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Analysis of the possible cytogenetic mechanism for overcoming hybrid lethality in an interspecific cross between Nicotiana suaveolens and Nicotiana tabacum.

ABSTRACT: Hybrid lethality is a type of reproductive isolation in which hybrids die before maturation, due to the interaction between the two causative genes derived from each of the hybrid parents. The interspecific hybrid of Nicotiana suaveolens × Nicotiana tabacum is a model plant used in studies on hybrid lethality. While most of the progeny produced from such a cross die, some individuals grow normally and mature. Separately, a technique for producing mature hybrids by artificial culture has been developed. However, the mechanism by which hybrids overcome lethality, either spontaneously or by artificial culture, remains unclear. In the present study, we found that some hybrids that overcome lethality, either spontaneously or by artificial culture, lack the distal part of the Q chromosome, a region that includes the gene responsible for lethality. Quantitative polymerase chain reaction results suggested that the distal deletion of the Q chromosome, detected in some hybrid seedlings that overcome lethality, is caused by reciprocal translocations between homoeologous chromosomes. The results showed that chromosomal instability during meiosis in amphidiploid N. tabacum as well as during artificial culturing of hybrid seedlings is involved in overcoming hybrid lethality in interspecific crosses of the genus Nicotiana.

SUBMITTER: Nakata K

PROVIDER: S-EPMC8035154 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Analysis of the possible cytogenetic mechanism for overcoming hybrid lethality in an interspecific cross between Nicotiana suaveolens and Nicotiana tabacum.

Nakata Kouki K Nagashima Hiroki H Inaba Natsuki N Yamashita Haruka H Shinozaki Yoshihito Y Kanekatsu Motoki M Marubashi Wataru W Yamada Tetsuya T

Scientific reports 20210409 1

Hybrid lethality is a type of reproductive isolation in which hybrids die before maturation, due to the interaction between the two causative genes derived from each of the hybrid parents. The interspecific hybrid of Nicotiana suaveolens × Nicotiana tabacum is a model plant used in studies on hybrid lethality. While most of the progeny produced from such a cross die, some individuals grow normally and mature. Separately, a technique for producing mature hybrids by artificial culture has been dev ...[more]

PMID: 33837225

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Project description:IntroductionMature seeds deteriorate gradually and die eventually during long-term storage. Controlled deterioration is often used to accelerate the seed deterioration rate to assess the seed vigor and physiological quality of seed lots.ObjectivesAlthough it is well known that the process of seed deterioration produced by controlled deterioration is distinct from that caused by long-term storage, the differences in transcriptional levels have not been reported. Clarifying the mechanism of seed deterioration is critical for identifying, conserving and utilizing germplasm resources.MethodsTobacco (Nicotiana tabacum L.) seeds were studied thoroughly using transcriptome, small RNA, and degradome sequencing after long-term storage (LS) and controlled deterioration (CD). Co-expression trend analysis identified transcripts involved in tobacco seed deterioration, while phylogenetic analysis helped to uncover comparable targets in rice (Oryza sativa L.) for further verification and utilization.ResultsIn LS and CD, a total of 2,112 genes and 164 miRNAs were differentially expressed, including 20 interaction miRNA-mRNA pairs with contrasting expression. Transcriptional multiomics found that the main causes of LS were plant hormone signal transduction and protein processing in the endoplasmic reticulum, whereas the primary cause of CD was nucleotide excision repair dysfunction. The homeostatic balance of RNA degradation and the spliceosome occurred in both modes of seed deterioration. Additionally, co-expression trend analysis identified two coherent pairs, nta-miR160b-NtARF18 and nta-miR396c-NtMBD10, as being significant in LS and CD, respectively. For utilization, rice homologous targets OsARF18 and OsMBD707 were verified to play similar roles in LS and CD, respectively.ConclusionThis study demonstrated the transcriptional mechanism of tobacco and key genes in seed deterioration. And the application of key genes in rice also verified the feasibility of the multiomics method, guiding the identification of candidate genes to precisely delay seed deterioration in other species of seed research.

Project description:Pollen, an extremely reduced bicellular or tricellular male reproductive structure of flowering plants, serves as a model for numerous studies covering wide range of developmental and physiological processes. The pollen development represents a fragile and vital phase of plant ontogenesis and pollen was among the first singular plant tissues thoroughly characterized at the transcriptomic level (Honys and Twell [5]). Arabidopsis pollen developmental transcriptome has been published over a decade ago (Honys and Twell, 2004) and transcriptomes of developing pollen of other species have followed (Rice, Deveshwar et al. [2]; Triticeae, Tran et al. [11]; upland cotton, Ma et al. [8]). However, the transcriptomic data describing the development of tobacco pollen, a bicellular model for cell biology studies, have been missing. Here we provide the transcriptomic data covering three stages (Tupý et al., 1983) of wild type tobacco (Nicotiana tabacum, cv. Samsun) pollen development: uninucleate microspores (UNM, stage 1), early bicellular pollen (eBCP, stage 3) and late bicellular pollen (lBCP, stage 5) as a supplement to the mature pollen (MP), 4 h-pollen tube (PT4), 24 h-pollen tubes (PT24), leaf (LF) and root (RT) transcriptomic data presented in our previous studies (Hafidh et al., 2012a; Hafidh et al., 2012b). We characterized these transcriptomes to refine the knowledge base of male gametophyte-enriched genes as well as genes expressed preferentially at the individual stages of pollen development. Alongside updating the list of tissue-specific genes, we have investigated differentially expressed genes with respect to early expressed genes. Pollen tube growth and competition of pollen tubes in female pistil can be viewed as a race of the fittest. Accordingly, there is an apparent evolutionary trend among higher plants to store significant material reserves and nutrients during pollen maturation. This supply ensures that after pollen germination, the pollen tube utilizes its resource predominantly for its rapid elongation in the female pistil. Previous transcriptomic data from Arabidopsis showed massive expression of genes encoding proteins forming both ribosomal subunits that were accumulated in developing pollen, whereas their expression was not detectable in growing pollen tubes (Honys and Twell, 2004). We observed a similar phenomenon in less advanced bicellular tobacco pollen. Here, we describe in detail how we obtained and analyzed validated microarray dataset deposited in Gene Expression Omnibus (GSE62349).

Dataset Information

Analysis of the possible cytogenetic mechanism for overcoming hybrid lethality in an interspecific cross between Nicotiana suaveolens and Nicotiana tabacum.

Publications

Analysis of the possible cytogenetic mechanism for overcoming hybrid lethality in an interspecific cross between Nicotiana suaveolens and Nicotiana tabacum.

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