Skip to main content
SpringerLink
Log in

In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

A conserved UPR machinery is required for Brachypodium ER stress resistance and grain filling.

Human and livestock diets depend on the accumulation of cereal storage proteins and carbohydrates, including mixed-linkage glucan (MLG), in the endosperm during seed development. Storage proteins and proteins responsible for the production of carbohydrates are synthesized in the endoplasmic reticulum (ER). Unfavorable conditions during growth that hamper the ER biosynthetic capacity, such as heat, can cause a potentially lethal condition known as ER stress, which activates the unfolded protein response (UPR), a signaling response designed to mitigate ER stress. The UPR relies primarily on a conserved ER-associated kinase and ribonuclease, IRE1, which splices the mRNA of a transcription factor (TF), such as bZIP60 in plants, to produce an active TF that controls the expression of ER resident chaperones. Here, we investigated activation of the UPR in Brachypodium, as a model to study the UPR in seeds of a monocotyledon species, as well as the consequences of heat stress on MLG deposition in seeds. We identified a Brachypodium bZIP60 orthologue and determined a positive correlation between bZIP60 splicing and ER stress induced by chemicals and heat. Each stress condition led to transcriptional modulation of several BiP genes, supporting the existence of condition-specific BiP regulation. Finally, we found that the UPR is elevated at the early stage of seed development and that MLG production is negatively affected by heat stress via modulation of MLG synthase accumulation. We propose that successful accomplishment of seed filling is strongly correlated with the ability of the plant to sustain ER stress via the UPR.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

MLG:

Mixed-linkage glucan

UPR:

Unfolded protein response

RIDD:

Regulated Ire1-dependent decay

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Bita C, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress tolerant crops. Front Plant Sci 4:273. doi:10.3389/fpls.2013.00273

    Article  PubMed  PubMed Central  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Burton RA, Wilson SM, Hrmova M, Harvey AJ, Shirley NJ, Medhurst A, Stone BA, Newbigin EJ, Bacic A, Fincher GB (2006) Cellulose synthase-like CslF genes mediate the synthesis of cell wall (1,3;1,4)-β-d-glucans. Science 311:1940–1942

    Article  CAS  PubMed  Google Scholar 

  • Buzeli RAA, JlCM Cascardo, Rodrigues LAZ, Andrade MO, Almeida RS, Loureiro ME, Otoni WC, Fontes EPB (2002) Tissue-specific regulation of BiP genes: a cis-acting regulatory domain is required for BiP promoter activity in plant meristems. Plant Mol Biol 50:757–771

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Brandizzi F (2012) AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis. Plant J 69:266–277

    Article  CAS  PubMed  Google Scholar 

  • Deng Y, Humbert S, Liu J-X, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng Y, Srivastava R, Howell SH (2013) Endoplasmic reticulum (ER) stress response and its physiological roles in plants. Int J Mol Sci 14:8188–8212

    Article  PubMed  PubMed Central  Google Scholar 

  • Fragkostefanakis S, Mesihovic A, Hu Y, Schleiff E (2016) Unfolded protein response in pollen development and heat stress tolerance. Plant Reprod 29:81–91

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guillon F, Bouchet B, Jamme F, Robert P, Quéméner B, Barron C, Larré C, Dumas P, Saulnier L (2011) Brachypodium distachyon grain: characterization of endosperm cell walls. J Exp Bot 62:1001–1015

    Article  CAS  PubMed  Google Scholar 

  • Hands P, Drea S (2012) A comparative view of grain development in Brachypodium distachyon. J Cereal Sci 56:2–8

    Article  Google Scholar 

  • Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5:897–904

    Article  CAS  PubMed  Google Scholar 

  • Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Soc 10(Part A):4–10

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hayashi S, Takahashi H, Wakasa Y, Kawakatsu T, Takaiwa F (2013) Identification of a cis-element that mediates multiple pathways of the endoplasmic reticulum stress response in rice. Plant J 74:248–257

    Article  CAS  PubMed  Google Scholar 

  • Henriquez-Valencia C, Moreno AA, Sandoval-Ibañez O, Mitina I, Blanco-Herrera F, Cifuentes-Esquivel N, Orellana A (2015) bZIP17 and bZIP60 regulate the expression of BiP3 and other salt stress responsive genes in an UPR-independent manner in Arabidopsis thaliana. J Cell Biochem 116:1638–1645

    Article  CAS  PubMed  Google Scholar 

  • Hofmann K, Stoffel W (1993) TMbase—a database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 374:166

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S-J, Zemelis S, Keegstra K, Brandizzi F (2015) The cytoplasmic localization of the catalytic site of CSLF6 supports a channeling model for the biosynthesis of mixed-linkage glucan. Plant J 81:537–547

    Article  CAS  PubMed  Google Scholar 

  • Lai Y-S, Stefano G, Brandizzi F (2014) ER stress signaling requires RHD3, a functionally conserved ER-shaping GTPase. J Cell Sci 127:3227–3232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larré C, Penninck S, Bouchet B, Lollier V, Tranquet O, Denery-Papini S, Guillon F, Rogniaux H (2010) Brachypodium distachyon grain: identification and subcellular localization of storage proteins. J Exp Bot 61:1771–1783

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Korennykh AV, Behrman SL, Walter P (2010) Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl Acad Sci USA 107:16113–16118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Humbert S, Howell SH (2012) ZmbZIP60 mRNA is spliced in maize in response to ER stress. BMC Res Notes 5:144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, LaVail MM, Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318:944–949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J-X, Howell SH (2010) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J-X, Srivastava R, Che P, Howell SH (2007) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu S-J, Yang Z-T, Sun L, Sun L, Song Z-T, Liu J-X (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 5:504–514

    Article  CAS  PubMed  Google Scholar 

  • Moreno AA, Mukhtar MS, Blanco F, Boatwright JL, Moreno I, Jordan MR, Chen Y, Brandizzi F, Dong X, Orellana A, Pajerowska-Mukhtar KM (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One 7(2):e31944. doi:10.1371/journal.pone.0031944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagashima Y, K-i Mishiba, 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Opanowicz M, Hands P, Betts D, Parker ML, Toole GA, Mills ENC, Doonan JH, Sa Drea (2011) Endosperm development in Brachypodium distachyon. J Exp Bot 62:735–748

    Article  CAS  PubMed  Google Scholar 

  • Parra-Rojas J, Moreno AA, Mitina I, Orellana A (2015) The dynamic of the splicing of bZIP60 and the proteins encoded by the spliced and unspliced mRNAs reveals some unique features during the activation of UPR in Arabidopsis thaliana. PLoS One 10(4):e0122936. doi:10.1371/journal.pone.0122936

    Article  PubMed  PubMed Central  Google Scholar 

  • Qu A-L, Ding Y-F, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    Article  CAS  PubMed  Google Scholar 

  • Ruberti C, Kim S-J, Stefano G, Brandizzi F (2015) Unfolded protein response in plants: one master, many questions. Curr Opin Plant Biol 27:59–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-May E, Kim SJ, Brandizzi F, Rose JKC (2012) The secreted plant N-glycoproteome and associated secretory pathways. Front Plant Sci 3:117. doi:10.3389/fpls.2012.00117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shang J, Lehrman MA (2004) Discordance of UPR signaling by ATF6 and IRE1p-XBP1 with levels of target transcripts. Biochem Biophys Res Commun 317:390–396

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3:99–111

    Article  CAS  PubMed  Google Scholar 

  • Shewry P, Halford N (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. doi:10.1038/msb.2011.75

    Article  PubMed  PubMed Central  Google Scholar 

  • Srivastava R, Deng Y, Shah S, Rao AG, Howell SH (2013) Binding protein is a master regulator of the endoplasmic reticulum stress sensor/transducer bZIP28 in Arabidopsis. Plant Cell 25:1416–1429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Yang Z-T, Song Z-T, Wang M-J, Sun L, Lu S-J, Liu J-X (2013) The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76:274–286

    CAS  PubMed  Google Scholar 

  • Vega-Sánchez ME, Verhertbruggen Y, Christensen U, Chen X, Sharma V, Varanasi P, Jobling SA, Talbot M, White RG, Joo M, Singh S, Auer M, Scheller HV, Ronald PC (2012) Loss of cellulose synthase-like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol 159:56–69

    Article  PubMed  PubMed Central  Google Scholar 

  • Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–1086

    Article  CAS  PubMed  Google Scholar 

  • Wilson SM, Ho YY, Lampugnani ER, Van de Meene A, Bain M, Bacic A, Doblin M (2015) Determining the subcellular location of synthesis and assembly of the cell wall polysaccharide (1,3; 1,4)-β-d-glucan in grasses. Plant Cell 27:754–771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K (2004) Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem 136:343–350

    Article  CAS  PubMed  Google Scholar 

  • Yanagitani K, Imagawa Y, Iwawaki T, Hosoda A, Saito M, Kimata Y, Kohno K (2009) Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol Cell 34:191–200

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Rawson RB, Komuro R, Chen X, Davé UP, Prywes R, Brown MS, Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355–1364

    Article  CAS  PubMed  Google Scholar 

  • York W, Darvill A, McNeil M, Stevenson TT, Albersheim P (1985) Isolation and characterization of plant cell walls and cell wall components. Methods Enzymol 118:3–40

    Article  Google Scholar 

  • Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107:881–891

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Luo N, He M, Chen G, Zhu J, Yin G, Li X, Hu Y, Li J, Yan Y (2014) Molecular characterization and expression profiling of the protein disulfide isomerase gene family in Brachypodium distachyon L. PLoS One 9(4):e94704. doi:10.1371/journal.pone.0094704

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31:3406–3415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Monika Doblin (University of Melbourne) for providing the anti-CSLF6 serum. This study was primarily supported by DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science DE-FC02-07ER64494), with contributing support from the Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences, Office of Science, U.S. Department of Energy (award number DE-FG02-91ER20021) for infrastructure, National Institutes of Health (GM101038), and AgBioResearch.

Author information

Authors and Affiliations

  1. Great Lakes Bioenergy Research Center, Michigan State University, East Lansing, MI, 48824, USA

    Sang-Jin Kim, Starla Zemelis-Durfee, Curtis Wilkerson & Federica Brandizzi

  2. MSU-DOE Plant Research Lab, Michigan State University, East Lansing, MI, 48824, USA

    Federica Brandizzi

  3. Department of Plant Biology, Michigan State University, East Lansing, MI, 48824, USA

    Curtis Wilkerson & Federica Brandizzi

Authors
  1. Sang-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Starla Zemelis-Durfee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Curtis Wilkerson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Federica Brandizzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Federica Brandizzi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, SJ., Zemelis-Durfee, S., Wilkerson, C. et al. In Brachypodium a complex signaling is actuated to protect cells from proteotoxic stress and facilitate seed filling. Planta 246, 75–89 (2017). https://doi.org/10.1007/s00425-017-2687-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2687-7

Keywords

Search

Navigation