Iron economy in Chlamydomonas reinhardtii

Glaesener, Anne G.; Merchant, Sabeeha; Blaby‐Haas, Crysten E.

doi:10.3389/fpls.2013.00337

Cited by 74 publications

(55 citation statements)

References 85 publications

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“…These transporters belong to a mix of protein families with origins in various lineages and unique phylogenetic occurrences (Figure 2). For instance, Fe uptake at the plasma membrane occurs by a reduction-oxidation-transport mechanism, involving FRE1 (Fe reductase), FOX1 (Fe oxidase) and FTR1 (permease) [15–19], which is found in other algae, such as rhodophytes and diatoms [20], but absent from most land plants and prasinophytes [21,22] (Figure 2A). Additional components of high-affinity Fe uptake include the soluble secreted proteins FEA1 and FEA2, which are only found in the algal lineages [17,23,24].…”

Section: Border Controlmentioning

confidence: 99%

Regulating cellular trace metal economy in algae

Blaby‐Haas

Merchant

2017

Current Opinion in Plant Biology

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As indispensable protein cofactors, Fe, Mn, Cu and Zn are at the center of multifaceted acclimation mechanisms that have evolved to ensure extracellular supply meets intracellular demand. Starting with selective transport at the plasma membrane and ending in protein metalation, metal homeostasis in algae involves regulated trafficking of metal ions across membranes, intracellular compartmentalization by proteins and organelles, and metal-sparing/recycling mechanisms to optimize metal-use efficiency. Overlaid on these processes are additional circuits that respond to the metabolic state as well as to the prior metal status of the cell. In this review, we focus on recent progress made toward understanding the pathways by which the single-celled, green alga Chlamydomonas reinhardtii controls its cellular trace metal economy. We also compare these mechanisms to characterized and putative processes in other algal lineages. Photosynthetic microbes continue to provide insight into cellular regulation and handling of Cu, Fe, Zn and Mn as a function of the nutritional supply and cellular demand for metal cofactors. New experimental tools such as RNA-Seq and subcellular metal imaging are bringing us closer to a molecular understanding of acclimation to supply dynamics in algae and beyond.

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Section: Border Controlmentioning

confidence: 99%

Regulating cellular trace metal economy in algae

Blaby‐Haas

Merchant

2017

Current Opinion in Plant Biology

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“…Metal toxicity has been associated with ROS production and oxidative stress signaling in plants and algae (28)(29)(30)(31)(32), but it remains unknown whether the cellular response to metals in these organisms may include the activation of autophagy. Chlamydomonas has been widely used to investigate metal metabolism and the cellular response to metal excess and metal-limiting conditions (28,33,34), and the development of genome-wide technologies has increased our current understanding about metal signaling in this alga. In this study, we show that high concentrations of nickel, cobalt, or copper trigger autophagy in Chlamydomonas.…”

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Activation of Autophagy by Metals in Chlamydomonas reinhardtii

et al. 2015

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Autophagy is an intracellular self-degradation pathway by which eukaryotic cells recycle their own material in response to specific stress conditions. Exposure to high concentrations of metals causes cell damage, although the effect of metal stress on autophagy has not been explored in photosynthetic organisms. In this study, we investigated the effect of metal excess on autophagy in the model unicellular green alga Chlamydomonas reinhardtii. We show in cells treated with nickel an upregulation of ATG8 that is independent of CRR1, a global regulator of copper signaling in Chlamydomonas. A similar effect on ATG8 was observed with copper and cobalt but not with cadmium or mercury ions. Transcriptome sequencing data revealed an increase in the abundance of the protein degradation machinery, including that responsible for autophagy, and a substantial overlap of that increased abundance with the hydrogen peroxide response in cells treated with nickel ions. Thus, our results indicate that metal stress triggers autophagy in Chlamydomonas and suggest that excess nickel may cause oxidative damage, which in turn activates degradative pathways, including autophagy, to clear impaired components and recover cellular homeostasis. Eukaryotic cells are able to degrade and recycle their own material when they are exposed to nutrient starvation or other adverse conditions through a catabolic pathway known as macroautophagy or autophagy. This process is characterized by the formation of double-membrane vesicles termed autophagosomes that engulf and deliver cytosolic components to the vacuole/lysosome for degradation (1-4). The primary function of autophagy is to recycle cytoplasmic material as well as to clear damaged organelles or toxic cellular components generated during stress in order to maintain cellular homeostasis. In higher eukaryotes, autophagy has also been implicated in cell differentiation, development and cell death, and several human pathologies, such as cancer and neurodegenerative diseases (5, 6).Autophagy is mediated by highly conserved autophagy-related (ATG) genes, which have been described in organisms ranging from yeasts to mammals. Some ATG proteins are required for the formation of the autophagosome and constitute the core autophagy machinery (4,7,8). This group of proteins includes the ATG8 and ATG12 ubiquitin-like systems required for vesicle expansion. The ATG8 protein has been widely used to monitor autophagy in many systems (9) because, unlike other ATG proteins, this protein firmly binds to the autophagosome membrane through a covalent bond to phosphatidylethanolamine (PE). Most of the core ATG proteins are conserved in land plants (10-12) and in evolutionarily distant algae, including freshwater species, such as the model green alga Chlamydomonas reinhardtii (herein referred to as Chlamydomonas) (13) and marine species (14). Our current knowledge about autophagy in algae is still limited compared to our knowledge about autophagy in other eukaryotes, but recent studies, mainly performed in Chlamydomon...

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“…C. reinhardtii is an important reference organism for diverse eukaryotic cellular and metabolic processes, including photosynthetic biology (Rochaix, 2001), flagellar function and biogenesis (Silflow and Lefebvre, 2001), nutrient homeostasis (Grossman, 2000;Merchant et al, 2006;Glaesener et al, 2013), and sexual cycles (Goodenough et al, 2007). The nuclear and chloroplast genomes of C. reinhardtii have been fully sequenced, enabling genomic and epigenomic analyses (Maul et al, 2002;Merchant et al, 2007).…”

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Dynamic changes in the transcriptome and methylome of Chlamydomonas reinhardtii throughout its life cycle

et al. 2015

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; 0000-0001-9355-9564 (M.P.).The green alga Chlamydomonas reinhardtii undergoes gametogenesis and mating upon nitrogen starvation. While the steps involved in its sexual reproductive cycle have been extensively characterized, the genome-wide transcriptional and epigenetic changes underlying different life cycle stages have yet to be fully described. Here, we performed transcriptome and methylome sequencing to quantify expression and DNA methylation from vegetative and gametic cells of each mating type and from zygotes. We identified 361 gametic genes with mating type-specific expression patterns and 627 genes that are specifically induced in zygotes; furthermore, these sex-related gene sets were enriched for secretory pathway and alga-specific genes. We also examined the C. reinhardtii nuclear methylation map with base-level resolution at different life cycle stages. Despite having low global levels of nuclear methylation, we detected 23 hypermethylated loci in gene-poor, repeat-rich regions. We observed mating type-specific differences in chloroplast DNA methylation levels in plus versus minus mating type gametes followed by chloroplast DNA hypermethylation in zygotes. Lastly, we examined the expression of candidate DNA methyltransferases and found three, DMT1a, DMT1b, and DMT4, that are differentially expressed during the life cycle and are candidate DNA methylases. The expression and methylation data we present provide insight into cell type-specific transcriptional and epigenetic programs during key stages of the C. reinhardtii life cycle.Chlamydomonas reinhardtii is a unicellular, biflagellate species of green alga found primarily in fresh water and soil (Harris et al., 2009). C. reinhardtii is an important reference organism for diverse eukaryotic cellular and metabolic processes, including photosynthetic biology (Rochaix, 2001), flagellar function and biogenesis (Silflow and Lefebvre, 2001), nutrient homeostasis (Grossman, 2000;Merchant et al., 2006;Glaesener et al., 2013), and sexual cycles (Goodenough et al., 2007). The nuclear and chloroplast genomes of C. reinhardtii have been fully sequenced, enabling genomic and epigenomic analyses (Maul et al., 2002;Merchant et al., 2007). The approximately 112-Mb haploid C. reinhardtii nuclear genome comprises 17 chromosomes. The circular chloroplast DNA (cpDNA) genome is 203 kb and present in 80 to 100 copies per cell that are organized into eight to 10 nucleoprotein complexes called nucleoids, which are distributed through the stroma.Like many unicellular eukaryotes, C. reinhardtii has a biphasic life cycle where haploid cells can reproduce vegetatively by mitotic division or, alternatively, undergo a sexual cycle. Vegetative cells can propagate indefinitely when provided with nutrients and light. Upon nitrogen starvation, however, cells stop dividing and differentiate into gametes whose mating type (plus or minus) is determined genetically by an approximately 300-kb mating type locus on chromosome 6, with two haplotypes, MT+ and MT2 (Umen, 2011; De Hoff et al.,...

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Iron economy in Chlamydomonas reinhardtii

Cited by 74 publications

References 85 publications

Regulating cellular trace metal economy in algae

Regulating cellular trace metal economy in algae

Activation of Autophagy by Metals in Chlamydomonas reinhardtii

Dynamic changes in the transcriptome and methylome of Chlamydomonas reinhardtii throughout its life cycle

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