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

Xu, Liai; Liu, Tingting; Xiong, Xingpeng; Shen, Xiuping; Huang, Li; Yu, Youjian; Cao, Jiashu

doi:10.3389/fpls.2022.932793

Cited by 3 publications

(16 citation statements)

References 53 publications

(61 reference statements)

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“…After HS, excitingly, it was observed high temperature changed GFP-LlC3H18 from being mainly dispersed in the cytoplasm to being aggregated into cytoplasmic foci, which was consistent with the distribution of the mCherry fluorescence of the PB marker mCherry-DCP2 and the SG maker mCherry-PABP8 (Fig. 2 A) (Decker and Parker 2012 ; Xu et al 2022 ). Due to both PB and SG are the mRNP granules, so these results indicated that LlC3H18 exhibited variable subcellular localization characteristics and may play roles in mRNA regulation with RNA-binding ability.…”

Section: Resultssupporting

confidence: 77%

“…Similar to the protein structure of Arabidopsis AtC3H18 (Xu et al 2022 ), LlC3H18 has a CCCH domain and two potential RBDs (Fig. S 3 ).…”

Section: Discussionmentioning

confidence: 74%

“…Our previous study has shown that lily LlMYB305 is a MYB21 homology whose expression is activated by high temperature and plays a positive role in thermotolerance (Wu et al 2021 ). In addition, MYB21 and C3H18 have been reported to participate in the same process of anther development (Cheng et al 2009 ; Huang et al 2020 ; Song et al 2011 ; Xu et al 2022 ). According to these results, we guessed that LlMYB305 might act as an upstream regulator of LlC3H18 .…”

Section: Resultsmentioning

confidence: 99%

“…In addition, CCCH proteins are divided into tandem CCCH-type zinc finger (TZF) and non-TZF proteins: TZF proteins contain two tandem CCCH-type ZNF motifs whereas non-TZF proteins have fewer or greater than two CCCH-type ZNF motifs (Bogamuwa and Jang 2014 ; Seok et al 2018 ). Except the ZNF domain, some members of CCCH family also had a LOTUS/OST-HTH (Limkain, Oskar, and TUdor-containing proteins 5 and 7) domain and an RRM (RNA-recognition motif) domain, both are putative RNA-binding domains, so they are always putative RNA-binding proteins for post-transcriptional regulation (Pomeranz et al 2010b ; Xu et al 2022 ). For AtTZF1, the TZF motif is important for RNA binding in a zinc-dependent fashion (Pomeranz et al 2010b ; Qu et al 2014 ).…”

Section: Introductionmentioning

confidence: 99%

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A LlMYB305-LlC3H18-LlWRKY33 module regulates thermotolerance in lily

Wu,

Liang,

et al. 2023

Mol Horticulture

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The CCCH proteins play important roles in plant growth and development, hormone response, pathogen defense and abiotic stress tolerance. However, the knowledge of their roles in thermotolerance are scarce. Here, we identified a heat-inducible CCCH gene LlC3H18 from lily. LlC3H18 was localized in the cytoplasm and nucleus under normal conditions, while it translocated in the cytoplasmic foci and co-located with the markers of two messenger ribonucleoprotein (mRNP) granules, processing bodies (PBs) and stress granules (SGs) under heat stress conditions, and it also exhibited RNA-binding ability. In addition, LlC3H18 exhibited transactivation activity in both yeast and plant cells. In lily and Arabidopsis, overexpression of LlC3H18 damaged their thermotolerances, and silencing of LlC3H18 in lily also impaired its thermotolerance. Similarly, Arabidopsis atc3h18 mutant also showed decreased thermotolerance. These results indicated that the appropriate expression of C3H18 was crucial for establishing thermotolerance. Further analysis found that LlC3H18 directly bound to the promoter of LlWRKY33 and activated its expression. Besides, it was found that LlMYB305 acted as an upstream factor of LlC3H18 and activated its expression. In conclusion, we demonstrated that there may be a LlMYB305-LlC3H18-LlWRKY33 regulatory module in lily that is involved in the establishment of thermotolerance and finely regulates heat stress response. Graphical Abstract

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Section: Resultssupporting

confidence: 77%

“…Similar to the protein structure of Arabidopsis AtC3H18 (Xu et al 2022 ), LlC3H18 has a CCCH domain and two potential RBDs (Fig. S 3 ).…”

Section: Discussionmentioning

confidence: 74%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A LlMYB305-LlC3H18-LlWRKY33 module regulates thermotolerance in lily

Wu,

Liang,

et al. 2023

Mol Horticulture

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“…Another Arabidopsis CCCH ZFP gene, AtC3H18 , is predominantly expressed in the developing microspores, and its gain-of-function mutant exhibited a male sterility phenotype. Further investigation suggested that AtC3H18 may modulate pollen mRNA by regulating the assembly/disassembly of messenger ribonucleoprotein (mRNP) granules, thereby affecting pollen development [ 146 ]. CCCH ZFP genes BcMF30a and BcMF30c are substantially expressed during microgametogenesis and pollen germination in B. campestris .…”

Section: Roles Of Tfs In Male Gametophyte Developmentmentioning

confidence: 99%

Transcription Factors and Their Regulatory Roles in the Male Gametophyte Development of Flowering Plants

Qian,

Shi,

Zhang

et al. 2024

IJMS

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Male gametophyte development in plants relies on the functions of numerous genes, whose expression is regulated by transcription factors (TFs), non-coding RNAs, hormones, and diverse environmental stresses. Several excellent reviews are available that address the genes and enzymes associated with male gametophyte development, especially pollen wall formation. Growing evidence from genetic studies, transcriptome analysis, and gene-by-gene studies suggests that TFs coordinate with epigenetic machinery to regulate the expression of these genes and enzymes for the sequential male gametophyte development. However, very little summarization has been performed to comprehensively review their intricate regulatory roles and discuss their downstream targets and upstream regulators in this unique process. In the present review, we highlight the research progress on the regulatory roles of TF families in the male gametophyte development of flowering plants. The transcriptional regulation, epigenetic control, and other regulators of TFs involved in male gametophyte development are also addressed.

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Heterologous Expression of Two Brassica campestris CCCH Zinc-Finger Proteins in Arabidopsis Induces Cytoplasmic Foci and Causes Pollen Abortion

Xu,

Xiong,

Liu

et al. 2023

IJMS

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The membrane-less organelles in cytoplasm that are presented as cytoplasmic foci were successively identified. Although multiple CCCH zinc-finger proteins have been found to be localized in cytoplasmic foci, the relationship between their specific localization and functions still needs further clarification. Here, we report that the heterologous expression of two Brassica campestris CCCH zinc-finger protein genes (BcMF30a and BcMF30c) in Arabidopsis thaliana can affect microgametogenesis by involving the formation of cytoplasmic foci. By monitoring the distribution of proteins and observing pollen phenotypes, we found that, when these two proteins were moderately expressed in pollen, they were mainly dispersed in the cytoplasm, and the pollen developed normally. However, high expression induced the assembly of cytoplasmic foci, leading to pollen abortion. These findings suggested that the continuous formation of BcMF30a/BcMF30c-associated cytoplasmic foci due to high expression was the inducement of male sterility. A co-localization analysis further showed that these two proteins can be recruited into two well-studied cytoplasmic foci, processing bodies (PBs), and stress granules (SGs), which were confirmed to function in mRNA metabolism. Together, our data suggested that BcMF30a and BcMF30c play component roles in the assembly of pollen cytoplasmic foci. Combined with our previous study on the homologous gene of BcMF30a/c in Arabidopsis, we concluded that the function of these homologous genes is conserved and that cytoplasmic foci containing BcMF30a/c may participate in the regulation of gene expression in pollen by regulating mRNA metabolism.

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

Cited by 3 publications

References 53 publications

A LlMYB305-LlC3H18-LlWRKY33 module regulates thermotolerance in lily

A LlMYB305-LlC3H18-LlWRKY33 module regulates thermotolerance in lily

Transcription Factors and Their Regulatory Roles in the Male Gametophyte Development of Flowering Plants

Heterologous Expression of Two Brassica campestris CCCH Zinc-Finger Proteins in Arabidopsis Induces Cytoplasmic Foci and Causes Pollen Abortion

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