The impact of genome evolution on the allotetraploid Nicotiana rustica – an intriguing story of enhanced alkaloid production

Sierro, Nicolas; Battey, James N. D.; Bovet, Lucien; Liedschulte, Verena; Ouadi, Sonia; Thomas, JH; Broye, Hervé; Laparra, Hélène; Vuarnoz, Aline; Lang, Gerhard K.; Goepfert, Simon; Peitsch, Manuel C.; Ivanov, Nikolai V.

doi:10.1186/s12864-018-5241-5

Cited by 32 publications

(27 citation statements)

References 39 publications

(39 reference statements)

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“…Our comparative plastid genome analysis revealed that the maternal parent of the tetraploid N. rustica was the common ancestor of N. paniculata and N. knightiana , and the later species is more closely related to N. rustica . The relaxed molecular clock analyses estimated that the speciation event between N. rustica and N. knightiana appeared ∼0.56 Ma (HPD 0.65–0.46) in line with previous findings (Sierro et al, 2018). Comparative analysis of the genomes of four related Nicotiana species revealed that N. rustica inherited about 41% of its nuclear genome from its paternal progenitor, N. undulata , the rest from its maternal progenitor, the common ancestor of N. paniculata and N. knightiana (Sierro et al, 2018), which has also been confirmed by our study.…”

Section: Discussionsupporting

confidence: 90%

“…The relaxed molecular clock analyses estimated that the speciation event between N. rustica and N. knightiana appeared ∼0.56 Ma (HPD 0.65–0.46) in line with previous findings (Sierro et al, 2018). Comparative analysis of the genomes of four related Nicotiana species revealed that N. rustica inherited about 41% of its nuclear genome from its paternal progenitor, N. undulata , the rest from its maternal progenitor, the common ancestor of N. paniculata and N. knightiana (Sierro et al, 2018), which has also been confirmed by our study. It has been shown that N. rustica and in fact all Nicotiana tetraploids, except species included in section Suaveolentes , originated from a doubling of the diploid chromosome for the genus.…”

Section: Discussionsupporting

confidence: 90%

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Plastid genomics of Nicotiana (Solanaceae): insights into molecular evolution, positive selection and the origin of the maternal genome of Aztec tobacco (Nicotiana rustica)

Mehmood

Abdullah

Ubaid

et al. 2020

Preprint

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The genus Nicotiana of the family Solanaceae, commonly referred to as tobacco plants, are a group cultivated as garden ornamentals. Besides their use in the worldwide production of tobacco leaves, they are also used as evolutionary model systems due to their complex development history, which is tangled by polyploidy and hybridization. Here, we assembled the plastid genomes of five tobacco species, namely N. knightiana, N. rustica, N. paniculata, N. obtusifolia and N. glauca. De novo assembled tobacco plastid genomes showed typical quadripartite structure, consisting of a pair of inverted repeats (IR) regions (25,323–25,369 bp each) separated by a large single copy (LSC) region (86,510 –86,716 bp) and a small single copy (SSC) region (18,441–18,555 bp). Comparative analyses of Nicotiana plastid genomes showed similar GC content, gene content, codon usage, simple sequence repeats, oligonucleotide repeats, RNA editing sites and substitutions with currently available Solanaceae genomes sequences. We identified twenty highly polymorphic regions mostly belonging to intergenic spacer regions (IGS), which could be appropriate for the development of robust and cost-effective markers to infer the phylogeny of genus Nicotiana and family Solanaceae. Our comparative plastid genome analysis revealed that the maternal parent of the tetraploid N. rustica was the common ancestor of N. paniculata and N. knightiana, and the later species is more closely related to N. rustica. The relaxed molecular clock analyses estimated that the speciation event between N. rustica and knightiana appeared 0.56 Ma (HPD 0.65–0.46). The biogeographical analysis showed a south-to-north range expansion and diversification for N. rustica and related species, where N. undulata and N. paniculata evolved in North/Central Peru, while N. rustica developed in Southern Peru and separated from N. knightiana, which adapted to the Southern coastal climatic regimes. We further inspected selective pressure on protein-coding genes among tobacco species to determine if this adaptation process affected the evolution of plastid genes. These analyses indicated that four genes involved in different plastid functions, such as DNA replication (rpoA) and photosynthesis (atpB, ndhD and ndhF), came under positive selective pressure as a result of specific environmental conditions. Genetic mutations of the following genes might have contributed to the survival and better adaptation during the evolutionary history of tobacco species.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionsupporting

confidence: 90%

Plastid genomics of Nicotiana (Solanaceae): insights into molecular evolution, positive selection and the origin of the maternal genome of Aztec tobacco (Nicotiana rustica)

Mehmood

Abdullah

Ubaid

et al. 2020

Preprint

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“…Similarly, the recent draft genome of N. rustica has suggested that approximately 59% originated from the maternal genome donor (N. knightiana/N. paniculata) versus 41% from the paternal genome donor, using a k-mer analysis of sequence data [24].…”

Section: Introductionmentioning

confidence: 99%

Repetitive DNA Restructuring Across Multiple Nicotiana Allopolyploidisation Events Shows a Lack of Strong Cytoplasmic Bias in Influencing Repeat Turnover

Dodsworth

Guignard

Pérez‐Escobar

et al. 2020

Genes

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Allopolyploidy is acknowledged as an important force in plant evolution. Frequent allopolyploidy in Nicotiana across different timescales permits the evaluation of genome restructuring and repeat dynamics through time. Here we use a clustering approach on high-throughput sequence reads to identify the main classes of repetitive elements following three allotetraploid events, and how these are inherited from the closest extant relatives of the maternal and paternal subgenome donors. In all three cases, there was a lack of clear maternal, cytoplasmic bias in repeat evolution, i.e., lack of a predicted bias towards maternal subgenome-derived repeats, with roughly equal contributions from both parental subgenomes. Different overall repeat dynamics were found across timescales of <0.5 (N. rustica L.), 4 (N. repanda Willd.) and 6 (N. benthamiana Domin) Ma, with nearly additive, genome upsizing, and genome downsizing, respectively. Lower copy repeats were inherited in similar abundance to the parental subgenomes, whereas higher copy repeats contributed the most to genome size change in N. repanda and N. benthamiana. Genome downsizing post-polyploidisation may be a general long-term trend across angiosperms, but at more recent timescales there is species-specific variance as found in Nicotiana.

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“…Tobacco is an allopolyploid species (2n = 4x = 48) that arose from a tetraploidization event of its basic chromosome number (n = 12), which is similar to numerous other solanaceous species such as tomato, potato, pepper, and eggplant (Clarkson et al 2005, Goodspeed 1954, Sierro et al 2018. It is also one of the most important non-food crops that are extensively cultivated globally.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide association study of leaf chemistry traits in tobacco

et al. 2020

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Leaf chemistry traits are some of the key factors influencing tobacco quality, which can be significantly reduced by lower chemical components in cured leaf. To improve tobacco quality through breeding, genetic diversity analysis, population structure analysis, and genome-wide association studies were performed in a panel of 347 tobacco germplasms and the markers associated with five leaf chemistry traits, including total sugar (TS), reducing sugar (RS), total nitrogen (TN), nicotine (NIC), and total potassium (TP) contents were identified. Four groups were classified at a genetic distance of 0.316 by genetic diversity analysis based on coefficient parameter NEI72 using a program NTSYS-pc2.10e, whereas four well-differentiated subpopulations were postulated in the 347 tobacco accessions. A total of 47 target trait-associated SNPs was detected in at least three environments as well as the best linear unbiased predictions (BLUPs) across all environments, among which two, two, four, six, and one highly suggestive associated SNPs were repeatedly detected in all environments and BLUPs for TS, RS, TN, NIC, and TP, respectively. On the basis of the phenotypic effects of the alleles corresponding to suggestive associated SNPs, five tobacco accessions harboring favorable alleles with elite phenotypic performance in leaf chemistry traits were identified. The results could facilitate quality tobacco breeding for higher leaf chemistry trait contents through molecular marker-assisted approaches.

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The impact of genome evolution on the allotetraploid Nicotiana rustica – an intriguing story of enhanced alkaloid production

Cited by 32 publications

References 39 publications

Plastid genomics of Nicotiana (Solanaceae): insights into molecular evolution, positive selection and the origin of the maternal genome of Aztec tobacco (Nicotiana rustica)

Plastid genomics of Nicotiana (Solanaceae): insights into molecular evolution, positive selection and the origin of the maternal genome of Aztec tobacco (Nicotiana rustica)

Repetitive DNA Restructuring Across Multiple Nicotiana Allopolyploidisation Events Shows a Lack of Strong Cytoplasmic Bias in Influencing Repeat Turnover

Genome-wide association study of leaf chemistry traits in tobacco

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