AtC3H18L is a stop-codon read-through gene and encodes a novel non-tandem CCCH zinc-finger protein that can form cytoplasmic foci similar to mRNP granules

Xu, Liai; Liu, Tingting; Xiong, Xingpeng; Liu, Weimiao; Yu, Youjian; Cao, Jiashu

doi:10.1016/j.bbrc.2020.05.081

Cited by 9 publications

(14 citation statements)

References 29 publications

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“…Moreover, the co-localization of Arabidopsis AtTZF1/4/5/6/9 and rice OsTZF1 with the marker proteins of PBs and SGs has also been verified Bogamuwa and Jang, 2013;Jan et al, 2013;Maldonado-Bonilla et al, 2014). Previously, we found that AtC3H18-Like (At3g52980) is the only non-TZF protein that has been identified to show cytoplasmic foci localization (Xu et al, 2020a). The similarity in the subcellular localization pattern implies that these CCCH zinc-finger proteins may share a general molecular mechanism to achieve their biological functions.…”

Section: Introductionmentioning

confidence: 71%

“…Eight putative paralogs of AtC3H18 were identified by BLASTP analysis, but their overall amino acid sequence identities were relatively low (9-55%, Supplementary Figures 1B,C). AtC3H18 is most closely phylogenetically related to AtC3H18-Like (AtC3H18L), another non-TZF protein that has been identified by our lab previously (Xu et al, 2020a).…”

Section: Atc3h18 Encodes a Non-tandem Zinc-finger Protein That Is Hig...mentioning

confidence: 86%

“…The atc3h18 homozygous mutants were identified by PCR and sequencing. RNA extraction and qRT-PCR were performed as described by Xu et al (2020a). TUB4 was selected as reference gene to normalize the quantity of total RNA.…”

Section: Transient and Stable Plant Transformationsmentioning

confidence: 99%

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Highly Overexpressed AtC3H18 Impairs Microgametogenesis via Promoting the Continuous Assembly of mRNP Granules

Liu

Xiong

et al. 2022

Front. Plant Sci.

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Plant CCCH zinc-finger proteins form a large family of regulatory proteins function in many aspects of plant growth, development and environmental responses. Despite increasing reports indicate that many CCCH zinc-finger proteins exhibit similar subcellular localization of being localized in cytoplasmic foci, the underlying molecular mechanism and the connection between this specific localization pattern and protein functions remain largely elusive. Here, we identified another cytoplasmic foci-localized CCCH zinc-finger protein, AtC3H18, in Arabidopsis thaliana. AtC3H18 is predominantly expressed in developing pollen during microgametogenesis. Although atc3h18 mutants did not show any abnormal phenotype, possibly due to redundant gene(s), aberrant AtC3H18 expression levels caused by overexpression resulted in the assembly of AtC3H18-positive granules in a dose-dependent manner, which in turn led to male sterility phenotype, highlighting the importance of fine-tuned AtC3H18 expression. Further analyzes demonstrated that AtC3H18-positive granules are messenger ribonucleoprotein (mRNP) granules, since they can exhibit liquid-like physical properties, and are associated with another two mRNP granules known as processing bodies (PBs) and stress granules (SGs), reservoirs of translationally inhibited mRNAs. Moreover, the assembly of AtC3H18-positive granules depends on mRNA availability. Combined with our previous findings on the AtC3H18 homologous genes in Brassica campestris, we concluded that appropriate expression level of AtC3H18 during microgametogenesis is essential for normal pollen development, and we also speculated that AtC3H18 may act as a key component of mRNP granules to modulate pollen mRNAs by regulating the assembly/disassembly of mRNP granules, thereby affecting pollen development.

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Section: Introductionmentioning

confidence: 71%

Section: Atc3h18 Encodes a Non-tandem Zinc-finger Protein That Is Hig...mentioning

confidence: 86%

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Highly Overexpressed AtC3H18 Impairs Microgametogenesis via Promoting the Continuous Assembly of mRNP Granules

Liu

Xiong

et al. 2022

Front. Plant Sci.

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“…Furthermore, the N terminus of CCCH zinc-finger proteins is highly conserved among plants and can bind to DNA and RNA [ 97 ]. Some CCCH proteins participate in RNA metabolism and many of these carry RNA recognition motifs (RRMs) [ 98 ]. The different domain structures of CCCH proteins will be described in more detail in the below section, where we discuss protein localization and function.…”

Section: Domain Structure Of Ccch Zinc-finger Proteinsmentioning

confidence: 99%

“…However, the researchers in that study did not use a natural mRNA target, but rather a generic ARE for research, so we lack direct evidence that plant CCCH zinc-finger proteins function in post-transcriptional regulation of gene expression in vivo. Recent research has found that two putative mRNA binding domains, LOTUS/OST-HTH and RRM, were detected in the AtC3H18L protein sequence; this CCCH zinc finger protein has been implicated in stop codon read-through in Arabidopsis [ 98 ].…”

Section: Transcriptional and Post-transcriptional Regulation By Ccch Zinc-finger Proteinsmentioning

confidence: 99%

The Roles of CCCH Zinc-Finger Proteins in Plant Abiotic Stress Tolerance

Han

Qiao

et al. 2021

IJMS

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Zinc-finger proteins, a superfamily of proteins with a typical structural domain that coordinates a zinc ion and binds nucleic acids, participate in the regulation of growth, development, and stress adaptation in plants. Most zinc fingers are C2H2-type or CCCC-type, named after the configuration of cysteine (C) and histidine (H); the less-common CCCH zinc-finger proteins are important in the regulation of plant stress responses. In this review, we introduce the domain structures, classification, and subcellular localization of CCCH zinc-finger proteins in plants and discuss their functions in transcriptional and post-transcriptional regulation via interactions with DNA, RNA, and other proteins. We describe the functions of CCCH zinc-finger proteins in plant development and tolerance to abiotic stresses such as salt, drought, flooding, cold temperatures and oxidative stress. Finally, we summarize the signal transduction pathways and regulatory networks of CCCH zinc-finger proteins in their responses to abiotic stress. CCCH zinc-finger proteins regulate the adaptation of plants to abiotic stress in various ways, but the specific molecular mechanisms need to be further explored, along with other mechanisms such as cytoplasm-to-nucleus shuttling and post-transcriptional regulation. Unraveling the molecular mechanisms by which CCCH zinc-finger proteins improve stress tolerance will facilitate the breeding and genetic engineering of crops with improved traits.

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Integration of C3H15‐mediated transcriptional and post‐transcriptional regulation confers plant thermotolerance in Arabidopsis

Chai,

Liu,

Zhang

et al. 2024

The Plant Journal

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SUMMARYHeat stress is an environmental factor that significantly threatens crop production worldwide. Nevertheless, the molecular mechanisms governing plant responses to heat stress are not fully understood. Plant zinc finger CCCH proteins have roles in stress responses as well as growth and development through protein–RNA, protein–DNA, and protein–protein interactions. Here, we reveal an integrated multi‐level regulation of plant thermotolerance that is mediated by the CCCH protein C3H15 in Arabidopsis. Heat stress rapidly suppressed C3H15 transcription, which attenuated C3H15‐inhibited expression of its target gene HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2), a central regulator of heat stress response (HSR), thereby activating HEAT SHOCK COGNATE 70 (HSC70.3) expression. The RING‐type E3 ligase MED25‐BINDING RING‐H2 PROTEIN 2 (MBR2) was identified as an interacting partner of C3H15. The mbr2 mutant was susceptible to heat stress compared to wild‐type plants, whereas plants overexpressing MBR2 showed increased heat tolerance. MBR2‐dependent ubiquitination mediated the degradation of phosphorylated C3H15 protein in the cytoplasm, which was enhanced by heat stress. Consistently, heat sensitivities of C3H15 overexpression lines increased in MBR2 loss‐of‐function and decreased in MBR2 overexpression backgrounds. Heat stress‐induced accumulation of HSC70.3 promoted MBR2‐mediated degradation of C3H15 protein, implying that an auto‐regulatory loop involving C3H15, HSFA2, and HSC70.3 regulates HSR. Heat stress also led to the accumulation of C3H15 in stress granules (SGs), a kind of cytoplasmic RNA granule. This study advances our understanding of the mechanisms plants use to respond to heat stress, which will facilitate technologies to improve thermotolerance in crops.

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AtC3H18L is a stop-codon read-through gene and encodes a novel non-tandem CCCH zinc-finger protein that can form cytoplasmic foci similar to mRNP granules

Cited by 9 publications

References 29 publications

Highly Overexpressed AtC3H18 Impairs Microgametogenesis via Promoting the Continuous Assembly of mRNP Granules

Highly Overexpressed AtC3H18 Impairs Microgametogenesis via Promoting the Continuous Assembly of mRNP Granules

The Roles of CCCH Zinc-Finger Proteins in Plant Abiotic Stress Tolerance

Integration of C3H15‐mediated transcriptional and post‐transcriptional regulation confers plant thermotolerance in Arabidopsis

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