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Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice

Coleoptile is the small conical, short-lived, sheath-like organ that safeguards the first leaf and shoot apex in cereals. It is also the first leaf-like organ to senesce that provides nutrition to the developing shoot and is, therefore, believed to play a crucial role in seedling establishment in ri...

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Autores principales: Sasi, Jyothish Madambikattil, VijayaKumar, Cheeni, Kukreja, Bharti, Budhwar, Roli, Shukla, Rohit Nandan, Agarwal, Manu, Katiyar-Agarwal, Surekha
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597502/
https://www.ncbi.nlm.nih.gov/pubmed/36311124
http://dx.doi.org/10.3389/fpls.2022.985402
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author Sasi, Jyothish Madambikattil
VijayaKumar, Cheeni
Kukreja, Bharti
Budhwar, Roli
Shukla, Rohit Nandan
Agarwal, Manu
Katiyar-Agarwal, Surekha
author_facet Sasi, Jyothish Madambikattil
VijayaKumar, Cheeni
Kukreja, Bharti
Budhwar, Roli
Shukla, Rohit Nandan
Agarwal, Manu
Katiyar-Agarwal, Surekha
author_sort Sasi, Jyothish Madambikattil
collection PubMed
description Coleoptile is the small conical, short-lived, sheath-like organ that safeguards the first leaf and shoot apex in cereals. It is also the first leaf-like organ to senesce that provides nutrition to the developing shoot and is, therefore, believed to play a crucial role in seedling establishment in rice and other grasses. Though histochemical studies have helped in understanding the pattern of cell death in senescing rice coleoptiles, genome-wide expression changes during coleoptile senescence have not yet been explored. With an aim to investigate the gene regulation underlying the coleoptile senescence (CS), we performed a combinatorial whole genome expression analysis by sequencing transcriptome and miRNAome of senescing coleoptiles. Transcriptome analysis revealed extensive reprogramming of 3439 genes belonging to several categories, the most prominent of which encoded for transporters, transcription factors (TFs), signaling components, cell wall organization enzymes, redox homeostasis, stress response and hormone metabolism. Small RNA sequencing identified 41 known and 21 novel miRNAs that were differentially expressed during CS. Comparison of gene expression and miRNA profiles generated for CS with publicly available leaf senescence (LS) datasets revealed that the two aging programs are remarkably distinct at molecular level in rice. Integration of expression data of transcriptome and miRNAome identified high confidence 140 miRNA-mRNA pairs forming 42 modules, thereby demonstrating multi-tiered regulation of CS. The present study has generated a comprehensive resource of the molecular networks that enrich our understanding of the fundamental pathways regulating coleoptile senescence in rice.
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spelling pubmed-95975022022-10-27 Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice Sasi, Jyothish Madambikattil VijayaKumar, Cheeni Kukreja, Bharti Budhwar, Roli Shukla, Rohit Nandan Agarwal, Manu Katiyar-Agarwal, Surekha Front Plant Sci Plant Science Coleoptile is the small conical, short-lived, sheath-like organ that safeguards the first leaf and shoot apex in cereals. It is also the first leaf-like organ to senesce that provides nutrition to the developing shoot and is, therefore, believed to play a crucial role in seedling establishment in rice and other grasses. Though histochemical studies have helped in understanding the pattern of cell death in senescing rice coleoptiles, genome-wide expression changes during coleoptile senescence have not yet been explored. With an aim to investigate the gene regulation underlying the coleoptile senescence (CS), we performed a combinatorial whole genome expression analysis by sequencing transcriptome and miRNAome of senescing coleoptiles. Transcriptome analysis revealed extensive reprogramming of 3439 genes belonging to several categories, the most prominent of which encoded for transporters, transcription factors (TFs), signaling components, cell wall organization enzymes, redox homeostasis, stress response and hormone metabolism. Small RNA sequencing identified 41 known and 21 novel miRNAs that were differentially expressed during CS. Comparison of gene expression and miRNA profiles generated for CS with publicly available leaf senescence (LS) datasets revealed that the two aging programs are remarkably distinct at molecular level in rice. Integration of expression data of transcriptome and miRNAome identified high confidence 140 miRNA-mRNA pairs forming 42 modules, thereby demonstrating multi-tiered regulation of CS. The present study has generated a comprehensive resource of the molecular networks that enrich our understanding of the fundamental pathways regulating coleoptile senescence in rice. Frontiers Media S.A. 2022-10-12 /pmc/articles/PMC9597502/ /pubmed/36311124 http://dx.doi.org/10.3389/fpls.2022.985402 Text en Copyright © 2022 Sasi, VijayaKumar, Kukreja, Budhwar, Shukla, Agarwal and Katiyar-Agarwal https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Sasi, Jyothish Madambikattil
VijayaKumar, Cheeni
Kukreja, Bharti
Budhwar, Roli
Shukla, Rohit Nandan
Agarwal, Manu
Katiyar-Agarwal, Surekha
Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title_full Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title_fullStr Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title_full_unstemmed Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title_short Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
title_sort integrated transcriptomics and mirnaomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597502/
https://www.ncbi.nlm.nih.gov/pubmed/36311124
http://dx.doi.org/10.3389/fpls.2022.985402
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