RLI2 regulates Arabidopsis female gametophyte and embryo development by facilitating the assembly of the translational machinery

Yu, Shi-Xia; Hu, Li-Qin; Yang, Luhan; Zhang, Tao; Dai, Renke; Zhang, Yanjie; Xie, Zhixun; Lin, Wen-Hui

doi:10.1016/j.celrep.2023.112741

Cited by 7 publications

(16 citation statements)

References 83 publications

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“…As expected, in AtABCE2 gene, known to be essential for the viability of an organism (Navarro-Quiles et al 2022; Yu et al 2023) only four non-synonymous SNPs residing in non-conserved regions were found among 1135 A. thaliana ecotypes (Supplementary Table S4). Importantly, the AtABCE2 gene seems to be hard to mutate, since up to now there is no T-DNA homozygous line available and only one viable, hypomorphic allele has been recently isolated after ethyl methanesulfonate mutagenesis (Navarro-Quiles et al, 2022).…”

Section: Discussionsupporting

confidence: 75%

“…In Arabidopsis, AtABCE1 and AtABCE2 exhibit partial functional redundancy. In contrast to AtABCE2, which is ubiquitously expressed, AtABCE1 is mostly present in generative organs and at relatively low levels (Yu et al 2023; Klepikova et al 2016; Navarro-Quiles et al 2022). This could mean an ongoing process of pseudogenization or subfunctionalization, where the paralogues acquire specific roles.…”

Section: Discussionmentioning

confidence: 98%

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Phylogenetic analysis ofABCEgenes across the plant kingdom

Jakobson,

Mõttus,

Suurväli

et al. 2023

Preprint

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ATP-BINDING CASSETTE SUBFAMILY E MEMBER (ABCE) proteins are one of the most conserved proteins across eukaryotes and archaea. Yeast and the vast majority of animals possess a singleABCEgene encoding the vital ABCE1 protein. We retrievedABCEgene sequences of 76 plant species from public genome databases and analyzed them with the reference toArabidopsis thaliana ABCE2gene (AtABCE2). Over half of the studied plant species possess two or moreABCEgenes. There can be as many as eightABCEgenes in a plant species. This suggest thatABCEgenes in plants can be classified as a low-copy gene family, rather than a single-copy gene family. Plant ABCE proteins showed overall high sequence conservation, sharing at least 78% of amino acid sequence identity with AtABCE2. The phylogenetic trees of full-length ABCE amino acid and CDS sequences demonstrated thatBrassicaceaeandPoaceaefamilies have independently undergone lineage-specific split of the ancestralABCEgene. Other plant species have gainedABCEgene copies through more recent duplication events. Deeper analysis ofAtABCE2and its paralogueAtABCE1from 1135Arabidopsis thalianaecotypes revealed 4 and 35 non-synonymous SNPs, respectively. The lower natural variation inAtABCE2compared toAtABCE1is in consistence with its crucial role for plant viability. Overall, while the sequence of the ABCE protein family is highly conserved in the plant kingdom, many plants have evolved to have more than one copy of this essential translational factor.Significance statementIn most eukaryotes there is a single ABCE protein, which is involved in many vital processes in cells. However, less is known about ABCEs specifically in plants. Here we show that while the sequence of ABCE proteins is highly conserved in plants, they have evolved to often have multiple copies of this essential translational factor. By studying 76 species from the entire plant kingdom, we observed as many as eightABCEgenes being present at a time, although most species have less. SomeABCEcopies appeared earlier than others and were found in multiple species. Thus, our findings indicate that ABCE genes in plants are not a single-copy gene family and should instead be re-classified as a low-copy gene family.

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Section: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 98%

Phylogenetic analysis ofABCEgenes across the plant kingdom

Jakobson,

Mõttus,

Suurväli

et al. 2023

Preprint

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“…In plants, there are various types of RNases (ribonucleases) that play crucial roles in the processing and degradation of RNA, which are important for the regulation of plant growth and development, as well as the response to stress conditions [44][45][46]. The dne1 mutant showed hypersensitivity to osmotic stress [47], and the DNE1 overexpression line exhibited more tolerance to oxidative stress [48].…”

Section: Dne1 Positively Regulates Arabidopsis Resistance To Er Stres...mentioning

confidence: 99%

Endoribonuclease DNE1 Promotes Ethylene Response by Modulating EBF1/2 mRNA Processing in Arabidopsis

Yan,

Guo,

2024

IJMS

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The gaseous phytohormone ethylene plays a crucial role in plant growth, development, and stress responses. In the ethylene signal transduction cascade, the F-box proteins EIN3-BINDING F-BOX 1 (EBF1) and EBF2 are identified as key negative regulators governing ethylene sensitivity. The translation and processing of EBF1/2 mRNAs are tightly controlled, and their 3′ untranslated regions (UTRs) are critical in these regulations. However, despite their significance, the exact mechanisms modulating the processing of EBF1/2 mRNAs remain poorly understood. In this work, we identified the gene DCP1-ASSOCIATED NYN ENDORIBONUCLEASE 1 (DNE1), which encodes an endoribonuclease and is induced by ethylene treatment, as a positive regulator of ethylene response. The loss of function mutant dne1-2 showed mild ethylene insensitivity, highlighting the importance of DNE1 in ethylene signaling. We also found that DNE1 colocalizes with ETHYLENE INSENSITIVE 2 (EIN2), the core factor manipulating the translation of EBF1/2, and targets the P-body in response to ethylene. Further analysis revealed that DNE1 negatively regulates the abundance of EBF1/2 mRNAs by recognizing and cleaving their 3′UTRs, and it also represses their translation. Moreover, the dne1 mutant displays hypersensitivity to 1,4-dithiothreitol (DTT)-induced ER stress and oxidative stress, indicating the function of DNE1 in stress responses. This study sheds light on the essential role of DNE1 as a modulator of ethylene signaling through regulation of EBF1/2 mRNA processing. Our findings contribute to the understanding of the intricate regulatory process of ethylene signaling and provide insights into the significance of ribonuclease in stress responses.

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“…Recently, AtABCE2 was found to interact with ribosomal proteins and translational factors, confirming its conserved ancestral function in translation that is coupled to general growth and vascular development, likely indirectly via auxin metabolism ( Navarro-Quiles et al, 2022 ). Furthermore, through regulation of translation AtABCE2 is involved in the development of gametophyte and embryo ( Yu, et al, 2023 ). In addition, AtABCE2 has been shown to suppress GFP transgene RNA silencing in heterologous system at the local and at the systemic levels by reducing accumulation of siRNAs ( Sarmiento et al, 2006 ; Kärblane et al, 2015 ).…”

Section: Introductionmentioning

confidence: 99%

“…This indicates that AtABCE2 might suppress RNA silencing via supporting translation-associated RNA degradation mechanisms. The role of AtABCE1 in A. thaliana , which is expressed almost exclusively in generative organs ( Navarro-Quiles et al, 2022 ; Yu et al, 2023 ), is yet to be studied.…”

Section: Introductionmentioning

confidence: 99%

Phylogenetic insight into ABCE gene subfamily in plants

Jakobson,

Mõttus,

Suurväli

et al. 2024

Front. Genet.

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ATP-BINDING CASSETTE SUBFAMILY E MEMBER (ABCE) proteins are one of the most conserved proteins across eukaryotes and archaea. Yeast and most animals possess a single ABCE gene encoding the critical translational factor ABCE1. In several plant species, including Arabidopsis thaliana and Oryza sativa, two or more ABCE gene copies have been identified, however information related to plant ABCE gene family is still missing. In this study we retrieved ABCE gene sequences of 76 plant species from public genome databases and comprehensively analyzed them with the reference to A. thaliana ABCE2 gene (AtABCE2). Using bioinformatic approach we assessed the conservation and phylogeny of plant ABCEs. In addition, we performed haplotype analysis of AtABCE2 and its paralogue AtABCE1 using genomic sequences of 1,135 A. thaliana ecotypes. Plant ABCE proteins showed overall high sequence conservation, sharing at least 78% of amino acid sequence identity with AtABCE2. We found that over half of the selected species have two to eight ABCE genes, suggesting that in plants ABCE genes can be classified as a low-copy gene family, rather than a single-copy gene family. The phylogenetic trees of ABCE protein sequences and the corresponding coding sequences demonstrated that Brassicaceae and Poaceae families have independently undergone lineage-specific split of the ancestral ABCE gene. Other plant species have gained ABCE gene copies through more recent duplication events. We also noticed that ploidy level but not ancient whole genome duplications experienced by a species impacts ABCE gene family size. Deeper analysis of AtABCE2 and AtABCE1 from 1,135 A. thaliana ecotypes revealed four and 35 non-synonymous SNPs, respectively. The lower natural variation in AtABCE2 compared to AtABCE1 is in consistence with its crucial role for plant viability. Overall, while the sequence of the ABCE protein family is highly conserved in the plant kingdom, many plants have evolved to have more than one copy of this essential translational factor.

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RLI2 regulates Arabidopsis female gametophyte and embryo development by facilitating the assembly of the translational machinery

Cited by 7 publications

References 83 publications

Phylogenetic analysis ofABCEgenes across the plant kingdom

Phylogenetic analysis ofABCEgenes across the plant kingdom

Endoribonuclease DNE1 Promotes Ethylene Response by Modulating EBF1/2 mRNA Processing in Arabidopsis

Phylogenetic insight into ABCE gene subfamily in plants

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