Distribution of plastids and mitochondria during male gametophyte formation in  Tinantia erecta  (Jacq.) Fenzl

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Abstract

During meiosis in microsporogenesis, autonomous cellular organelles, i.e., plastids and mitochondria, move and separate into daughter cells according to a specific pattern. This process called chondriokinesis is characteristic for a given plant species. The key criterion for classification of the chondriokinesis types was the arrangement of cell organelles during two meiosis phases: metaphase I and telophase I. The autonomous organelles participate in cytoplasmic inheritance; therefore, their precise distribution to daughter cells determines formation of identical viable microspores. In this study, the course of chondriokinesis during the development of the male gametophyte in Tinantia erecta was analyzed. The study was conducted using optical and transmission electron microscopes. During microsporogenesis in T. erecta, autonomous cell organelles moved in a manner defined as a neutral-equatorial type of chondriokinesis. Therefore, metaphase I plastids and mitochondria were evenly dispersed around the metaphase plate and formed an equatorial plate between the daughter nuclei in early telophase I. Changes in the ultrastructure of plastids and mitochondria during pollen microsporogenesis were also observed.

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Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions.

Christine D. Chase (2007)

Mitochondrial function depends on the coordinate action of nuclear and mitochondrial genomes. The genetic dissection of these interactions presents special challenges in obligate aerobes, because the viability of these organisms depends on mitochondrial respiration. The plant trait cytoplasmic male sterility (CMS) is determined by the mitochondrial genome and is associated with a pollen sterility phenotype that can be suppressed or counteracted by nuclear genes known as restorer-of-fertility genes. Here, I review the nature and the origin of the genes that determine CMS, together with recent investigations that have exploited CMS to provide new insights into plant mitochondrial-nuclear communication. These studies have implicated mitochondrial signaling pathways, including those involved in regulating cell death and nuclear gene expression, in the elaboration of CMS. The molecular cloning of nuclear genes that restore fertility (i.e. restorer-of-fertility genes) has identified genes encoding pentatricopeptide-repeat proteins as key regulators of plant mitochondrial gene expression.

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Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing.

Zhonghua Wang, Yanjiao Zou, Xiaoyu Li … (2006)

Cytoplasmic male sterility (CMS) and nucleus-controlled fertility restoration are widespread plant reproductive features that provide useful tools to exploit heterosis in crops. However, the molecular mechanism underlying this kind of cytoplasmic-nuclear interaction remains unclear. Here, we show in rice (Oryza sativa) with Boro II cytoplasm that an abnormal mitochondrial open reading frame, orf79, is cotranscribed with a duplicated atp6 (B-atp6) gene and encodes a cytotoxic peptide. Expression of orf79 in CMS lines and transgenic rice plants caused gametophytic male sterility. Immunoblot analysis showed that the ORF79 protein accumulates specifically in microspores. Two fertility restorer genes, Rf1a and Rf1b, were identified at the classical locus Rf-1 as members of a multigene cluster that encode pentatricopeptide repeat proteins. RF1A and RF1B are both targeted to mitochondria and can restore male fertility by blocking ORF79 production via endonucleolytic cleavage (RF1A) or degradation (RF1B) of dicistronic B-atp6/orf79 mRNA. In the presence of both restorers, RF1A was epistatic over RF1B in the mRNA processing. We have also shown that RF1A plays an additional role in promoting the editing of atp6 mRNAs, independent of its cleavage function.

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Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species.

Sodmergen, Yang Liu, Zu-Quan Zhang (2003)

Mature pollen grains of 295 angiosperm species were screened by epifluorescence microscopy for a marker that denotes the mode of cytoplasmic inheritance. We used the DNA fluorochrome DAPI (4',6-diamidino-2-phenylindole) for pollen cell staining. The presence or absence of fluorescence of cytoplasmic DNA in the generative cell or sperm cells was examined in each species. The species examined represented 254 genera and 98 families, and 40 of these families had not been previously studied in this regard. The cytoplasmic DNA of the generative cell or sperm cells did not fluoresce in 81% of the species examined, from 83% of the genera and 87% of the families examined, indicating the potential for maternal cytoplasmic inheritance in these species. In contrast, the male reproductive cells of 19% of the species, from 17% of the genera and 26% of the families examined, displayed fluorescence of the cytoplasmic DNA, indicating the potential for biparental cytoplasmic inheritance in these species. The results revealed the potential for biparental cytoplasmic inheritance in several species in which the inheritance mode was previously unknown, including plants in the Bignoniaceae, Cornaceae, Cruciferae (Brassicaceae), Cyperaceae, Dipsacaceae, Hydrocharitaceae, Papaveraceae, Portulacaceae, Tiliaceae, Valerianaceae, and Zingiberaceae. Electron microscopy revealed that the sperm cells of Portulaca grandiflora contain both plastid and mitochondrial DNA. However, in the generative cells of Musella lasiocarpa, the mitochondria contain DNA, but the plastids do not. These data provide a foundation for further studies of cytoplasmic inheritance in angiosperms.

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Author and article information

Contributors

Krystyna Winiarczyk: + 48 81 537 50 37 , krystyna.winiarczyk@umcs.pl

Journal

Journal ID (nlm-ta): Protoplasma

Journal ID (iso-abbrev): Protoplasma

Title: Protoplasma

Publisher: Springer Vienna (Vienna )

ISSN (Print): 0033-183X

ISSN (Electronic): 1615-6102

Publication date (Electronic): 9 March 2019

Publication date PMC-release: 9 March 2019

Publication date (Print): 2019

Volume: 256

Issue: 4

Pages: 1051-1063

Affiliations

[1 ]ISNI 0000 0004 1937 1303, GRID grid.29328.32, Department of Plant Anatomy and Cytology, , Maria Curie-Skłodowska University, ; Akademicka 19, 20-033 Lublin, Poland

[2 ]ISNI 0000 0001 0664 8391, GRID grid.37179.3b, Confocal and Electron Microscopy Laboratory, Centre for Interdisciplinary Research, , John Paul II Catholic University of Lublin, ; Al. Kraśnicka 102, 20-718 Lublin, Poland

Author notes

Handling Editor: Benedikt Kost

Article

Publisher ID: 1363

DOI: 10.1007/s00709-019-01363-5

PMC ID: 6579867

PubMed ID: 30852672

SO-VID: 9443aef8-c0ad-4331-8220-25cff9289bc5

License:

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 15 November 2018

Date accepted : 20 February 2019

Funding

Funded by: Maria Curie-Sklodowska University in Lublin

Custom metadata

ScienceOpen disciplines: Molecular biology

Keywords: microsporogenesis,microgametogenesis,chondriokinesis,plastids,mitochondria,tinantia erecta

Data availability:

ScienceOpen disciplines: Molecular biology

Keywords: microsporogenesis, microgametogenesis, chondriokinesis, plastids, mitochondria, tinantia erecta

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Distribution of plastids and mitochondria during male gametophyte formation in Tinantia erecta (Jacq.) Fenzl

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Abstract

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Higher order chromatin architecture

Most cited references 83

Cytoplasmic male sterility: a window to the world of plant mitochondrial-nuclear interactions.

Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing.

Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species.

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