The long intergenic noncoding RNA ARES modulates root architecture in Arabidopsis.
ARES
ARF7
AUXIN
SOLITARYROOT
lateral root development
long noncoding RNA
Journal
IUBMB life
ISSN: 1521-6551
Titre abrégé: IUBMB Life
Pays: England
ID NLM: 100888706
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
06
07
2022
accepted:
24
05
2023
medline:
14
9
2023
pubmed:
6
7
2023
entrez:
6
7
2023
Statut:
ppublish
Résumé
Long noncoding RNAs (lncRNAs) have emerged as important regulators of gene expression in plants. They have been linked to a wide range of molecular mechanisms, including epigenetics, miRNA activity, RNA processing and translation, and protein localization or stability. In Arabidopsis, characterized lncRNAs have been implicated in several physiological contexts, including plant development and the response to the environment. Here we searched for lncRNA loci located nearby key genes involved in root development and identified the lncRNA ARES (AUXIN REGULATOR ELEMENT DOWNSTREAM SOLITARYROOT) downstream of the lateral root master gene IAA14/SOLITARYROOT (SLR). Although ARES and IAA14 are co-regulated during development, the knockdown and knockout of ARES did not affect IAA14 expression. However, in response to exogenous auxin, ARES knockdown impairs the induction of its other neighboring gene encoding the transcription factor NF-YB3. Furthermore, knockdown/out of ARES results in a root developmental phenotype in control conditions. Accordingly, a transcriptomic analysis revealed that a subset of ARF7-dependent genes is deregulated. Altogether, our results hint at the lncRNA ARES as a novel regulator of the auxin response governing lateral root development, likely by modulating gene expression in trans.
Substances chimiques
Arabidopsis Proteins
0
RNA, Long Noncoding
0
Transcription Factors
0
Indoleacetic Acids
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
880-892Informations de copyright
© 2023 The Authors. IUBMB Life published by Wiley Periodicals LLC on behalf of International Union of Biochemistry and Molecular Biology.
Références
Lucero L, Fonouni-Farde C, Crespi M, Ariel F. Long noncoding RNAs shape transcription in plants. Transcription. 2020;11(3-4):160-171.
Romero-Barrios N, Legascue MF, Benhamed M, Ariel F, Crespi M. Survey and summary splicing regulation by long noncoding RNAs. Nucleic Acids Res. 2018;46(5):2169-2184.
Fonouni-Farde C, Ariel F, Crespi M. Plant long noncoding rnas: New players in the field of post-transcriptional regulations. Noncoding RNA. 2021;7(1):1-17.
Roulé T, Christ A, Hussain N, et al. The lncRNA MARS modulates the epigenetic reprogramming of the marneral cluster in response to ABA. Mol Plant. 2022;15:840-856.
Kindgren P, Ard R, Ivanov M, Marquardt S. Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat Commun. 2018;9(1):4561.
Jabnoune M, Secco D, Lecampion C, Robaglia C, Shu Q, Poirier Y. A Rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell. 2013;25(10):4166-4182.
Ariel F, Jegu T, Latrasse D, et al. Noncoding transcription by alternative rna polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell. 2014;55(3):383-396.
Kim DH, Sung S. Vernalization-triggered intragenic chromatin-loop formation by long noncoding RNAs. Dev Cell. 2017;176(1):100-106.
Ariel F, Lucero L, Christ A, et al. R-loop mediated trans action of the APOLO long noncoding RNA. Mol Cell. 2020;77(5):1055-1065.e4.
Moison M, Pacheco JM, Lucero L, et al. The lncRNA APOLO interacts with the transcription factor WRKY42 to trigger root hair cell expansion in response to cold. Mol Plant. 2021;14(6):937-948.
Blein T, Balzergue C, Roulé T, et al. Landscape of the non-coding transcriptome response of two Arabidopsis ecotypes to phosphate starvation. Plant Physiol. 2020;183:1058-1072.
Fukaki H, Tameda S, Masuda H, Tasaka M. Lateral root formation is blocked by a gain-of-function mutation in the solitary-root/IAA14 gene of Arabidopsis. Plant J. 2002;29(2):153-168.
Berardini TZ, Mundodi S, Reiser L, et al. Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol. 2004;135(2):745-755.
Hruz T, Laule O, Szabo G, et al. Genevestigator V3: A reference expression database for the meta-analysis of transcriptomes. Adv Bioinform. 2008;2008:1-5.
Nielsen M, Ard R, Leng X, et al. Transcription-driven chromatin repression of Intragenic transcription start sites. PLoS Genet. 2019;15(2):e1007969. https://doi.org/10.1371/journal.pgen.1007969.
Thieffry A, Vigh ML, Bornholdt J, Ivanov M, Brodersen P, Sandelin A. Characterization of arabidopsis thaliana promoter bidirectionality and antisense RNAs by inactivation of nuclear RNA decay pathways. Plant Cell. 2020;32(6):1845-1867.
Himanen K, Boucheron E, Vanneste S, Engler JDA, Inzé D, Beeckman T. Auxin-mediated cell cycle activation during early lateral root initiation. Planta. 2002;14:2339-2351.
Lavenus J, Goh T, Guyomarc'h S, et al. Inference of the arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones. Plant Cell. 2015;27(5):1368-1388.
Jia Z, Giehl RFH, von Wirén N. Local auxin biosynthesis acts downstream of brassinosteroids to trigger root foraging for nitrogen. Nat Commun. 2021;12(1):5437.
Zhang S, Yu R, Yu D, et al. The calcium signaling module CaM-IQM destabilizes IAA-ARF interaction to regulate callus and lateral root formation. Proc Natl Acad Sci USA. 2022;119:e2202669119.
Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H. Multiple AUX/IAA-ARF modules regulate lateral root formation: The role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos Transact R Soc B: Biol Sci. 2012;367(1595):1461-1468.
Fukaki H, Nakao Y, Okushima Y, Theologis A, Tasaka M. Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J. 2005;44(3):382-395.
Vanneste S, de Rybel B, Beemster GTS, et al. Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell. 2005;17(11):3035-3050.
Okushima Y, Overvoorde PJ, Arima K, et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell. 2005;17(2):444-463.
Du Y, Scheres B. Lateral root formation and the multiple roles of auxin. J Exp Bot. 2018;69(2):155-167.
Roulé T, Crespi M, Blein T. Regulatory long non-coding RNAs in root growth and development. Biochem Soc Trans. 2021;50:403-412.
Heo JB, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science. 2011;331(6013):76-79.
Wu HW, Deng S, Xu H, et al. A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves. New Phytol. 2018;219(4):1480-1491.
Wang Y, Luo X, Sun F, et al. Overexpressing lncRNA LAIR increases grain yield and regulates neighbouring gene cluster expression in rice. Nat Commun. 2018;9(1):1-9.
Zhao X, Li J, Lian B, Gu H, Li Y, Qi Y. Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nat Commun. 2018;9(1):1-12.
Sato H, Suzuki T, Takahashi F, Shinozaki K, Yamaguchi-Shinozaki K. NF-YB2 and NF-YB3 have functionally diverged and differentially induce drought and heat stress-specific genes. Plant Physiol. 2019;180(3):1677-1690.
Hong L, Ye C, Lin J, Fu H, Wu X, Li QQ. Alternative polyadenylation is involved in auxin-based plant growth and development. Plant J. 2018;93(2):246-258.
Wang Y, Fan X, Lin F, et al. Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc Natl Acad Sci USA. 2014;111(28):10359-10364.
Wang D, Qu Z, Yang L, et al. Transposable elements (TEs) contribute to stress-related long intergenic noncoding RNAs in plants. Plant J. 2017;90(1):133-146.
Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26(6):841-842.
Ariel F, Brault-Hernandez M, Laffont C, et al. Two direct targets of cytokinin signaling regulate symbiotic nodulation in medicago truncatula. Plant Cell. 2012;24(9):3838-3852.
Clough SJ, Bent AF. Floral dip: A simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735-743.
Pound MP, French AP, Atkinson JA, Wells DM, Bennett MJ, Pridmore T. RootNav: Navigating images of complex root architectures. Plant Physiol. 2013;162(4):1802-1814.
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139:5-17.
Kopylova E, Noé L, Touzet H. SortMeRNA: Fast and accurate filtering of ribosomal RNAs in metatranscriptomic data. Bioinformatics. 2012;28(24):3211-3217.
Lamesch P, Berardini TZ, Li D, et al. The Arabidopsis Information resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Res. 2012;40(D1):1202-1210.
Dobin A, Davis CA, Schlesinger F, et al. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15-21.
Liao Y, Smyth GK, Shi W. FeatureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923-930.
Lambert I, Paysant-Le Roux C, Colella S, Martin-Magniette ML. DiCoExpress: A tool to process multifactorial RNAseq experiments from quality controls to co-expression analysis through differential analysis based on contrasts inside GLM models. Plant Methods. 2020;16(1):68.
Kong L, Zhang Y, Ye ZQ, et al. CPC: Assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 2007;35(Suppl 2):345-349.
Kang YJ, Yang DC, Kong L, et al. CPC2: A fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res. 2017;45(W1):W12-W16.
Parizot B, de Rybel B, Beeckman T. VisuaLRTC: A new view on lateral root initiation by combining specific transcriptome data sets. Plant Physiol. 2010;153(1):34-40.
Bardou F, Ariel F, Simpson CG, et al. Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev Cell. 2014;30(2):166-176.
Trincado JL, Entizne JC, Hysenaj G, et al. SUPPA2: Fast, accurate, and uncertainty-aware differential splicing analysis across multiple conditions. Genome Biol. 2018;19(1):40.
Zhang R, Kuo R, Coulter M, et al. A high-resolution single-molecule sequencing-based Arabidopsis transcriptome using novel methods of iso-seq analysis. Genome Biol. 2022;23(1):149.
Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nat Biotechnol. 2016;34(5):525-527.