Assembly and analysis of a male sterile rubber tree mitochondrial genome reveals DNA rearrangement events and a novel transcript
© Shearman et al.; licensee BioMed Central Ltd. 2014
Received: 20 December 2013
Accepted: 7 February 2014
Published: 10 February 2014
The rubber tree, Hevea brasiliensis, is an important plant species that is commercially grown to produce latex rubber in many countries. The rubber tree variety BPM 24 exhibits cytoplasmic male sterility, inherited from the variety GT 1.
We constructed the rubber tree mitochondrial genome of a cytoplasmic male sterile variety, BPM 24, using 454 sequencing, including 8 kb paired-end libraries, plus Illumina paired-end sequencing. We annotated this mitochondrial genome with the aid of Illumina RNA-seq data and performed comparative analysis. We then compared the sequence of BPM 24 to the contigs of the published rubber tree, variety RRIM 600, and identified a rearrangement that is unique to BPM 24 resulting in a novel transcript containing a portion of atp9.
The novel transcript is consistent with changes that cause cytoplasmic male sterility through a slight reduction to ATP production efficiency. The exhaustive nature of the search rules out alternative causes and supports previous findings of novel transcripts causing cytoplasmic male sterility.
Mitochondria are membrane-bounded organelles that function in energy metabolism, biosynthesis of cofactors and vitamins, cellular differentiation, signalling, cell growth, and cell death . They contain their own genomes which are inherited maternally in most plant species. The first flowering plant mitochondrial DNA (mtDNA) to be completely sequenced was Arabidopsis thaliana, since then there have only been 37 additional mitochondrial genomes sequenced and analyzed from flowering plants [http://www.ncbi.nlm.nih.gov/Genomes/]. These additional mitochondrial genomes have increased our understanding of genome rearrangement, DNA transfer and phylogenetic diversity. Plant mitochondrial genomes encode tRNAs, rRNAs, proteins and ribosomal proteins and range in size from 200 Kb in Brassica hirta to 2.74 Mb in Cucumis melo. Mitochondrial genome expansion in land plants is primarily due to large intergenic regions, repeated segments, intron expansion and incorporation of foreign DNA such as plastid and nuclear DNA [5, 6]. Accumulation of repetitive sequences in plant mitochondrial genomes cause frequent recombination events and dynamic genome rearrangements within a species [7, 8]. Several mutations by gene rearrangement of the mitochondrial genes were found associated with cytoplasmic male sterility (CMS) such as the T-urf13 gene in maize , pcf gene (a fusion of atp9 and cox2 portions) in petunia , cox1 in rice  and mutations in ATPase subunits in sunflower  and Brassica . RNA processing also plays an important role in controlling CMS as evidenced in orf355/orf77 (atp9) and T-urf13 in maize [14, 15].
Conventional strategies for obtaining mitochondrial genome sequencing involve isolation of mitochondrial DNA, cloning and sequencing. However, problems with this approach of mitochondrial genome sequencing include difficulty resolving sequence of the mitochondrial genome from the nuclear genome and assembly of a single circular genome due to the highly dynamic genome structure. Rivarola et al.  suggested that examination of the read depths of the resulting assemblies could be used to separate reads of nuclear, chloroplast and mitochondria origin. With the development of next generation sequencing (NGS) technologies, new strategies have been used to obtain plant mitochondrial genomes. A combination approach of shotgun and paired-end NGS sequencing from non-enriched whole genome DNA libraries have been successfully used to obtain the mitochondrial genomes of melon , carrot  and date palm .
Hevea brasiliensis, or rubber tree, is an important economical plant that can produce natural latex at a commercial scale. Sequencing information of its nuclear genome , plastid genome  and mitochondrial genome is important for genetic improvement and understanding of biological mechanisms of the plant species. The closest plant species to H. brasiliensis with a mitochondrial genome draft reported is from Ricinus communis which is in the same Euphorbiaceae family . In this study, we obtained a draft of the rubber tree mitochondrial genome of the variety BPM 24, a cytoplasmic male sterile descendant of a GT 1 (female) × AVROS 1734 (male) cross . The variety GT 1 is male sterile, its offspring BPM 24 is male sterile and the offspring of BPM 24 are also male sterile. Thus the cause for male sterility in this line is cytoplasmically inherited, which makes the mitochondrion the most probable cause. The assembled BPM 24 genome was characterized for gene annotation, transcription analysis, RNA editing events, sequence variation and recombinations within the species that cause cytoplasmic male sterility in rubber tree.
Shoot apical meristem samples of H. brasiliensis (varieties BPM 24, RRII 105, RRIC 110, PB 235, RRIT 251 and RRIM 600) were collected for DNA and RNA extraction from an experimental field at the Rubber Research Institute of Thailand, Ministry of Agriculture and Cooperatives, Thailand. The samples for DNA extraction were processed using the DNeasy Plant Mini Kit (Qiagen, CA, USA). The samples for RNA extraction were immediately frozen in liquid nitrogen and stored at -80°C until RNA extraction following the protocols in Triwitayakorn et al. .
The DNA from variety BPM 24 was sequenced in house on a Genome Sequencer (GS) FLX platform (Roche, USA) using two libraries: shotgun sequencing and 8-kb paired-end sequencing according to Roche protocols. In addition this sample was sequenced on a Hiseq 2000 platform (Illumina, USA) using paired-end sequencing at Macrogen (Korea). The genomic sequencing reads from 454 were assembled de novo using gsAssembler (Newbler, version 2.7, Roche, USA). Scaffolds were produced using SSPACE_basic_V2.0 . The scaffold graph was produced using bb.454contignet . The assembled contigs were searched for sequence homology against the publicly available plant mitochondrial genomes and repeats were identified using Reputer. The Illumina data was mapped to the 454 assembled contigs to improve on the assembly and the sequence depth was used to differentiate between mitochondrial sequences and nuclear encoded mitochondrial copies. To identify regions of plastid origin, the assembled sequences were aligned against the rubber tree chloroplast genome  using BLAST. Comparison of mitochondrial genome structures of rice, tobacco, castor bean and rubber tree was performed using MAUVE .
The extracted RNA from the six rubber tree varieties were sequenced on an Illumina HiSeq2000 at Macrogen (Korea). RNA sequence data quality was checked using FastQC and was cleaned using TRIMMOMATIC v0.27 . The reads were mapped to the assembled genome using TopHat (v2.0.9)  with bowtie (v1.0.0)  and the fusion search option.
Open Reading Frames (ORFs) were predicted using Open Reading Frame Finder [https://www.ncbi.nlm.nih.gov/gorf/gorf.html]. The tRNA genes were searched using tRNAscan-SE . The annotated genes were also checked with the plant mitochondrial genome annotation program Mitofy . All predicted ORFs, tRNA genes and rRNA genes were searched against the publicly available mitochondrial nucleotide and protein sequence database. Expression of genes was checked by mapping the RNA sequencing data from each sample to the assembled genome using TopHat. RNA-editing events were identified from this mapping data using VarScan (v2.3.4) , in addition RNA-editing events were predicted using PREP-Mt . RNA-editing events were compared to other plant species by obtaining sequences from genbank with RNA-editing information and performing an alignment. Trans-membrane domains were predicted using TMHMM (v2.0) .
PCR and Sanger confirmation
The contig graph was confirmed by PCR using 50 primer pairs (see Additional file 1). PCR for rearrangement sites was performed for each of the six varieties of rubber tree in both genomic and cDNA samples. Primers for suspected rearrangement sites were designed so that they flanked the suspected rearrangement site in non repetitive genomic DNA and additional primers were designed within the regions indicated as expressed by the RNA-seq mapping data (see Additional file 2).
The phylogenetic tree was constructed using seven species (Ricinus communis, Hevea brasiliensis, Carica papaya, Brassica napus, Raphanus sativus, Arabidopsis thaliana and Cycas taitungensis as an outgroup). Gene sequences from each species for 21 conserved genes (nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, nad9, cob, cox1, cox2, cox3, atp1, atp4, atp6, atp8, atp9, rps3, rps4, rps12) were compared and a maximum likelihood tree was constructed using MEGA 5 with 1000 bootstrap replications .
Results and discussion
Mitochondrial sequence assembly
Several studies have attempted to identify the mechanism of plant mitochondrial DNA replication (for review see ) with evidence found for rolling circle replication and recombination mediated replication. However, the exact mechanism remains to be fully elucidated. In addition, studies using pulse field gel electrophoresis and electron microscopy failed to find a single circular strand of DNA, instead finding many smaller subgenomic circles and linear strands of DNA consistent with rolling circle replication products ( and references). Recent efforts to sequence plant mitochondrial genomes have also found evidence for subgenomic circles in the form of scaffold graphs of varying complexity [36–42], much like what we found in this study. In fact some studies have suggested that subgenomic circles are the native state of plant mitochondrial genomes [36, 40], and must therefore be self replicating. With so many repeat sequences it is quite possible that an origin of replication sequence could exist multiple times in plant mitochondrial genomes allowing for independently replicating subgenomic circles to exist. Furthermore it is difficult to imagine how such diversity in mitochondrial genome size and subgenomic circle number could exist if there was but a single origin of replication with only the complete master circle able to segregate to dividing mitochondria. Such a mechanism would surely result in loss of non essential sequence and evolution towards more compact mitochondrial genomes as observed in mammalian mitochondrial genomes . Thus our data adds to the growing body of evidence that plant mitochondrial genomes can consist of several independently replicating subgenomic circular DNA strands, a single circular DNA strand, or a mixture of both. Despite this, it is common practice to reconstruct a single ‘master circle’ DNA strand to represent the complete mitochondrial genome [36, 39].
Size, number and direction of repeat sequences in the rubber tree mitochondrial genome
Repeat length (bp)
Number of repeats
% genome size
Annotation of the mitochondrial genome
Coding information of the rubber tree mitochondrial genome
(2x)nad1, (2x)nad2, nad3, nad4, (2x)nad4L, nad5, (2x)nad6, (2x)nad7, (2x)nad9
cox1, (2x)cox2, cox3
(2x)atp1, (2x)atp4, (2x)atp6, (2x)atp8, atp9
(2x)ccmB, (2x)ccmC, ccmFc, ccmFn
5S rRNA, 18S rRNA, 26S rRNA
Ribosomal protein small subunit
rps1, rps3, (2x)rps4, rps12, rps13
Ribusomal protein large subunit
(2x)rpl5, (2x)rpl10, rpl16
Chloroplast transferred complete genes
(2x)4.5S rRNA, (2x)5S rRNA, 16S rRNA, (2x)psaA, (2x)ycf3
Conserved Hypothetical genes
orf101, orf122, orf126, (2x)orf128, orf129, (2x)orf190
(2x)trnC-GCA, trnD-GUC, trnD-GUC-cp, (2x)trnE-UUC, (2x)trnF-GAA, trnG-GCC, (2x)trnH-GUG-cp, trnK-UUU, (2x)trnL-UAA, (4x)trnM-CAU, (2x)trnM-CAU-cp, (4x)trnN-GUU-cp, trnP-UGG, (2x)trnP-UGG-cp, trnQ-UUG, (2x)trnR-ACG-cp, trnS-GCT, (2x)trnS-TGA, trnV-GAC-cp, (2x)trnW-CCA-cp, (2x)trnY-GTA
rpl2, (2x)rps2, (2x)rps14, rps19
cp-derived gene fragment transfer
16S rRNA, 23S rRNA, atpE, ndhF, (2x)psaB, (2x)psbC, (2x)rpoA, rps12_3end, (2x)ycf1, (2x)ycf15, (2x)ycf2, ycf68
Lost gene (transferred to nucleus)
There were 19 tRNA genes identified, five of which occurred twice in the assembled mitochondrial master circle (Table 2). Seven of the tRNA genes plus 12 other genes are also found on the rubber tree chloroplast genome suggesting that they have been transferred from the chloroplast to the mitochondrial genome. It is unlikely to be chloroplast DNA contamination as these sequences differ from those in the chloroplast genome at multiple sites and there are sequencing reads extending from mitochondrial sequence to these transferred chloroplast fragments. Gene transfer from chloroplast to mitochondria is a common phenomenon in plants and the chloroplast copies that we found in the rubber tree mitochondria are largely consistent with previously identified chloroplast gene transfer events . Exceptions include two genes, trnS-GGA and trnI-CAU, that have been transferred from chloroplast to mitochondria in a range of species but were not found in the rubber tree mitochondrial genome. A third gene, trnE-UUC, also known to have been transferred from chloroplast to mitochondria in other species, was found in the rubber tree mitochondria, but did not appear to be from the chloroplast DNA. Ricinus communis was similar to rubber tree in that it lacked the trnI-CAU gene and had a mitochondrial copy of trnE-UUC that was different to the chloroplast copy, but unlike rubber tree had a chloroplast copy of trnS-GGA. This shows that the chloroplast-derived trnS-GGA was lost to rubber tree after the split from Ricinus and that the either chloroplast-derived trnI-CAU and trnE-UUC genes were lost to the Ricinus/rubber tree clade or that the transfer occurred after this clade split from the other species.
We identified cases of RNA editing by mapping the RNA-seq data to the assembled mitochondrial genome. This identified 224 cases among the six samples where the RNA-seq base was a thymine while the genomic base was a cytosine (see Additional file 4). Out of these sites 184 were also predicted to be RNA editing sites based on information from other species and 199 changed an amino acid. The most common amino acid changes were S to L with 52 events, P to L with 42 events and S to F with 29 events. RNA-editing was compared across 29 species, where data was available, and found to be highly conserved across all species (see Additional file 4). We found 8 cases where a C was edited to a U in rubber tree, in genes atp4, cox1, cox2, matR, nad1, nad2 and nad7, but remained an unedited C in all other species (see Additional file 4). There was a single case, in cytochrome c biogenesis factor C (ccmFC), where RNA-editing was required to produce a stop codon, this RNA-editing site was highly conserved among many species. The most heavily edited gene was cytochrome c oxidase subunit 2 (cox2) with 15 RNA-editing events in 783 bp of sequence.
Two cases were found where BPM 24 showed a lack of RNA-editing at a location where all the other rubber tree samples showed either RNA-editing or a variant, one was in succinate dehydrogenase subunit 3 (sdh3) and the other was in maturase-R (matR). The sdh3 RNA-editing event did not change an amino acid and was not found in any other species so is unlikely to have a significant effect. The RNA-editing event in matR changes a hystidine residue (positively charged) to a tyrosine residue (hydrophobic with a negative dipole) which may be required for correct protein folding, but is not in a functional motif. The RNA-editing in matR was observed in four other species while six other species showed a T variant. There were only two cases where a species with RNA-editing information had the same base (C) as BPM 24 at this locus, however, this could represent incomplete information rather than a lack of RNA-editing. Mitochondrial encoded maturases have been found to be required for the proper splicing of some group II introns in Arabidopsis with mutations resulting in retarded growth and developmental phenotypes [49, 50]. However, the specific function of matR remains unknown so whether this lack of RNA-editing plays a role in the CMS phenotype or not is unclear.
Blast result of published contigs (RRIM 600) vs BPM 24 master circle showing 11 rearranged contigs
The second rearrangement was identified by the 11561 bp contig AJJZ010174367.1 from RRIM 600 that maps to four separate sections of the master circle (Table 3). The most interesting of these is Section 5871–7413 bp of the published RRIM 600 contig that matches 156744–158290 bp of the master circle, and similar to the first rearrangement, has a 29 bp repeat sequence near the break site and RNA-seq data supporting expression with 128 bp of extra sequence unique to BPM 24. Using PCR primers that flanked the rearrangement site within the expressed section we found that the published contig sequence is present in all varieties and the rearranged sequence is found and expressed only in BPM 24 (see Additional file 2). The expressed sequence at this site matches ATPase subunit 1 (atp1) which is annotated at 156716–158245 bp on the master circle negative strand, placing one of the break points 45 bp before the start codon of atp1 and the other 28 bp before the end of atp1. All varieties had RNA-seq data consistent with a complete and functional copy of atp1 with the extra sequence in BPM 24 occurring after the stop codon suggesting that this variant is unlikely to affect the protein product.
A novel or fusion transcript is a common occurrence in CMS plants and often involves a portion of, or is near an ATP synthase subunit gene . In total, nine cases of a novel transcript containing part of an ATP synthase gene have been found in CMS plants which are not found in control plants: atp1 in eggplant ; atp6 in maize , Brassica tournefortii, wheat  and chilli ; atp8 in sunflower ; atp9 in petunia , rapeseed  and sorghum . In addition, disruptions to the ATP synthase complex, not featuring fusion transcripts, in plant mitochondria have been associated with CMS in chilli , Oryza rufipogon, Arabidopsis thaliana, wheat , maize  and tobacco . Since the observed novel transcript in rubber tree is both a novel fustion transcript and includes a portion of an ATP synthase subunit, typical of a CMS causing change, it is highly likely to be the cause of CMS in rubber tree. While it may be difficult to imagine how disruption to such a fundamental function as energy production could result in male sterility but not affect any other cell type or developmental process, there is evidence that some cell types are more sensitive than others to perturbation of mitochondrial efficiency. A prime example of this is Leber’s hereditary optic neuropathy in human where a mitochondrial mutation in an oxidative phosphorylation gene only affects retinal ganglion cells . The most common finding in CMS plants is an additional transcript that contains part of an ATP synthase gene and is thus a gain of function change which explains how it can be specific to anthers. Anther development has a high energy demand and mitochondria undergo rapid expansion in copy number early during anther growth, increasing by as much as 40 fold per cell . Anthers of CMS maize begin to breakdown shortly after this mitochondrial expansion suggesting a link between the two processes . Indeed, cell death of sunflower CMS anthers has been associated with the release of mitochondrial cytochrome c oxidase into the cytosol , which is an activation signal for apoptosis-like cell death . This particular form of sunflower CMS is caused by a novel transcript with atp8-like sequence and has been shown to have reduced ATP hydrolysis function . Thus novel transcripts that encode part of an ATP synthase gene, such as the one identified in BPM 24, cause CMS, at least in some cases, by slightly reducing the ATP synthase complex activity to a point where mitochondria cannot generate sufficient energy for the highly energy reliant anthers resulting in mitochondria mediated apoptosis-like cell death.
We have reconstructed the mitochondrial sequence of rubber tree clone BPM 24 and identified coding sequences and repeat elements. We then used the published contigs from RRIM 600 to identify rearrangements in BPM 24 that result in fusion transcripts for atp1 and atp9, with the atp9 fusion transcript likely reducing the efficiency of ATP production and resulting in cytoplasmic male sterility. Since BPM 24 is the offspring of the variety GT 1, we have indirectly identified the cause of CMS in GT 1 also. The exhaustive nature of this search approach rules out any other cause for the observed CMS in BPM 24 rubber tree and corroborates findings by other groups, often using less exhaustive search approaches, that novel fusion transcripts of ATP synthase genes can cause CMS.
Availability of supporting data
Rubber tree mitochondrial genome master circle: DDBJ: AP014526.
Rubber tree mitochondrial genome raw reads: DDBJ: DRA001347.
Samples and funding for this work were supplied by the Rubber Research Institute of Thailand (RRIT).
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