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Mitochondrial genome map of HA89(ANN2) cytoplasmic male sterility (CMS) line of sunflower. Intron containing genes are marked by an asterisk (*) symbol. Trans-spliced genes are presented as the compilation of exons (ex).
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This study provides insights into the flexibility of the mitochondrial genome in sunflower (Helianthus annuus L.) as well as into the causes of ANN2-type cytoplasmic male sterility (CMS). De novo assembly of the mitochondrial genome of male-sterile HA89(ANN2) sunflower line was performed using high-throughput sequencing technologies. Analysis of CM...
Contexts in source publication
Context 1
... assembled the complete mitochondrial genome of the HA89 sunflower line with ANN2 cytoplasmic sterility type (NCBI accession MN175741.1). The master chromosome of HA89 (ANN2) consists of 306,018 bp ( Figure 1), and it is 5071 bp longer than the mitogenome of the male-fertile isonuclear line HA89 (NCBI accession MN171345.1). ...
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... assembled the complete mitochondrial genome of the HA89 sunflower line with ANN2 cytoplasmic sterility type (NCBI accession MN175741.1). The master chromosome of HA89 (ANN2) consists of 306,018 bp (Figure 1), and it is 5071 bp longer than the mitogenome of the male-fertile isonuclear line HA89 (NCBI accession MN171345.1). The mitochondrial genomes of male-sterile ANN2 and male-fertile HA89 share 14 complementary regions, but their localizations and orientation differ. ...
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... prediction of transmembrane domains was made with TMHMM Server v.2.0 (http://www.cbs.dtu.dk/services/TMHMM-2.0/). The scheme of the bioinformatic pipeline is presented in Supplementary Figure S1. ...
Citations
... As shown in Fig. 3 and Table 1, the contigs of the four reassembled mitogenomes almost completely cover their corresponding reference mitogenomes [40][41][42][43][44], confirming the validity and accuracy of our assembling procedure. The A. thaliana Col-0 mitogenome was reassembled into a typical single circular chromosome with a length of 367 810 bp, showing only 2 bp difference from the published A. thaliana Col-0 mitogenome (accession number NC_037304.1, ...
... length 367 808 bp). The reassembled H. annuus cytoplasmic fertile (ANN1372-3) mitogenome was 300 887 bp in length, only 58 and 60 bp shorter than the other two H. annuus cytoplasmic fertile mitogenomes (HA412 and HA89), respectively [42,43]. The differences in mitogenome sizes between cytoplasmic fertile and CMS lines are due to several deletions and insertions [43]. ...
... The reassembled H. annuus cytoplasmic fertile (ANN1372-3) mitogenome was 300 887 bp in length, only 58 and 60 bp shorter than the other two H. annuus cytoplasmic fertile mitogenomes (HA412 and HA89), respectively [42,43]. The differences in mitogenome sizes between cytoplasmic fertile and CMS lines are due to several deletions and insertions [43]. The M. domestica mitogenome was also reassembled into a single circular chromosome (length 396 949 bp), showing only 2 bp difference from the published M. domestica mitogenome (accession number NC_018554.1, ...
Complete mitochondrial genome (mitogenome) of plants are valuable resources for nucleocytoplasmic interactions, plant evolution, and plant cytoplasmic male sterile line breeding. However, the complete assembly of plant mitogenomes is challenging due to frequent recombination events and horizontal gene transfers. Previous studies have adopted Illumina, PacBio, and Nanopore sequencing data to assemble plant mitogenomes, but the poor assembly completeness, low sequencing accuracy, and high-cost limit the sampling capacity. Here, we present an efficient assembly toolkit (PMAT) for de novo assembly of plant mitogenomes using low-coverage HiFi sequencing data. PMAT has been applied to the de novo assembly of 13 broadly representative plant mitogenomes, outperforming existing organelle genome assemblers in terms of assembly accuracy and completeness. By evaluating the assembly of plant mitogenomes from different sequencing data, it was confirmed that PMAT only requires 1× HiFi sequencing data to obtain a complete plant mitogenome. The source code for PMAT is available at https://github.com/bichangwei/PMAT. The developed PMAT toolkit will indeed accelerate the understanding of evolutionary variation and breeding application of plant mitogenomes.
... More than 70 types of CMS are known in sunflowers, some of which are described at the molecular level (Reddemann & Horn, 2018;Makarenko et al., 2019a;Makarenko et al., 2019b). However, CMS-PET1, discovered by Leclerc and obtained through the interspecific crossing of H. petiolaris with H. annuus , remains dominant in commercial hybrid breeding. ...
The vast majority of commercial sunflower hybrids worldwide are produced using cytoplasmic male sterility (CMS) of the PET1 type, resulting from the interspecific hybridization of Helianthus petiolaris with Helianthus annuus. In this study, the open reading frame, orfH522, associated with the CMS-PET1 phenotype, was revealed for the first time in the 3’-flanking region of the mitochondrial atpA gene in wild H. annuus. An analysis of whole genome data from 1089 accessions showed that the frequency of occurrence of CMS-orfH522 in wild H. annuus populations is 3.58%, while in wild H. petiolaris populations, it is 1.26%. The presence of additional genomic data with insufficient coverage of the orfH522 sequence indicates that the potential frequency of occurrence of CMS-orfH522 in natural sunflower populations may be two times higher. Based on these results and previous studies, PET1-CMS was suggested to be a natural cytotype of H. annuus, and the appearance of the CMS phenotype in cultivated sunflowers is associated with the loss of stabilizing nuclear genes of fertility restorers, which occurred during interspecific hybridization. These data may explain the patterns of differential cytoplasmic and nuclear introgression occurring in wild sunflower and are useful for further evolutionary studies.
... Additionally, plant mitochondria contain mitochondrial-encoded cytoplasmic male sterility (CMS) genes, which are related to the production of functional pollen or functional male reproductive organs [12]. Also, CMS genes affect the evolution of the mitochondrial genome by influencing mitochondrial recombination and rearrangement [13][14][15][16]. ...
... Previous studies have shown that the wild beet (Beta vulgaris ssp. vulgaris) [46], sunflower (Helianthus annuus) [16] and Brassica [47] mitogenomes contain two copies of cox2 gene associated with CMS. Accordingly, our study provides clues regarding the evolution of CMS in Orobanchaceae. ...
Orobanchaceae have become a model group for studies on the evolution of parasitic flowering plants, and Aeginetia indica, a holoparasitic plant, is a member of this family. In this study, we assembled the complete chloroplast and mitochondrial genomes of A. indica. The chloroplast and mitochondrial genomes were 56,381 bp and 401,628 bp long, respectively. The chloroplast genome of A. indica shows massive plastid genes and the loss of one IR (inverted repeat). A comparison of the A. indica chloroplast genome sequence with that of a previous study demonstrated that the two chloroplast genomes encode a similar number of proteins (except atpH) but differ greatly in length. The A. indica mitochondrial genome has 53 genes, including 35 protein-coding genes (34 native mitochondrial genes and one chloroplast gene), 15 tRNA (11 native mitochondrial genes and four chloroplast genes) genes, and three rRNA genes. Evidence for intracellular gene transfer (IGT) and horizontal gene transfer (HGT) was obtained for plastid and mitochondrial genomes. ψndhB and ψcemA in the A. indica mitogenome were transferred from the plastid genome of A. indica. The atpH gene in the plastid of A. indica was transferred from another plastid angiosperm plastid and the atpI gene in mitogenome A. indica was transferred from a host plant like Miscanthus siensis. Cox2 (orf43) encodes proteins containing a membrane domain, making ORF (Open Reading Frame) the most likely candidate gene for CMS development in A. indica.
... The protein encoded by orf188 in H. grosseserratus shares almost the same structure as the cox2-chimeric protein (QFS00065.1), which we identified in ANN2, a CMS line of sunflower in a previous study [29]. According to GenBank data, orf316 is an ORF common to sunflower mtDNA. ...
... The orf188 that we annotated in the H. grosseserratus mitogenome is similar to the previously described cox2-chimeric ORF (QFS00065.1), potentially playing a role in the formation of ANN2 CMS type in sunflower [29]. Nevertheless, the coding sequences of these two ORFs are not identical (about 76% similarity), but they have the same appearance in mtDNA. ...
The genus Helianthus is a diverse taxonomic group with approximately 50 species. Most sunflower genomic investigations are devoted to economically valuable species, e.g., H. annuus, while other Helianthus species, especially perennial, are predominantly a blind spot. In the current study, we have assembled the complete mitogenomes of two perennial species: H. grosseserratus (273,543 bp) and H. strumosus (281,055 bp). We analyzed their sequences and gene profiles in comparison to the available complete mitogenomes of H. annuus. Except for sdh4 and trnA-UGC, both perennial sunflower species had the same gene content and almost identical protein-coding sequences when compared with each other and with annual sunflowers (H. annuus). Common mitochondrial open reading frames (ORFs) (orf117, orf139, and orf334) in sunflowers and unique ORFs for H. grosseserratus (orf633) and H. strumosus (orf126, orf184, orf207) were identified. The maintenance of plastid-derived coding sequences in the mitogenomes of both annual and perennial sunflowers and the low frequency of nonsynonymous mutations point at an extremely low variability of mitochondrial DNA (mtDNA) coding sequences in the Helianthus genus.
... It is well known that atp6 is a key component of the transmembrane Fo portion of the ATP synthase and it is frequently associated with CMS phenomena both in monocotyledon species such as rice [52], maize [53], and dicotyledon species such as pepper [5], sugar beet [13], brown mustard [12], carrot [39], kenaf [54], and sunflower [55]. ...
Cytoplasmic male sterility (CMS) has always aroused interest among researchers and breeders, being a valuable resource widely exploited not only to breed F1 hybrid varieties but also to investigate genes that control stamen and pollen development. With the aim of identifying candidate genes for CMS in fennel, we adopted an effective strategy relying on the comparison between mitochondrial genomes (mtDNA) of both fertile and sterile genotypes. mtDNA raw reads derived from a CMS genotype were assembled in a single molecule (296,483 bp), while a draft mtDNA assembly (166,124 nucleotides, 94 contigs) was performed using male fertile sample (MF) sequences. From their annotation and alignment, two atp6-like sequences were identified. atp6-, the putative mutant copy with a 300 bp truncation at the 5'-end, was found only in the mtDNA of CMS samples, while the wild type copy (atp6 +) was detected only in the MF mtDNA. Further analyses (i.e., reads mapping and Sanger sequencing), revealed an atp6 + copy also in CMS samples, probably in the nuclear DNA. However, qPCRs performed on different tissues proved that, despite its availability, atp6 + is expressed only in MF samples, while apt6-mRNA was always detected in CMS individuals. In the light of these findings, the energy deficiency model could explain the pollen deficiency observed in male sterile flower. atp6-could represent a gene whose mRNA is translated into a not-fully functional protein leading to suboptimal ATP production that guarantees essential cellular processes but not a high energy demand process such as pollen development. Our study provides novel insights into the fennel mtDNA genome and its atp6 genes, and paves the way for further studies aimed at understanding their functional roles in the determination of male sterility.
... One of the spontaneously occurring CMS sources in sunflower is ANN2, which is quite complicated and cannot be restored completely. Makarenko et al. [7] used the WGS method to gain insights into the structural reorganization of the mitochondrial genome that generates ANN2 in sunflower. The authors compared the mitochondrial genome sequences from a male sterile line with that of a male-fertile line and observed several reorganization events (deletions and insertions) and several new transcriptionally active open reading frames (ORFs) in the mitochondrial genome of the male sterile line. ...
Plant cells contain two double membrane bound organelles, plastids and mitochondria, that contain their own genomes. There is a very large variation in the sizes of mitochondrial genomes in higher plants, while the plastid genome remains relatively uniform across different species. One of the curious features of the organelle DNA is that it exists in a high copy number per mitochondria or chloroplast, which varies greatly in different tissues during plant development. The variations in copy number, morphology and genomic content reflect the diversity in organelle functions. The link between the metabolic needs of a cell and the capacity of mitochondria and chloroplasts to fulfill this demand is thought to act as a selective force on the number of organelles and genome copies per organelle. However, it is not yet clear how the activities of mitochondria and chloroplasts are coordinated in response to cellular and environmental cues. The relationship between genome copy number variation and the mechanism(s) by which the genomes are maintained through different developmental stages are yet to be fully understood. This Special Issue has several contributions that address current knowledge of higher plant organelle DNA. Here we briefly introduce these articles that discuss the importance of different aspects of the organelle genome in higher plants.
Commercial hybrid development is one of the most common goals in crop improvement because it allows farmers to harvest considerably higher seed yields from a uniform crop with improved characteristics and enhanced crop efficiency due to the effects of heterosis. Male sterility is a practical method of producing single-cross hybrids because it eliminates the need for time-consuming and labor-intensive hand emasculation and provides 100% male sterility, consequently eliminating the possibility of selfing. Despite the availability of a large number of male sterility systems, only single-source PET-1 has been widely used worldwide due to several advantages. The development of hybrids of sunflower has been investigated, and extensive efforts have been made to identify stable male sterility systems. Hybrids have several advantages over open-pollinated varieties, including higher seed yield (20–30%), greater uniformity in maturity and plant height, and the ability to be harvested at the same time, making them suitable for combine harvesting. They respond to high input agriculture and high autogamy, which reduces the urgency for bees for cross-pollination. F1 hybrids are more tolerant or resistant to major biotic and abiotic stresses. In this chapter, emphasis has been given to the significant achievements in the development of male sterility systems and commercial hybrid seed production in sunflower crops, and it discusses the drawbacks and perspectives of this technology. The use of biotechnological tools and highlighting the prospects of applications of molecular markers in the genetic improvement of sunflower is also discussed.KeywordsCytoplasmic male sterilityHeterosisHybrid seed productionFertility restorationMarker-assisted selection (MAS)
