Characterization of Schizosaccharomyces pombe Copper Transporter Proteins in Meiotic and Sporulating Cells

Plante, Samuel; Ioannoni, Raphaël; Beaudoin, Jude; Labbé, Simon

doi:10.1074/jbc.m113.543678

Cited by 11 publications

(36 citation statements)

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“…Based on the fact that meiosis requires copper to successfully undertake and complete its differentiation program, expression and localization of the Ctr4 and Ctr5 proteins have been investigated in meiotic and sporulating cells (21,22). When the cells switch from mitosis to meiosis, expression and localization profiles of Ctr4 and Ctr5 show that the two proteins are still synchronously co-expressed and co-localized at the cell surface of zygotes but only during the early steps of the meiotic program (22). After meiotic divisions, the transcript levels of ctr4 ϩ and ctr5 ϩ are extinguished with the concomitant disappearance of their encoded proteins.…”

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Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Plante

Normant

Ramos-Torres

et al. 2017

Journal of Biological Chemistry

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During fungal spore germination, a resting spore returns to a conventional mode of cell division and resumes vegetative growth, but the requirements for spore germination are incompletely understood. Here, we show that copper is essential for spore germination in Germinating spores develop a single germ tube that emerges from the outer spore wall in a process called outgrowth. Under low-copper conditions, the copper transporters Ctr4 and Ctr5 are maximally expressed at the onset of outgrowth. In the case of Ctr6, its expression is broader, taking place before and during outgrowth. Spores lacking Ctr4, Ctr5, and the copper sensor Cuf1 exhibit complete germination arrest at outgrowth. In contrast, deletion only partially interferes with formation of outgrowing spores. At outgrowth, Ctr4-GFP and Ctr5-Cherry first co-localize at the spore contour, followed by re-location to a middle peripheral spore region. Subsequently, they move away from the spore body to occupy the periphery of the nascent cell. After breaking of spore dormancy, Ctr6 localizes to the vacuole membranes that are enriched in the spore body relative to the germ tube. Using a copper-binding tracker, results showed that labile copper is preferentially localized to the spore body. Further analysis showed that Ctr4 and Ctr6 are required for copper-dependent activation of the superoxide dismutase 1 (SOD1) during spore germination. This activation is critical because the loss of SOD1 activity blocked spore germination at outgrowth. Taken together, these results indicate that cell-surface copper transporters and SOD1 are required for completion of the spore germination program.

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“…Ctr6 is an integral membrane protein that assembles as a homotrimer (23). A deletion of the ctr6 ϩ gene (ctr6⌬) results in a reduction of SOD1 activity (22,23). Similarly, inactivation of ctr4 ϩ (ctr4⌬) also causes a decrease of SOD1 activity but to a greater extent.…”

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confidence: 99%

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Plante

Normant

Ramos-Torres

et al. 2017

Journal of Biological Chemistry

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“…2). In the absence of Cuf1 (cuf1⌬), ctr4 ϩ mRNA was not detected because its expression is dependent of Cuf1 (28,42). Together, the results revealed that cum1 ϩ transcripts are found exclusively during meiosis.…”

Section: Cum1mentioning

confidence: 50%

“…To eliminate cum1 ϩ sense transcripts in vegetative cells, the mechanism of antisense-mediated transcriptional repression should be efficient, especially under low copper conditions. In this situation, cum1 ϩ mRNA levels are induced by Cuf1, which is active during both mitotic and meiotic cell division programs (28,42). One possibility is that the long iss1 ϩ antisense tran- ϩ , iss1 ϩ -PAS, and cum1 ϩ alleles.…”

Section: Discussion Cum1mentioning

confidence: 99%

An Antisense RNA-mediated Mechanism Eliminates a Meiosis-specific Copper-regulated Transcript in Mitotic Cells

Normant

Beaudoin

Labbé

2015

Journal of Biological Chemistry

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“…In turn, the GX3G motif is essential to the trimeric assembly of Ctr proteins in yeast Aller et al, 2004). Both motifs are thought to play a role in the Cu 2+ uptake and assembly of the functional heterotrimeric Ctr4/Ctr5 in yeast Aller et al, 2004;Ioannoni et al, 2010;Beaudoin et al, 2011;Plante et al, 2014). With the exception of ScCTR3, all Ctr family members are rich in methionine residues within their hydrophilic N-terminal tails .…”

Section: The Copper Transporter Family In Plantsmentioning

confidence: 99%

Analysis of Membrane Transporter Systems Expressed During Symbiotic Nitrogen Fixation in the Model Legume Medicago Truncatula

Wyman¹

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As the second largest crop family, legumes provide a significant component to the human diet as well as livestock nutrition through forage species. Unique from most other plants groups, legumes are able to form a symbiosis with naturally occurring soil rhizobia, diazotrophs, which are able to reduce atmospheric nitrogen to usable forms of nitrogen for the plant. In return for providing reduced nitrogen, differentiated rhizobia are sustained by dicarboxylates, branched chain amino acids, and other nutrients from the plant. In order for the movement of nutrients to be translocated between symbionts and from the cytosol to cell organelles, other cells, and plant tissues, membrane transporters must be present to move substrates across lipid bilayers. Secondary transporters supply the necessary amino acids and additional nutrients to and from the nitrogen fixation zone of nodules to support symbiotic nitrogen fixation. While the biosynthesis pathways of amino acids to feed symbiosis is well understood, the involved transporters, including importers and exporters, of amino acids, as well as transporters of other nutrients to support infected cells are largely unknown and relatively few transporters have been functionally characterized in legumes. In order to assess potential amino acid transporters, I performed a genomic inventory of putative transporters belonging to the Amino Acid Polyamine-Organocation superfamily by compiling a list of transporters classified under the superfamily in the Transporter Classification Database, along with their protein size, transmembrane domains (TMDs), and compared them to characterized members of transporter families to determine confidence of functionality. I also compiled expression data to determine expression patterns to manually annotate candidate nodule specific transporters of interest for further study. Using the model species Medicago truncatula to study symbiotic nitrogen fixation, I genetically characterized the nodule specific membrane transporter, MtAPC1 through in silico analysis of expression patterns, followed by transcriptional analysis of inoculation with rhizobial mutants to determine essential steps of infection necessary for gene expression. Transcriptional activity of MtAPC1 was also fine-tuned to identify cell-type within the nodule and the impact of the MtAPC1 knockdown in nodule development during symbiotic nitrogen fixation. I also characterized expression patterns of a copper transporter, MtCOPT1, regarding its transcriptional activity in nodules and its capability of importing copper into the cell cytosol. In addition, I preliminarily analyzed of two putative nodule-specific transporters, MtSEN1 and MtOPT1 for iron and short oligopeptides (3-8 amino acids in length) though in silico analysis with publicly available datasets, as well as determined expression patterns by RT-qPCR of nodulating root inoculated with rhizobial mutants and wild-type rhizobia. v

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Characterization of Schizosaccharomyces pombe Copper Transporter Proteins in Meiotic and Sporulating Cells

Cited by 11 publications

References 50 publications

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

Cell-surface copper transporters and superoxide dismutase 1 are essential for outgrowth during fungal spore germination

An Antisense RNA-mediated Mechanism Eliminates a Meiosis-specific Copper-regulated Transcript in Mitotic Cells

Analysis of Membrane Transporter Systems Expressed During Symbiotic Nitrogen Fixation in the Model Legume Medicago Truncatula

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