Overexpression of ZmNF-YC14 confers plant ER stress tolerance and ABA sensitivity in Arabidopsis

• Autorzy: Wang L. , Mei X. , Nan J. , Liu C. , Zhou L. , Cai Y.
• Języki publikacji: EN

Abstrakty

EN

The correct folding of proteins in the endoplasmic reticulum (ER) is vital for plant adaptation to adverse environmental conditions. The genes related to the ER stress response in maize are far from clear. In this study, a maize nuclear factor, NF-YC14, was identified in the regulation of the ER stress response. Overexpression of NF-YC14 improves plant ER stress tolerance and up-regulates the expression of downstream ER stress response genes. Moreover, NF-YC14 involves abscisic acid (ABA) signaling and overexpression of NF-YC14 confers plant hypersensitivity to ABA. Furthermore, overexpression of NF-YC14 enhances the expression of downstream ER stress response genes mediated by the ABA signaling pathway in Arabidopsis. These results indicate that NF-YC14 and ABA signaling regulate the expression of ER stress response genes and NF-YC14 links ER stress response to ABA signaling.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2019
• Tom: 41
• Numer: 08
• Opis fizyczny: Article 138 [9p.], fig.,ref.

Twórcy

autor

Wang L.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

autor

Mei X.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

autor

Nan J.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

autor

Liu C.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

autor

Zhou L.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

autor

Cai Y.

• College of Agronomy and Biotechnology, Southwest University, Tiansheng Road, No. 2, Beibei District, Chongqing 400715 China

Bibliografia

• Alvim FC, Carolino SMB, Cascardo JCM, Nunes CC, Martinez CA, Otoni WC, Fontes EPB (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water stress. Plant Physiol 126:1042–1054
• Cagliari A, Turchetto-Zolet AC, Maraschin FS, Loss G, Margis R, Margis-Pinheiro M (2011) The evolutionary history of CBF transcription factors: gene duplication of CCAAT-binding factors NF-Y in plants. Gene Duplication, Intech
• Chen M, Zhao Y, Zhuo C, Lu S, Guo Z (2015) Overexpression of a NF-YC transcription factor from Bermudagrass confers tolerance to drought and salinity in transgenic rice. Plant Biotech J 13:482–491
• Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679
• Demir F, Horntrich C, Blachutzik JO, Scherzer S, Reinders Y, Kierszniowska S, Schulze WX, Harms GS, Hedrich R, Geiger D, Kreuzer I (2013) Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci USA 110:8296–8301
• Deng Y, Humbert S, Liu J, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108:7247–7252
• Fujita M, Mizukado S, Fujita Y, Ichikawa T, Nakazawa M, Seki M, Matsui M, Yamaguchi-Shinozaki K, Shinozaki K (2007) Identification of stress-tolerance-related transcription-factor genes via mini-scale full-length cDNA over-eXpressor (FOX) gene hunting system. Biochem Biophys Res Commun 364:250–257
• Gao H, Brandizzi F, Benning C, Larkin RM (2008) A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:16398–16403
• Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheld KA, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430
• Geiger D, Maierhofer T, AL-Rasheid KAS, Scherzer S, Mumm P, Liese P, Ache P, Wellmann C, Marten I, Grill E, Romeis T, Hedrich R (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4:ra32
• Han X, Tang S, An Y, Zheng D, Xia X, Yin W (2013) Overexpression of the poplar NF-YB7 transcription factor confers drought tolerance and improves water-use efficiency in Arabidopsis. J Exp Bot 64:4589–4601
• Hauser F, Waadt R, Schroeder Julian I (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:R346–R355
• Hayashi S, Wakasa Y, Takahashi H, Kawakatsu T, Takaiwa F (2012) Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. Plant J 69:946–956
• Higaki T, Hashimoto-Sugimoto M, Akita K, Iba K, Hasezawa S (2014) Dynamics and environmental responses of PATROL1 in Arabidopsis subsidiary cells. Plant Cell Physiol 55:773–780
• Hoagland D (1950) D. I. Arnon. The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359
• Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477–499
• Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20:3107–3121
• Kovalchuk N, Jia W, Eini O, Morran S, Pyvovarenko T, Fletcher S, Bazanova N, Harris J, Beck-Oldach K, Shavrukov Y, Langridge P, Lopato S (2013) Optimization of TaDREB3 gene expression in transgenic barley using cold-inducible promoters. Plant Biotech J 11:659–670
• Lee KPK, Dey M, Neculai D, Cao C, Dever TE, Sicheri F (2008) Structure of the dual enzyme IRE1 reveals the basis for catalysis and regulation in nonconventional RNA splicing. Cell 132:89–100
• Lee SC, Lan W-Z, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106:21419–21424
• Li Y, Humbert S, Howell SH (2012) ZmbZIP60 mRNA is spliced in maize in response to ER stress. BMC Res Notes 5:144
• Liu J, Howell SH (2010a) bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell 22:782–796
• Liu J, Howell SH (2010b) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942
• Liu J, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119
• Liu J, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909
• Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X (2016) The NF-YC-RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun 7:12768
• Lu S, Yang Z, Sun L, Sun L, Song Z, Liu J (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 5:504–514
• Mei X, Li P, Wang L, Liu C, Zhou L, Cai Y (2018) Molecular and functional characterization of ZmNF-YC14 in transgenic Arabidopsis. J Plant Biol 61:410–423
• Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Müller A, Giraudat J, Leung J (2007) Constitutive activation of a plasma membrane H⁺-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J 26:3216–3226
• Nagashima Y, Mishiba K-i, Suzuki E, Shimada Y, Iwata Y, Koizumi N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1:29
• Petroni K, Kumimoto RW, Gnesutta N, Calvenzani V, Fornari M, Tonelli C, Holt BF, Mantovani R (2012) The promiscuous life of plant nuclear factor Y transcription factors. Plant Cell 24:4777–4792
• Planes MD, Ninoles R, Rubio L, Bissoli G, Bueso E, Garcia-Sanchez MJ, Alejandro S, Gonzalez-Guzman M, Hedrich R, Rodriguez PL, Fernandez JA, Serrano R (2015) A mechanism of growth inhibition by abscisic acid in germinating seeds of Arabidopsis thaliana based on inhibition of plasma membrane H⁺-ATPase and decreased cytosolic pH, K⁺, and anions. J Exp Bot 66:813–825
• Rodriguez L, Gonzalez-Guzman M, Diaz M, Rodrigues A, Izquierdo-Garcia AC, Peirats-Llobet M, Fernandez MA, Antoni R, Fernandez D, Marquez JA, Mulet JM, Albert A, Rodriguez PL (2014) C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis. Plant Cell 26:4802–4820
• Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529
• Sato A, Gambale F, Dreyer I, Uozumi N (2010) Modulation of the Arabidopsis KAT1 channel by an activator of protein kinase C in Xenopus laevis oocytes. FEBS J 277:2318–2328
• Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223
• Sidrauski C, Walter P (1997) The transmembrane kinase IRE1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1031–1039
• Tajima H, Iwata Y, Iwano M, Takayama S, Koizumi N (2008) Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response. Biochem Biophys Res Commun 374:242–247
• Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53:144–153
• Valente MAS, Faria JAQA, Soares-Ramos JRL, Reis PAB, Pinheiro GL, Piovesan ND, Morais AT, Menezes CC, Cano MAO, Fietto LG, Loureiro ME, Aragão FJL, Fontes EPB (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J Exp Bot 60:533–546
• Vitale A, Boston RS (2008) Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9:1581–1588
• Yang Y, Lv W, Li M, Wang B, Sun D, Deng X (2013) Maize membrane-bound transcription factor Zmbzip17 is a key regulator in the cross-talk of ER quality control and ABA signaling. Plant Cell Physiol 54:2020–2033
• Yang Z, Wang M, Sun L, Lu S, Bi D, Sun L, Song Z, Zhang S, Zhou S, Liu J (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10(3):e1004243
• Yang M, Zhao Y, Shi S, Du X, Gu J, Xiao K (2017) Wheat nuclear factor Y (NF-Y) B subfamily gene TaNF-YB3;l confers critical drought tolerance through modulation of the ABA-associated signaling pathway. Plant Cell Tiss Org 128:97–111
• Ye C, Dickman MB, Whitham SA, Payton M, Verchot J (2011) The unfolded protein response is triggered by a plant viral movement protein. Plant Physiol 156:741–755

Identyfikatory

DOI

10.1007/s11738-019-2922-x