strand (Fig. 1 and Table 1). This strand specific genes organization of L. coffeella mitogenome is highly conserved with either the evolutionary closed L. malifoliella or the more distant Bombycoidea insects10,22.
The circular mitochondrial genome of Leucoptera coffeella. The J-strand (+) is visualized on the outer circle, and the N-strand (−) on the inner circle.
The length of L. coffeella mitogenome (16,407 bp) is larger than L. malifoliella (15,646 bp) and in the range of lepidoptera mitogenomes chosen in our study (15,027–17,050 bp) (Table 2). The nucleotide composition of L. coffeella is as presented in Table 3 with 41.4%, 40.5%, 7.5% and 10.6% for A, T, G and C, respectively, and is A+T-rich (81.9%) as often described for lepidopteran mitogenomes. The higher bias is in the control region of L. coffeella mitogenome (95.6% of A + T), then 84.7% in ribosomal RNAs, 80.9% in transfer RNAs and 79.2% in PCGs.
The lepidopterans have the second most biased nucleotide composition of the insect orders after Hymenoptera9. The AT skew is not significant with 0.011 and the GC skew is moderate with − 0.17 which indicates bias towards the use of As and Cs.
Protein-coding genes and codon usage
Thirteen Protein Coding Genes are found in the mitogenome of L. coffeella and the average AT content of the PCGs is 79.2%. PCGs displayed nucleotide bias with an AT skew of -0.141 and a GC skew of 0.048 showing that T and G are more abundant than A and C (Table 3). All PCGs use standard ATN start codons and terminate with TAA as codon except for NADH3 using TAG as stop codon (Table 1). Relative synonymous codon usage (RSCU) values for L. coffeella are summarized in Table 4 and Fig. 2. NNA and NNT co-dons are more frequent than NNC and NNG indicating a strong A or T bias in the third codon position. The most used amino acids in mitochondrial protein are Ile, Leu and Phe.
Count (A) and frequency values of Relative Synonymous Codon Usage (RSCU) (B) in the 13 Protein-Coding Genes of Leucoptera coffeella mitochondrial genome.
Overlapping and intergenic spacer regions
Six tRNAs (trnT (TGT), trnL2 (TAA), trnD (GTC), trnG (TCC), trnA (TGC) and trnN (GTT)) do not have intergenic nucleotides. Twenty intergenic spacer regions (Table 1) of a total of 381 nucleotides were identified, ranging from 2 to 64 nt. The latter is located between the control region and trnM. Control region, trnQ (TTG), rrnS, and COII are the features with the higher intergenic spacer regions size with 64 nt, 59 nt, 57 nt, and 35 nt, respectively (Table 1). Region overlaps from 1 to 47 nt were observed for eleven gene pairs (Table 1). One of these regions overlaps is a 7 bp motif (ATGATAA) found in L. coffeella mitogenome between ATP8 and ATP6. This motif was found at the same position in another Yponomeutidae mitogenome23 but also in Danaidae24,25 and Coleoptera genomes25,26. It is also found in our mitogenome at the beginning of NADH4 and NADH4L genes as well as in the coding regions of 4 other genes (rrnL, rrnS, NADH2 and trnN).
Transfer RNA genes (tRNA) and Ribosomal RNA genes
L. coffeella mitogenome contains 22 tRNAs, one for each of the 20 amino acids with an additional isotype for each of the two sixfold degenerate amino acids Leucine and Serine. Seven of these tRNAs (trnF, trnH, trnP, trnV, trnQ, trnC, trnY) are coded by the minority strand (Table 1) while the other fifteen tRNA genes are encoded by the majority strand.
The total length of the 22 tRNA is 1467 bp with lengths ranging from 61 to 71 bp and their A-T content is 80.9%. The AT skew is slightly positive, 0.016 and the CG skew is positive, 0.131 (Table 3).
The clover-leaf structure is found for all the 22 tRNAs from L. coffeella with the exception of trnS1 and trnS2 (Fig. 3). The trnS1 is missing the dihydrouridine (DHU) arm replaced by an unstable loop while the trnS2 has an additional loop in the anticodon-stem and loop. These two tRNAs are found on the minority strand. Lack of the DHU stem-loop in trnS1 is nearly ubiquitous in insect mitochondrial genomes9.
Secondary cloverleaf structure for the 22 tRNAs of Leucoptera coffeella mitochondrial genome.
The 16S RNA (rrnL) is located between tnrL1 and trnV and its length is 1345 bp whereas the 12S RNA (rrnS), located between trnV and the control region, is 761 bp. The A + T content of the two rRNAs genes is 84.7% (Table 3).
The A + T-rich region (control region)
The mitochondrial genome of L. coffeella contains a 1363 bp A + T-rich region or control region located between rrnS and trnM genes (Table 1). It is one of the largest A + T-rich region found in the Lepidoptera order, and with the highest A + T content, 95.6% (Table 3). This control region includes initiation sites for transcription and replication.
The structure of the A + T-rich region of L. coffeella is composed of five tandem repeats elements and a motif containing the origin of replication 'ATAGT' (Fig. 4). We found five repeats composed of a 57 bp (in blue) and a 159 bp (in yellow) sequences, and four (TA)n microsatellite regions (in red) (Fig. 4). Five Poly(T)7 and Poly(A)5 were also found but these repetitions are shorter compare to other lepidopteran’s control regions22,23. The A + T-rich region of L. coffeella mitochondrial genome presents differences compared to other Lyonetiidae, such as L. malifoliella mitogenome which has a shorter control region of 733 bp and the ATAGA motif (Fig. S1)10. We did not find the poly-T stretch downstream of the rrnS gene that is widely conserved in lepidopteran mitogenome. L. coffeella control region is also missing the poly-A stretch immediately upstream of the trnM gene, a feature commonly observed in other lepidopteran mitogenomes including L. malifoliella. Both L. malifoliella and L. coffeella have a stem-loop structure in the control region (Fig. S2). Such a feature seems to be intrinsic to the control region of Leucoptera species10.
Control region of Leucoptera coffeella mitochondrial genome. In red: 15 nt repeat, in blue: 57 nt repeat, in yellow: 159 nt repeat, in black: origin of replication. Poly-T and poly-A stretches are in bold and underlined. rrnS and trnM are the genes surrounding the control region.
The presence of a stable stem-loop structure in the A + T-rich region of Leucoptera appears to be as important as the presence of a stretch poly-T microsatellite in other insects, which, unless associated with a recognition of the light stretch origin of replication, has not yet been fully explored27.
The lack of molecular data for other Leucoptera species limits this interpretation and reinforces the need to expand the sampling sizes and deepen our understanding of the replication and transcription origin of the mt genome of Leucoptera species.
Gene rearrangements
We compare L. coffeella gene order to insect and Lepidoptera ancestral gene rearrangements9 in order to identify possible reorganization such as duplication, deletion, or inversion-translocation. We analyzed gene rearrangements using qMGR program28.
L. coffeella has exactly the same genes order than the two other Lyonetiidae mitogenomes available (Fig. 5). It is also identical to the gene order model proposed for ancestral Lepidoptera mitogenome which exhibits the trnM, trnI, trnQ (MIQ) common rearrangement with trnM on the minority strand. MIQ is found in most ditrysians between the A + T rich region and NADH29. L. coffeella also shares the A-R-N-S1-E-F gene rearrangement of insect ancestor between NADH3 and NADH5. L. coffeella mitogenome gene arrangement is identical to the ancestral Lepidoptera mitogenome organization proposed by Cameron9 and Moreno-Carmona et al.29.
Comparison of gene rearrangement for Leucoptera coffeella mitochondrial genome (in red) with insect Ancestral genome, Lepidoptera ancestor, L. malifoliella, L. clerkella and P. oleae mitogenomes.
Phylogenetic relationships
The phylogenetic analysis was performed with the ML method using 13 concatenated PCG from 18 lepidopteran species and one Diptera (Table 2; Fig. S3). The topologies of the phylogenetic trees were identical using either nucleotides (Fig. 6B) or amino acids data (Fig. 6B). A backbone in the phylogenetic tree was found: ((((((Lyonetiidae), ((Plutellidae, Scythropiidae), (Praydidae, Attevidae))), Gracillariidae), (Gelechiidae, Geometridae)), (Tineidae, Psychidae)), (Drosophilidae)).
Phylogenetic trees of Leucoptera coffeella using the 13 concatenated PCGs using (A) nucleotide sequences and (B) amino acid sequences data. Bootstrap values are indicated on each branch. Maximum-Likelihood method was used. The yellow circle indicates the lepidopteran’s leaf miners.
All Yponomeutoidea’s families form a monophyletic clade and are found in a clade with the Gracillariidae from Gracillarioidea. The Gracillarioidea, with Gracillariidae, Psychidae and Tineidae, forms a polyphyletic group as it was previously described in a phylogenetic study based on 794 lepidopteran mitogenomes30. Within Yponomeutoidea, Praydidae and Attevidae form a sister group (PrAt) with a high BS of 96. Plutellidae and Scythropiidae from a sister group (PlSc) with a BS of 80. We obtained better BS values for these four relationships compared to another phylogenetical study recently published31. The alignment of our sequences after concatenation using mafft might explain the improvement of nodal values (se Fig. S3). However, we did not improve the nodal support between PrAt and PlSc (54) and in this case more data are needed. Gracillariidae and Yponomeutoidea are present in the same clade with bootstrap value of 88. Leaf-mining feeding behaviors was characterized in Gracillariidae as the most phylogenetically conserved trait32.
A most recent study including 130 gracillariid species linked mining as an ancestral larval behavior of Gracilllariidae that has evolved several times33. All or part of the larval period as a leaf-miner might confer ecological advantage such as protection from natural enemies (predators, parasitoids, pathogens), from variation in their environment (UV radiation, hygrothermy)34. Another hypothesis is that leaf miners fed selectively on the most nutritious layers of foliage tissue avoiding plant defenses. L. coffeella is found in the same clade as L. malifoliella and L. clerkella, two other leaf miners of the Lyonetiidae family with bootstrap of 100 and 97 for nucleotides and amino acids phylogenies, respectively. The Lyonetiidae family includes leaf miners considered as agronomic pests, however, insufficient molecular data is limiting the phylogenetic inferences about this family.
Only the three Lyonetiidae species included in our phylogeny have been sequenced. We only observed the presence of leaf miners which diverged in their host-plant preferences. L. coffeella feeds exclusively on coffee plants35.
L. malifoliella is polyphagous36 and L. clerkella feeds on Malus sp. and Prunus sp. species37. In Yponomeutoidea, the large proportion of representatives are oligophagous38. Further molecular studies of lepidopteran leaf miners are needed to better understand how this feeding habit innovation occurs in Lyonetiidae and Gracillariidae. The host plant range in these two families should also be further study to confirm the preference for shrubs and trees34,38, 39.
Conclusions
Mitochondrial genomes sequences are increasingly used as informative molecular markers for systematics, phylogenetics, population genetics and evolutionary studies because of its conserved gene content, its small size, its fast rate of evolution, its minimal or absent sequence recombination, its maternal inheritance and its abundant markers types. Here we report the first complete mitochondrial genome of L. coffeella. It consists of a circular double stranded DNA of 16,407 bp containing the conserved trnM-trnI-trnQ gene rearrangement found in Lepidoptera ancestors9.
We found 22 tRNAs showing conserved clover leaf structure, except for the trnS1 and trnS2 coding for serine tRNAs. We also observed a codon usage bias, with high variability detected in the third position of codons. Regarding the most closely related mitogenome, the main difference between L. coffeella and L. malifoliella is in the control region size, with 1363 bp and 733bp, respectively.
Our phylogenetic study based on Maximum-likelihood estimation confirms the presence of L. coffeella and L. malifoliella in the Lyonetiidae clade and in the Yponomeutoidea superfamily with insects from Plutellidae and Praydidae. Our phylogeny points out that the leaf-mining habit was acquired several times through the evolution of Lepidoptera, as we can for instance found leaf-miners in both the Lyonetiidae family as well as in Gracillariidae clades. The acquisition of this innovation was followed by host-plant specialization with L. coffeella on coffee tree, L. clerkella on Malus and Prunus, and L. malifoliella being polyphagous.
Acquisition of more genomic data in this part of the tree is needed to confirm this hypothesis. We have acquired molecular data that can now be used to learn more about the history of L. coffeella introduction and its invasive route in the Neotropical Americas. How this insect has adapted to the conditions of coffee crops in these regions might help the development of Integrated Pest Management programs and the use of for instance parasitoids.
Materials and methods
Ethics statement
Our study did not involve any endangered or protected species. No specific permits were required for the insect or plant specimen collection in this study. The collection and use of plant and insect materials in the study comply with relevant institutional, national, and international guidelines and legislation.
Leucoptera coffeella genomic DNA
Genomic DNA (gDNA) was obtained from a pool of individuals at the pupae stage feeding on Coffea arabica (L.) (Rubiaceae) leaves at latitude − 15.72812S; longitude − 47.90277W, Brasilia-DF (Brazil). High-quality gDNA samples were extracted as described in40 and sequenced using PacBio HiFi technology (DNA Link Sequencing Lab DNALINK, Seoul, Republic of Korea). The sequencing was performed using PacBio HiFi technology. The genome assembly is described by Martins et al.21, and is available at GenBank BioProject ID PRJNA83259821.
Genome assembly and annotation
We used two mitochondrial genes fragments from L. coffeella available in GenBank, COI (MF987402) and Cytb (MF987470) and the orthologous genes from L. malifoliella, COI (GU929715) and Cytb (NC_018547) to search the mitochondrial sequences present in the genome assembly (PRJNA832598). From the blastn search, we retrieved one contig containing two matches for each gene query containing COI and Cytb. To assemble the whole mitochondrial genome of L. coffeella, we used the raw reads used for the genome assembly and submitted the raw reads to Aladin v.3.0 software (https://github.com/GDKO/aladin) using the L. malifoliella mitochondrial genome as seed10.
We annotated the mitogenome sequence obtained from Aladin with MITOS2 web-server (http://mitos.bioinf.uni-leipzig.de/index.py)41 with reference ‘RefSeq 81 Metazoa’ invertebrate ‘5’ genetic code. The mitogenome data from L. coffeella was deposited in Genbank at NCBI (submission ID: BankIt2758416 OR753213, Supplementary data).
Bioinformatics analysis
The nucleotide base composition was determined using ‘wordcount’ program of the EMBOSS toolkit v. 6.6.0.042, and the AT/CG skewness was calculated using the formula AT skew = [A − T]/[A + T] while GC skew = [G − C]/[G + C]43. The tRNA genes, their secondary structures, the gene overlapping, and intergenic spacers were predicted using MITOS2.
The tandem repeats in the control region were located using MEME suite (https://meme-suite.org/meme/)44. MEME version 5.5.3 was used to search for repeat motifs between 6 to 300 nt within the control region of L. coffeella or L. malifoliella. The comparison of L. coffeella mitochondrial genome gene order with the Lepidoptera ancestor’s rearrangement (trnI-trnQ-trnM)9 was performed using the program qMGR program28. The Relative Synonymous Codon Usage (RSCU) of PCGs was determined using MEGA1145. The representation of the mitogenome circular map was done with the web tool OGDRAW v.1.3.146 by MPI-MP CHLOROBOX.
Phylogenetic analysis
We aligned 18 mitochondrial Lepidopteran genomes of Yponomeutoidea, Tineoidea, Gracillarioidea; Gelechioidea, Geometroidea and Ephydroidea species (Table 2) to reconstruct the phylogenetic trees, with Drosophila melanogaster as the outgroup. The nucleotide sequences of the selected species were downloaded from NCBI database (https://www.ncbi.nlm.nih.gov, June 2023). We emphasized in taxon sampling some Lepidopteran’s leaf miner species with assembled and annotated complete mitochondrial genomes publicly available in GenBank.
The 13 PCG genes (COI, COII, COIII, Cytb, ATP6, ATP8, NADH1-NADH6 and NADH4L) of each species were translated to amino acid sequences using TransDecoder v.5.5.0 [https://github.com/TransDecoder/TransDecoder] and concatenated with the perl script FASconCAT v.1.1147. The concatenated PCG sequences were globally and locally aligned using the program MAFFT v7.47548 with the Needleman-Wunsch algorithm for nucleotide sequences (mafft G-INS-i) and Smith-Waterman for amino acid sequences (mafft L-INS-i) and 1000 maximum refinement interactions. The amino-acid and nucleotidic alignments are available at https://doi.org/10.57745/NA3OZ2. The evolutionary models for phylogenetic trees were determined using ModelTest-NG49. The GTR substitution model with gamma-distributed rate variation and proportion of invariable sites (GTR + I + G4) was selected for nucleotide sequences, (BIC score: 20,6910.5687 and weight: 1.0000), and the model MTART + I + G4 + F was selected for amino acid sequences (BIC score: 11,1197.8918 and weight: 1.0000). The Maximum-likelihood analysis was performed with RAxML-NG v. 0.9.050 with 1000 of bootstrap replicates.
Figure S3 is the bioinformatic pipeline of the Leucoptera coffeella mitochondrial genome obtention. The amino-acid and nucleotide alignments used for the phylogeny of Fig. 6 can be found at https://doi.org/10.57745/NA3OZ2.
Data availability
The datasets generated and analyzed during the current study are available in the NCBI repository (BankIt2758416 OR753213).
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Acknowledgements
We would like to thanks Etienne Danchin for valuable discussions during the conceptualization of the project as well as in the preparation of the manuscript. We would like to thank Mateus P. dos Santos for the Leucoptera coffeella artwork in Fig. 1.
Funding
This research and fellowships to M.P.D.S, E.V.S.A. and N.F.M. were funded by National Council for Scientific and Technological Development—CNPq, grant number 402834/2022-4.
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F.H., E.V.S.A., A.P.Z.M. Conceptualization; E.F.B.N., V.S.L-L., A.Z.M. and R.T methodology; M.P.D.S., F.H., R.C.T. and A.Z.M formal analysis; E.V.S.A. resources; M.D.P.S. and A.Z.M. data curation; F.H., M.P.D.S., A.Z.M., E.V.S.A. and N.F.M. writing—original draft preparation; F.H., M.P.D.S., A.Z.M., E.V.S.A., N.F.M, M.A.C. writing—review and editing; M.A.C, A.M.Z. and F.H. supervision; E.V.S.A. project administration; E.V.S.A. funding acquisition. All authors have read and agreed to the published version of the manuscript.
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Pereira dos Santos, M., Zotta Mota, A.P., Coiti Togawa, R. et al. The complete mitochondrial genome of Leucoptera coffeella (Lepidoptera: Lyonetiidae) and phylogenetic relationships within the Yponomeutoidea superfamily. Sci Rep 14, 7119 (2024). https://doi.org/10.1038/s41598-024-57869-3
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DOI: https://doi.org/10.1038/s41598-024-57869-3
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