Transcription Factor–Dependent Chromatin Remodeling at Heat Shock and Copper-Responsive Promoters in <i>Chlamydomonas reinhardtii</i>

Strenkert, Daniela; Schmollinger, Stefan; Sommer, Frederik; Schulz-Raffelt, Miriam; Schroda, Michael

doi:10.1105/tpc.111.085266

Cited by 68 publications

(85 citation statements)

References 72 publications

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“…It has been shown recently that the effect of CRR1 on transcription of CYC6, CPX1, and CRD1 is mediated by an opening of the chromatin structure of the respective promoter regions (Strenkert et al, 2011). Due to the constitutively open chromatin state of the CRD1 promoter under noninducing conditions, the authors suggested that an additional unknown factor is probably involved in CRD1 gene expression (Strenkert et al, 2011).…”

Section: Activation Of Hyda1 Expression Requires Additional Regulatormentioning

confidence: 99%

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Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1

et al. 2012

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The unicellular green alga Chlamydomonas reinhardtii adapts to anaerobic or hypoxic conditions by developing a complex fermentative metabolism including the production of molecular hydrogen by [FeFe]-hydrogenase isoform1 (HYDA1). HYDA1 transcript and hydrogenase protein accumulate in the absence of oxygen or copper (Cu). Factors regulating this differential gene expression have been unknown so far. In this study, we report on the isolation of a Chlamydomonas mutant strain impaired in HYDA1 gene expression by screening an insertional mutagenesis library for HYDA1 promoter activity using the arylsulfatase-encoding ARYLSULFATASE2 gene as a selection marker. The mutant strain has a deletion of the COPPER RESPONSE REGULATOR1 (CRR1) gene encoding for CRR1, indicating that this SQUAMOSA-PROMOTER BINDING PROTEIN (SBP) domain transcription factor is involved in the regulation of HYDA1 transcription. Treating the C. reinhardtii wild type with mercuric ions, which were shown to inhibit the binding of the SBP domain to DNA, prevented or deactivated HYDA1 gene expression. Reporter gene analyses of the HYDA1 promoter revealed that two GTAC motifs, which are known to be the cores of CRR1 binding sites, are necessary for full promoter activity in hypoxic conditions or upon Cu starvation. However, mutations of the GTAC sites had a much stronger impact on reporter gene expression in Cu-deficient cells. Electrophoretic mobility shift assays showed that the CRR1 SBP domain binds to one of the GTAC cores in vitro. These combined results prove that CRR1 is involved in HYDA1 promoter activation.

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Section: Activation Of Hyda1 Expression Requires Additional Regulatormentioning

confidence: 99%

“…Due to the constitutively open chromatin state of the CRD1 promoter under noninducing conditions, the authors suggested that an additional unknown factor is probably involved in CRD1 gene expression (Strenkert et al, 2011).…”

Section: Activation Of Hyda1 Expression Requires Additional Regulatormentioning

confidence: 99%

Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1

et al. 2012

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“…In plants and yeast, the histone variant H2A.Z is possibly a determinant in gene regulation associated with temperature responsiveness (Kumar and Wigge, 2010). In the green alga Chlamydomonas reinhardtii, HS-activated HSF1 is also involved in chromatin remodeling (Strenkert et al, 2011). Mechanisms of gene regulation affected by HS are more complicated by including the translational control.…”

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confidence: 99%

Genome-Wide Analysis of Heat-Sensitive Alternative Splicing in Physcomitrella patens

2014

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Plant growth and development are constantly influenced by temperature fluctuations. To respond to temperature changes, different levels of gene regulation are modulated in the cell. Alternative splicing (AS) is a widespread mechanism increasing transcriptome complexity and proteome diversity. Although genome-wide studies have revealed complex AS patterns in plants, whether AS impacts the stress defense of plants is not known. We used heat shock (HS) treatments at nondamaging temperature and messenger RNA sequencing to obtain HS transcriptomes in the moss Physcomitrella patens. Data analysis identified a significant number of novel AS events in the moss protonema. Nearly 50% of genes are alternatively spliced. Intron retention (IR) is markedly repressed under elevated temperature but alternative donor/acceptor site and exon skipping are mainly induced, indicating differential regulation of AS in response to heat stress. Transcripts undergoing heat-sensitive IR are mostly involved in specific functions, which suggests that plants regulate AS with transcript specificity under elevated temperature. An exonic GAG-repeat motif in these IR regions may function as a regulatory cis-element in heat-mediated AS regulation. A conserved AS pattern for HS transcription factors in P. patens and Arabidopsis (Arabidopsis thaliana) reveals that heat regulation for AS evolved early during land colonization of green plants. Our results support that AS of specific genes, including key HS regulators, is fine-tuned under elevated temperature to modulate gene regulation and reorganize metabolic processes.Global warming in recent decades has caused annual temperature extremes that are becoming harmful for all living organisms. Although all living cells show rapid responses to changes of ambient temperature, unlike animals, plants are sessile and cannot escape adverse temperature conditions. Challenged by temperature changes, plants have evolved rapid and complex systems to sense the temperature signal and translate it into cellular defenses for acquired tolerance, such as enhancing protein folding/unfolding activities and maintaining membrane fluidity (Sung et al., 2003). Understanding how plants adapt to temperature stresses has been an important topic in improving thermotolerance in crops.The heat shock response (HSR) is conserved in eukaryotes in response to elevated temperature and induces the activity of heat shock transcription factors (HSFs) to promote the expression of HSR-related genes. Different mechanisms for temperature sensing and signal transduction have been proposed. The general model suggests that constitutively expressed chaperones in the cytoplasm form inactive complexes with HSFs. Upon heat shock (HS), cytosolic chaperones are recruited by misfolded proteins, thus allowing the release of HSFs for phosphorylation, oligomerization, and nuclear localization to regulate gene expression (Mosser et al

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“…qRT-PCR was performed using the StepOnePlus RT-PCR system (Applied Biosystems) and the Maxima SYBR Green kit from Fermentas as described previously (Strenkert et al, 2011). Primers for LHCSR3.1 were the same as described by Peers et al (2009).…”

Section: Rna Extraction and Qrt-pcrmentioning

confidence: 99%

TEF30 Interacts with Photosystem II Monomers and Is Involved in the Repair of Photodamaged Photosystem II in Chlamydomonas reinhardtii

et al. 2015

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The remarkable capability of photosystem II (PSII) to oxidize water comes along with its vulnerability to oxidative damage. Accordingly, organisms harboring PSII have developed strategies to protect PSII from oxidative damage and to repair damaged PSII. Here, we report on the characterization of the THYLAKOID ENRICHED FRACTION30 (TEF30) protein in Chlamydomonas reinhardtii, which is conserved in the green lineage and induced by high light. Fractionation studies revealed that TEF30 is associated with the stromal side of thylakoid membranes. By using blue native/Deriphat-polyacrylamide gel electrophoresis, sucrose density gradients, and isolated PSII particles, we found TEF30 to quantitatively interact with monomeric PSII complexes. Electron microscopy images revealed significantly reduced thylakoid membrane stacking in TEF30-underexpressing cells when compared with control cells. Biophysical and immunological data point to an impaired PSII repair cycle in TEF30-underexpressing cells and a reduced ability to form PSII supercomplexes after high-light exposure. Taken together, our data suggest potential roles for TEF30 in facilitating the incorporation of a new D1 protein and/or the reintegration of CP43 into repaired PSII monomers, protecting repaired PSII monomers from undergoing repeated repair cycles or facilitating the migration of repaired PSII monomers back to stacked regions for supercomplex reassembly.Oxygenic photosynthesis is essential for almost all life on Earth, as it provides the reduced carbon and the oxygen required for respiration. A key enzyme in oxygenic photosynthesis is PSII, which catalyzes the light-driven oxidation of water. The core of PSII in algae and land plants contains D1 (PsbA), D2 (PsbD), CP43 (PsbC), CP47 (PsbB), the a-subunit (PsbE) and b-subunit (PsbF) of cytochrome b 559 , as well as several intrinsic low-molecular-mass subunits. The core monomer is associated with the extrinsic oxygen-evolving complex (OEC) consisting of OEE1 (PSBO), OEE2 (PSBP), and OEE3 (PSBQ), which stabilize the inorganic Mn 4 O 5 Ca cluster required for water oxidation (for review, see Pagliano et al., 2013). PSII core monomers assemble into dimers to which, at both sides, lightharvesting proteins (LHCII) bind to form PSII supercomplexes. In land plants, each PSII dimer binds two each of the monomeric minor LHCII proteins CP24, CP26, and CP29 in addition to up to four major LHCII trimers (Caffarri et al., 2009;Kou ril et al., 2011). Biochemical evidence suggests that, in the thylakoid membrane, up to eight LHCII trimers can be present per PSII core dimer, presumably because of the existence of a pool of extra LHCII (Kou ril et al., 2013). In Chlamydomonas reinhardtii, lacking CP24, each PSII dimer binds two each of the CP26 and CP29 monomers as well as up to six major LHCII trimers (Tokutsu et al., 2012). The reaction center proteins D1 and D2 bind all the redox-active cofactors required for PSII electron transport (Umena et al., 2011). Light captured by the internal antenna proteins CP43 and CP47 and the o...

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Transcription Factor–Dependent Chromatin Remodeling at Heat Shock and Copper-Responsive Promoters in Chlamydomonas reinhardtii

Cited by 68 publications

References 72 publications

Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1

Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1

Genome-Wide Analysis of Heat-Sensitive Alternative Splicing in Physcomitrella patens

TEF30 Interacts with Photosystem II Monomers and Is Involved in the Repair of Photodamaged Photosystem II in Chlamydomonas reinhardtii

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