The mitochondrial genome sequence of Syagrus coronata (Mart.) Becc. (Arecaceae) is characterized by gene insertion within intergenic spaces

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The mitochondrial genome sequence of Syagrus coronata (Mart.) Becc.

(Arecaceae) is characterized by gene insertion within intergenic spaces

Article in Tree Genetics & Genomes · March 2024

DOI: 10.1007/s11295-024-01643-z

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SHORT COMMUNICATION

The mitochondrial genome sequence of Syagrus coronata (Mart.) Becc.

(Arecaceae) is characterized by gene insertion within intergenic spaces

Suzyanne Morais Firmino de Melo¹ · André Marques² · Cícero Almeida¹

Received: 21 August 2023 / Revised: 8 January 2024 / Accepted: 18 March 2024

Abstract

Syagrus coronata (Mart.) Becc. belongs to the Arecaceae family. It is a species native to Brazil of ecological, social, and economic importance. To date, there are few mitochondrial genomes in Arecaceae (Cocos nucifera and Phoenix dactylifera L.), and studies of the mitochondrial genome are essential to understand the evolution of the Arecaceae family. This study reports and compares the newly sequenced genome of S. coronata. Single-end and paired-end reads were used to obtain de novo contigs. The mitochondrial contigs were selected using C. nucifera as a reference and were merged using mate paired-end reads. The mitochondrial genome showed 642,817 bp, circular structure, containing 73 predicted functional genes, including four ribosomal RNA (rRNA) genes, 27 transfer RNA (tRNA) genes, and 42 coding protein genes. Large chloroplast genomic fragments were identified in the mitochondrial genome, and large DNA repetitive fragments were into intergenic space regions. Arecaceae mitochondrial genomes showed partial similarities in size, genome structure, and gene content. However, they exhibited numerous rearrangements. In summary, (1) we sequenced the mitochondrial genome of S. coronata and compared with other mitogenomes of Arecaceae. (2) Genomic rearrangements and gene transfer have been identified from the chloroplast genome to the mitochondrial genome. (3) The mitochondrial genome of Arecareae showed similarities in size, structure, and gene content. (4) The expansion of intergenic space size occurs due to the insertion of genes originating from the nucleus.

Keywords Mitogenome · Arecaceae · Ouricuri

Introduction

The mitochondria produce most of the energy of eukaryotic cells and are derived from an ancient endosymbiotic event (Ogihara et al. 2005). The mitochondrial DNA (referred to as mitogenomes) in most eukaryotes is inherited from only one parent (Gualberto and Newton 2017) and exhibits a wide diversity in size, organization, and gene content. The structure of mitochondrial genomes is organized into a circular chromosome, which

can be a single chromosome or multiple smaller chromosomes.

However, linear chromosomes have also been reported. (Wu et al. 2015; Shearman et al. 2016; Sloan et al. 2012). In plants, the size of the mitogenome is highly variable, ranging from 100 Kbp in bryophyte Mielichhoferia elongata Hoppe & Hornsch (Goruynov et al. 2018) to 11.3 Mbp in Silene conica (Sloan et al.

2012). A large variation is observed in the genus Silene, where the size ranges from 253 Kbp to 11 Mbp (Sloan et al. 2012), and these differences are attributed to the size of intergenic regions.

The transfer of genes from the chloroplast genome and repetitive DNA in intergenic regions partially explains the high variation in genome sizes (Choi et al. 2019; Martins et al.

2019). However, the large size of the mitochondrial genome in angiosperms is due to a currently unknown mechanism. Due to chromosomal rearrangements and the large amount of repetitive DNA, mitogenomes are more challenging to obtain than plas- tomes, requiring sequences with large inserts (mate paired-end reads) or long reads (PacBio or Nanopore). However, in some angiosperm genera, it has been possible to obtain mitogenomes using short reads (Oliveira et al. 2021).

Communicated by G.G. Vendramin

* Cícero Almeida

[email protected]

1 Genetic Resources Laboratory, Campus Arapiraca, Federal University of Alagoas, Avenida Manoel Severino Barbosa S/N, Highway AL 115, Km 6.5. Bom Sucesso Neighborhood, Arapiraca, AL, Brazil

2 Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, 50829 Cologne, NRW, Germany

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Tree Genetics & Genomes (2024) 20:10 10 Page 2 of 9

The Arecaceae family represents one of the most diverse monocot families, with a 181 genera and 2600 species, distributed across five subfamilies (Baker et al. 2016). Para- doxically, however, there are few available mitochondrial genomes. At the time of writing this study, only the complete mitochondrial genera of Phoenix dactylifera L. (Fang et al.

2012) and Cocos nucifera (Aljohi et al. 2016) are available. For chloroplast genomes, over 200 genomes have been sequenced, including the genomes of C. nucifera, P. dactyl- ifera, and S. coronata (Áquila et al. 2018; Huang et al. 2013;

Yang et al. 2010).

Cocos nucifera and S. coronata (Mart.) Becc. belong to the subfamily Arecoideae (tribe Cocoseae), while P. dactyl- ifera is a species of the subfamily Coryphoideae (Baker et al.

2016). Syagrus coronata is a native species of Brazil with ecological, social, and economic importance, distributed in the Atlantic Forest and Caatinga biomes (Souza et al. 2018).

We conducted the following experiment: (1) Using Illumina paired-end and mate paired-end sequencing, we assembled and annotated the complete mitochondrial genome of S. cor- onata. (2) We assessed the transfer of chloroplast sequences to the mitogenomes. (3) We comparatively analyzed the diversity in genome size, structure, and genetic content, as well as the rearrangements of Arecaceae mitogenomes.

Material and methods

Plant material and DNA isolation

The plant material of S. coronata was collected in the state of Alagoas, Brazil, and the total DNA was extracted (including nuclear DNA, chloroplast, and mitochondrial) using

approximately 5 g of the leaves following the cetyltrimeth- ylammonium bromide (CTAB) extraction method (Doyle and Doyle 1987). The quantity and quality of extracted DNA were analyzed by visualization on 1% agarose gel.

High‑throughput DNA sequencing

The DNA sample was fragmented into 400–600 bp to con- struct the sequencing paired-end and single-end libraries.

The fragments were ligated with adapters using the “Nextera DNA Sample Preparation” (Illumina) the 2 × 100 bp paired- end, and 1 × 100 bp single-end reads were sequenced on the Illumina HiSeq2500 platform. The mate-pair library was prepared with high molecular weight genomic DNA using Illumina Nextera Mate Pair Sample Preparation Kit, accord- ing to the manufacturer’s instructions for a gel-free preparation of > 2 kbp insert size library and sequenced on the Illu- mina HiSeq2500 platform. The sequencing was performed at the Central Laboratory for High-Performance Technologies in Life Sciences (LacTad-Laboratório Central de Tecnolo- gias de Alto Desempenho em Ciências da Vida) at the State University of Campinas UNICAMP, São Paulo, Brazil.

Mitogenome assembly and annotation

The Illumina reads were filtered using BBDuk (implemented in Geneious R9.1 software) to remove the Illumina adapters, artifacts and quality-trim. A total of 9,558,758 single-end reads and 18,673,124 paired-end reads were used for de novo assembly using the Ray software version 2.3.1 (Boisvert et al.

2012) and the SPAdes software version 3.12.0 (Bankevich et al.

2012). For de novo assembly, a k-mer of 31 was determined, and contigs with a minimum size of 1 kb for both approaches. All

Table 1 Genomic features of the mitochondrial genome of S.

coronata

Gene function Gene names

Complex I nad1, nad2, nad4, nad4L, nad5, nad6, nad7, nad9

Complex II sdh3, sdh4

Complex III Cob

Complex IV cox1, cox2, cox3

ATP synthase atp1, atp4, atp6, atp8, atp9

Cytochrome c-type ccmB, ccmC, ccmFC, ccmFN1, ccmFN2

Ribosomal protein, small rps1, rps2, rps3, rps4, rps7, rps10, rps11, rps12, rps13, rps14, rps19 Ribosomal protein, large rpl5, rpl10, rpl4, rpl16, rpl33

SecY-independent transport matR, mttB

Transfer RNAs tRNA-Cys(2x), tRNA-Asp, tRNA-Glu, tRNA-Phe, tRNA-Ser, tRNA- His, tRNA-Ile(3x), tRNA-Lys(4x), tRNA-Met(3x), tRNA-Asn(3x), tRNA-Pro, tRNA-Gln, tRNA-Arg, tRNA-Ser(2x), tRNA-Thr, tRNA- Tyr

Ribosomal RNAs rrn5 (2x), rrn18, rrn26

Gene length 37,855 bp

Repeat lenght 38.046 bp (> 40bp)

Intergene length 606.915 pb

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contigs obtained from de novo assembly were used to filter the mitochondrial contigs. The mitochondrial contigs of S. coro- nata were filtered by mapping using gene sequences from C.

nucifera (KX028885) as a reference in the Geneious software, using the mapping tool. To filter the S. coronata contigs using C. nucifera genes, a minimum of 70% sequence identity was determined. The Cocos and Syagrus genera are closely related,

and mitochondrial genome studies in plants have shown that the number of genes and sequence identity are conserved in plants. A total of 28 contigs were identified as mitochondrial and were manually assembled using mate pair reads. The assembly method involved mapping reads to the ends of contigs and identifying which pairs of reads were present in different contigs (Figure S1). After obtaining the circular genome, the

Fig. 1 Circular map of Syagrus coronata mitochondrial genome. Gene map showing 73 annotated genes of different functional groups

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mate-paired end reads were mapped using bwa, and the coverage distribution was analyzed to verify the correct order of the contigs (Figure S2).

Genome annotation was performed by homology using the Geneious software, with the mitochondrial genome of C. nucifera used as a reference, with a parameter of 70%

identity cutoff between the two genomes. All annotations were compared and validated using the annotations obtained from Mitofy (Alverson et al. 2010). All annotations were individually verified and manually corrected in search of start and stop codons. Annotation was performed using Domain-based Annotation of Transposable Elements through DANTE (https:// repea texpl orer- elixir. cerit- sc. cz/

galaxy/). A graphical representation was generated using Genoma Organelar DRAW (Lohse et al. 2013).

Mitogenome analysis

The mitogenomes of C. nucifera (KX028885) and P. dactylifera (JN375330) were downloaded from NCBI (https:// www. ncbi.

nlm. nih. gov). The identification of repetitive regions within the mitogenomes of S. coronata, C. nucifera, and P. dactylifera was conducted using BLAST, implemented in the circoletto software (Darzentas 2010). The transfer of DNA from the chloroplast to the mitogenome and the comparison between mitogenomas were measured using the AliTV software (Ankenbrand et al.

2017), where the genomes are aligned using lastz and subse- quently visualized using graph approach. The analyses in the Circoletto and AliTV software were conducted using the default parameters of each software. Microsatellite analysis was conducted using the phobos software (Mayer 2008), implemented in the Geneious software, searching for di-, tri-, tetra-, penta-, hexa-, and hepta-nucleotide motifs, with a minimum of five repetitions.

Intergenic spacer analysis

To analyze the intergenic spaces, an ab initio gene prediction was performed using the Augustus software (Hoff and Stanke 2019), implemented in the galaxy platform (http://

www. usega laxy. eu). A functional annotation was performed using homology (blastx) and orthologous genes using Inter- ProScan (https:// www. ebi. ac. uk/ inter pro/ search/ seque nce/) (Blum et al. 2021). The results were depicted in a graph using the R package circlize (Gu et al. 2014).

Results

Mitogenome assembly and annotation

De novo assembly resulted in 28 contigs that were merged to obtain a single circular chromosome, with a coverage of

126 × and a broad distribution across the genome (Fig. S2).

The mitogenome exhibited 642,817 bp, with a multipartite structure, comprising 73 predicted genes, identified through homology, including four ribosomal RNA (rRNA) genes, 27 transfer RNA (tRNA) genes, and 42 protein-coding genes.

The microsatellites (shortest repetitive sequences) revealed 22 dinucleotides, five trinucleotides, and one tetranucleotide in the mitogenome of S. coronata. Among coding protein genes, eight are NADH (Complex I—nad1, nad2, nad4, nad4L, nad5, nad6, nad7, and nad9), two succinate dehy- drogenase (Complex II—sdh3 and sdh4), one cytochrome b (Complex III—cob), three cytochrome c oxidase (Complex IV—cox1, cox2, and cox3), five adenosine triphosphate synthase (Complex V—atp1, atp4, atp6, atp8, and atp9), five cytochrome c-type biogenesis protein (ccmB, ccmC, ccmFC, ccmFN1, and ccmFN2), 11 ribosomal protein-small (rps1, rps2, rps3, rps4, rps7, rps10, rps11, rps12, rps13, rps14, and rps19), five ribosomal protein large (rpl2, rpl5, rpl10, and rpl16), and two SecY-independent transport (matR, mttB) (Table 1 and Fig. 1). The genome was annotated using DANTE to identify regions corresponding to protein domains of TEs, and the results revealed 111 regions annotated as TEs, with 110 in intergenic regions and only one in annotated genes (Table 3 and Table S1).

Comparative analysis in Arecaceae mitogenomes The genome sizes in Arecaceae are similar, with 642,817 bp (S. coronata), 687,653 bp (C. nucifera), and 715,001 bp (P.

dactylifera). The number of protein-coding genes among the mitogenomes was most similar between C. nucifera and S.

coronata, with 41 and 42 genes, respectively, while P. dac- tylifera had fewer protein-coding genes. Syagrus coronata exhibited four rRNA genes, while C. nucifera and P. dactylif- era revealed three. However, for tRNA genes, a greater variation was observed, with C. nucifera showing 23 genes, S.

coronata with 27, and P. dactylifera with 30 genes (Table 2).

Table 2 Comparison of genomic features, chloroplast DNA transfer, and intergenic region sizes in the mitogenomes of Syagrus coronata, Cocos nucifera, and Phoenix dactylifera

* Fang et al. 2012; **Aljohi et al. 2016 Syagrus coro-

nata Cocos nucif-

era* Phoenix dac-

tylifera**

Genome size (pb) 642,817 678,653 715,001

Coding-proteina 42 41 38

rRNA 4 3 3

tRNA 27 23 30

DNA from chloro-

plast 4.0% 5.07% 10.3%

Intergentic size 94.4% 88.57% 93.5%

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The transfer of DNA fragments from chloroplast genomes to mitogenomes was 4% in S. coronata, 5.07% in C. nucif- era, and 10.3% in P. dactylifera (Table 2), and the distribution

of DNA fragments was dispersed throughout the genome, suggesting that the incorporation occurred in small blocks (Fig. 2A–C). Repetitive DNA was observed in large blocks in

Fig. 2 Schematic representation of DNA transfer between chloroplast and mitochondrial genome in three Arecaceae species, in which the green ribbons represent similarly high regions between cpDNA and mtDNA (A–C). Repeat distribution in the Arecaceae mitogenomes, being the circle, reveals the distribution of repeats in mitogenomes,

with curved lines and ribbons connecting pairs of repeats and proportional width to repeat size (D–F). Dynamic rearrangements among mitogenomes, with curved ribbons connecting pairs of syntenic blocks and width proportional to block size (G–I)

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S. coronata and C. nucifera, while in P. dactylifera, it was in small blocks distributed throughout the genome (Fig. 2D–F).

Remarkably, repetitive DNA does not account for the genome size, as non-repetitive intergenic regions make up the majority of the genome size. When the mitogenomes were compared using sequence similarity, the results showed that the mitogenomes share many sequences (Fig. 2G–I).

The comparison between S. coronata and C. nucifera revealed a total of 618,160 bp, distributed in 366 regions, are highly shared between the mitogenomes. This sharing is lower when the species are more phylogenetically distant.

Plant mitogenomes are highly variable in genome structure, with generalized intramolecular homologous recombination leading to significant differences between mitogenomes that differ in structure but are identical in sequence. The comparison between the three mitogenomes revealed high differences in structure and low differences in sequences.

An analysis of the intergenic region using gene prediction with the Augustus detected 332 genes, corresponding to 321,951 bp (53% of the genome length—Table 3), distributed throughout the genome (Fig. 3). Functional annotations using homology and orthology, revealed 242 genes with homology in NCBI and 119 annotated with orthologous terms (Table 3). The intersection of these annotations showed that 95 predicted genes for intergenic regions were also annotated with protein domain annotations of transposable elements, distributed across the genome (Fig. 3), and only one gene annotated by homology was also annotated with domain annotations of transposable elements (26S rRNA). Functional analysis revealed that the predicted genes are associated with various functions, distributed across molecular function, biological process, and cellular process (Figure S3). The Blast revealed that many of these genes are associated with hypothetical proteins or truncated genes from the mitochondrial genome.

Discussion

Plant mitogenomes undergo intense and rapid structural changes, resulting in complex genomic structures with numerous rearrangements and DNA transfers from the plastome. These characteristics make the sequencing and assembly of these genomes more challenging than plastome, requiring DNA reads from large inserts or long reads. While the structure of the plant mitochondrial genome typically presents as a single circular chromosome (Martins et al.

2019), some mitogenomes cannot be assembled into a single circle and are represented as a linear molecule. Our assembly approach utilized paired-end reads (short insert length) and mate paired-end reads (long insert length), efficiently obtaining the complete mitogenome.

The mitogenome of S. coronata was assembled into a single circular molecule, with a similar number of genes and genome size within Arecaceae. Arecaceae encompasses over 2600 species, across more than 180 genera (Baker et al.

2016), and at the time of writing this study, the complete mitochondrial genomes of P. dactylifera (Fang et al. 2012), C. nucifera (Aljohi et al. 2016), and S. coronata obtained in this study are available.

Three mitogenomes are a small sample for the family, but it allows for an analysis that suggests the main changes in the mitogenomes. The results revealed numerous rearrangements, possibly due to the abundance of repetitive DNA sequences; all mitogenomes showed incorporation of chloroplast DNA, and the number of genes is similar among the mitogenomes. Notably, the transfer between genomic com- partments does not seem to contribute to increasing genome size, ranging from 4 to 10.3% of the mitogenome size. Angi- osperm mitogenomes typically have sequences derived from plastids, with variable proportions, as observed in Spondias (Martins et al. 2019), Mangifera (Niu et al. 2022), Nym- phaea colorata (Dong et al. 2018). However, the proportion is not high, suggesting that the incorporation of chloroplast DNA does not explain the expansion of mitogenomes.

Plant mitochondrial genomes have long been known to be rich in repeated sequences and large intergenic spacers, which explain the differences in mitogenome sizes. Among the repetitive sequences, Simple Sequence Repeats (SSRs), which are tandem repeats consisting of 1 to 6 nucleotides, are abundant in plant genomes. However, in S. coronata, only 28 SSR loci were observed, making a low contri- bution to the genome size. This suggests that the expansion of mitogenomes in S. coronata is likely due to an increase in intergenic spaces, through a mechanism that is still unknown. The repeats observed in Arecaceae mitogenomes are not tandem repeats, suggesting that the expansion of intergenic spacers remains a mystery. Comparison among 168 plant mitogenomes revealed a strong correlation between intergenic spacer size and genome size. However,

Table 3 Genetic analysis of functional genes and intergenic regions Functional genes Intergenic space

GC content 45.7% 45.6%

Min length (bp) 47 18

Max length (bp) 3,425 33,414

Number 73 69

DANTE annotation 1 110

Length (bp) 37,855 606,915

ab initio gene prediction 29 332

ab initio gene length (bp) 21,447 321,951

Blast 29 242

Gene onthology annotation 28 119

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the regions containing tandem repeats are relatively short, while non-tandem repeats contribute to the increase in genome size (Martins et al. 2019).

What is the origin of the intergenic sequences? In an attempt to address this inquiry, a gene prediction using an ab initio approach proved to be pivotal. It was revealed that a significant portion of these sequences comprises genes originating from the nucleus. Specifically, 332 genes were

predicted, accounting for 321,951 base pairs. The majority of these genes were identified in the NCBI database and were also annotated with transposable element domains and orthologous genes. Notably, transposable elements are likely involved in this migration of genes from the nuclear genome to the mitochondrial genome. The transfer of DNA segments from mitochondria and chloroplasts to the nuclear genome of plants is documented (Zhang et al. 2023), and the

Fig. 3 Annotation of gene and intergenic regions. The first circle cor- responds to annotated genes (names are on the outer), the second circle contains genes predicted using ab initio methods, the third circle represents annotations using DANTE, and the fourth circle indicates

the AT (black) and CG (red) content. In the center of the circle, there is a Venn diagram depicting the intersections of gene annotations, DANTE annotations, and genes predicted by ab initio method

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hypothesis is that the migration of DNA from the nucleus to the mitochondrial genome explains the increase in mitochondrial genome size.

Supplementary Information The online version contains supplementary material available at https:// doi. org/ 10. 1007/ s11295- 024- 01643-z.

Acknowledgements We would like to thank the Federal University of Alagoas for the access to laboratories and scientific support, the Fundação de Amparo à Pesquisa de Alagoas (FAPEAL) for funding this project, and the National Council for the Improvement of Higher Education (CAPES).

Declarations

Competing interests The authors declare no competing interests.

Data archiving statement The assembled mitochondrium has been deposited in the public database of National Center of Biotechnol- ogy Information under OR147828, and SRA data have been deposited under bioproject PRJNA935685.

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