A dynamic intron retention program regulates the expression of several hundred genes during pollen meiosis

Golicz, Agnieszka A.; Allu, Annapurna Devi; Li, Wei; Lohani, Neeta; Singh, Mohan B.; Bhalla, Prem L.

doi:10.1007/s00497-021-00411-6

Cited by 17 publications

(18 citation statements)

References 77 publications

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“…These AS events would be of potential interest to detect and quantify at tissue level resolution to determine whether they are involved in the regulation of RTEL1 expression in plants. Indeed, AS and in particular intron retention was shown to control the timely usage of transcripts during meiosis in mice ( Naro et al, 2017 ) and Brassica ( Golicz et al, 2021 ). RTEL1 expression was found to be highest in spikes compared to other barley tissues and developmental stages and highest in isolated anthers at the pre-meiosis stage, concurrent with its known function in DNA replication.…”

Section: Discussionmentioning

confidence: 99%

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

et al. 2021

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Programmed meiotic DNA double-strand breaks (DSBs), necessary for proper chromosomal segregation and viable gamete formation, are repaired by homologous recombination (HR) as crossovers (COs) or non-crossovers (NCOs). The mechanisms regulating the number and distribution of COs are still poorly understood. The regulator of telomere elongation helicase 1 (RTEL1) DNA helicase was previously shown to enforce the number of meiotic COs in Caenorhabditis elegans but its function in plants has been studied only in the vegetative phase. Here, we characterised barley RTEL1 gene structure and expression using RNA-seq data previously obtained from vegetative and reproductive organs and tissues. Using RNAi, we downregulated RTEL1 expression specifically in reproductive tissues and analysed its impact on recombination using a barley 50k iSelect SNP Array. Unlike in C. elegans, in a population segregating for RTEL1 downregulated by RNAi, high resolution genome-wide genetic analysis revealed a significant increase of COs at distal chromosomal regions of barley without a change in their total number. Our data reveal the important role of RTEL1 helicase in plant meiosis and control of recombination.

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Section: Discussionmentioning

confidence: 99%

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

et al. 2021

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“…The plants were grown in a growth cabinet under the following conditions (21/18°C Day/night, a photoperiod of 16/8 hours light/dark, 200μmol m -2 s -1 light intensity and 60% humidity). The different stages of pollen development were harvested as per previously published protocol [60, 61]. Briefly, the following five groups of buds were identified: <0.5mm buds (pollen/microspore mother cells, PMC), 0.8-1mm buds (tetrads, TET), 1-2.5mm (microspores to polarised microspores, MIC), 3-4.5mm (early to late bi-nucleate pollen, BIN) and 5-6mm (tri-nucleate pollen, POL).…”

Section: Methodsmentioning

confidence: 99%

Genome-wide analysis of lncRNAs points to their roles in the modulation of developmental regulator expression during plant male germline development

Lohani

Golicz

Allu

et al. 2022

Preprint

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LncRNAs can function in regulating of gene expression, but their roles as essential regulators of developmental processes and organismal phenotypes remain largely unclear. Especially the roles of lncRNAs in plants are largely unexplored. However, it has been proposed that plant lncRNAs act as regulators of protein-coding genes during development and that the similar roles of animal and plant lncRNAs result from convergent evolution. Since pollen development follows an established program with well-defined and characterized stages, we have used it as a model for studying plant lncRNAs and their roles in reproductive development. We investigated of lncRNA expression and function during pollen formation in field mustard (Brassica rapa). Reference-based transcriptome assembly performed to update the existing genome annotation identified novel expressed protein-coding genes and long non-coding RNAs (lncRNAs), including 4,347 long intergenic non-coding RNAs (lincRNAs, 1058 expressed) and 2,045 lncRNAs overlapping protein-coding genes on the opposite strand (lncNATs, 780 expressed). The analysis of expression profiles reveals that lncRNAs are significant and stage-specific contributors to the gene expression profile of developing pollen. Gene co-expression networks accompanied by genome location analysis identified 38 cis-acting lincRNA, 31 cis-acting lncNAT, 7 trans-acting lincRNA and 14 trans-acting lncNAT to be substantially co-expressed with target protein-coding genes involved in biological processes regulating pollen development and male lineage specification. These findings provide a foundation for future research aiming at developing strategies to employ lncRNAs as regulatory tools for gene expression control during reproductive development.

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“…Pollen development occurs inside the locules of anthers, starting with diploid microspore mother cells that undergo meiotic cell division resulting in four haploid microspores ( Haerizadeh et al, 2006 ; Singh and Bhalla, 2007 ). Meiosis is tightly regulated genetically during pollen development ( Golicz et al, 2021 ). The uninucleate microspores undergo two successive mitotic divisions to form mature trinucleate pollen grain.…”

Section: Introductionmentioning

confidence: 99%

Rapid Transcriptional Reprogramming Associated With Heat Stress-Induced Unfolded Protein Response in Developing Brassica napus Anthers

2022

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Climate change associated increases in the frequency and intensity of extreme temperature events negatively impact agricultural productivity and global food security. During the reproductive phase of a plant’s life cycle, such high temperatures hinder pollen development, preventing fertilization, and seed formation. At the molecular level, heat stress-induced accumulation of misfolded proteins activates a signaling pathway called unfolded protein response (UPR) in the endoplasmic reticulum (ER) and the cytoplasm to enhance the protein folding capacity of the cell. Here, we report transcriptional responses of Brassica napus anthers exposed to high temperature for 5, 15, and 30 min to decipher the rapid transcriptional reprogramming associated with the unfolded protein response. Functional classification of the upregulated transcripts highlighted rapid activation of the ER-UPR signaling pathway mediated by ER membrane-anchored transcription factor within 5 min of heat stress exposure. KEGG pathway enrichment analysis also identified “Protein processing in ER” as the most significantly enriched pathway, indicating that the unfolded protein response (UPR) is an immediate heat stress-responsive pathway during B. napus anther development. Five minutes of heat stress also led to robust induction of the cytosolic HSF-HSP heat response network. Our results present a perspective of the rapid and massive transcriptional reprogramming during heat stress in pollen development and highlight the need for investigating the nature and function of very early stress-responsive networks in plant cells. Research focusing on very early molecular responses of plant cells to external stresses has the potential to reveal new stress-responsive gene networks that can be explored further for developing climate change resilient crops.

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A dynamic intron retention program regulates the expression of several hundred genes during pollen meiosis

Cited by 17 publications

References 77 publications

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

Downregulation of Barley Regulator of Telomere Elongation Helicase 1 Alters the Distribution of Meiotic Crossovers

Genome-wide analysis of lncRNAs points to their roles in the modulation of developmental regulator expression during plant male germline development

Rapid Transcriptional Reprogramming Associated With Heat Stress-Induced Unfolded Protein Response in Developing Brassica napus Anthers

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