Plants are constantly subjected to adverse environmental conditions, such as extremes of temperature, cold, salinity and drought. As a consequence, plant cells have developed coordinated and integrated mechanisms that respond to these injuries and are immediately activated upon stresses. To cope with the stress, cell signaling pathways are activated and promote up or down regulation of specific genes, which minimize the deleterious effect of stresses within the cell. The endoplasmic reticulum (ER) is a key signaling organelle involved in the activation of cellular stress responses in eukaryotic cells. One such well-characterized signaling event is the unfolded protein response (UPR), which is activated to cope with the disruption of ER homeostasis that results in the accumulation of unfolded or misfolded proteins in the lumen of the organelle. Upon disruption of ER homeostasis, plant cells activate at least two branches of the unfolded protein response (UPR) through IRE1-like (Inositol-Requiring Enzyme 1) and ATF6-like (Activating Transcription factor 6) transducers, resulting in the up-regulation of ER-resident molecular chaperones and the activation of the ER-associated degradation protein system. However, if ER stress is sustained, an apoptotic pathway is activated. Persistent ER stress has been shown to trigger both ER-stress specific apoptotic pathways and shared PCD (programmed cell death) signaling pathways elicited by other death stimuli. One plant-specific, ER stress-shared response is the ER and osmotic stress-integrated signaling, which converges on N-rich proteins (NRPs) to transduce a cell death signal. NRP-mediated cell death signaling is a distinct, plant-specific branch of the ER stress pathway that has been shown to integrate the ER and osmotic stress signals into a full response. This ER- and osmotic-stress induced cell death signaling pathway has been uncovered in soybean and constitutes the major focus of this chapter. A second cell death pathway induced by ER stress has been shown to be mediated by the G protein in Arabidopsis, but it remains to be determined whether it operates in soybean as well.
2. ER stress response: The cytoprotective unfolded protein response
The ER is a highly dynamic organelle, which mediates several cellular functions, such as the folding and post-translational modification of secretory proteins and protein quality control in addition to maintaining Ca2+ homeostasis (Schröder 2008). The loading of unfolded protein in the lumen of ER for maturation is tightly controlled and dependent on the cellular requirements. Under stress conditions, the folding capacity of the ER can be overloaded causing the accumulation of unfolded proteins and disruption of cellular homeostasis (Xu, Bailly-Maitre & Reed 2005). To cope with this stress condition, eukaryotic cells evolved a sophisticated signaling mechanism referred to as unfolded protein response (UPR; Malhotra and Kaufman., 2007). In mammalian cells, the UPR is transduced through three distinct ER-transmembrane sensors: PERK (protein kinase RNA-like ER kinase), Ire1 (inositol-requiring enzyme-1) and the basic leucine zipper transcription factor ATF6 (activating transcription factor-6; Ron and Walter, 2007; Malhotra and Kaufman, 2007, Kapoor and Sanyal, 2009). The activation of the UPR allows the ER processing and folding capacities to be balanced with protein loading into the lumen of the organelle under conditions of ER stress (Malhotra and Kaufman, 2007). This balance is achieved by (i) shutting down protein synthesis via PERK activation, (ii) up-regulating the expression of ER-resident processing proteins, such as molecular chaperones and foldases, via activation of Ire1 and ATF6, and (iii) inducing the ER-associated protein degradation (ERAD) machinery, through activation of Ire1, which mediates the targeting and subsequent degradation of unfolded proteins by the proteosome. However, if the ER stress is sustained, multiple apoptotic pathways can be activated in mammalian cells.
In plants, the UPR seems to operate as a bipartite module, as the ER stress signal is transduced through homologs of the Ire1 and ATF6 transducers, but a PERK-mediated branch of the UPR has not been shown (Urade 2009; Chen and Brandizzi., 2012). Two components of the Ire1-mediaded branch of the UPR is known. The first one is the Ire1 ortholog that is represented by two copies in the Arabidopsis genome, Ire1a and Ire1b, and one copy, OsIre1, in the rice genome. Like the mammalian counterpart, plant Ire1 is associated with the ER membrane and exhibits ribonuclease activity and autophosphorylation activities, as shown for Ire1a, Ire1b and OsIre1(Koizumi et al., 2001; Okushima et al., 2002). The second component is ER membrane-associated transcription factor bZIP60. Upon ER stress, bZIP60 mRNA is spliced in an IRE1-mediated process to generate an alternatively spliced transcript that lacks the transmembrane domain-encoding sequences (Liu et al., 2007 e 2008 ; Deng et al., 2011; Nagashima et al., 2011). This splicing leads to the synthesis of a soluble and functional bZIP60 transfactor that can be translocated to the nucleus, where it activates ER stress inducible promoters, such as the BiP3 promoter. Likewise, OsbZIP74 or OsbZIP50 from rice, an ortholog of Arabidopsis AtbZIP60, is regulated through the IRE1-mediated splicing of its RNA to render the activation of ER stress-inducible promoters (Hayashi et al., 2011; Lu et al., 2011).
The second branch of UPR in plants mechanistically resembles the ATF6-mediated transduction of the ER stress signal. Upon ER stress, the membrane-associated Arabidopsis ATF6 homologs bZIP17 and bZIP28 are relocated to the Golgi, where their transcriptional domains are proteolytically released from the membrane by SP2 (Tajima et al., 2008: Che et al., 2010). The released bZIP domain of these transfactors is then translocated to the nucleus, where it acts in concert with the heterotrimeric NF-Y complex to activate UPR genes (Liu e Howel., 2010). The NF-Y complex is composed the transcriptional factors NF-YA4, NF-YB3 and NF-YC2.
Comprehensive genome-wide evaluations of ER stress-induced changes in gene expression have provided evidence that the UPR operates in a similar fashion in both soybean and Arabidopsis (Irsigler et al., 2007). Inducers of ER stress, such as tunicamycin and AZC, promote the up-regulation of a class of genes that functions in protein folding and ERAD. In the protein folding category, the up-regulated genes include ER-resident molecular chaperones such as BiP, calreticulin, calnexin, and the folding catalyst protein disulfide isomerase (PDI). ERAD-associated genes that are up-regulated by ER stress in soybean include those encoding polyubiquitin, ubiquitin conjugating enzyme, the alpha subunit of the proteasome, CDC48 and Derlin. These genomic analyses suggested that soybean, like Arabidopsis, have evolved at least two different mechanisms that mediate UPR: (i) transcriptional induction of genes encoding chaperones and vesicle trafficking proteins and (ii) upregulation of the ER-associated protein degradation (ERAD) system for rapid disposal of unfolded proteins in the ER as a protective measure.
In addition to the cytoprotective bipartite response to ER stress in plants, two apparently distinct branches of the ER stress-induced pathways have been shown to transduce a cell death signal: (i) the ER membrane associated Gβ-Gγ heterodimer-mediated signaling events that trigger UPR-associated cell death in
3. The ER-stress-induced NRP-mediated cell death response
NRP-mediated cell death signaling is a distinct, plant-specific branch of the ER stress pathway that has been uncovered in soybean and has been shown to integrate the ER and osmotic stress signals into a full response. This integrative pathway was first identified through genome-wide approaches and expression profiling, which revealed the existence of a modest overlap of the ER and osmotic stress-induced transcriptomes in soybean seedlings treated with PEG (an inducer of osmotic stress) or tunicamycin and AZC (potent inducers of ER stress; Irsigler et al., 2007). The co-regulated genes were first considered to be downstream targets of the integrated pathway based on similar induction kinetics and a synergistic response to the combination of osmotic and ER stress-inducing treatments. Based on these criteria, the selected downstream components of this ER and osmotic stress response-integrating pathway encode proteins with diverse roles, such as plant-specific development and cell death (DCD) domain-containing proteins (NRP-A and NRP-B), an ubiquitin-associated (UBA) protein homolog and NAC domain-containing proteins (GmNAC6). Among them, NRP-A and NRP-B were the first ones to be characterized and to show to induce a cell death response when ectopically expressed in tobacco leaves or soybean protoplasts (Costa et al., 2008). As a consequence, the ER and osmotic stress response-integrating pathway has been designated as the NRP-mediated cell death response.
An upstream component of the NRP-mediated cell death response, GmERD15 (
3.1. GmERD15 is a ssDNA binding transcriptional activator
The Early Responsive Dehydration (ERD) genes are rapidly induced in response to water deficit and form a family comprised by ERD1 to ERD16 representatives. The ERD encoded proteins exhibit diverse and heterogeneous biochemical functions and fall into different classes of proteins, such as chloroplast ATP-dependent protease (ERD1), cytosolic HSP70 (ERD2), glutationa-S-transferases (ERD9,ERD11, ERD13) among others (Soitano et al., 2008; Kiyosue et al., 1994; Kiyosue et al., 1993). ERD15 was first identified in Arabidopsis as a hydrophilic protein that possesses a PAM2 domain that interacts with polyA-binding proteins (PABP11; Kiyosue et al., 1994; Kariola et al., 2006)., ERD15 has been shown to function as a negative regulator of the abcisic acid (ABA)-mediated response (Kariola et al., 2006). Overexpression of ERD15 reduces the ABA sensitivity of Arabidopsis, whereas silencing of ERD15 by RNAi promotes hypersensitivity to the hormone. The negative effect of ERD15 on ABA signaling enhances salicylic acid-dependent defense because overexpression of ERD15 was associated with increased resistance to the bacterial necrotroph Erwiniacarotovora, and the enhanced induction of marker genes for systemic acquired resistance. These results are consistent with the observed antagonistic effect of ABA on salicylic acid-mediated defense and may implicate ERD15 as a shared component of these responses.
The soybean GmERD15 homolog has been described as a new ER stress- and osmotic stress-induced transcription factor that binds to the promoter and induces the expression of the NRP-B gene. In fact, GmERD15 was isolated by its capacity to associate stably with the promoter of NRP-B in yeast cells using the one-hybrid system (Alves et al., 2011). The GmERD15 binding site in the NRP-B promoter was mapped to a 12-bp palindromic sequence (511 AGCAnnnnTGCT -500) that resembles binding sites for ssDNA binding proteins, such as NF1C and PBF2 that recognize the sequences -TTGGCnnnnnGCCAA-3' and 5- TGACAnnnnTGTCA-3’, respectively (Wang and Kiledjian., 2000). Furthermore, GmERD15 is located in the nucleus, and chromatin immunoprecipitation (ChIP) assays revealed that it binds to the NRP-B promoter in vivo (Alves et al., 2011). The ectopic expression of GmERD15 in soybean cells activates the NRP-B promoter and induces NRP-B expression. Collectively, these results indicate that GmERD15 functions as an upstream component of the NRP-mediated cell death signaling pathway that is induced by ER stress and osmotic stress
3.2. NRPs: Molecular and functional characterization
The N Rich Protein (NRP) gene was first identified by its rapid induction in response to pathogen incompatible interactions in soybean (Ludwig and Tenhaken, 2001). The NRP designation was derived from its high content of asparagine residue, about 25 %. NRP is represented in the soybean genome by a small family of three genes: NRP-A, NRP-B and NRP-C. The encoded proteins share a highly conserved development and cell death (DCD) domain at the C-terminal portion in addition to a high content of asparagine residues at their more divergent N termini. The asparagine rich domain is not well characterized but harbors putative glycosylation and myristoylation sites that may be relevant for function. The DCD domain is found exclusively in plant proteins and it is composed of about 130 amino acid residues, organized into several conserved motifs: FGLP and LFL in the N-treminal region of the domain, PAQV and PLxE at its C-terminus (Tenhaken et al; 2005). DCD domain-containing proteins may be subdivided into four groups, according to the localization of the DCD domain in the primary structure. NRPs belong to the the subgroup I of DCD domain-containing family of proteins, as their domains are located at the C-terminal portion of the protein (Tenhaken et al; 2005).
NRPs are critical mediators of ER and osmotic stress-induced cell death in soybeans (Costa et al., 2008). The cell death response mediated by NRPs resembles a programmed cell death event. The overexpression of NRPs in soybean protoplasts induces caspase-3-like activity and promotes extensive DNA fragmentation. Furthermore, the transient expression of NRPs in plants causes leaf yellowing, chlorophyll loss, malondialdehyde production, ethylene evolution and the induction of senescence marker genes, which are hallmarks of leaf senescence.
NRPs are up-regulated by ER or osmotic stress but need both stress signals for full induction (Isrigler et al., 2007). This synergistic interaction of both signals upon NRP induction indicates that the ER stress and osmotic stress responses converge at the level of gene expression to potentiate a NRP-mediated cell death response (Costa et al., 2008). NRPs are also up-regulated by other abiotic and biotic signals, such as salt stress, oxidative stress and pathogens. Because the NRP-mediated cell death signaling pathway represents a shared response to multiple stress signals in plants, it might permit coordinate adaptive cellular responses under a large array of stress conditions
3.3. GmNAC6 as a downstream component of the NRP-mediated cell death response
NAC domain-containing proteins are plant-specific transcriptional factors that are expressed in several tissues and developmental stages. The NAC transfactors are organized into a general structure that consists of a highly conserved N-terminal domain involved in DNA binding (called NAC domain) and a C-terminal region highly divergent in sequence and length that functions as the activation domain. The NAC domain was derived from comparison of consensus sequences among NAM from Petunia, ATAF1/2 and CUC2 from Arabidopsis (Souer et al., 1996.). It comprises nearly 160 amino acid residues, divided into five subdomains (A–E) exhibiting a negative net charge and a nuclear localization signal (Xie et al., 1999; Seoet al., 2008). The subdomains A, C and D are conserved among plant species whereas B and E subdomains are variable (Ooka et al., 2003). The C- terminus harbors a protein-protein interaction domain in some NAC-containing proteins while a transmembrane domain is present in other transcriptional factors (Seo et al., 2008). Therefore, the NAC family is comprised by both soluble, nuclear transactivators and membrane proteins.
The members of the NAC gene family are involved in a variety of developmental events and defense responses, such as shoot apical meristem formation and maintenance (SAM; Aida et al., 1997; Souer et al.,1996; Weir et al., 2004), hormone signaling (Fujita et al., 2004; Xie et al., 2000), response to pathogen infection (Ren et al., 2000; Selth et al., 2005; Xie et al., 1999), leaf senescence (John et al., 1997) and response to different abiotic stresses (Hegedus et al., 2003; Tran et al.,2004).
The soybean NAC family is comprised by 180 putative sequences of NAC domain-containing proteins, which display different expression profiles in response to distinct environmental stress conditions and developmental signals (Mochida et al.,2009; Mochida et al., 2010; Wang et al., 2010). Frequently, the stress-induced expression profile of the soybean NAC genes reflects the functional profile of the encoded protein (Pinheiro et al., 2009). GmNAC6 was identified by its synergistic induction in response to a combined treatment of inducers of osmotic stress (polyethylene glycol) and ER stress (tunicamycin) and was functionally linked to the NRP-mediated cell death response (Faria et al., 2011). Transient expression of GmNAC6 promotes cell death and hypersensitive-like responses
GmNAC6 encodes a 33kDa protein that belongs to the TERN (Tobacco elicitor-responsive gene encoding NAC domain protein) group of the NAC family, which is induced by elicitors of the pathogen response (Ooka et al.,2003). Likewise, GmNAC6 is induced by the pathogenic bacteria
This research was supported by the Brazilian Government Agencies CNPq grants 559602/2009-0, 573600/2008-2 and 470878/2006-1 (to E.P.B.F.), the FAPEMIG grant CBB-APQ-00070-09, and the FINEP grant 01.09.0625.00 (to E.P.B.F.). P.A.B.R. is supported by CNPq graduate fellowships.
Aida M. Ishida T. Fukaki H. Fujisawa H. Tasaka M. 1997 Genes involved in organ separation in Arabidopsis, an analysis of the cup-shaped cotyledon mutant.The Plant Cell, 9 841 857 0153-2298X
Alves M. S. Reis P. A. B. Dadalto S. P. Faria J. A. Q. A. Fontes E. P. B. Fietto L. G. 2010 A novel transcription factor, early responsive to dehydration 15, connects ER stress with an osmotic stress-induced cell death signal. Journal of Biological Chemistry, 286 20020 20030 0108-3351X
Che, P.; Bussell, J.D.; Zhou, W.; Estavillo, G.M.; Pogson, B.J.; Smith, S.M. (2010) Signaling from the Endoplasmic Reticulum Activates Brassinosteroid Signaling and Promotes Acclimation to Stress in Arabidopsis. Science Signaling, 3: ra69, ISSN 1945-0877
Chen Y. Brandizzi F. 2012 AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis 69 266 277 0136-5313X
Costa M. D. L. Reis P. A. B. Valente M. A. S. Irsigler A. S. T. Carvalho C. M. Loureiro M. E. Aragaão F. J. L. Boston R. S. Fietto L. G. . Fontes E. P. B. 2008 A new branch of endoplasmic reticulum stress signaling and the osmotic signal converge on plant-specific asparagine-rich proteins to promote cell death 20209 20219 0108-3351X
Deng Y. Humbert S. Liu J. X. Srivastava R. J. Rothstein J. S. Howell S. H. 2011 Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in ArabidopsisProceedings of the National Academy of Sciences, 108 7247 7252 1091-6490
Faria J. A. Q. A. Reis P. A. B. Reis M. T. B. Rosado G. L. Pinheiro G. L. Mendes G. C. Fontes E. P. B. 2011 The NAC domain-containing protein, GmNAC6, is a downstream component of the ER stress- and osmotic stress-induced NRP-mediated cell-death signaling pathwayBMC Plant Biology, 11: 129, 1471-2229 1471 2229
Fujita M. Fujita Y. Maruyama K. Seki Motoaki. Hiratsu K. Ohme-Takagi M. Tran-S L. P. Yamaguchi-Shinozaki K. Shinozaki K. 2004 A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway 39 863 876 0136-5313X
Hayashy S. Wakasa Y. Takahashi H. Kawakatsu T. Takaiwa F. 2012Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the endoplasmic reticulum stress response of rice. The Plant Journal, 69 946 956 0136-5313X
Hegedus D.. Yu M. Baldwin D. Gruber M. Sharpe A. Parkin I. Whitwill S. Lydiate D. . 2003 Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. 383 397 1572-9818
Irsigler A. S. T. Costa M. D. L. Zhang P. Reis P. A. B. Dewey R. E. Boston R. S. . Fontes E. P. B. 2007 Expression profiling on soybean leaves reveals integration of ER- and osmotic-stress pathways. 1471-2164 1471 2164
John I. Hackett R. Cooper W. Drake R. Farrell A. Grierson D. 1997 Cloning and characterization of tomato leaf senescence-related cDNAs. 33 641 651 1572-9818
Kapoor A. Sanyal A. J. 2009 Endoplasmic Reticulum Stress and the Unfolded Protein Response 581 590 1089-3261
Kariola T. Brader G. Helenius E. Li J. Heino P. Palva E. T. 2006 EARLY RESPONSIVE to DEHYDRATION 15, a negative regulator of abscisic acid responses in Arabidopsis.Plant Physiology, 142 1559 73 1532-2548
Kiyosue T. Yamaguchi-Shinozaki K. Shinozaki K. 1994 Cloning of cDNAs for genes that are early-responsive to dehydration stress (ERDs) in Arabidopsis thaliana L.: identification of three ERDs as HSP cognate genes. 25 791 8 1572-9818
Kiyosue T. Yamaguchi-Shinozaki K. Shinozaki K. 1993Characterization of two cDNAs (ERD11 and ERD13) for dehydrationinducible genes that encode putative glutathione S-transferases in Arabidopsis thaliana L. FEBS Letters, 335 189 92 0014-5793
Koizumi N. Martinez I. M. Kimata Y. Kohno K. Sano H. Chrispeels M. J. 2001 Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases.Plant Physiology, 127 949 962 1532-2548
Liu J. X. Srivastava R. . Che P. . Howell S. H. 2007 Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signalingThe Plant Journal, 51 897 909 0136-5313X
Liu J. X. Srivastava R. Howell S. H. 2008 Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in ArabidopsisCell & Environment. 31 1735 1743 1365-3040
Liu J. X. Howell S. H. 2010 Endoplasmic Reticulum Protein Quality Control and Its Relationship to Environmental Stress Responses in PlantsThe Plant Cell, 22 1 13 0153-2298X
Lu-J S. Yang-T Z. Sun L. Sun L. Song-T Z. Liu-X J. 2011 Conservation of IRE 1-Regulated bZIP74 mRNA Unconventional Splicing in Rice (Oryza sativa L.) Involved in ER Stress Responses 1752-9867
Ludwig A. A. Tenhaken R. (2001 2001 A new cell wall located N-rich protein is strongly induced during the hypersensitive response in Glycine max L. 107 323 336 1573-8469
Malhotra J. D. . Kaufman R. J. 2007 The Endoplasmic Reticulum and the Unfolded Protein ResponseSemininars in Cell and Developmental Biology, 18 716 73 1084-9521
Mochida K. Yoshida T. Sakurai T. Yamaguchi-Shinozaki K. Shinozaki K. Tran L. S. 2009 In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybeanDNA Research., 16 353 69 1756-1663
Mochida K. Yoshida T. Sakurai T. Yamaguchi-Shinozaki K. Shinozaki K. Tran L. S. 2010a LegumeTFDB: an integrative database of Glycine max, Lotus japonicus and Medicagotruncatula transcription factors. 26 290 1 1460-2059
Nagashima Y. Mishiba K. Suzuki E. Shimada Y. Iwata Y. Koizumi N. 2011Arabidopsis IRE1 catalyses unconventional splicing ofbZIP60 mRNA to produce the active transcription factor. Scientific Reports, 1:29, 2045-2322 2045 2322
Okushima Y. Koizumi N. Yamaguchi Y. Kimata . Kohno K. Sano H. 2002 Isolation and characterization of a putative transducer of endoplasmic reticulum stress in Oryza sativaPlant Cell Physiology, 43 532 539 1471-9053
Ooka H. Satoh K. Doi K. et al. et al. 2003 Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana.DNA Research. 10; 239 247 1756-1663
Pinheiro G. L. Marques C. S. Costa M. D. B. L. Reis P. A. B. Alves M. S. Carvalho C. M. Fietto L. G. . Fontes E. P. B. 2009 Complete inventory of soybean NAC transcription factors: Sequence conservation and expression analysis uncover their distinct roles in stress response 444 10 23 0378-1119
Reis, P.A.B and Fontes, E.P.B. 2012N-rich protein (NRP)-mediated cell death signaling: a new branch of the ER stress response with implications for plant biotechnology. Plant Signaling & Behavior. 7 1559-2316
Ren T. Qu F. Morris T. J. 2000 HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virusThe Plant Cell 12 1917 1926 0153-2298X
Ron D. Walter P. 2007 Signal integration in the endoplasmic reticulum unfolded protein response.Molecular Cell Biology 8 519 529 1471-0072
Schröder M. 2008 Endoplasmic reticulum stress responses 65 862 894 0142-0682X
Selth L. A. Dogra S. C. Rasheed M. S. Healy H. Randles J. W. Rezaian M. A. 2005 A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replicationThe Plant Cell 17 311 325 0153-2298X
Seo P. J. Kim S. G. Park C. M. 2008Membrane bound transcription factors in plants. 13 550 6 1360-1385
Souer E. van Houwelingen A. Kloos D. Mol J. Koes R. 1996The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordial boundaries. Cell, 85 159 70 0092-8674
Tajima H. Iwata Y. Iwano M. Takayama S. Koizumi N. 2008Identification ofan Arabidopsis transmembranebZIP transcription factor involved in the endoplasmicreticulum stress response. Biochemical and Biophysical Research Communications, 374 242 247 0000-6291X
Tenhaken R. Doerks T. Bork P. 2005DCD- a novel plant specific domain in proteins involved in development and programmed cell death. BMC Bioinformatics 6:169, 1471-2105 1471 2105
Tran L. S. Nakashima K. Sakuma Y. et al. 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 16 2481 2498 0153-2298X
Udvardi M. K. Kakar K. Wandrey M. et al. 2007 Legume transcription factors: global regulators of plant development and response to the environment. 144 538 49 1532-2548
Wang S. Narendra S. Fedoroff N. 2007 Heterotrimeric G protein signaling in the Arabidopsis unfolded protein responseProceedings of the National Academy of Sciences, 104 3817 3822ISSN 1091-6490
Wang Z. Kiledjian M. 2000The Poly(A)-Binding Protein and an mRNA Stability Protein
Jointly Regulate an Endoribonuclease Activity.Molecular and Cellular Biology, 20 6334 6341 1098-5549
Wang Z. Libault M. Joshi T. et al. 2010 SoyDB: a knowledge database of soybean transcription factorsBMC Plant Biology, 10: 14, 1471-2229 1471 2229
Weir I. Lu J. Cook H. Causier B. Schwarz-Sommer Z. Davies B. 2004 CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum 131 915 922 1011-6370
Xie Q. Sanz-Burgos A. P. Guo H. Garcia J. A. Gutierrez C. 1999GRAB proteins, novelmembers of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Molecular Biology 39 647 656 1572-9818
Xu C. Bailly-Maitre B. Reed J. C. 2005 Endoplasmic reticulum stress: cell life and death decisionsJournal of Clinical Investigation. 115 2656 2664 0021-9738