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Genome Biol Evol
Genome Biol Evol
gbe
Genome Biology and Evolution
1759-6653
Oxford University Press UK

10.1093/gbe/evae184
evae184
Letter
AcademicSubjects/SCI01130
AcademicSubjects/SCI01140
New Insights into the Diversity of Mitochondrial Plastid DNA
https://orcid.org/0000-0002-0505-5946
Nhat Nam Nguyen School of Agriculture and Aquaculture, Tra Vinh University, Tra Vinh City, Vietnam

https://orcid.org/0009-0001-9732-6116
Pham Anh Thi Nguyen Department of Molecular Biology, Institute of Food and Biotechnology, Can Tho University, Can Tho City, Vietnam

https://orcid.org/0000-0002-7970-9359
Do Hoang Dang Khoa Functional Genomics Research Center, NTT Hi-Tech Institute, Nguyen Tat Thanh University, Ho Chi Minh City, Vietnam

Piganeau Gwenael Associate Editor
Corresponding author: E-mail: dhdkhoa@ntt.edu.vn.
9 2024
04 9 2024
04 9 2024
16 9 evae18418 8 2024
04 9 2024
© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.
2024
https://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

Abstract

The mitochondrial plastid DNAs (MTPTs) in seed plants were reported more than 40 years ago and exhibited a high diversity regarding gene content, quantity, and size. However, the mechanism that resulted in the current diversity of MTPTs in angiosperms has not been fully discovered. In this study, we sequenced and characterized the complete organelle genomes of Limonia acidissima L., a monotypic species of Rutaceae. The newly generated and previously published organelle genomes of 42 species were used to explore the diversity of MTPTs regarding quantity, gene content, size, and coverage of chloroplast genome (cpDNA) regions. The results showed that the number of MTPTs ranged from three to 74, of which the lengths were from 100 to 53,731 bp. The highest coverage of MTPTs was found in the inverted repeat region, whereas the small single repeat region had the lowest coverage. Based on the previous data and current results, we propose a scenario for the diversity of MTPTs in angiosperms. In the first stage, the whole cpDNA might migrate to the mitogenome. Then, different genomic events, such as duplication, deletion, substitution, and inversion, have occurred continuously and independently and resulted in extremely variable profiles of mitogenomes among angiosperms. Our hypothesis provides a new and possibly reliable scenario for explaining the present circumstances of MTPTs in angiosperms. However, more genomic data should be mined, and more studies should be conducted to clarify this natural phenomenon in plants.

chloroplast-derived sequence
DNA transfer
MTPT
Nanopore
Tra Vinh University 10.13039/100018444 279/2022/HĐ.HĐKH&ĐT-ĐHTV
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pmcSignificance

The migration of plastid DNA to the mitochondrial genome via intracellular gene transfer has occurred naturally among plants and exhibited a high variation. We hypothesize a scenario for the current diversity of mitochondrial plastid DNA through an initial transfer of the entire chloroplast genome followed by various genomic events (i.e. duplication, substitution, and deletion) within the mitochondrial genome. This scenario provides a reliable explanation for the diversity of plastid-derived mitochondrial DNAs that are flexible in size, include all genes of the chloroplast genome, contain shared regions, and are unique for species.

Introduction

The DNA transfers from the chloroplast genome (cpDNA) to the mitochondrial genome (mitogenome) are a natural phenomenon in angiosperms, which was first described in maize (Stern and Lonsdale 1982). After the recognition of the 12-kb shared sequence in organelle genomes of maize, a set of 16 cpDNA sequences was found in the mitogenome of rice, of which the sizes were from 32 to 6,800 bp (Nakazono and Hirai 1993). Further investigation showed that the mitochondrial plastid DNA (MTPT) was not only found in maize and rice but also in other Gramineae species such as sorghum, wheat, and Italian ryegrass (Watanabe et al. 1994). Recent studies also revealed different profiles of MTPTs of various species, such as watermelon (Citrullus lanatus), melon (Cucumis melo), mangoes (Mangifera sp.), sweet potato (Ipomoea batatas), yellow nutsedge (Cyperus esculentus), Rhododendron × pulchrum, and Suaeda glauca (Cheng et al. 2021; Cui et al. 2021; Niu, Zhang, et al. 2022; Niu, Gao, et al. 2022; Shen et al. 2022; Yang et al. 2022). Previously, the diversity of MTPTs was investigated among 73 species and revealed that all genes of cpDNA could be found in MTPTs (Wang et al. 2017). They also discovered that the number of transferred genes differed among examined seed plants of which the closely related taxa had some shared MTPTs. Additionally, their results suggested five hot spots (i.e. trnW_CCA, trnA_UGC, rpl2, rpl23, and trnI_GAU) and three cold spots (i.e. rps16—trnQ_UUG—psbK—psbI—trnS-GCU—trnG_UCC, trnS_UGA—psbZ—trnG_GCC, and ndhF—rpl32—trnL_UAG—ccsA—ndhD) in cpDNA for DNA transfer. Besides the diversity of MTPTs, the time for transfer of MTPTs was estimated at least 300 million years ago (Wang et al. 2007). These results exhibited a long history and extreme diversity of MTPTs among seed plants. However, the scenarios for MTPTs have remained unclear.

Limonia acidissima, a member of the subfamily Aurantioideae of Rutaceae, has a close relationship to Citrus and Atalantia, of which the common ancestor diverged at least 17 million years ago (Bayer et al. 2009; Shi et al. 2023). As a monotypic species, L. acidissima might contain significant information for tracing the evolutionary history of MTPTs in comparison to its related genera of Citrus and Atalantia, which consist of more than 20 species. Therefore, in this study, we sequenced and characterized the organelle genomes of L. acidissima using the short-read sequencing method (Illumina platform) and long-read sequencing approach (MinION, Oxford Nanopore Technologies). The newly sequenced organelle genomes of L. acidissima and previously published sequences of other 41 angiosperms were used to track the features of MTPTs regarding quantity, length, and location in cpDNAs. Finally, we proposed a scenario for the rise of MTPTs among angiosperms.

Results

The complete cpDNA of L. acidissima was a quadripartite molecule of 159,712 bp in length (average coverage = 176×; Fig. 1a). This genome contained 79 protein-coding genes, 30 tRNA genes, and four rRNA genes (supplementary table S2, Supplementary Material online). The mitochondrial genome (mitogenome) of L. acidissima was 545,150 bp in length (average coverage = 49.6×) and contained 34 protein-coding genes, 19 tRNA genes, and three rRNA genes (Fig. 1b; supplementary table S3, Supplementary Material online). The BLAST result revealed 11 mitochondrial plastid DNAs (MTPTs) in the mitogenome of L. acidissima, ranging from 181 to 8,477 bp (Table 1). The longest MTPT included partial ycf2, trnL_CAA, ndhB, rps7, and rps12 exon 2 and exon 3 (supplementary table S4, Supplementary Material online). In contrast, the smallest MTPT sequence contained only trnS-GGA. A total of 25,167 bp (accounting for 15.75%) of cpDNA was found in the mitogenome of L. acidissima.

Fig. 1. The map of organelle genomes of L. acidissima. a) The cpDNA map of L. acidissima. LSC, large single-copy region; SSC, small single-copy region; IRA/IRB, inverted repeat region. b) The mitochondrial genome map of L. acidissima. In both organelle genome maps, the inner circle indicates the AT content (light gray) and the GC content (dark gray). The genes are coded with various colors, which represent different functional groups. The double-headed arrows with Roman numbers from I to XI indicate the regions of cpDNA sequences that are present in the mitochondrial genomes. The different sizes of the arrows mean different lengths of the DNA sequences, but the arrow sizes do not show the exact scales among the DNA sequences.

Table 1 Quantity and size of plastid-derived mitochondrial DNA among 42 examined angiosperms

Group	Order	Species	Quantity of plastid-derived sequences	Length of sequences (bp)	
Basal angiosperms	Amborellales	Amborella trichopoda	63	137 to 6,352	
Nymphaeales	Nymphaea colorata	15	106 to 2,001	
Austrobaileyales	Schisandra sphenanthera	36	105 to 6,388	
Magnoliidae	Magnoliales	Liriodendron tulipifera	17	117 to 6,665	
Monocots (Lilidae)	Alismatales	Butomus umbellatus	3	156 to 4,917	
Spirodela polyrhiza	15	103 to 1,032	
Acorales	Cocos nucifera	29	107 to 3,535	
Poales	Oryza sativa	20	123 to 4,778	
Asparagales	Asparagus officinalis	8	143 to 2,013	
Allium cepa	15	126 to 13,989	
Eudicots	Proteales	Macadamia integrifolia	11	106 to 5,212	
Nelumbo nucifera	9	138 to 1,431	
Ranunculales	Anemone maxima	7	102 to 7,103	
Aconitum kusnezoffii	3	117 to 1,240	
Trochodendrales	Tetracentron sinense	10	185 to 7,013	
Vitales	Vitis vinifera	24	106 to 7,248	
Rosales	Hemiptelea davidii	3	146 to 6,244	
Cannabis sativa	9	136 to 1,090	
Malvales	Gossypium arboreum	9	110 to 2,199	
Aquilaria sinensis	8	231 to 14,637	
Sapindales	Citrus sinensis	19	181 to 53,731	
Citrus maxima	10	181 to 9,308	
Citrus unshiu	8	181 to 9,302	
Limonia acidissima	11	181 to 8,477	
Caryophyllales	Suaeda glauca	15	111 to 3,942	
Silene vulgaris	7	260 to 2,638	
Fallopia aubertii	10	124 to 11,211	
Santanales	Viscum album	3	105 to 6,636	
Malania oleifera	47	100 to 2,159	
Tolypanthus maclurei	31	106 to 2,616	
Ericales	Rhododendron simsii	9	146 to 656	
Camellia sinensis	8	116 to 6,663	
Vaccinium macrocarpon	17	106 to 920	
Solanales	Capsicum annuum	39	118 to 5,614	
Physochlaina orientalis	31	107 to 6,585	
Hyoscyamus niger	15	186 to 2,902	
Lamiales	Utricularia reniformis	74	104 to 1,777	
Castilleja paramensis	48	111 to 6,618	
Rotheca serrata	14	124 to 4,206	
Aquifoliales	Ilex pubescens	11	147 to 1,563	
Asterales	Platycodon grandiflorus	42	108 to 5,862	
Codonopsis lanceolata	5	121 to 2,995	

Further investigation of MTPTs revealed that the sequences of cpDNA were present in the mitogenomes of other 41 examined angiosperms with different quantities (supplementary table S4, Supplementary Material online). Specifically, the lowest number of MTPT (three sequences) was found in Butomus umbellatus (Butomaceae, Alismatales), Aconitum kusnezoffii (Ranunculaceae, Ranunculales), Hemiptelea davidii (Ulmaceae, Rosales), and Viscum album (Santalaceae, Santanales). In contrast, the highest number of MTPT was found in Utricularia reniformis (Lentibulariaceae, Lamiales), followed by Castilleja paramensis (Orobanchaceae, Lamiales) and Malania oleifera (Olacaceae, Santanales) with 74, 48, and 47 sequences, respectively. Similarly, the size of MTPT ranged from 100 to 53,731 bp among surveyed species (Table 1). Particularly, the largest MTPT was found in the mitogenome of Citrus sinensis (Rutaceae, Sapindales), whereas the shortest one was located in M. oleifera (Olacaceae, Santanales). Although U. reniformis had the highest number of MTPT, its largest MTPT was 1,777 bp.

The mapping result of MTPTs to the cpDNA of L. acidissima revealed that most of the cpDNA sequence could be the origin of MTPTs (Fig. 2). Notably, an abundance of MTPT originated from the inverted repeat (IR) region, followed by the large single-copy (LSC) region. The small single-copy region has the lowest quantity of MTPT compared to other regions. The two long MTPTs covered the entire LSC region, whereas other large MTPTs belonged to the IR region. Although a majority of the cpDNA sequence was covered by MTPTs, some regions were commonly found in many examined species such as psbA, trnD_GUC, psbC, psaB-psaA, trnS_GGA, trnP_UGG-trnW_CCA, rpl2-rpl23, ycf2, rrn16-trnI_CAU-trnA_UGC-rrn23, and ndhD.

Fig. 2. The mapping result of MTPTs of 42 species to the cpDNA of L. acidissima. The bar with numbers indicates the cpDNA sequence and nucleotide sites of L. acidissima. The bars which are different in length mean the MTPTs from 42 surveyed angiosperm. The graph indicates the coverage of MTPTs to the cpDNA of L. acidissima. The small bars under the graph indicate low-coverage sites. The blurry bars represent the MTPTs of L. acidissima. LSC, large single-copy region; SSC, small single-copy region; IR, inverted repeat region.

Discussion

The current results were similar to a previous study about the diversity of MTPTs in seed plants regarding gene content in MTPTs, quantities of MTPTs, hot spots of MTPTs, and shared MTPTs among related species (Wang et al. 2017). Specifically, all protein-coding genes, tRNA genes, and rRNA genes of cpDNA could be found in MTPTs of examined species (Fig. 2; supplementary table S4, Supplementary Material online). Additionally, the previous five hot spots for DNA transfer were confirmed. However, some additional hot spots were identified in the current study according to regions of cpDNA, including psbA, trnD_GUC, psbC, and psaB-psaA of the LSC region, ycf2 of the IR region, and ndhD of the SSC region. Similarly, new cold spots were located at ycf1, ndhA intron, and intergenic spacer region between petA and psbJ of cpDNA. Notably, the previous cold spot of trnS_UGA-psbZ-trnG_GCC was commonly found in the currently examined species (Fig. 2; supplementary table S4, Supplementary Material online). The number of surveyed species might cause these differences. Therefore, further investigation covering more seed plants might provide more profound information about the frequency of cpDNA content in MTPTs. Besides the common features of MTPTs among seed plants, the closely related species shared similar MTPTs, which were previously reported (Wang et al. 2017). In the current study, the mitogenome of Citrus and Limonia species of Rutaceae had similar MTPTs such as partial rrn23, partial rbcL, ycf3 exon1, and entire trnS_GGA (supplementary table S4, Supplementary Material online). This phenomenon suggested an early transformation of MTPTs at the divergence period of angiosperm families.

It is clear that MTPTs exhibited a high diversity among angiosperms regarding gene content, quantity, and size (Fig. 2, Table 1, and supplementary table S4, Supplementary Material online). Particularly, all protein-coding genes, tRNA genes, and rRNA genes of cpDNA can be identified in MTPTs (Wang et al. 2017). Furthermore, a previous study showed that the MTPTs might originate from random sites of cpDNA (Wang et al. 2007). These findings revealed the current status of MTPTs in angiosperms. However, the mechanism that resulted in the present profiles of MTPTs in seed plants remains unclear. Whether different cpDNA fragments migrate to the mitogenome continuously and independently? Previously, it was proposed that the plastid sequences integrated into the mitogenome via intracellular gene transfer and then became a foreign plastid through horizontal gene transfer between distantly related plants (Gandini and Sanchez-Puerta 2017). Based on the previous and current results, we hypothesize that there should be an initial transfer of the entire cpDNA to the mitogenome. Then, different genomic events, such as duplication, deletion, inversion, and substitution have occurred in the mitogenome independently and resulted in the current circumstances of MTPTs among angiosperms. In Fig. 2, although 42 examined species had different numbers and various lengths of MTPTs, their MTPTs could cover all regions of the cpDNA. Furthermore, multiple MTPTs from different species originated from the same areas of cpDNA such as psbA, trnD_GUC, psbC, psaB-psaA, trnS_GGA, trnP_UGG-trnW_CCA, rpl2-rpl23, ycf2, rrn16-trnI_CAU-trnA_UGC-rrn23, and ndhD. These landscapes of MTPTs revealed a possibility of the initial transfer of the whole cpDNA followed by independent fragmentation that resulted in the current diversity of MTPTs in angiosperms. In this study, a contig that could cover the entire cpDNA was absent (Fig. 2). Additionally, the presence of entire cpDNA in the mitogenome of land plants has not been reported. However, the transfer of the entire mitogenomes of moss and algae to the mitogenome of Amborella trichopoda was reported (Rice et al. 2013). Moreover, in the current study, long MTPTs that covered the most parts of cpDNA regions were found in examined angiosperms, suggesting the possibility of the presence of the entire cpDNA in the mitogenome before the fragmentation process. Further studies that sequence and characterize more mitogenomes of land plants might add critical evidence for the initial transfer of the entire cpDNA to mitogenome. Another attention for the MTPTs identification is the foreign cpDNA sequences, of which the transfer of trnA intron from a noneudicot plant to Phaseolus vulgaris was previously reported (Woloszynska et al. 2004; Gandini and Sanchez-Puerta 2017). This issue might be resolved by the current large database of cpDNAs from various species.

After the initial transfer of the cpDNA to the mitogenome, we hypothesize that the independent occurrence of deletion, substitution, duplication, and inversion caused the diversity of MTPTs in angiosperms. In Fig. 2, different numbers of MTPTs varied in size and gene content, resulting from independent deletion of the initially transferred cpDNA in 42 examined species (Table 1; supplementary table S4, Supplementary Material online). For example, in four examined species of Rutaceae, the numbers of MTPTs were ranged from 8 to 19 (Table 1). Although L. acidissima is a monotypic species and is assumed to exhibit a low evolutionary rate of MTPTs, its MTPT features are similar to those of Citrus maxima and Citrus unshiu (Table 1). In contrast, C. sinensis had the largest number and the longest length of MTPTs in Rutaceae, accounting for 19 records and 53,731 bp, respectively. Additionally, the coverage of MTPTs was lowest in the SSC region, and there were common MTPTs found in various examined angiosperms (Fig. 2). This phenomenon suggested a common mechanism for deleting MTPTs after the initial transfer of the whole cpDNA to the mitogenome. Further analysis of pairwise identity between the MTPTs and original sequences in the cpDNA revealed a range of similarity from 80% to 100%, suggesting random substitution events of the MTPTs during the evolution of angiosperm mitogenomes (supplementary table S4, Supplementary Material online). Among the MTPTs, there were shared gene contents, suggesting the presence of the duplication events of MTPTs during the transformation history of mitogenomes. Specifically, in the mitogenome of C. sinensis, psaB-psaA and rpl2-rpl23-ycf2 regions were found in different MTPTs (supplementary table S4, Supplementary Material online). A similar trend was also found in the MTPTs of A. trichopoda, Capsicum annuum, Schisandra sphenanthera, Oryza sativa, M. oleifera, C. paramensis, Vitis vinifera, and Cocos nucifera (supplementary table S4, Supplementary Material online). Therefore, further studies examining copies of MTPTs should be conducted to clarify this issue. In this study, we did not survey the inversion of MTPTs; however, we suggest that the inversion might relate to deletion and duplication events. Additionally, the deletion, substitution, duplication, and inversion mechanisms were not discussed. However, a previous study revealed that highly active recombination activities resulted in structural diversity, mutation, and genome stability of plant mitogenomes (Gualberto and Newton 2017). Therefore, we assumed that the genomic events related to MTPTs might have a strong relationship to the recombination activities of mitogenomes.

Last but not least, although our hypothesis was not strongly supported by direct genomic evidence, it was partly proven by the current circumstances of MTPTs. To confirm our hypothesis, some issues should be addressed in further studies, including (i) the record of mitogenome that contains the whole cpDNA sequence, (ii) the identity of MTPTs from the initial transfer and the secondary insertion, and (iii) the time of MTPTs insertion.

Materials and Methods

Sampling, DNA Extraction, Sequencing, and Genome Assembly

The leaf samples of L. acidissima L. were collected at Tra Vinh Province, Vietnam (9°55′12.5″N, 106°20′56.8″E). The leaves were dried using silica gel beads and stored at the Applied Biology Center of Tra Vinh University (Vietnam). The leaves were used to extract the total genomic DNA using DNeasy Plant Mini Kit (Qiagen, USA). The quality of the DNA samples was checked using gel electrophoresis and NanoDrop OneC spectrophotometer (Thermo Fisher Scientific, USA). For the short-read sequencing process, the library was prepared using the TruSeq Nano DNA Sample Preparation Kit (Illumina, USA). Then, the MiniSeq platform was used to sequence and generate paired-end reads of 151 bp. Meanwhile, the long-read data were generated using a ligation sequencing kit (SQK-LSK 109) and MinION Mk1B device with R9.4.1 flow cells following the manufacturer's protocols (Oxford Nanopore Technologies, UK). The raw Illumina data were qualified and filtered using the fastp tool (Chen et al. 2018), whereas the long-read data were checked using NanoPack tools (De Coster et al. 2018). The NOVOPlasty program was used to assemble the cpDNA with the seed sequence of L. acidissima rbcL (GenBank accession number AB505963) (Dierckxsens et al. 2017 ). The complete mitochondrial genome was assembled using Unicycler v0.5.0 based on a combination of short-read and long-read data (Wick et al. 2017). The gene content of the chloroplast and mitochondrial genomes was annotated using GeSeq (Tillich et al. 2017). The maps of organelle genomes were illustrated using OGDRAW (Greiner et al. 2019).

Comparison of Gene Transfer in Organelle Genomes of Angiosperms

The complete chloroplast and mitochondrial genomes of various species from different angiosperm orders were downloaded from the GenBank database (supplementary table S1, Supplementary Material online). Then, BLAST was used to locate plastid-derived sequences in the mitochondrial genome with at least 80% similarity and a minimum length of 100 bp (Johnson et al. 2008). The Geneious Prime v2023.2 was used to map the MTPT sequences to the cpDNA of L. acidissima to compare the MTPT sequences among examining species regarding size and location in cpDNA. The options for this assembly were “Allow Gaps” with a maximum gap size of 1,000 and a maximum per read of 30%, “Ignore Words repeated more than” 20 times, and “Maximum Mismatches Per Read” of 60%. The Geneious Prime v2023.2 was also used to visualize the mapping result.

Supplementary Material

evae184_Supplementary_Data

Acknowledgments

This work was fully funded by Tra Vinh University under grant contract number 279/2022/HĐ.HĐKH&ĐT-ĐHTV. The authors also thank Can Tho University and Nguyen Tat Thanh University for supporting other facilities to conduct this study.

Supplementary Material

Supplementary material is available at Genome Biology and Evolution online.

Author Contributions

H.D.K.D. designed the research, performed the genome sequencing, analyzed the data, and wrote the manuscript. N.N.N. and N.P.A.T. contributed to the sample collection and experiment conduction and wrote the manuscript. N.N.N. raised the funding. All the authors approved the final version of the manuscript.

Data Availability

The complete chloroplast genome and mitochondrial genome were submitted to GenBank under the accession numbers PP331238 and PP331239, respectively.
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