-
Nature Plants Jan 2023The genomes of cytoplasmic organelles (mitochondria and plastids) are maternally inherited in most eukaryotes, thus excluding organellar genomes from the benefits of...
The genomes of cytoplasmic organelles (mitochondria and plastids) are maternally inherited in most eukaryotes, thus excluding organellar genomes from the benefits of sexual reproduction and recombination. The mechanisms underlying maternal inheritance are largely unknown. Here we demonstrate that two independently acting mechanisms ensure maternal inheritance of the plastid (chloroplast) genome. Conducting large-scale genetic screens for paternal plastid transmission, we discovered that mild chilling stress during male gametogenesis leads to increased entry of paternal plastids into sperm cells and strongly increased paternal plastid transmission. We further show that the inheritance of paternal plastid genomes is controlled by the activity of a genome-degrading exonuclease during pollen maturation. Our data reveal that (1) maternal inheritance breaks down under specific environmental conditions, (2) an organelle exclusion mechanism and a genome degradation mechanism act in concert to prevent paternal transmission of plastid genes and (3) plastid inheritance is determined by complex gene-environment interactions.
Topics: Pollen; Seeds; Plastids; Mitochondria; Chloroplasts
PubMed: 36646831
DOI: 10.1038/s41477-022-01323-7 -
Annals of Botany Apr 2007The continuity of chloroplasts is maintained by division of pre-existing chloroplasts. Chloroplasts originated as bacterial endosymbionts; however, the majority of... (Review)
Review
BACKGROUND
The continuity of chloroplasts is maintained by division of pre-existing chloroplasts. Chloroplasts originated as bacterial endosymbionts; however, the majority of bacterial division factors are absent from chloroplasts and the eukaryotic host has added several new components. For example, the ftsZ gene has been duplicated and modified, and the Min system has retained MinE and MinD but lost MinC, acquiring at least one new component ARC3. Further, the mechanism has evolved to include two members of the dynamin protein family, ARC5 and FZL, and plastid-dividing (PD) rings were most probably added by the eukaryotic host.
SCOPE
Deciphering how the division of plastids is coordinated and controlled by nuclear-encoded factors is key to our understanding of this important biological process. Through a number of molecular-genetic and biochemical approaches, it is evident that FtsZ initiates plastid division where the coordinated action of MinD and MinE ensures correct FtsZ (Z)-ring placement. Although the classical FtsZ antagonist MinC does not exist in plants, ARC3 may fulfil this role. Together with other prokaryotic-derived proteins such as ARC6 and GC1 and key eukaryotic-derived proteins such as ARC5 and FZL, these proteins make up a sophisticated division machinery. The regulation of plastid division in a cellular context is largely unknown; however, recent microarray data shed light on this. Here the current understanding of the mechanism of chloroplast division in higher plants is reviewed with an emphasis on how recent findings are beginning to shape our understanding of the function and evolution of the components.
CONCLUSIONS
Extrapolation from the mechanism of bacterial cell division provides valuable clues as to how the chloroplast division process is achieved in plant cells. However, it is becoming increasingly clear that the highly regulated mechanism of plastid division within the host cell has led to the evolution of features unique to the plastid division process.
Topics: Arabidopsis Proteins; Biological Evolution; Cell Division; Chloroplasts; Escherichia coli; Models, Biological; Plant Proteins; Plastids
PubMed: 17138581
DOI: 10.1093/aob/mcl249 -
Protoplasma Oct 2012Plastid genetic engineering has come of age, becoming today an attractive alternative approach for the expression of foreign genes, as it offers several advantages over... (Review)
Review
Plastid genetic engineering has come of age, becoming today an attractive alternative approach for the expression of foreign genes, as it offers several advantages over nuclear transformants. Significant progress has been made in plastid genetic engineering in tobacco and other Solanaceae plants, through the use of improved regeneration procedures and transformation vectors with efficient promoters and untranslated regions. Many genes encoding for industrially important proteins and vaccines, as well as genes conferring important agronomic traits, have been stably integrated and expressed in the plastid genome. Despite these advances, it remains a challenge to achieve marked levels of plastid transgene expression in non-green tissues. In this review, we summarize the basic requirements of plastid genetic engineering and discuss the current status, limitations, and the potential of plastid transformation for expanding future studies relating to Solanaceae plants.
Topics: Genetic Engineering; Genetic Vectors; Plastids; Solanaceae
PubMed: 22395455
DOI: 10.1007/s00709-012-0391-9 -
Protoplasma Jul 2020
Topics: Evolution, Molecular; Humans; Plastids
PubMed: 32572583
DOI: 10.1007/s00709-020-01526-9 -
Annual Review of Plant Biology 2013Intracellular signaling from plastids to the nucleus, called retrograde signaling, coordinates the expression of nuclear and plastid genes and is essential for plastid... (Review)
Review
Intracellular signaling from plastids to the nucleus, called retrograde signaling, coordinates the expression of nuclear and plastid genes and is essential for plastid biogenesis and for maintaining plastid function at optimal levels. Recent identification of several components involved in plastid retrograde generation, transmission, and control of nuclear gene expression has provided significant insight into the regulatory network of plastid retrograde signaling. Here, we review the current knowledge of multiple plastid retrograde signaling pathways, which are derived from distinct sources, and of possible plastid signaling molecules. We describe the retrograde signaling-dependent regulation of nuclear gene expression, which involves multilayered transcriptional control, as well as the transcription factors involved. We also summarize recent advances in the identification of key components mediating signal transduction from plastids to the nucleus.
Topics: Cell Nucleus; Gene Expression Regulation, Plant; Plant Cells; Plants; Plastids; Signal Transduction; Transcription Factors
PubMed: 23394498
DOI: 10.1146/annurev-arplant-050312-120147 -
International Journal of Molecular... Mar 2021Plant prenyllipids, especially isoprenoid chromanols and quinols, are very efficient low-molecular-weight lipophilic antioxidants, protecting membranes and storage... (Review)
Review
Plant prenyllipids, especially isoprenoid chromanols and quinols, are very efficient low-molecular-weight lipophilic antioxidants, protecting membranes and storage lipids from reactive oxygen species (ROS). ROS are byproducts of aerobic metabolism that can damage cell components, they are also known to play a role in signaling. Plants are particularly prone to oxidative damage because oxygenic photosynthesis results in O formation in their green tissues. In addition, the photosynthetic electron transfer chain is an important source of ROS. Therefore, chloroplasts are the main site of ROS generation in plant cells during the light reactions of photosynthesis, and plastidic antioxidants are crucial to prevent oxidative stress, which occurs when plants are exposed to various types of stress factors, both biotic and abiotic. The increase in antioxidant content during stress acclimation is a common phenomenon. In the present review, we describe the mechanisms of ROS (singlet oxygen, superoxide, hydrogen peroxide and hydroxyl radical) production in chloroplasts in general and during exposure to abiotic stress factors, such as high light, low temperature, drought and salinity. We highlight the dual role of their presence: negative (i.e., lipid peroxidation, pigment and protein oxidation) and positive (i.e., contribution in redox-based physiological processes). Then we provide a summary of current knowledge concerning plastidic prenyllipid antioxidants belonging to isoprenoid chromanols and quinols, as well as their structure, occurrence, biosynthesis and function both in ROS detoxification and signaling.
Topics: Antioxidants; Chloroplasts; Chromans; Plastids; Quinones; Reactive Oxygen Species; Terpenes
PubMed: 33799456
DOI: 10.3390/ijms22062950 -
Biomolecules Jul 2019Plastid genome sequences are becoming more readily available with the increase in high-throughput sequencing, and whole-organelle genetic data is available for algae and... (Review)
Review
Plastid genome sequences are becoming more readily available with the increase in high-throughput sequencing, and whole-organelle genetic data is available for algae and plants from across the diversity of photosynthetic eukaryotes. This has provided incredible opportunities for studying species which may not be amenable to in vivo study or genetic manipulation or may not yet have been cultured. Research into plastid genomes has pushed the limits of what can be deduced from genomic information, and in particular genomic information obtained from public databases. In this Review, we discuss how research into plastid genomes has benefitted enormously from the explosion of publicly available genome sequence. We describe two case studies in how using publicly available gene data has supported previously held hypotheses about plastid traits from lineage-restricted experiments across algal and plant diversity. We propose how this approach could be used across disciplines for inferring functional and biological characteristics from genomic approaches, including integration of new computational and bioinformatic approaches such as machine learning. We argue that the techniques developed to gain the maximum possible insight from plastid genomes can be applied across the eukaryotic tree of life.
Topics: Big Data; Computational Biology; Evolution, Molecular; Genome Size; Genome, Plastid; Genomics; High-Throughput Nucleotide Sequencing; Machine Learning; Phylogeny; Plants; Plastids
PubMed: 31344945
DOI: 10.3390/biom9080299 -
Journal of Experimental Botany Nov 2016Plastid transformation has emerged as an alternative platform to generate transgenic plants. Attractive features of this technology include specific integration of... (Review)
Review
Plastid transformation has emerged as an alternative platform to generate transgenic plants. Attractive features of this technology include specific integration of transgenes-either individually or as operons-into the plastid genome through homologous recombination, the potential for high-level protein expression, and transgene containment because of the maternal inheritance of plastids. Several issues associated with nuclear transformation such as gene silencing, variable gene expression due to the Mendelian laws of inheritance, and epigenetic regulation have not been observed in the plastid genome. Plastid transformation has been successfully used for the production of therapeutics, vaccines, antigens, and commercial enzymes, and for engineering various agronomic traits including resistance to biotic and abiotic stresses. However, these demonstrations have usually focused on model systems such as tobacco, and the technology per se has not yet reached the market. Technical factors limiting this technology include the lack of efficient protocols for the transformation of cereals, poor transgene expression in non-green plastids, a limited number of selection markers, and the lengthy procedures required to recover fully segregated plants. This article discusses the technology of transforming the plastid genome, the positive and negative features compared with nuclear transformation, and the current challenges that need to be addressed for successful commercialization.
Topics: Genetic Engineering; Plants, Genetically Modified; Plastids; Transformation, Genetic
PubMed: 27697788
DOI: 10.1093/jxb/erw360 -
Plant & Cell Physiology May 2024Plastids are essential organelles in angiosperms and show non-Mendelian inheritance due to their evolution as endosymbionts. In approximately 80% of angiosperms,... (Review)
Review
Plastids are essential organelles in angiosperms and show non-Mendelian inheritance due to their evolution as endosymbionts. In approximately 80% of angiosperms, plastids are thought to be inherited from the maternal parent, whereas other species transmit plastids biparentally. Maternal inheritance can be generally explained by the stochastic segregation of maternal plastids after fertilization because the zygote is overwhelmed by the maternal cytoplasm. In contrast, biparental inheritance shows the transmission of organelles from both parents. In some species, maternal inheritance is not absolute and paternal leakage occurs at a very low frequency (∼10-5). A key process controlling the inheritance mode lies in the behavior of plastids during male gametophyte (pollen) development, with accumulating evidence indicating that the plastids themselves or their DNAs are eliminated during pollen maturation or at fertilization. Cytological observations in numerous angiosperm species have revealed several critical steps that mutually influence the degree of plastid transmission quantitatively among different species. This review revisits plastid inheritance from a mechanistic viewpoint. Particularly, we focus on a recent finding demonstrating that both low temperature and plastid DNA degradation mediated by the organelle exonuclease DEFECTIVE IN POLLEN ORGANELLE DNA DEGRADATION1 (DPD1) influence the degree of paternal leakage significantly in tobacco. Given these findings, we also highlight the emerging role of DPD1 in organelle DNA degradation.
Topics: Plastids; Magnoliopsida; DNA, Plant; Pollen; Organelles
PubMed: 37702423
DOI: 10.1093/pcp/pcad104 -
Plant Physiology Apr 2011
Review
Topics: Agriculture; Biotechnology; Chlamydomonas; Genetic Engineering; Genome, Chloroplast; Metabolic Networks and Pathways; Molecular Farming; Plants, Genetically Modified; Plastids; Recombinant Proteins; Transformation, Genetic; Transgenes
PubMed: 21239622
DOI: 10.1104/pp.110.170969