Role of lncRNAs in cis- and trans-regulatory responses to salt in Populus trichocarpa.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
05 2022
Historique:
revised: 19 02 2022
received: 15 12 2019
accepted: 22 02 2022
pubmed: 27 2 2022
medline: 31 5 2022
entrez: 26 2 2022
Statut: ppublish

Résumé

Long non-coding RNAs (lncRNAs) are emerging as versatile regulators in diverse biological processes. However, little is known about their cis- and trans-regulatory contributions in gene expression under salt stress. Using 27 RNA-seq data sets from Populus trichocarpa leaves, stems and roots, we identified 2988 high-confidence lncRNAs, including 1183 salt-induced differentially expressed lncRNAs. Among them, 301 lncRNAs have potential for positively affecting their neighboring genes, predominantly in a cis-regulatory manner rather than by co-transcription. Additionally, a co-expression network identified six striking salt-associated modules with a total of 5639 genes, including 426 lncRNAs, and in these lncRNA sequences, the DNA/RNA binding motifs are enriched. This suggests that lncRNAs might contribute to distant gene expression of the salt-associated modules in a trans-regulatory manner. Moreover, we found 30 lncRNAs that have potential to simultaneously cis- and trans-regulate salt-responsive homologous genes, and Ptlinc-NAC72, significantly induced under long-term salt stress, was selected for validating its regulation of the expression and functional roles of the homologs PtNAC72.A and PtNAC72.B (PtNAC72.A/B). The transient transformation of Ptlinc-NAC72 and a dual-luciferase assay of Ptlinc-NAC72 and PtNAC72.A/B promoters confirmed that Ptlinc-NAC72 can directly upregulate PtNAC72.A/B expression, and a presence/absence assay was further conducted to show that the regulation is probably mediated by Ptlinc-NAC72 recognizing the tandem elements (GAAAAA) in the PtNAC72.A/B 5' untranslated region (5'-UTR). Finally, the overexpression of Ptlinc-NAC72 produces a hypersensitive phenotype under salt stress. Altogether, our results shed light on the cis- and trans-regulation of gene expression by lncRNAs in Populus and provides an example of long-term salt-induced Ptlinc-NAC72 that could be used to mitigate growth costs by conferring plant resilience to salt stress.

Identifiants

pubmed: 35218100
doi: 10.1111/tpj.15714
doi:

Substances chimiques

RNA, Long Noncoding 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

978-993

Informations de copyright

© 2022 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Bailey, T.L. (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics, 27, 1653-1659.
Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., D'Aubenton-Carafa, Y., Hirsch, J. et al. (2008) Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Research, 19, 57-69.
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Buske, F.A., Bodén, M., Bauer, D.C. & Bailey, T.L. (2010) Assigning roles to DNA regulatory motifs using comparative genomics. Bioinformatics, 26, 860-866.
Cabili, M.N., Trapnell, C., Goff, L., Koziol, M., Tazon-Vega, B., Regev, A. et al. (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Gene Development, 25, 1915-1927.
Chekanova, J.A. (2015) Long non-coding RNAs and their functions in plants. Current Opinion in Plant Biology, 27, 207-216.
Chen, M., Wang, C., Bao, H., Chen, H. & Wang, Y. (2016) Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency. Molecular Genetics and Genomics, 291, 1663-1680.
Chen, Q., Liu, K., Yu, R., Zhou, B., Huang, P., Cao, Z. et al. (2021) From "dark matter" to "star": insight into the regulation mechanisms of plant functional long non-coding RNAs. Frontiers in Plant Science, 12, 650926.
Cui, J., Luan, Y., Jiang, N., Bao, H. & Meng, J. (2017) Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin. The Plant Journal, 89, 577-589.
Di, C., Yuan, J., Wu, Y., Li, J., Lin, H., Hu, L. et al. (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. The Plant Journal, 80, 848-861.
Filichkin, S.A., Hamilton, M., Dharmawardhana, P.D., Singh, S.K., Sullivan, C., Ben-Hur, A. et al. (2018) Abiotic stresses modulate landscape of poplar transcriptome via alternative splicing, differential intron retention, and isoform ratio switching. Frontiers in Plant Science, 9, 5.
Flynn, R.A. & Chang, H.Y. (2014) Long noncoding RNAs in cell-fate programming and reprogramming. Cell Stem Cell, 14, 752-761.
Forestan, C., Aiese Cigliano, R., Farinati, S., Lunardon, A., Sanseverino, W. & Varotto, S. (2016) Stress-induced and epigenetic-mediated maize transcriptome regulation study by means of transcriptome reannotation and differential expression analysis. Sci Rep-Uk, 6, 30446.
Frazee, A.C., Pertea, G., Jaffe, A.E., Langmead, B., Salzberg, S.L. & Leek, J.T. (2015) Ballgown bridges the gap between transcriptome assembly and expression analysis. Nature Biotechnology, 33, 243-246.
Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme Takagi, M. et al. (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. The Plant Journal, 39, 863-876.
Guan, H., Liu, X., Niu, F., Zhao, Q., Fan, N., Cao, D. et al. (2019) OoNAC72, a NAC-type Oxytropis ochrocephala transcription factor, conferring enhanced drought and salt stress tolerance in Arabidopsis. Frontiers in Plant Science, 10, 890.
Guttman, M., Russell, P., Ingolia, N.T., Weissman, J.S. & Lander, E.S. (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell, 154, 240-251.
Hao, Z., Fan, C., Cheng, T., Su, Y., Wei, Q. & Li, G. (2015) Genome-wide identification, characterization and evolutionary analysis of Long intergenic noncoding RNAs in cucumber. PLoS One, 10, e121800.
He, X., Mu, R., Cao, W., Zhang, Z., Zhang, J. & Chen, S. (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. The Plant Journal, 44, 903-916.
Jefferson, R.A., Kavanagh, T.A. & Bevan, M.W. (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal, 6, 3901-3907.
Jiang, Y. & Deyholos, M.K. (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Molecular Biology, 69, 91-105.
Jin, J., Tian, F., Yang, D., Meng, Y., Kong, L., Luo, J. et al. (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research, 45, D1040-D1045.
Kang, Y., Yang, D., Kong, L., Hou, M., Meng, Y., Wei, L. et al. (2017) CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Research, 45, W12-W16.
Kim, D., Langmead, B. & Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods, 12, 357-360.
Kim, E.D. & Sung, S. (2012) Long noncoding RNA: unveiling hidden layer of gene regulatory networks. Trends Plant Science, 17, 16-21.
Krishnamurthy, P., Mohanty, B., Wijaya, E., Lee, D., Lim, T., Lin, Q. et al. (2017) Transcriptomics analysis of salt stress tolerance in the roots of the mangrove Avicennia officinalis. Sci Rep-Uk, 7, 10019-10031.
Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D. et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Research, 19, 1639-1645.
Langfelder, P. & Horvath, S. (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559.
Li, J., Wu, B., Xu, J. & Liu, C. (2014) Genome-wide identification and characterization of long intergenic non-coding RNAs in Ganoderma lucidum. PLoS One, 9, e99442.
Li, J., Zhang, J., Jia, H., Li, Y., Xu, X., Wang, L. et al. (2016) The Populus trichocarpa PtHSP17.8 involved in heat and salt stress tolerances. Plant Cell Reports, 35, 1587-1599.
Li, L., Eichten, S.R., Shimizu, R., Petsch, K., Yeh, C.T., Wu, W. et al. (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biology, 15, R40.
Li, X., Li, X., Li, M., Yan, Y., Liu, X. & Li, L. (2016) Dual function of NAC072 in ABF3-mediated ABA-responsive gene regulation in Arabidopsis. Frontiers in Plant Science, 7, 1075.
Li, S., Zhen, C., Xu, W., Wang, C. & Cheng, Y. (2017) Simple, rapid and efficient transformation of genotype Nisqually-1: a basic tool for the first sequenced model tree. Sci Report, 7, 2638.
Liu, J., Jung, C., Xu, J., Wang, H., Deng, S., Bernad, L. et al. (2012) Genome-wide analysis uncovers regulation of Long intergenic noncoding RNAs in Arabidopsis. The Plant Cell, 24, 4333-4345.
Liu, Y., Ji, X., Zheng, L., Nie, X. & Wang, Y. (2013) Microarray analysis of transcriptional responses to abscisic acid and salt stress in Arabidopsis thaliana. International Journal of Molecular Sciences, 14, 9979-9998.
Long, Y., Wang, X., Youmans, D.T. & Cech, T.R. (2017) How do lncRNAs regulate transcription? Science Advances, 3, o2110.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
MacIntosh, G.C., Wilkerson, C. & Green, P.J. (2001) Identification and analysis of Arabidopsis expressed sequence tags characteristic of non-coding RNAs. Plant Physiology, 127, 765-776.
Necsulea, A., Soumillon, M., Warnefors, M., Liechti, A., Daish, T., Zeller, U. et al. (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature, 505, 635-640.
Park, H.C., Kim, M.L., Kang, Y.H., Jeon, J.M., Yoo, J.H., Kim, M.C. et al. (2004) Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiology, 135, 2150-2161.
Pertea, M., Kim, D., Pertea, G.M., Leek, J.T. & Salzberg, S.L. (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and ballgown. Nature Protocols, 11, 1650-1667.
Qin, T., Zhao, H., Cui, P., Albesher, N. & Xiong, L. (2017) A nucleus-localized Long non-coding RNA enhances drought and salt stress tolerance. Plant Physiology, 175, 1321-1336.
Rice, P., Longden, I. & Bleasby, A. (2000) EMBOSS: the European molecular biology open software suite. Trends in Genetics, 16, 276-277.
Rinn, J.L. & Chang, H.Y. (2012) Genome regulation by Long noncoding RNAs. Annual Review of Biochemistry, 81, 145-166.
Robinson, M.D., McCarthy, D.J. & Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
Ruiz-Orera, J., Messeguer, X., Subirana, J.A. & Alba, M.M. (2014) Long non-coding RNAs as a source of new peptides. eLife, 3, e03523.
Shahmuradov, I.A., Gammerman, A.J., Hancock, J.M., Bramley, P.M. & Solovyev, V.V. (2003) PlantProm: a database of plant promoter sequences. Nucleic Acids Research, 31, 114-117.
Shimada, A., Okumura, A., Yamasaki, S., Iwata, Y., Koizumi, N., Nishihara, M. et al. (2017) A 64-bp sequence containing the GAAGA motif is essential for CaMV-35S promoter methylation in gentian. Biochim Biophys Acta Gene Regul Mech, 1860, 861-869.
Shuai, P., Liang, D., Tang, S., Zhang, Z., Ye, C., Su, Y. et al. (2014) Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. Journal of Experimental Botany, 65, 4975-4983.
Singh, U., Khemka, N., Rajkumar, M.S., Garg, R. & Jain, M. (2017) PLncPRO for prediction of long non-coding RNAs (lncRNAs) in plants and its application for discovery of abiotic stress-responsive lncRNAs in rice and chickpea. Nucleic Acids Research, 45, e183.
Sohn, K.H., Lee, S.C., Jung, H.W., Hong, J.K. & Hwang, B.K. (2006) Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Molecular Biology, 61, 897-915.
Sun, M. & Kraus, W.L. (2015) From discovery to function: the expanding roles of Long NonCoding RNAs in physiology and disease. Endocrine Reviews, 36, 25-64.
Szcześniak, M.W., Rosikiewicz, W. & Makałowska, I. (2015) CANTATAdb: a collection of plant Long non-coding RNAs. Plant & Cell Physiology, 57, e8.
Tang, R., Liu, H., Bao, Y., Lv, Q., Yang, L. & Zhang, H. (2010) The woody plant poplar has a functionally conserved salt overly sensitive pathway in response to salinity stress. Plant Molecular Biology, 74, 367-380.
Tang, R.J., Yang, Y., Yang, L., Liu, H., Wang, C.T., Yu, M.M. et al. (2014) Poplar calcineurin B-like proteins PtCBL10A and PtCBL10B regulate shoot salt tolerance through interaction with PtSOS2 in the vacuolar membrane. Plant Cell & Environment, 37, 573-588.
Tran, L.S.P. (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell, 16, 2481-2498.
Tuskan, G.A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U. et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596-1604.
Ulitsky, I., Shkumatava, A., Jan, C.H., Sive, H. & Bartel, D.P. (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell, 147, 1537-1550.
Wang, C., Yang, Y., Wang, H., Ran, X., Li, B., Zhang, J. et al. (2016) Ectopic expression of a cytochrome P450 monooxygenase gene PtCYP714A3 from Populus trichocarpa reduces shoot growth and improves tolerance to salt stress in transgenic rice. Plant Biotechnology Journal, 14, 1838-1851.
Wang, H., Niu, Q.W., Wu, H.W., Liu, J., Ye, J., Yu, N. et al. (2015) Analysis of non-coding transcriptome in rice and maize uncovers roles of conserved lncRNAs associated with agriculture traits. The Plant Journal, 84, 404-416.
Wang, S., Huang, H., Han, R., Chen, J., Jiang, J., Li, H. et al. (2019) BpAP1 directly regulates BpDEF to promote male inflorescence formation in Betula platyphylla × B. pendula. Tree Physiology, 39, 1046-1060.
Wang, S., Huang, H., Han, R., Liu, C., Qiu, Z., Liu, G. et al. (2019) Negative feedback loop between BpAP1 and BpPI/BpDEF heterodimer in Betula platyphylla × B. pendula. Plant Science, 289, 110280.
Washietl, S., Kellis, M. & Garber, M. (2014) Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Research, 24, 616-628.
Wierzbicki, A.T., Blevins, T. & Swiezewski, S. (2021) Long noncoding RNAs in plants. Annual Review of Plant Biology, 17, 245-271.
Wu, H., Fu, B., Sun, P., Xiao, C. & Liu, J. (2016) A NAC transcription factor represses putrescine biosynthesis and affects drought tolerance. Plant Physiology, 172, 1532-1547.
Wu M, Gu L (2017). TCseq: time course sequencing data analysis. R package version 1.8.0.
Wucher, V., Legeai, F., Hédan, B., Rizk, G., Lagoutte, L., Leeb, T. et al. (2017) FEELnc: a tool for long non-coding RNA annotation and its application to the dog transcriptome. Nucleic Acids Research, 45, e57.
Xu, W., Yang, T., Wang, B., Han, B., Zhou, H., Wang, Y. et al. (2018) Differential expression networks and inheritance patterns of long non-coding RNAs in castor bean seeds. The Plant Journal, 95, 324-340.
Yang, A., Dai, X. & Zhang, W. (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. Journal of Experimental Botany, 63, 2541-2556.
Young, M.D., Wakefield, M.J., Smyth, G.K. & Oshlack, A. (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology, 11, R14.
Yuan, J., Li, J., Yang, Y., Tan, C., Zhu, Y., Hu, L. et al. (2018) Stress-responsive regulation of long non-coding RNA polyadenylation in Oryza sativa. The Plant Journal, 93, 814-827.
Zhang, X., Liu, L., Chen, B., Qin, Z., Xiao, Y., Zhang, Y. et al. (2019) Progress in understanding the physiological and molecular responses of Populus to salt stress. International Journal of Molecular Sciences, 20, 1312.
Zhang, X., Shen, J., Xu, Q., Dong, J., Song, L., Wang, W. et al. (2021) Long noncoding RNA lncRNA354 functions as a competing endogenous RNA of miR160b to regulate ARF genes in response to salt stress in upland cotton. Plant Cell & Environment, 44, 3302-3321.
Zhang, Y., Liao, J., Li, Z., Yu, Y., Zhang, J., Li, Q. et al. (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biology, 15, 512.
Zhao, H., Jiang, J., Li, K. & Liu, G. (2017) Populus simonii × Populus nigra WRKY70 is involved in salt stress and leaf blight disease responses. Tree Physiology, 37, 827-844.
Zhao, X., Li, J., Lian, B., Gu, H., Li, Y. & Qi, Y. (2018) Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nature Communications, 9, 5056.
Zhao, X., Tan, L., Wang, S., Shen, Y., Guo, L., Ye, X. et al. (2021) The SR splicing factors: providing perspectives on their evolution, expression, alternative splicing, and function in Populus trichocarpa. International Journal of Molecular Sciences, 22, 11369.
Zhou, D., Du, Q., Chen, J., Wang, Q. & Zhang, D. (2017) Identification and allelic dissection uncover roles of lncRNAs in secondary growth of Populus tomentosa. DNA Research, 24, 473-486.
Zhou, X., Sunkar, R., Jin, H., Zhu, J.K. & Zhang, W. (2008) Genome-wide identification and analysis of small RNAs originated from natural antisense transcripts in Oryza sativa. Genome Research, 19, 70-78.
Zhu, B., Yang, Y., Li, R., Fu, D., Wen, L., Luo, Y. et al. (2015) RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. Journal of Experimental Botany, 66, 4483-4495.
Zhu, J. (2001) Plant salt tolerance. Trends in Plant Science, 6, 1360-1385.

Auteurs

Xiaoxue Ye (X)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.
Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Science, Northeast Forestry University, Harbin, 150040, China.
Institute of Tropical Biosciences and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, China.

Shuo Wang (S)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Xijuan Zhao (X)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Ni Gao (N)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Yao Wang (Y)

Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Science, Northeast Forestry University, Harbin, 150040, China.

Yanmei Yang (Y)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Ernest Wu (E)

Department of Forest & Conservation Sciences, Faculty of Forestry, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.

Cheng Jiang (C)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Yuxiang Cheng (Y)

State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University), School of Forestry, Northeast Forestry University, Harbin, 150040, China.

Wenwu Wu (W)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

Shenkui Liu (S)

State Key Laboratory of Subtropical Silviculture, Zhejiang A&F University, Lin'an, Hangzhou, 311300, China.

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