Arabidopsis <i>PIRL6</i> Is Essential for Male and Female Gametogenesis and Is Regulated by Alternative Splicing

Forsthoefel, Nancy R.; Klag, Kendra A.; McNichol, Savannah R.; Arnold, Claire E.; Vernon, C.; Wood, Whitney W.; Vernon, Daniel M.

doi:10.1104/pp.18.00329

Cited by 10 publications

(11 citation statements)

References 81 publications

(87 reference statements)

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“…Loraine et al revealed that AS participants in the reproduction development of Arabidopsis [62]. AS has been reported to regulate the formation of male and female gametogenesis in Arabidopsis [63], which also led to the male sterile in rice [23]. In this study, we have detected seven AS modes in the ovule of P. tabuliformis, there are more AS events in the FER than STE ovule (Fig.…”

Section: Discussionsupporting

confidence: 55%

Single molecular real-time sequencing revealing the ovule abortion regulatory mechanisms in the female-sterile line of Pinus tabuliformis Carr.

Gong¹,

Han²,

Zhang³

et al. 2020

Preprint

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Background Ovule abortion is a common phenomenon in plants, which has an essential significance in seed production. The development of the female gametophyte (FG) is one of the crucial processes of the life cycle, and FG dysplasia is a significant cause contribute to ovule abortion in many species. However, because it is difficult to acquire the mutant about ovule development in gymnosperms, previous studies of the ovule and FG development are mainly focused on angiosperms, especially in Arabidopsis thaliana. Thus the investigation on this field of gymnosperms remains unclear. Results In this study, we investigated the transcriptome data of wild-type (female fertile line, FER) and natural ovule abortion mutant (female sterile line, STE) of Pinus tabuliformis Carr. to evaluate the mechanism of ovule abortion during the process of free nuclear mitosis (FNM). Using single molecule real-time (SMRT) sequencing and next-generation sequencing (NGS), we obtained 202,869 (FER), 197,977 (STE) mapped full-length non-chimeric (FLNC) reads and analyzed 18 cDNA libraries. Based on the SMRT sequencing, we found that both GO annotation and KEGG pathway terms results were similar in FER and STE. NGS analysis further showed altogether 99 differentially expressed genes (DEGs) with opposite expression patterns during the FNM process in FER and STE. According to SMRT sequencing, we found that the number of isoforms and alternative splicing (AS) patterns are variable between FER and STE. Moreover, 5,530 and 5,096 potential simple sequence repeats (SSRs) were identified in FER and STE, respectively. Functional annotation results demonstrated that genes involved in energy metabolism, signal transduction, cell division, and stress response were differentially expressed in different lines, 9 pairs of which were confirmed by quantitative real-time PCR. Conclusion Taken together, these results provide some new insights about the ovule abortion in gymnosperms and further reveal the regulatory mechanisms of ovule development.

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Section: Discussionsupporting

confidence: 55%

Single molecular real-time sequencing revealing the ovule abortion regulatory mechanisms in the female-sterile line of Pinus tabuliformis Carr.

Gong¹,

Han²,

Zhang³

et al. 2020

Preprint

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“…In A. thaliana, a splice variant of auxin response factor 8 has been found to play a role in regulating endothecium lignification and stamen elongation (Ghelli et al, 2018). Plant intracellular Ras-group leucine-rich repeat protein 6 is necessary for female and male gametogenesis in A. thaliana, and it is regulated by AS (Forsthoefel et al, 2018). Moreover, many studies on AS have been performed in different plant species, such as A. thaliana, tomato, moso bamboo, and peanut (Wang et al, 2014;Wang et al, 2017;Ruan et al, 2018;Zhao et al, 2018;Clark et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…For example, in peanut (Arachis hypogaea), Arabidopsis thaliana, soybean (Glycine max), tomato (Solanum lycopersicum) and moso bamboo (Phyllostachys edulis), approximately 37%, 61%, 63%, 65%, and 49% of multi-exon genes undergo AS events, respectively (Marquez et al, 2012;Shen et al, 2014;Ruan et al, 2018;Zhao et al, 2018;Clark et al, 2019). Furthermore, researchers have found that AS also plays important roles in male and female gametogenesis, seed germination in A. thaliana, plant-pathogen interactions in wheat (Triticum aestivum), and mineral nutrient homeostasis maintenance in rice (Oryza sativa) (Dong et al, 2018;Forsthoefel et al, 2018;Tognacca et al, 2019;Zhang H. et al, 2019). These findings indicate that AS is essential for plant survival and reproduction.…”

Section: Introductionmentioning

confidence: 99%

Alternative Splicing Enhances the Transcriptome Complexity of Liriodendron chinense

Tu¹,

Shen²,

Wen³

et al. 2020

Front. Plant Sci.

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Alternative splicing (AS) plays pivotal roles in regulating plant growth and development, flowering, biological rhythms, signal transduction, and stress responses. However, no studies on AS have been performed in Liriodendron chinense, a deciduous tree species that has high economic and ecological value. In this study, we used multiple tools and algorithms to analyze transcriptome data derived from seven tissues via hybrid sequencing. Although only 17.56% (8,503/48,408) of genes in L. chinense were alternatively spliced, these AS genes occurred in 37,844 AS events. Among these events, intron retention was the most frequent AS event, producing 1,656 PTCcontaining and 3,310 non-PTC-containing transcripts. Moreover, 183 long noncoding RNAs (lncRNAs) also underwent AS events. Furthermore, weighted gene coexpression network analysis (WGCNA) revealed that there were great differences in the activities of transcription and post-transcriptional regulation between pistils and leaves, and AS had an impact on many physiological and biochemical processes in L. chinense, such as photosynthesis, sphingolipid metabolism, fatty acid biosynthesis and metabolism. Moreover, our analysis showed that the features of genes may affect AS, as AS genes and non-AS genes had differences in the exon/intron length, transcript length, and number of exons/introns. In addition, the structure of AS genes may impact the frequencies and types of AS because AS genes with more exons or introns tended to exhibit more AS events, and shorter introns tended to be retained, whereas shorter exons tended to be skipped. Furthermore, eight AS genes were verified, and the results were consistent with our analysis. Overall, this study reveals that AS and gene interaction are mutual-on one hand, AS can affect gene expression and translation, while on the other hand, the structural characteristics of the gene can also affect AS. This work is the first to comprehensively report on AS in L. chinense, and it can provide a reference for further research on AS in L. chinense.

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“…GEM1 encodes a microtubule-associated protein and GEM3 is required for microtubule organisation and mitotic progression. Additional proteins that are essential for gametophyte development include ABORTED GAMETOPHYTE 1 (Cui et al, 2015), the DC1-domain protein VACUOLELESS GAMETOPHYTES (D’Ippólito et al, 2017), and the leucine-rich repeat protein PIRL6 (Forsthoefel et al, 2018). Whether AOG2 acts upstream or downstream of these other factors remains to be determined, but if any of them are translated in the ER, they are putative AOG2 targets.…”

Section: Resultsmentioning

confidence: 99%

A Musashi-Related Protein is Essential for Gametogenesis in Arabidopsis

Moody

Rabbinowitsch

Dickinson

et al. 2019

Preprint

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Musashi (Msi) proteins are an evolutionarily conserved group of RNA-binding proteins, required for targeted control of mRNA translation during many important developmental processes in animals. Most notably, Msi proteins play important roles during both spermatogenesis and oogenesis. Msi proteins also exist in plants but these are largely uncharacterized. Here we report the functional characterization of an Arabidopsis Msi ortholog ABORTED GAMETOPHYTE 2 (AOG2), which encodes a protein containing two RNA recognition motifs and an ER-targeting signal. AOG2-GFP translational fusions were localized to the ER in transient assays, suggesting that AOG2 most likely binds to ER-targeted mRNAs.We show that disrupted AOG2 function leads to a high rate of both ovule and seed abortion, and that homozygous loss of function mutants are embryo lethal. Furthermore, we demonstrate that AOG2 is required to establish asymmetry during pollen mitosis I, and that loss of AOG2 function leads to loss of pollen viability. Collectively the results reveal that AOG2 is required for the establishment of polarity and/or the progression of mitosis during gametophyte development in Arabidopsis, and thus Msi-related proteins have an evolutionarily conserved role in gametogenesis in both animals and plants. SIGNIFICANCE STATEMENT (75 WORDS) = 2 SENTENCES MAXABORTED GAMETOPHYTE 2 (AOG2) encodes a Musashi-related RNA-binding protein that is required for gametogenesis and embryogenesis in Arabidopsis. AOG2 is required for the establishment of polarity and/or the progression of mitosis during gametophyte development in Arabidopsis, and thus Musashi-related proteins have an evolutionarily conserved role in gametogenesis in both animals and plants.

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Arabidopsis PIRL6 Is Essential for Male and Female Gametogenesis and Is Regulated by Alternative Splicing

Cited by 10 publications

References 81 publications

Single molecular real-time sequencing revealing the ovule abortion regulatory mechanisms in the female-sterile line of Pinus tabuliformis Carr.

Single molecular real-time sequencing revealing the ovule abortion regulatory mechanisms in the female-sterile line of Pinus tabuliformis Carr.

Alternative Splicing Enhances the Transcriptome Complexity of Liriodendron chinense

A Musashi-Related Protein is Essential for Gametogenesis in Arabidopsis

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