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Cell Oct 2023Gravity controls directional growth of plants, and the classical starch-statolith hypothesis proposed more than a century ago postulates that amyloplast sedimentation in...
Gravity controls directional growth of plants, and the classical starch-statolith hypothesis proposed more than a century ago postulates that amyloplast sedimentation in specialized cells initiates gravity sensing, but the molecular mechanism remains uncharacterized. The LAZY proteins are known as key regulators of gravitropism, and lazy mutants show striking gravitropic defects. Here, we report that gravistimulation by reorientation triggers mitogen-activated protein kinase (MAPK) signaling-mediated phosphorylation of Arabidopsis LAZY proteins basally polarized in root columella cells. Phosphorylation of LAZY increases its interaction with several translocons at the outer envelope membrane of chloroplasts (TOC) proteins on the surface of amyloplasts, facilitating enrichment of LAZY proteins on amyloplasts. Amyloplast sedimentation subsequently guides LAZY to relocate to the new lower side of the plasma membrane in columella cells, where LAZY induces asymmetrical auxin distribution and root differential growth. Together, this study provides a molecular interpretation for the starch-statolith hypothesis: the organelle-movement-triggered molecular polarity formation.
Topics: Arabidopsis; Arabidopsis Proteins; Gravity Sensing; Plant Roots; Plastids; Starch; Membrane Proteins
PubMed: 37741279
DOI: 10.1016/j.cell.2023.09.014 -
Science (New York, N.Y.) Apr 2024Symbiotic interactions were key to the evolution of chloroplast and mitochondria organelles, which mediate carbon and energy metabolism in eukaryotes. Biological...
Symbiotic interactions were key to the evolution of chloroplast and mitochondria organelles, which mediate carbon and energy metabolism in eukaryotes. Biological nitrogen fixation, the reduction of abundant atmospheric nitrogen gas (N) to biologically available ammonia, is a key metabolic process performed exclusively by prokaryotes. Atelocyanobacterium thalassa, or UCYN-A, is a metabolically streamlined N-fixing cyanobacterium previously reported to be an endosymbiont of a marine unicellular alga. Here we show that UCYN-A has been tightly integrated into algal cell architecture and organellar division and that it imports proteins encoded by the algal genome. These are characteristics of organelles and show that UCYN-A has evolved beyond endosymbiosis and functions as an early evolutionary stage N-fixing organelle, or "nitroplast."
Topics: Cyanobacteria; Haptophyta; Nitrogen; Nitrogen Fixation; Seawater; Symbiosis; Mitochondria; Chloroplasts
PubMed: 38603509
DOI: 10.1126/science.adk1075 -
Plant Communications Sep 2023Chloroplasts evolved from an ancient cyanobacterial endosymbiont more than 1.5 billion years ago. During subsequent coevolution with the nuclear genome, the chloroplast... (Review)
Review
Chloroplasts evolved from an ancient cyanobacterial endosymbiont more than 1.5 billion years ago. During subsequent coevolution with the nuclear genome, the chloroplast genome has remained independent, albeit strongly reduced, with its own transcriptional machinery and distinct features, such as chloroplast-specific innovations in gene expression and complicated post-transcriptional processing. Light activates the expression of chloroplast genes via mechanisms that optimize photosynthesis, minimize photodamage, and prioritize energy investments. Over the past few years, studies have moved from describing phases of chloroplast gene expression to exploring the underlying mechanisms. In this review, we focus on recent advances and emerging principles that govern chloroplast gene expression in land plants. We discuss engineering of pentatricopeptide repeat proteins and its biotechnological effects on chloroplast RNA research; new techniques for characterizing the molecular mechanisms of chloroplast gene expression; and important aspects of chloroplast gene expression for improving crop yield and stress tolerance. We also discuss biological and mechanistic questions that remain to be answered in the future.
Topics: Genes, Chloroplast; Chloroplasts; Photosynthesis
PubMed: 37147800
DOI: 10.1016/j.xplc.2023.100611 -
The EMBO Journal Jul 2023Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the...
Chloroplasts are plant organelles responsible for photosynthesis and environmental sensing. Most chloroplast proteins are imported from the cytosol through the translocon at the outer envelope membrane of chloroplasts (TOC). Previous work has shown that TOC components are regulated by the ubiquitin-proteasome system (UPS) to control the chloroplast proteome, which is crucial for the organelle's function and plant development. Here, we demonstrate that the TOC apparatus is also subject to K63-linked polyubiquitination and regulation by selective autophagy, potentially promoting plant stress tolerance. We identify NBR1 as a selective autophagy adaptor targeting TOC components, and mediating their relocation into vacuoles for autophagic degradation. Such selective autophagy is shown to control TOC protein levels and chloroplast protein import and to influence photosynthetic activity as well as tolerance to UV-B irradiation and heat stress in Arabidopsis plants. These findings uncover the vital role of selective autophagy in the proteolytic regulation of specific chloroplast proteins, and how dynamic control of chloroplast protein import is critically important for plants to cope with challenging environments.
Topics: Chloroplasts; Plants; Organelles; Protein Transport; Chloroplast Proteins; Arabidopsis; Autophagy; Plant Proteins; Arabidopsis Proteins; Carrier Proteins
PubMed: 37248861
DOI: 10.15252/embj.2022112534 -
Cell Aug 2023Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition,...
Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition, function, and spatial organization remains limited. Here, we determined the localizations of 1,034 candidate chloroplast proteins using fluorescent protein tagging in the model alga Chlamydomonas reinhardtii. The localizations provide insights into the functions of poorly characterized proteins; identify novel components of nucleoids, plastoglobules, and the pyrenoid; and reveal widespread protein targeting to multiple compartments. We discovered and further characterized cellular organizational features, including eleven chloroplast punctate structures, cytosolic crescent structures, and unexpected spatial distributions of enzymes within the chloroplast. We also used machine learning to predict the localizations of other nuclear-encoded Chlamydomonas proteins. The strains and localization atlas developed here will serve as a resource to accelerate studies of chloroplast architecture and functions.
Topics: Biosynthetic Pathways; Chlamydomonas reinhardtii; Chloroplast Proteins; Chloroplasts; Photosynthesis
PubMed: 37437571
DOI: 10.1016/j.cell.2023.06.008 -
Protoplasma Jan 2024
Topics: Plastids
PubMed: 38102506
DOI: 10.1007/s00709-023-01913-y -
Science (New York, N.Y.) Sep 2023Organisms have evolved under gravitational force, and many sense the direction of gravity by means of statoliths in specialized cells. In flowering plants,...
Organisms have evolved under gravitational force, and many sense the direction of gravity by means of statoliths in specialized cells. In flowering plants, starch-accumulating plastids, known as amyloplasts, act as statoliths to facilitate downstream gravitropism. The gravity-sensing mechanism has long been considered a mechanosensing process by which amyloplasts transmit forces to intracellular structures, but the molecular mechanism underlying this has not been elucidated. We show here that LAZY1-LIKE (LZY) family proteins involved in statocyte gravity signaling associate with amyloplasts and the proximal plasma membrane. This results in polar localization according to the direction of gravity. We propose a gravity-sensing mechanism by which LZY translocation to the plasma membrane signals the direction of gravity by transmitting information on the position of amyloplasts.
Topics: Humans; Cell Membrane; Cell Polarity; Gravitation; Gravitropism; Gravity Sensing; Plastids; Protein Transport; Arabidopsis Proteins; Arabidopsis
PubMed: 37561884
DOI: 10.1126/science.adh9978 -
Photosynthesis Research Sep 2023I provide here both my personal and scientific autobiography. After giving a background and summary of most of my research, I present information on my parents, my...
I provide here both my personal and scientific autobiography. After giving a background and summary of most of my research, I present information on my parents, my childhood, schooling, university education, and postdoctoral research, all in Australia. This is followed by a presentation of my life and research in Cambridge, UK and then at the Commonwealth Scientific and Industrial Research Organisation (CSIRO), in Australia, since 1955, where most of my research was done, especially on photosynthesis which included the following areas: Purification of a protochlorophyllide-protein complex; separation of the photochemical systems of photosynthesis; development of photochemical activity in photosynthesis; protein synthesis in plants; comparative photosynthesis of sun and shade plants; role of chlorophyll b in photosynthesis; photochemical properties of C4 plants; molecular interaction of thylakoid membranes; electron transport and ATP formation; and solar energy conversion in photosynthesis. In addition to research on the basics and applications of photosynthesis, I also mention at the end my service as a member of the executive of CSIRO.
Topics: Humans; Child; Photosynthesis; Chlorophyll; Electron Transport; Thylakoids; Sunlight; Plants
PubMed: 37155083
DOI: 10.1007/s11120-023-01021-1 -
Plant & Cell Physiology May 2024
Topics: Mitochondria; Plastids; Plants
PubMed: 38590035
DOI: 10.1093/pcp/pcae036 -
Plant & Cell Physiology May 2024The formation of chloroplasts can be traced back to an ancient event in which a eukaryotic host cell containing mitochondria ingested a cyanobacterium. Since then,... (Review)
Review
The formation of chloroplasts can be traced back to an ancient event in which a eukaryotic host cell containing mitochondria ingested a cyanobacterium. Since then, chloroplasts have retained many characteristics of their bacterial ancestor, including their transcription and translation machinery. In this review, recent research on the maturation of rRNA and ribosome assembly in chloroplasts is explored, along with their crucial role in plant survival and their implications for plant acclimation to changing environments. A comparison is made between the ribosome composition and auxiliary factors of ancient and modern chloroplasts, providing insights into the evolution of ribosome assembly factors. Although the chloroplast contains ancient proteins with conserved functions in ribosome assembly, newly evolved factors have also emerged to help plants acclimate to changes in their environment and internal signals. Overall, this review offers a comprehensive analysis of the molecular mechanisms underlying chloroplast ribosome assembly and highlights the importance of this process in plant survival, acclimation and adaptation.
Topics: Ribosomes; Chloroplasts; RNA, Ribosomal; Plants
PubMed: 37498958
DOI: 10.1093/pcp/pcad082