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Molecular Plant Jun 2019Mitochondria and plastids form dynamic, evolving populations physically embedded in the fluctuating environment of the plant cell. Their evolutionary heritage has shaped... (Review)
Review
Mitochondria and plastids form dynamic, evolving populations physically embedded in the fluctuating environment of the plant cell. Their evolutionary heritage has shaped how the cell controls the genetic structure and the physical behavior of its organelle populations. While the specific genes involved in these processes are gradually being revealed, the governing principles underlying this controlled behavior remain poorly understood. As the genetic and physical dynamics of these organelles are central to bioenergetic performance and plant physiology, this challenges both fundamental biology and strategies to engineer better-performing plants. This article reviews current knowledge of the physical and genetic behavior of mitochondria and chloroplasts in plant cells. An overarching hypothesis is proposed whereby organelles face a tension between genetic robustness and individual control and responsiveness, and different species resolve this tension in different ways. As plants are immobile and thus subject to fluctuating environments, their organelles are proposed to favor individual responsiveness, sacrificing genetic robustness. Several notable features of plant organelles, including large genomes, mtDNA recombination, fragmented organelles, and plastid/mitochondrial differences may potentially be explained by this hypothesis. Finally, the ways that quantitative and systems biology can help shed light on the plethora of open questions in this field are highlighted.
Topics: Cell Nucleus; Chloroplasts; Mitochondria; Organelles; Plant Cells; Plastids
PubMed: 30445187
DOI: 10.1016/j.molp.2018.11.002 -
Current Opinion in Microbiology Aug 1999The discovery of a plastid in Plasmodium, Toxoplasma and related protozoan parasites provides a satisfying resolution to several long-standing mysteries: the mechanism... (Review)
Review
The discovery of a plastid in Plasmodium, Toxoplasma and related protozoan parasites provides a satisfying resolution to several long-standing mysteries: the mechanism of action for various surprisingly effective antibiotics; the subcellular location of an enigmatic 35 kb episomal DNA; and the nature of an unusual intracellular structure containing multiple membranes. The apicomplexan plastid highlights the importance of lateral genetic transfer in evolution and provides an accessible system for the investigation of protein targeting to secondary endosymbiotic organelles. Combining molecular genetic identification of targeting signals with whole genome analysis promises to yield a complete picture of organellar metabolic pathways and new targets for drug design.
Topics: Animals; Apicomplexa; Biological Evolution; Biological Transport; Plastids; Protozoan Proteins
PubMed: 10458993
DOI: 10.1016/S1369-5274(99)80075-7 -
BMC Biology Feb 2014A study in BMC Evolutionary Biology represents the most comprehensive effort to clarify the phylogeny of green plants using sequences from the plastid genome. This study...
A study in BMC Evolutionary Biology represents the most comprehensive effort to clarify the phylogeny of green plants using sequences from the plastid genome. This study highlights the strengths and limitations of plastome data for resolving the green plant phylogeny, and points toward an exciting future for plant phylogenetics, during which the vast and largely untapped territory of nuclear genomes will be explored.
Topics: Chlorophyta; Genome, Plastid; Magnoliopsida; Plastids; Viridiplantae
PubMed: 24533863
DOI: 10.1186/1741-7007-12-11 -
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 -
Plant Signaling & Behavior Feb 2013Plastid retrograde signaling (chloroplast to nucleus) has been proposed to play an important role in the acclimation of plant function to environmental stress. Although... (Review)
Review
Plastid retrograde signaling (chloroplast to nucleus) has been proposed to play an important role in the acclimation of plant function to environmental stress. Although several pathways and molecular components, as well as some signals, have been identified in recent years, our understanding of the communication between plastid and nucleus under stress remains fragmentary. This mini-review summarizes the properties of currently proposed candidate signals, chief molecular components, and their roles in the plastid retrograde signaling network in a variety of stress responses. We provide special emphasis on the recently characterized AMOS1/EGY1-dependent plastid retrograde signaling pathways engaged during ammonium stress.
Topics: Ammonium Compounds; Gene Expression Regulation, Plant; Plant Proteins; Plastids; Signal Transduction
PubMed: 23299427
DOI: 10.4161/psb.23107 -
Philosophical Transactions of the Royal... Mar 2010Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the... (Review)
Review
Plastids and mitochondria each arose from a single endosymbiotic event and share many similarities in how they were reduced and integrated with their host. However, the subsequent evolution of the two organelles could hardly be more different: mitochondria are a stable fixture of eukaryotic cells that are neither lost nor shuffled between lineages, whereas plastid evolution has been a complex mix of movement, loss and replacement. Molecular data from the past decade have substantially untangled this complex history, and we now know that plastids are derived from a single endosymbiotic event in the ancestor of glaucophytes, red algae and green algae (including plants). The plastids of both red algae and green algae were subsequently transferred to other lineages by secondary endosymbiosis. Green algal plastids were taken up by euglenids and chlorarachniophytes, as well as one small group of dinoflagellates. Red algae appear to have been taken up only once, giving rise to a diverse group called chromalveolates. Additional layers of complexity come from plastid loss, which has happened at least once and probably many times, and replacement. Plastid loss is difficult to prove, and cryptic, non-photosynthetic plastids are being found in many non-photosynthetic lineages. In other cases, photosynthetic lineages are now understood to have evolved from ancestors with a plastid of different origin, so an ancestral plastid has been replaced with a new one. Such replacement has taken place in several dinoflagellates (by tertiary endosymbiosis with other chromalveolates or serial secondary endosymbiosis with a green alga), and apparently also in two rhizarian lineages: chlorarachniophytes and Paulinella (which appear to have evolved from chromalveolate ancestors). The many twists and turns of plastid evolution each represent major evolutionary transitions, and each offers a glimpse into how genomes evolve and how cells integrate through gene transfers and protein trafficking.
Topics: Biological Evolution; Chlorophyta; Dinoflagellida; Eukaryota; Gene Transfer, Horizontal; Mitochondria; Models, Biological; Phylogeny; Plastids; Rhodophyta; Symbiosis
PubMed: 20124341
DOI: 10.1098/rstb.2009.0103 -
Proceedings of the National Academy of... Mar 2022SignificanceAlthough plastid division is critical for plant development, how components of the plastid division machinery (PDM) are imported into plastids remains...
SignificanceAlthough plastid division is critical for plant development, how components of the plastid division machinery (PDM) are imported into plastids remains unexplored. A forward genetic screen to identify suppressors of a () mutant deficient in plastid division led us to find dominant gain-of-function (GF) mutations in , which significantly increases the import of PDM components and completely rescues phenotypes. The defective plastid division phenotypes in and mutants and CRL-TIC236 association in a functional complex indicate that the CRL-TIC236 module is vital for plastid division. Hence, we report the first GF translocon mutants and unveil CRL as a novel functional partner of TIC236 for PDM import.
Topics: Arabidopsis; Arabidopsis Proteins; Cell Division; Chloroplast Proteins; Gain of Function Mutation; Membrane Transport Proteins; Plastids; Protein Transport
PubMed: 35275795
DOI: 10.1073/pnas.2123353119 -
Cell Reports Aug 2020Plastid-nucleus genome coordination is crucial for plastid activity, but the mechanisms remain unclear. By treating Arabidopsis plants with the organellar...
Plastid-nucleus genome coordination is crucial for plastid activity, but the mechanisms remain unclear. By treating Arabidopsis plants with the organellar genome-damaging agent ciprofloxacin, we found that plastid genome instability can alter endoreplication and the cell cycle. Similar results are observed in the plastid genome instability mutants of reca1why1why3. Cell division and embryo development are disturbed in the reca1why1why3 mutant. Notably, SMR5 and SMR7 genes, which encode cell-cycle kinase inhibitors, are upregulated in plastid genome instability plants, and the mutation of SMR7 can restore the endoreplication and growth phenotype of reca1why1why3 plants. Furthermore, we establish that the DNA damage response transcription factor SOG1 mediates the alteration of endoreplication and cell cycle triggered by plastid genome instability. Finally, we demonstrate that reactive oxygen species produced in plastids are important for plastid-nucleus genome coordination. Our findings uncover a molecular mechanism for the coordination of plastid and nuclear genomes during plant growth and development.
Topics: Arabidopsis; Arabidopsis Proteins; Cell Cycle; Cell Cycle Proteins; Cell Nucleus; Endoreduplication; Gene Expression Regulation, Plant; Genome, Plant; Genome, Plastid; Genomic Instability; Plant Development; Plastids; Reactive Oxygen Species; Signal Transduction; Transcription Factors
PubMed: 32783941
DOI: 10.1016/j.celrep.2020.108019 -
Proceedings of the National Academy of... Aug 2015Apicomplexans are a major lineage of parasites, including causative agents of malaria and toxoplasmosis. How such highly adapted parasites evolved from free-living...
Apicomplexans are a major lineage of parasites, including causative agents of malaria and toxoplasmosis. How such highly adapted parasites evolved from free-living ancestors is poorly understood, particularly because they contain nonphotosynthetic plastids with which they have a complex metabolic dependency. Here, we examine the origin of apicomplexan parasitism by resolving the evolutionary distribution of several key characteristics in their closest free-living relatives, photosynthetic chromerids and predatory colpodellids. Using environmental sequence data, we describe the diversity of these apicomplexan-related lineages and select five species that represent this diversity for transcriptome sequencing. Phylogenomic analysis recovered a monophyletic lineage of chromerids and colpodellids as the sister group to apicomplexans, and a complex distribution of retention versus loss for photosynthesis, plastid genomes, and plastid organelles. Reconstructing the evolution of all plastid and cytosolic metabolic pathways related to apicomplexan plastid function revealed an ancient dependency on plastid isoprenoid biosynthesis, predating the divergence of apicomplexan and dinoflagellates. Similarly, plastid genome retention is strongly linked to the retention of two genes in the plastid genome, sufB and clpC, altogether suggesting a relatively simple model for plastid retention and loss. Lastly, we examine the broader distribution of a suite of molecular characteristics previously linked to the origins of apicomplexan parasitism and find that virtually all are present in their free-living relatives. The emergence of parasitism may not be driven by acquisition of novel components, but rather by loss and modification of the existing, conserved traits.
Topics: Animals; Apicomplexa; Apicoplasts; Base Sequence; Bayes Theorem; Cell Lineage; Computational Biology; Cytosol; DNA, Ribosomal; Genes, Bacterial; Genome; Likelihood Functions; Metabolic Networks and Pathways; Molecular Sequence Data; Parasites; Photosynthesis; Phylogeny; Plastids
PubMed: 25717057
DOI: 10.1073/pnas.1423790112 -
Current Biology : CB Jan 2009A comprehensive understanding of the origin and spread of plastids remains an important yet elusive goal in the field of eukaryotic evolution. Combined with the... (Review)
Review
A comprehensive understanding of the origin and spread of plastids remains an important yet elusive goal in the field of eukaryotic evolution. Combined with the discovery of new photosynthetic and non-photosynthetic protist lineages, the results of recent taxonomically broad phylogenomic studies suggest that a re-shuffling of higher-level eukaryote systematics is in order. Consequently, new models of plastid evolution involving ancient secondary and tertiary endosymbioses are needed to explain the full spectrum of photosynthetic eukaryotes.
Topics: Animals; Biological Evolution; Cyanobacteria; Eukaryotic Cells; Gene Transfer, Horizontal; Photosynthesis; Phylogeny; Plastids; Symbiosis
PubMed: 19174147
DOI: 10.1016/j.cub.2008.11.067