Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L.

Zhou, Xuhong; Mo, Xijun; Gui, Min; Wu, Xiaosheng; Ya-lian, Jiang; Ma, Li-na; Shi, Ziming; Luo, Ying; Tang, Wenru

doi:10.1016/j.plaphy.2015.10.003

Cited by 18 publications

(21 citation statements)

References 41 publications

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“…The species appears to have originated somewhere in central Eurasia in conjunction with the last glacial maximum, and subsequently migrated to Fennoscandinavia. A possibility is that hybridization was facilitated by the production of an unusually high frequency of unreduced A. thaliana ovules in a population containing both parental species, perhaps as a result of environmental stress (Madlung 2013; Vanneste, Maere, et al 2014; Mason and Pires 2015; Zhou et al 2015). The transition to self-fertilization may have been facilitated by the dominance of the non-functional S-allele from A. thaliana over the S-allele from A. arenosa , followed by inactivation of the latter.…”

Section: Resultsmentioning

confidence: 99%

Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica

et al. 2017

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Polyploidy is an example of instantaneous speciation when it involves the formation of a new cytotype that is incompatible with the parental species. Because new polyploid individuals are likely to be rare, establishment of a new species is unlikely unless polyploids are able to reproduce through self-fertilization (selfing), or asexually. Conversely, selfing (or asexuality) makes it possible for polyploid species to originate from a single individual—a bona fide speciation event. The extent to which this happens is not known. Here, we consider the origin of Arabidopsis suecica, a selfing allopolyploid between Arabidopsis thaliana and Arabidopsis arenosa, which has hitherto been considered to be an example of a unique origin. Based on whole-genome re-sequencing of 15 natural A. suecica accessions, we identify ubiquitous shared polymorphism with the parental species, and hence conclusively reject a unique origin in favor of multiple founding individuals. We further estimate that the species originated after the last glacial maximum in Eastern Europe or central Eurasia (rather than Sweden, as the name might suggest). Finally, annotation of the self-incompatibility loci in A. suecica revealed that both loci carry non-functional alleles. The locus inherited from the selfing A. thaliana is fixed for an ancestral non-functional allele, whereas the locus inherited from the outcrossing A. arenosa is fixed for a novel loss-of-function allele. Furthermore, the allele inherited from A. thaliana is predicted to transcriptionally silence the allele inherited from A. arenosa, suggesting that loss of self-incompatibility may have been instantaneous.

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Section: Resultsmentioning

confidence: 99%

Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica

et al. 2017

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“…The experiments were carried out in four diploid carnation (2n = 30) cultivars: Promesa, Guernse Yellow, Nogalte, and YunhongErhao, which displayed high pollen viability. The frequency of dyad production in 'Nogalte' in June 2013 was 3.3%, and the frequency of 2n pollen was 1.63% (Zhou et al, 2015). The percentage of 2n pollen in 'Promesa', 'Guernse Yellow', and 'YunhongErhao' was 0.06%, 3.09%, and 1.72%, respectively (Zhou et al, 2015).…”

Section: Methodsmentioning

confidence: 96%

“…It is a member of the Caryophyllaceae. Most carnation cultivars can produce 2n gametes, and the frequency of 2n pollen produced ranged from 0% to 4.17% (Zhou et al, 2012(Zhou et al, , 2015. Spindle abnormalities during metaphase II have been considered to be the major cytological mechanism involved in the formation of 2n pollen in carnation (Zhou et al, 2015).…”

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confidence: 99%

“…Most carnation cultivars can produce 2n gametes, and the frequency of 2n pollen produced ranged from 0% to 4.17% (Zhou et al, 2012(Zhou et al, , 2015. Spindle abnormalities during metaphase II have been considered to be the major cytological mechanism involved in the formation of 2n pollen in carnation (Zhou et al, 2015). In this study, we describe another abnormality mechanism and found some cells were normal in the first meiotic division; however, a failure occurred in the second meiotic division, which generated dyads during microsporogenesis.…”

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confidence: 99%

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Cloning and Expression of Omission of Second Division-like Genes from Carnation

Zhou¹,

Mo²,

Ya-lian³

et al. 2017

J. Amer. Soc. Hort. Sci.

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The omission of second division gene (OSD1) gene plays a fundamental role in meiosis and is associated with 2n gamete formation in Arabidopsis thaliana. The objective of this work was to unravel the mechanisms leading to 2n pollen production, and isolate and analyze the expression patterns of OSD-like (OSDL) genes in carnation (Dianthus caryophyllus). We found an absence of the second meiotic division caused the formation of 2n pollen. Three homoeologous genes were cloned and labeled as OSDLa, OSDLb, and OSDLc in a diploid carnation. The cDNAs were 1180 bp for OSDLa, 1288 bp for OSDLb, and 971 bp for OSDLc. A strong similarity was found between the amino sequences of OSDLb and OSDLc. An evident feature of OSDLs proteins is the presence of D-box and MR-tail domains; however, the GxEN/KEN-box domain, which is distinct among the other plant proteins was absent. Quantitative real time polymerase chain reaction (qRT-PCR) analysis showed that OSDL genes maintain continuous expression in buds and other tissues. OSDLa has the highest expression in buds of 1.1–1.2 cm long (stage 2), and OSDLb has a high level of expression in buds of 0.9–1.0 cm long (stage 1) and stage 2 buds and ovary tissues in three carnation cultivars. The expression level of OSDLc was highest in ovaries. These expression patterns strongly suggest that OSDLs in carnation involve male meiosis and ovary development. These findings can have potential applications in fundamental polyploidization research and plant breeding programs in carnation.

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“…Besides being induced by genetic defects, meiotic restitution and alterations in the consistency of the gametophytic ploidy may also result from environmental stresses, such as heat and cold (Pécrix et al, 2011;De Storme et al, 2012;De Storme and Mason, 2014;Zhou et al, 2015). Although progress has been made in understanding the cellular mechanisms and genetic factors involved in 2n gamete formation, the molecular factors and signaling pathways involved remain largely unknown.…”

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confidence: 99%

Gibberellin Induces Diploid Pollen Formation by Interfering with Meiotic Cytokinesis

2016

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The plant hormone gibberellic acid (GA) controls many physiological processes, including cell differentiation, cell elongation, seed germination, and response to abiotic stress. In this study, we report that exogenous treatment of flowering Arabidopsis (Arabidopsis thaliana) plants with GA specifically affects the process of male meiotic cytokinesis leading to meiotic restitution and the production of diploid (2n) pollen grains. Similar defects in meiotic cell division and reproductive ploidy stability occur in Arabidopsis plants depleted of RGA and GAI, two members of the DELLA family that function as suppressor of GA signaling. Cytological analysis of the double rga-24 gai-t6 mutant revealed that defects in male meiotic cytokinesis are not caused by alterations in meiosis I (MI or meiosis II (MII) chromosome dynamics, but instead result from aberrations in the spatial organization of the phragmoplast-like radial microtubule arrays (RMAs) at the end of meiosis II. In line with a role for GA in the genetic regulation of the male reproductive system, we additionally show that DELLA downstream targets MYB33 and MYB65 are redundantly required for functional RMA biosynthesis and male meiotic cytokinesis. By analyzing the expression of pRGA::GFP-RGA in the wild-type Landsberg erecta background, we demonstrate that the GFP-RGA protein is specifically expressed in the anther cell layers surrounding the meiocytes and microspores, suggesting that appropriate GA signaling in the somatic anther tissue is critical for male meiotic cell wall formation and thus plays an important role in consolidating the male gametophytic ploidy consistency.

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Cytological, molecular mechanisms and temperature stress regulating production of diploid male gametes in Dianthus caryophyllus L.

Cited by 18 publications

References 41 publications

Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica

Genome sequencing reveals the origin of the allotetraploid Arabidopsis suecica

Cloning and Expression of Omission of Second Division-like Genes from Carnation

Gibberellin Induces Diploid Pollen Formation by Interfering with Meiotic Cytokinesis

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