Inference of the gene regulatory network acting downstream of CROWN ROOTLESS 1 in rice reveals a regulatory cascade linking genes involved in auxin signaling, crown root initiation, and root meristem specification and maintenance.


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:
12 2019
Historique:
received: 16 04 2019
revised: 16 07 2019
accepted: 17 07 2019
pubmed: 2 8 2019
medline: 31 7 2020
entrez: 2 8 2019
Statut: ppublish

Résumé

Crown roots (CRs) are essential components of the rice root system. Several genes involved in CR initiation or development have been identified but our knowledge about how they organize to form a gene regulatory network (GRN) is still limited. To characterize the regulatory cascades acting during CR formation, we used a systems biology approach to infer the GRN controlling CR formation downstream of CROWN ROOTLESS 1 (CRL1), coding for an ASL (asymmetric leaves-2-like)/LBD (LOB domain) transcription factor necessary for CR initiation. A time-series transcriptomic dataset was generated after synchronized induction of CR formation by dexamethasone-mediated expression of CRL1 expression in a crl1 mutant background. This time series revealed three different genome expression phases during the early steps of CR formation and was further exploited to infer a GRN using a dedicated algorithm. The predicted GRN was confronted with experimental data and 72% of the inferred links were validated. Interestingly, this network revealed a regulatory cascade linking CRL1 to other genes involved in CR initiation, root meristem specification and maintenance, such as QUIESCENT-CENTER-SPECIFIC HOMEOBOX, and in auxin signalling. This predicted regulatory cascade was validated in vivo using transient activation assays. Thus, the CRL1-dependant GRN reflects major gene regulation events at play during CR formation and constitutes a valuable source of discovery to better understand this developmental process.

Identifiants

pubmed: 31369175
doi: 10.1111/tpj.14487
doi:

Substances chimiques

Indoleacetic Acids 0
Plant Proteins 0
Transcription Factors 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

954-968

Informations de copyright

© 2019 The Authors The Plant Journal © 2019 John Wiley & Sons Ltd.

Références

Abe, M., Kuroshita, H., Umeda, M., Itoh, J.I. and Nagato, Y. (2008) The rice FLATTENED SHOOT MERISTEM, encoding CAF-1 p150 subunit, is required for meristem maintenance by regulating the cell-cycle period. Dev. Biol. 319, 384-393.
Assenov, Y., Ramírez, F., Schelhorn, S.E.S.E., Lengauer, T. and Albrecht, M. (2008) Computing topological parameters of biological networks. Bioinformatics, 24, 282-284.
Barabasi, A.L., Oltvai, Z.N., Barabási, A.-L., Oltvai, Z.N., Barabasi, A.L. and Oltvai, Z.N. (2004). Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5, 101-113.
Bruex, A., Kainkaryam, R.M., Wieckowski, Y. et al. (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet. 8, e1002446.
Cacas, J.L., Pré, M., Pizot, M., Cissoko, M., Diedhiou, I., Jalloul, A., Doumas, P., Nicole, M. and Champion, A. (2017) GhERF-IIb3 regulates the accumulation of jasmonate and leads to enhanced cotton resistance to blight disease. Mol. Plant Pathol. 18, 825-836.
Caldana, C., Scheible, W.-R., Mueller-Roeber, B. and Ruzicic, S. (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods, 3, 7.
Carbon, S., Ireland, A., Mungall, C.J. et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics, 25, 288-289.
Carbon, S., Dietze, H., Lewis, S.E. et al. (2017) Expansion of the gene ontology knowledgebase and resources: the gene ontology consortium. Nucleic Acids Res. 45, D331-D338.
Cheng, S., Zhou, D.-X. and Zhao, Y. (2016) WUSCHEL-related homeobox gene WOX11 increases rice drought resistance by controlling root hair formation and root system development. Plant Signal. Behav. 11, e1130198. https://doi.org/10.1080/15592324.2015
Coudert, Y., Bès, M., Le, T.V.A., Pré, M., Guiderdoni, E. and Gantet, P. (2011) Transcript profiling of crown rootless1 mutant stem base reveals new elements associated with crown root development in rice. BMC Genom., 12, 387.
Coudert, Y., Dievart, A., Droc, G. and Gantet, P. (2013) ASL/LBD phylogeny suggests that genetic mechanisms of root initiation downstream of auxin are distinct in lycophytes and euphyllophytes. Mol. Biol. Evol. 30, 569-572.
Coudert, Y., Le, V.A.T., Adam, H., Bès, M., Vignols, F., Jouannic, S., Guiderdoni, E. and Gantet, P. (2015) Identification of CROWN ROOTLESS1-regulated genes in rice reveals specific and conserved elements of postembryonic root formation. New Phytol. 206, 243-254.
De Rybel, B., Vassileva, V., Parizot, B. et al. (2010) A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 20, 1697-1706.
De Sutter, V., Vanderhaeghen, R., Tilleman, S., Lammertyn, F., Vanhoutte, I., Karimi, M., Inzé, D., Goossens, A. and Hilson, P. (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J. 44, 1065-1076.
Dong, J. and Horvath, S. (2007) Understanding network concepts in modules. BMC Syst. Biol. 1, 1-20.
Du, H., Wu, N., Fu, J., Wang, S., Li, X., Xiao, J. and Xiong, L. (2012) A GH3 family member, OsGH3-2, modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice. J. Exp. Bot. 63, 6467-6480.
Edgar, R. (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210.
Gómez-Vela, F., Lagares, J.A. and Díaz-Díaz, N. (2015) Gene network coherence based on prior knowledge using direct and indirect relationships. Comput. Biol. Chem. 56, 142-151.
Hu, X. and Xu, L. (2016) Transcription factors WOX11/12 directly activate WOX5/7 to promote root primordia initiation and organogenesis. Plant Physiol. 172, 2363-2373.
Inukai, Y., Mawi, M., Nagato, Y., Kitano, H. and Yamauchi, A. (2001) Characterization of rice mutants deficient in the formation of crown roots. Breed. Sci. 51, 123-129.
Inukai, Y., Sakamoto, T., Ueguchi-tanaka, M., Shibata, Y., Gomi, K., Umemura, I., Hasegawa, Y., Ashikari, M., Kitano, H. and Matsuoka, M. (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell, 17, 1387-1396.
Irizarry, R.A. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
Itoh, J.-I., Nonomura, K.-I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H. and Nagato, Y. (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol. 46, 23-47.
Jiang, W., Zhou, S., Zhang, Q., Song, H., Zhou, D.-X. and Zhao, Y. (2017) Transcriptional regulatory network of WOX11 is involved in the control of crown root development, cytokinin signals, and redox in rice. J. Exp. Bot. 68, 2787-2798.
Jin, J., Tian, F., Yang, D.-C., Meng, Y.-Q., Kong, L., Luo, J. and Gao, G. (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 45, D1040-D1045.
Jun, N., Gaohang, W., Zhenxing, Z., Huanhuan, Z., Yunrong, W. and Ping, W. (2011) OsIAA23-mediated auxin signaling defines postembryonic maintenance of QC in rice. Plant J. 68, 433-442.
Jung, H., Lee, D.K., Choi, Y.Do and Kim, J.K. (2015) OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci. 236, 304-312.
Kamiya, N., Nagasaki, H., Morikami, A., Sato, Y. and Matsuoka, M. (2003) Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. Plant J. 35, 429-441.
Kaya, H., Shibahara, K.I., Taoka, K.I., Iwabuchi, M., Stillman, B. and Araki, T. (2001) FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell, 104, 131-142.
Kitomi, Y., Inahashi, H., Takehisa, H., Sato, Y. and Inukai, Y. (2012) OsIAA13-mediated auxin signaling is involved in lateral root initiation in rice. Plant Sci. 190, 116-122.
Lavenus, J., Goh, T., Guyomarc'h, S. et al. (2015) Inference of the Arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones. Plant Cell, 27, 1368-1388.
Le, D.-H. and Kwon, Y.-K. (2011) NetDS: a Cytoscape plugin to analyze the robustness of dynamics and feedforward/feedback loop structures of biological networks. Bioinformatics, 27, 2767-2768.
Lee, S.C., Kim, S.J., Han, S.K., An, G. and Kim, S.R. (2017) A gibberellin-stimulated transcript, OsGASR1, controls seedling growth and α-amylase expression in rice. J. Plant Physiol. 214, 116-122.
Liu, H., Wang, S., Yu, X., Yu, J., He, X., Zhang, S., Shou, H. and Wu, P. (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J. 43, 47-56.
Ma, X., Ma, J., Zhai, H., Xin, P., Chu, J., Qiao, Y. and Han, L. (2015) CHR729 is a CHD3 protein that controls seedling development in rice. PLoS ONE, 10, e0138934. https://doi.org/10.1371/journal.pone.0138934.
Mai, C.D., Phung, N.T., To, H.T., Gonin, M., Hoang, G.T., Nguyen, K.L., Do, V.N., Courtois, B. and Gantet, P. (2014) Genes controlling root development in rice. Rice, 7, 30.
Mayer, K. F., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G and Laux, T. (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815.
Mi, H., Muruganujan, A., Casagrande, J.T. and Thomas, P.D. (2013) Large-scale gene function analysis with the PANTHER classification system. Nat. Protoc. 8, 1551-1566.
Ni, J., Zhu, Z., Wang, G., Shen, Y., Zhang, Y. and Wu, P. (2014) Intragenic suppressor of Osiaa23 revealed a conserved Tryptophan residue crucial for protein-protein interactions. PLoS ONE, 9, 1-9.
Orman-Ligeza, B., Parizot, B., Gantet, P.P., Beeckman, T., Bennett, M.J. and Draye, X. (2013) Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci. 18, 459-467.
Pasquali, G., Ouwerkerk, P.B.F. and Memelink, J. (1994) Versatile transformation vectors to assay the promoter activity of DNA elements in plants. Gene, 149, 373-374.
Qiao, H., Yin, Y., Zhao, Y., Zhang, T., Li, R., Xing, J., Yan, L. and Wang, R. (2018) The YUCCA-Auxin-WOX11 module controls crown root development in rice. Front. Plant Sci. 9, 1-10.
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Rogg, L.E., Lasswell, J. and Bartel, B. (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell, 13, 465-480.
Ruffel, S., Krouk, G. and Coruzzi, G.M. (2010) A systems view of responses to nutritional cues in Arabidopsis: toward a paradigm shift for predictive network modeling. Plant Physiol. 152, 445-452.
Ruijter, J.M., Ruiz Villalba, A., Hellemans, J., Untergasser, A. and van den Hoff, M.J.B. (2015) Removal of between-run variation in a multi-plate qPCR experiment. Biomol. Detect. Quantif. 5, 10-14.
Sakai, H., Lee, S.S., Tanaka, T. et al. (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol. 54, e6.
Schindelin, J., Arganda-Carreras, I., Frise, E. et al. (2012) Fiji: an open-source platform for biological-image analysis. Nat. Methods, 9, 676-682.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B.B. and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.
The Gene Ontology Consortium (2000). Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25-29.
Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L.A., Rhee, S.Y. and Stitt, M. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 37, 914-939.
Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z., Xu, W. and Su, Z. (2017) AgriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122-W129.
Töpfer, R., Matzeit, V., Gronenborn, B., Schell, J. and Steinbiss, H.H. (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res. 15, 5890.
Wang, Y.Y., Wang, D., Gan, T. et al. (2016) CRL6, a member of the CHD protein family, is required for crown root development in rice. Plant Physiol. Biochem. 105, 185-194.
Xu, J., Wang, L., Zhou, M. et al. (2017) Narrow albino leaf 1 is allelic to CHR729, regulates leaf morphogenesis and development by affecting auxin metabolism in rice. Plant Growth Regul. 82, 175-186.
Yoo, S.D., Cho, Y.H. and Sheen, J. (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
Zarei, A., Körbes, A.P., Younessi, P., Montiel, G., Champion, A. and Memelink, J. (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol. Biol. 75, 321-331.
Zhang, S., Wang, S., Xu, Y., Yu, C., Shen, C., Qian, Q., Geisler, M., Jiang, D.A. and Qi, Y. (2015) The auxin response factor, OsARF19, controls rice leaf angles through positively regulating OsGH3-5 and OsBRI1. Plant, Cell Environ. 38, 638-654.
Zhao, Y.Y., Hu, Y., Dai, M., Huang, L. and Zhou, D.-X.D. (2009) The WUSCHEL-related homeobox gene WOX11 is required to activate shoot-borne crown root development in rice. Plant Cell Online, 21, 736-748.
Zhao, C., Xu, J., Chen, Y., Mao, C., Zhang, S., Bai, Y., Jiang, D. and Wu, P. (2012) Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll. Planta, 236, 1165-1176.
Zhao, Y., Cheng, S., Song, Y., Huang, Y., Zhou, S., Liu, X. and Zhou, D.-X. (2015) The interaction between Rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell, 27, 2469-2483.
Zhou, S., Jiang, W., Long, F., Cheng, S., Yang, W., zhao, Y. and Zhou, D.-X. (2017) Rice homeodomain protein WOX11 recruits a histone acetyltransferase complex to establish programs of cell proliferation of crown root meristem. Plant Cell, 29, 1088-1104.

Auteurs

Jérémy Lavarenne (J)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.
Centre de Recherches de Chappes, Biogemma, Route d'Ennezat, 63720, Chappes, France.

Mathieu Gonin (M)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Soazig Guyomarc'h (S)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Jacques Rouster (J)

Centre de Recherches de Chappes, Biogemma, Route d'Ennezat, 63720, Chappes, France.

Antony Champion (A)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Christophe Sallaud (C)

Centre de Recherches de Chappes, Biogemma, Route d'Ennezat, 63720, Chappes, France.

Laurent Laplaze (L)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Pascal Gantet (P)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Mikaël Lucas (M)

UMR DIADE, Université de Montpellier, IRD, 911 Avenue Agropolis, 34394, Montpellier Cedex 5, France.

Articles similaires

Databases, Protein Protein Domains Protein Folding Proteins Deep Learning
Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Arabidopsis Arabidopsis Proteins Osmotic Pressure Cytoplasm RNA, Messenger

Classifications MeSH