AtERF#111/ABR1 is a transcriptional activator involved in the wounding response.
Abscisic Acid
/ metabolism
Arabidopsis
/ drug effects
Arabidopsis Proteins
/ genetics
Droughts
Gene Expression Regulation, Plant
/ drug effects
Gene Ontology
Phenotype
Plant Leaves
/ genetics
Plant Roots
/ genetics
Plant Shoots
/ genetics
Plants, Genetically Modified
Promoter Regions, Genetic
Proteasome Endopeptidase Complex
/ metabolism
RNA-Seq
Stress, Physiological
/ genetics
Transcription Factors
/ genetics
Ubiquitin-Protein Ligases
/ genetics
Ubiquitination
Arabidopsis thaliana
ERF/AP2 transcription factors
PRT6 N-degron pathway
abscisic acid
hypoxia
submergence
wounding
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
12 2019
Historique:
received:
10
07
2019
revised:
24
07
2019
accepted:
29
07
2019
pubmed:
7
8
2019
medline:
31
7
2020
entrez:
7
8
2019
Statut:
ppublish
Résumé
AtERF#111/ABR1 belongs to the group X of the ERF/AP2 transcription factor family (GXERFs) and is shoot specifically induced under submergence and hypoxia. It was described to be an ABA-response repressor, but our data reveal a completely different function. Surprisingly, AtERF#111 expression is strongly responsive to wounding stress. Expression profiling of ERF#111-overexpressing (OE) plants, which show morphological phenotypes like increased root hair length and number, strengthens the hypothesis of AtERF#111 being involved in the wounding response, thereby acting as a transcriptional activator of gene expression. Consistent with a potential function outside of oxygen signalling, we could not assign AtERF#111 as a target of the PRT6 N-degron pathway, even though it starts with a highly conserved N-terminal Met-Cys (MC) motif. However, the protein is unstable as it is degraded in an ubiquitin-dependent manner. Finally, direct target genes of AtERF#111 were identified by microarray analyses and subsequently confirmed by protoplast transactivation assays. The special roles of diverse members of the plant-specific GXERFs in coordinating stress signalling and wound repair mechanisms have been recently hypothesized, and our data suggest that AtERF#111 is indeed involved in these processes.
Substances chimiques
ABR1 protein, Arabidopsis
0
Arabidopsis Proteins
0
Transcription Factors
0
Abscisic Acid
72S9A8J5GW
PRT6 protein, Arabidopsis
EC 2.3.2.27
Ubiquitin-Protein Ligases
EC 2.3.2.27
Proteasome Endopeptidase Complex
EC 3.4.25.1
Banques de données
GENBANK
['GSE48949', 'GSE42290', 'GSE121587']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
969-990Informations de copyright
© 2019 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Alfieri, L., Bisselink, B., Dottori, F., Naumann, G., de Roo, A., Salamon, P., Wyser, K. and Feyen, L. (2017) Global projections of river flood risk in a warmer world. Earths Future, 5, 171-182.
Bailey-Serres, J. and Voesenek, L.A.C.J. (2008) Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313-339.
Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F., Perata, P., Voesenek, L.A.C.J. and van Dongen, J.T. (2012) Making sense of low oxygen sensing. Trends Plant Sci. 17, 129-138.
Bhargava, A., Clabaugh, I., To, J.P., Maxwell, B.B., Chiang, Y.-H., Schaller, G.E., Loraine, A. and Kieber, J.J. (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 162, 272-294.
Birkenbihl, R.P., Kracher, B. and Somssich, I.E. (2017) Induced genome-wide binding of three Arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell, 29, 20-38.
Branco-Price, C., Kaiser, K.A., Jang, C.J.H., Larive, C.K. and Bailey-Serres, J. (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56, 743-755.
Bui, L.T., Giuntoli, B., Kosmacz, M., Parlanti, S. and Licausi, F. (2015) Constitutively expressed ERF-VII transcription factors redundantly activate the core anaerobic response in Arabidopsis thaliana. Plant Sci. 236, 37-43.
Cai, X.-T., Xu, P., Zhao, P.-X., Liu, R., Yu, L.-H. and Xiang, C.-B. (2014) Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat. Commun. 5, 5833.
Cho, H.-T. and Cosgrove, D.J. (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell, 14, 3237-3253.
Choi, D., Cho, H.-T. and Lee, Y. (2006) Expansins: expanding importance in plant growth and development. Physiol. Plant. 126, 511-518.
Choy, M.-K., Sullivan, J.A., Theobald, J.C., Davies, W.J. and Gray, J.C. (2008) An Arabidopsis mutant able to green after extended dark periods shows decreased transcripts of seed protein genes and altered sensitivity to abscisic acid. J. Exp. Bot. 59, 3869-3884.
Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
Cosgrove, D.J. (2000) Loosening of plant cell walls by expansins. Nature, 407, 321-326.
Curtis, M.D. and Grossniklaus, U. (2003) A Gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469.
Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R. and Abrams, S.R. (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61, 651-679.
Dissmeyer, N. (2019) Conditional protein function via N-degron pathway-mediated proteostasis in stress physiology. Annu. Rev. Plant Biol. 70, 83-117.
Dissmeyer, N., Rivas, S. and Graciet, E. (2018) Life and death of proteins after protease cleavage: protein degradation by the N-end rule pathway. New Phytol. 218, 929-935.
Dolan, L., Ducket, C.M., Grierson, C., Linstead, P., Schneider, K., Lawson, E., Dean, C., Poethig, S. and Roberts, K. (1994) Clonal relationships and cell patterning of the root epidermis of Arabidopsis. Development, 2465-2474.
Ehlert, A., Weltmeier, F., Wang, X., Mayer, C.S., Smeekens, S., Vicente-Carbajosa, J. and Dröge-Laser, W. (2006) Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J. 46, 890-900.
Finkelstein, R.R., Gampala, S.S.L. and Rock, C.D. (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell, 14, S15-S45.
Fukao, T., Yeung, E. and Bailey-Serres, J. (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell, 23, 412-427.
Gasch, P., Fundinger, M., Müller, J. T., Lee, T., Bailey-Serres, J., Mustroph, A. (2016) Redundant ERF-VII transcription factors bind to an evolutionarily conserved cis-motif to regulate hypoxia-responsive gene expression in Arabidopsis. Plant Cell, 28, 160-180.
Gelhaye, E., Rouhier, N., Navrot, N. and Jacquot, J.P. (2005) The plant thioredoxin system. Cell. Mol. Life Sci. 62, 24-35.
Gibbs, D.J., Lee, S.C., Isa, N.M. et al. (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479, 415-418.
Gibbs, D.J., Md Isa, N., Movahedi, M. et al. (2014) Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol. Cell, 53, 369-379.
Gibbs, D.J., Bailey, M., Tedds, H.M. and Holdsworth, M.J. (2016) From start to finish: amino-terminal protein modifications as degradation signals in plants. New Phytol. 211, 1188-1194.
Gibbs, D.J., Tedds, H.M., Labandera, A.-M. et al. (2018) Oxygen-dependent proteolysis regulates the stability of angiosperm polycomb repressive complex 2 subunit VERNALIZATION 2. Nat. Commun. 9, 5438.
Graciet, E., Walter, F., Ó’Maoiléidigh, D.S., Pollmann, S., Meyerowitz, E.M., Varshavsky, A. and Wellmer, F. (2009) The N-end rule pathway controls multiple functions during Arabidopsis shoot and leaf development. Proc. Natl Acad. Sci. USA, 106(32), 13618-13623.
Ha, C.V., Leyva-González, M.A., Osakabe, Y. et al. (2014) Positive regulatory role of strigolactone in plant responses to drought. Proc. Natl Acad. Sci. USA, 111, 851-856.
Heyman, J., Cools, T., Vandenbussche, F. et al. (2013) ERF115 controls root quiescent center cell division and stem cell replenishment. Science, 342, 860-863.
Heyman, J., Cools, T., Canher, B. et al. (2016) The heterodimeric transcription factor complex ERF115-PAT1 grants regeneration competence. Nat. Plants, 2, 16165.
Heyman, J., Canher, B., Bisht, A., Christiaens, F. and De Veylder, L. (2018) Emerging role of the plant ERF transcription factors in coordinating wound defense responses and repair. J. Cell Sci. 131, pii: jcs208215.
Hirabayashi, Y., Kanae, S., Emori, S., Oki, T. and Kimoto, M. (2008) Global projections of changing risks of floods and droughts in a changing climate. Hydrol. Sci. J. 53, 754-772.
Hirabayashi, Y., Mahendran, R., Koirala, S., Konoshima, L., Yamazaki, D., Watanabe, S., Kim, H. and Kanae, S. (2013) Global flood risk under climate change. Nat. Clim. Chang. 3, 816-821.
Holman, T.J., Jones, P.D., Russell, L. et al. (2009) The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 4549-4554.
Horan, K., Jang, C., Bailey-Serres, J., Mittler, R., Shelton, C., Harper, J.F., Zhu, J.K., Cushman, J.C., Gollery, M. and Girke, T. (2008) Annotating genes of known and unknown function by large-scale coexpression analysis. Plant Physiol. 147, 41-57.
Hsu, F.C., Chou, M.Y., Chou, S.J., Li, Y.R., Peng, H.P. and Shih, M.C. (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. Plant Cell, 25, 2699-2713.
Ikeuchi, M., Iwase, A., Rymen, B. et al. (2017) Wounding Triggers Callus Formation via Dynamic Hormonal and Transcriptional Changes. Plant Physiology, 175, 1158-1174.
Karimi, M., de Meyer, B. and Hilson, P. (2005) Modular cloning in plant cells. Trends Plant Sci. 10, 103-105.
Klecker, M., Gasch, P., Peisker, H., Dörmann, P., Schlicke, H., Grimm, B. and Mustroph, A. (2014) A shoot-specific hypoxic response of Arabidopsis sheds light on the role of the phosphate-responsive transcription factor PHOSPHATE STARVATION RESPONSE1. Plant Physiol. 165, 774-790.
Koncz, C., Kreuzaler, F., Kalman, Z. and Schell, J. (1984) A simple method to transfer, integrate and study expression of foreign genes, such as chicken ovalbumin and alpha-actin in plant tumors. EMBO J. 3, 1029-1037.
Laloi, C., Mestres-Ortega, D., Marco, Y., Meyer, Y. and Reichheld, J.-P. (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol. 134, 1006-1016.
Lee, S.C., Mustroph, A., Sasidharan, R., Vashisht, D., Pedersen, O., Oosumi, T., Voesenek, L.A. and Bailey-Serres, J. (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol. 190(2), 457-471.
León, J., Rojo, E. and Sánchez-Serrano, J.J. (2001) Wound signalling in plants. J. Exp. Bot. 52, 1-9.
Licausi, F., Kosmacz, M., Weits, D.A., Giuntoli, B., Giorgi, F.M., Voesenek, L.A., Perata, P. and van Dongen, J.T. (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature, 479, 419-422.
Lin, C.C., Chao, Y.T., Chen, W.C. et al. (2019) Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. Proc. Natl Acad. Sci. USA, 116, 3300-3309.
Liu, Y., Ji, X., Zheng, L., Nie, X. and Wang, Y. (2013) Microarray analysis of transcriptional responses to abscisic acid and salt stress in Arabidopsis thaliana. Int. J. Mol. Sci. 14, 9979-9998.
Lorang, J., Kidarsa, T., Bradford, C.S., Gilbert, B., Curtis, M., Tzeng, S.C., Maier, C.S. and Wolpert, T.J. (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science, 338, 659-662.
Matsuo, M., Johnson, J.M., Hieno, A. et al. (2015) High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots. Mol. Plant, 8, 1253-1273.
Meyer, Y., Vignols, F. and Reichheld, J.P. (2002) Classification of plant thioredoxins by sequence similarity and intron position. Methods Enzymol. 347, 394-402.
Müller, M. and Schmidt, W. (2004) Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol. 134, 409-419.
Mustroph, A., Zanetti, M.E., Jang, C.J., Holtan, H.E., Repetti, P.P., Galbraith, D.W., Girke, T. and Bailey-Serres, J. (2009) Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc. Natl Acad. Sci. USA, 106, 18843-18848.
Mustroph, A., Lee, S.C., Oosumi, T., Zanetti, M.E., Yang, H., Ma, K., Yaghoubi-Masihi, A., Fukao, T. and Bailey-Serres, J. (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol. 152, 1484-1500.
Nakano, T., Suzuki, K., Fujimura, T. and Shinshi, H. (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140, 411-432.
Nishiyama, R., Watanabe, Y., Leyva-Gonzalez, M.A. et al. (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc. Natl Acad. Sci. USA, 110, 4840-4845.
Pacifici, E., Polverari, L. and Sabatini, S. (2015) Plant hormone cross-talk: the pivot of root growth. J. Exp. Bot. 66, 1113-1121.
Pacifici, E., Di Mambro, R., Dello Ioio, R., Costantino, P. and Sabatini, S. (2018) Acidic cell elongation drives cell differentiation in the Arabidopsis root. EMBO J. 37, pii: e99134.
Pandey, G.K., Grant, J.J., Cheong, Y.H., Kim, B.G., Li, L. and Luan, S. (2005) ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiol. 139, 1185-1193.
Pandey, S.P., Roccaro, M., Schön, M., Logemann, E. and Somssich, I.E. (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J. 64, 912-923.
Park, S.Y., Fung, P., Nishimura, N. et al. (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068-1071.
Reichheld, J.-P., Mestres-Ortega, D., Laloi, C. and Meyer, Y. (2002) The multigenic family of thioredoxin h in Arabidopsis thaliana: specific expression and stress response. Plant Physiol. Biochem. 40, 685-690.
Riber, W., Müller, J.T., Visser, E.J., Sasidharan, R., Voesenek, L.A. and Mustroph, A. (2015) The greening after extended darkness1 is an N-end rule pathway mutant with high tolerance to submergence and starvation. Plant Physiol. 167, 1616-1629.
Sah, S.K., Reddy, K.R. and Li, J. (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7, 571.
Sasidharan, R., Hartman, S., Liu, Z., Martopawiro, S., Sajeev, N., van Veen, H., Yeung, E. and Voesenek, L.A.C.J. (2018) Signal dynamics and interactions during flooding stress. Plant Physiol. 176, 1106-1117.
Seki, M., Ishida, J., Narusaka, M. et al. (2002) Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr. Genomics, 2, 282-291.
Song, L., Huang, S.C., Wise, A., Castanon, R., Nery, J.R., Chen, H., Watanabe, M., Thomas, J., Bar-Joseph, Z. and Ecker, J.R. (2016) A transcription factor hierarchy defines an environmental stress response network. Science, 354, pii: aag1550.
Stahl, D.J., Kloos, D.U. and Hehl, R. (2004) A sugar beet chlorophyll a/b binding protein promoter void of G-box like elements confers strong and leaf specific reporter gene expression in transgenic sugar beet. BMC Biotechnol. 4, 31.
Sweat, T.A. and Wolpert, T.J. (2007) Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell, 19, 673-687.
Tsai, K.J., Lin, C.Y., Ting, C.Y. and Shih, M.C. (2014) Ethylene plays an essential role in the recovery of Arabidopsis during post-anaerobiosis reoxygenation. Plant, Cell Environ. 37, 2391-2405.
van Veen, H., Vashisht, D., Akman, M. et al. (2016) Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress. Plant Physiol. 172, 668-689.
Vicente, J., Mendiondo, G.M., Movahedi, M. et al. (2017) The Cys-Arg/N-end rule pathway is a general sensor of abiotic stress in flowering plants. Curr. Biol. 27, 3183-3190.e4.
Vicente, J., Mendiondo, G.M., Pauwels, J. et al. (2018) Distinct branches of the N-end rule pathway modulate the plant immune response. New Phytol. https://doi.org/10.1111/nph.15387.
Walton, A., Stes, E., Cybulski, N. et al. (2016) It's time for some “site”-seeing: novel tools to monitor the ubiquitin landscape in Arabidopsis thaliana. Plant Cell, 28, 6-16.
Wang, Z., Cao, G., Wang, X., Miao, J., Liu, X., Chen, Z., Qu, L.J. and Gu, H. (2008) Identification and characterization of COI1-dependent transcription factor genes involved in JA-mediated response to wounding in Arabidopsis plants. Plant Cell Rep. 27, 125-135.
Wang, C., Ding, Y., Yao, J., Zhang, Y., Sun, Y., Colee, J. and Mou, Z. (2015) Arabidopsis Elongator subunit 2 positively contributes to resistance to the necrotrophic fungal pathogens Botrytis cinerea and Alternaria brassicicola. Plant J. 83, 1019-1033.
Wehner, N., Hartmann, L., Ehlert, A., Böttner, S., Oñate-Sánchez, L. and Dröge-Laser, W. (2011) High-throughput protoplast transactivation (PTA) system for the analysis of Arabidopsis transcription factor function. Plant J. 68, 560-569.
Weits, D.A., Giuntoli, B., Kosmacz, M., Parlanti, S., Hubberten, H.M., Riegler, H., Hoefgen, R., Perata, P., van Dongen, J.T. and Licausi, F. (2014) Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat. Commun. 5, 3425.
Weits, D.A., Kunkowska, A.B., Kamps, N.C.W. et al. (2019) An apical hypoxic niche sets the pace of shoot meristem activity. Nature, 569, 714-717.
White, M.D., Klecker, M., Hopkinson, R.J. et al. (2017) Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nat. Commun. 8, 14690.
White, M.D., Kamps, J.J.A.G., East, S., Taylor Kearney, L.J. and Flashman, E. (2018) The plant cysteine oxidases from Arabidopsis thaliana are kinetically tailored to act as oxygen sensors. J. Biol. Chem. 293, 11786-11795.
Wu, F.-H., Shen, S.-C., Lee, L.-Y., Lee, S.-H., Chan, M.-T. and Lin, C.-S. (2009) Tape-Arabidopsis Sandwich - a simpler Arabidopsis protoplast isolation method. Plant Methods, 5, 16.
Yeung, E., van Veen, H., Vashisht, D. et al. (2018) A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 115, E6085-E6094.
Yoshida, S., Ito, M., Callis, J., Nishida, I. and Watanabe, A. (2002) A delayed leaf senescence mutant is defective in arginyl-tRNA: protein arginyltransferase, a component of the N-end rule pathway in Arabidopsis. Plant J. 32, 129-137.