Dataset Information

A high maternal genome excess causes severe seed abortion leading to ovary abscission in Nicotiana interploidy-interspecific crosses.

ABSTRACT: Seed abortion and ovary abscission, two types of postzygotic reproductive barriers, are often observed in interspecific and/or interploidy crosses in plants. However, the mechanisms underlying these reproductive barriers remain unclear. Here, we show that the distinct types of seed developmental abnormalities (type I and type II seed abortion) occur in a phased manner as maternal to paternal genome dosage increases and that type II seed abortion is followed by ovary abscission. We revealed that these two types of seed developmental abnormalities are observed during seed development in the interploidy-interspecific crosses of Nicotiana suaveolens and N. tabacum. Moreover, in the cross showing type II seed abortion, several events, such as changes in abscission-related gene expression and lignin deposition, occurred in the ovary abscission zone, eventually leading to ovary abscission. Notably, successive increases in maternal ploidy using ploidy manipulated lines resulted in successive type I and type II seed abortions, and the latter was accompanied by ovary abscission. Conversely, both types of seed abortion and ovary abscission could be overcome with a ploidy manipulation technique that balances parental ploidy levels. We thus concluded that a high maternal genome excess cross may cause severe seed developmental defects and ovary abscission. Based on our findings, we propose a model explaining the abortion phenomena, where an interaction between the promotive and inhibitive effects of the parental genomes determines the developmental destiny of seeds. Significance statement:We demonstrate that a stepwise increase in maternal ploidy results in a stepwise increase in seed abortion severity, leading to ovary abscission in plants. We propose a model explaining the abortion phenomena, where an interaction between the promotive and inhibitive effects of the parental genomes determines the developmental destiny of seeds.

SUBMITTER: He H

PROVIDER: S-EPMC7430375 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

A high maternal genome excess causes severe seed abortion leading to ovary abscission in <i>Nicotiana</i> interploidy-interspecific crosses.

He Hai H Yokoi Shuji S Tezuka Takahiro T

Plant direct 20200817 8

Seed abortion and ovary abscission, two types of postzygotic reproductive barriers, are often observed in interspecific and/or interploidy crosses in plants. However, the mechanisms underlying these reproductive barriers remain unclear. Here, we show that the distinct types of seed developmental abnormalities (type I and type II seed abortion) occur in a phased manner as maternal to paternal genome dosage increases and that type II seed abortion is followed by ovary abscission. We revealed that ...[more]

PMID: 32821875

Similar Datasets

Project description:BackgroundAbscission is an active, organized, and highly coordinated cell separation process enabling the detachment of aerial organs through the modification of cell-to-cell adhesion and breakdown of cell walls at specific sites on the plant body known as abscission zones. In Arabidopsis thaliana, abscission of floral organs and cauline leaves is regulated by the interaction of the hormonal peptide INFLORESCENCE DEFICIENT IN ABSCISSION (IDA), a pair of redundant receptor-like protein kinases, HAESA (HAE) and HAESA-LIKE2 (HSL2), and SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE (SERK) co-receptors. However, the functionality of this abscission signaling module has not yet been demonstrated in other plant species.ResultsThe expression of the pair of NbenIDA1 homeologs and the receptor NbenHAE.1 was supressed at the base of the corolla tube by the inoculation of two virus-induced gene silencing (VIGS) constructs in Nicotiana benthamiana. These gene suppression events arrested corolla abscission but did not produce any obvious effect on plant growth. VIGS plants retained a higher number of corollas attached to the flowers than control plants, an observation related to a greater corolla breakstrength. The arrest of corolla abscission was associated with the preservation of the parenchyma tissue at the base of the corolla tube that, in contrast, was virtually collapsed in normal corollas. In contrast, the inoculation of a viral vector construct that increased the expression of NbenIDA1A at the base of the corolla tube negatively affected the growth of the inoculated plants accelerating the timing of both corolla senescence and abscission. However, the heterologous ectopic overexpression of citrus CitIDA3 and Arabidopsis AtIDA in N. benthamiana did not alter the standard plant phenotype suggesting that the proteolytic processing machinery was unable to yield active peptides.ConclusionHere, we demonstrate that the pair of NbenIDA1 homeologs encoding small peptides of the IDA-like family and the receptor NbenHAE.1 control cellular breakdown at the base of the corolla tube awhere an adventitious AZ should be formed and, therefore, corolla abscission in N. benthamiana flowers. Altogether, our results provide the first evidence supporting the notion that the IDA-HAE/HSL2 signaling module is conserved in angiosperms.

Project description:BACKGROUND:IDA (INFLORESCENCE DEFICIENT IN ABSCISSION)-like signaling peptides and the associated HAE (HAESA)-like family of receptor kinases were originally reported in the model plant Arabidopsis thaliana (Arabidopsis) to be deeply involved in the regulation of abscission. Actually, IDA peptides, as cell-to-cell communication elements, appear to be implicated in many developmental processes that rely on cell separation events, and even in the responses to abiotic stresses. However, the knowledge related to the molecular machinery regulating abscission in economically important crops is scarce. In this work, we determined the conservation and phylogeny of the IDA-like and HAE-like gene families in relevant species of the Solanaceae family and analyzed the expression of these genes in the allopolyploid Nicotiana benthamiana, in order to identify members involved in abscission, stem growth and in the response to drought conditions. RESULTS:The phylogenetic relationships among the IDA-like members of the Solanaceae studied, grouped the two pairs of NbenIDA1 and NbenIDA2 protein homeologs with the Arabidopsis prepropeptides related to abscission. Analysis of promoter regions searching for regulatory elements showed that these two pairs of homeologs contained both hormonal and drought response elements, although NbenIDA2A lacked the hormonal regulatory elements. Expression analyses showed that the pair of NbenIDA1 homeologs were upregulated during corolla abscission. NbenIDA1 and NbenIDA2 pairs showed tissue differential expression under water stress conditions, since NbenIDA1 homeologs were highly expressed in stressed leaves while NbenIDA2 homeologs, especially NbenIDA2B, were highly expressed in stressed roots. In non-stressed active growing plants, nodes and internodes were the tissues with the highest expression levels of all members of the IDA-like family and their putative HAE-like receptors. CONCLUSION:Our results suggest that the pair of NbenIDA1 homeologs are involved in the natural process of corolla abscission while both pairs of NbenIDA1 and NbenIDA2 homeologs are implicated in the response to water stress. The data also suggest that IDA peptides may be important during stem growth and development. These results provide additional evidence that the functional module formed by IDA peptides and its receptor kinases, as defined in Arabidopsis, may also be conserved in Solanaceae.

Dataset Information

A high maternal genome excess causes severe seed abortion leading to ovary abscission in Nicotiana interploidy-interspecific crosses.

Publications

A high maternal genome excess causes severe seed abortion leading to ovary abscission in <i>Nicotiana</i> interploidy-interspecific crosses.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets