BLISTER-regulated vegetative growth is dependent on the protein kinase domain of ER stress modulator IRE1A in Arabidopsis thaliana

English version

Autoři: Zheng-Hui Hong ^aff001; Tao Qing ^aff002; Daniel Schubert ^aff003; Julia Anna Kleinmanns ^aff003; Jian-Xiang Liu ^aff001
Působiště autorů: State Key Laboratory of Genetic Engineering, School of Life Sciences, Fudan University, Shanghai, China ^aff001; State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, China ^aff002; Plant Developmental Epigenetics, Heinrich Heine University Düsseldorf, Düsseldorf, Germany ^aff003; Epigenetics of Plants, Freie Universität Berlin, Berlin, Germany ^aff004
Vyšlo v časopise: BLISTER-regulated vegetative growth is dependent on the protein kinase domain of ER stress modulator IRE1A in Arabidopsis thaliana. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008563
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1008563

Souhrn

The unfolded protein response (UPR) is required for protein homeostasis in the endoplasmic reticulum (ER) when plants are challenged by adverse environmental conditions. Inositol-requiring enzyme 1 (IRE1), the bifunctional protein kinase / ribonuclease, is an important UPR regulator in plants mediating cytoplasmic splicing of the mRNA encoding the transcription factor bZIP60. This activates the UPR signaling pathway and regulates canonical UPR genes. However, how the protein activity of IRE1 is controlled during plant growth and development is largely unknown. In the present study, we demonstrate that the nuclear and Golgi-localized protein BLISTER (BLI) negatively controls the activity of IRE1A/IRE1B under normal growth condition in Arabidopsis. Loss-of-function mutation of BLI results in chronic up-regulation of a set of both canonical UPR genes and non-canonical UPR downstream genes, leading to cell death and growth retardation. Genetic analysis indicates that BLI-regulated vegetative growth phenotype is dependent on IRE1A/IRE1B but not their canonical splicing target bZIP60. Genetic complementation with mutation analysis suggests that the D570/K572 residues in the ATP-binding pocket and N780 residue in the RNase domain of IRE1A are required for the activation of canonical UPR gene expression, in contrast, the D570/K572 residues and D590 residue in the protein kinase domain of IRE1A are important for the induction of non-canonical UPR downstream genes in the BLI mutant background, which correlates with the shoot growth phenotype. Hence, our results reveal the important role of IRE1A in plant growth and development, and BLI negatively controls IRE1A’s function under normal growth condition in plants.

Klíčová slova:

Gene expression – Phenotypes – Transcription factors – Seedlings – Arabidopsis thaliana – Protein kinases – Ribonucleases – Root growth

Zdroje

1. Liu JX, Howell SH (2016) Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytol 211: 418–428. doi: 10.1111/nph.13915 26990454

2. Walter P, Ron D (2011) The unfolded protein response: From stress pathway to homeostatic regulation. Science 334: 1081–1086. doi: 10.1126/science.1209038 22116877

3. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22: 2930–2942. doi: 10.1105/tpc.110.078154 20876830

4. Liu JX, 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. doi: 10.1105/tpc.106.050021 18156219

5. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, et al. (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. doi: 10.1073/pnas.1102117108 21482766

6. Yang ZT, Lu SJ, Wang MJ, Bi DL, Sun L, et al. (2014) A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis. Plant J 79: 1033–1043. doi: 10.1111/tpj.12604 24961665

7. Yang ZT, Wang MJ, Sun L, Lu SJ, Bi DL, et al. (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLOS Genet 10: e1004243. doi: 10.1371/journal.pgen.1004243 24675811

8. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102: 5280–5285. doi: 10.1073/pnas.0408941102 15781873

9. 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 Biophy Res Commun 374: 242–247.

10. Moreno AA, Mukhtar MS, Blanco F, Boatwright JL, Moreno I, et al. (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLOS One 7: e31944. doi: 10.1371/journal.pone.0031944 22359644

11. 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. doi: 10.1111/j.1365-313X.2011.04844.x 22050533

12. Lu SJ, Yang ZT, Sun L, Sun L, Song ZT, et al. (2012) Conservation of IRE1-regulated bZIP74 mRNA unconventional splicing in rice (Oryza sativa L.) involved in ER stress responses. Mol Plant 5: 504–514. doi: 10.1093/mp/ssr115 22199238

13. 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. doi: 10.1093/pcp/pcr157 22084314

14. Nagashima Y, Mishiba KI, Suzuki E, Shimada Y, Iwata Y, et al. (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1: doi: 10.1038/srep00029 22355548

15. 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. doi: 10.1073/pnas.0808463105 18849477

16. Che P, Bussell JD, Zhou WX, Estavillo GM, Pogson BJ, et al. (2010) Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci Signal 3: ra69. doi: 10.1126/scisignal.2001140 20876872

17. Sun L, Lu SJ, Zhang SS, Zhou SF, Sun L, et al. (2013) The lumen-facing domain is important for the biological function and organelle-to-organelle movement of bZIP28 during ER stress in Arabidopsis. Mol Plant 6: 1605–1615. doi: 10.1093/mp/sst059 23558471

18. Sun L, Zhang SS, Lu SJ, Liu JX (2015) Site-1 protease cleavage site is important for the ER stress-induced activation of membrane-associated transcription factor bZIP28 in Arabidopsis. Sci China-Life Sci 58: 270–275. doi: 10.1007/s11427-015-4807-6 25634523

19. Tian L, Zhang Y, Ma EKH, Zhao H, Yuan M, et al. (2018) Basic-Leucine Zipper 17 and HMG-CoA reductase degradation 3A are involved in salt acclimation memory in Arabidopsis. J Integr Plant Biol doi: 10.1111/jipb.12744 30450762

20. Liu JX, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51: 897–909. doi: 10.1111/j.1365-313X.2007.03195.x 17662035

21. Deng Y, Srivastava R, Quilichini TD, Dong H, Bao Y, et al. (2016) IRE1, a component of the unfolded protein response signaling pathway, protects pollen development in Arabidopsis from heat stress. Plant J 88: 193–204. doi: 10.1111/tpj.13239 27304577

22. Sun L, Yang ZT, Song ZT, Wang MJ, Sun L, et al. (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. doi: 10.1111/tpj.12287 23869562

23. Mishiba KI, Nagashima Y, Suzuki E, Hayashi N, Ogata Y, et al. (2013) Defects in IRE1 enhance cell death and fail to degrade mRNAs encoding secretory pathway proteins in the Arabidopsis unfolded protein response. Proc Natl Acad Sci USA 110: 5713–5718. doi: 10.1073/pnas.1219047110 23509268

24. Wang QL, Sun AZ, Chen ST, Chen LS, Guo FQ (2018) SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice. Nat Plant 4: 280–288.

25. Schatlowski N, Stahl Y, Hohenstatt ML, Goodrich J, Schubert D (2010) The CURLY LEAF interacting protein BLISTER controls expression of polycomb-group target genes and cellular differentiation of Arabidopsis thaliana. Plant Cell 22: 2291–2305. doi: 10.1105/tpc.109.073403 20647345

26. Kleinmanns JA, Schatlowski N, Heckmann D, Schubert D (2017) BLISTER regulates polycomb-target genes, represses stress-regulated genes and promotes stress responses in Arabidopsis thaliana. Front Plant Sci 8: 1530. doi: 10.3389/fpls.2017.01530 28955347

27. Song ZT, Sun L, Lu SJ, Tian Y, Ding Y, et al. (2015) Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants. Proc Natl Acad Sci USA 112: 2900–2905. doi: 10.1073/pnas.1419703112 25730865

28. Geldner N, Dénervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, et al. (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59: 169–178. doi: 10.1111/j.1365-313X.2009.03851.x 19309456

29. Ruberti C, Lai Y, Brandizzi F (2018) Recovery from temporary endoplasmic reticulum stress in plants relies on the tissue-specific and largely independent roles of bZIP28 and bZIP60, as well as an antagonizing function of BAX-Inhibitor1 upon the pro-adaptive signaling mediated by bZIP28. Plant J 93: 155–165. doi: 10.1111/tpj.13768 29124827

30. Deng Y, Srivastava R, Howell SH (2013) Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis. Proc Natl Acad Sci USA 110: 19633–19638. doi: 10.1073/pnas.1314749110 24145452

31. Rubio C, Pincus D, Korennykh A, Schuck S, El-Samad H, et al. (2011) Homeostatic adaptation to endoplasmic reticulum stress depends on Ire1 kinase activity. J Cell Biol 193: 171–184. doi: 10.1083/jcb.201007077 21444684

32. Chawla A, Chakrabarti S, Ghosh G, Niwa M (2011) Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J Cell Biol 193: 41–50. doi: 10.1083/jcb.201008071 21444691

33. Korennykh AV, Korostelev AA, Egea PF, Finer-Moore J, Stroud RM, et al. (2011) Structural and functional basis for RNA cleavage by IRE1. BMC Biol 9: 15. doi: 10.1186/1741-7007-9-15

34. Bertolotti A, Zhang YH, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326–332. doi: 10.1038/35014014 10854322

35. Chen Y, Brandizzi F (2013) IRE1: ER stress sensor and cell fate executor. Trend Cell Biol 23: 547–555.

36. Hetz C, Glimcher LH (2009) Fine-tuning of the unfolded protein response: Assembling the IRE1 alpha interactome. Mol Cell 35: 551–561. doi: 10.1016/j.molcel.2009.08.021 19748352

37. Koizumi N, Ujino T, Sano H, Chrispeels MJ (1999) Overexpression of a gene that encodes the first enzyme in the biosynthesis of asparagine-linked glycans makes plants resistant to tunicamycin and obviates the tunicamycin-induced unfolded protein response. Plant Physiol 121: 353–361. doi: 10.1104/pp.121.2.353 10517826

38. Bao Y, Pu Y, Yu X, Gregory BD, Srivastava R, et al. (2018) IRE1B degrades RNAs encoding proteins that interfere with the induction of autophagy by ER stress in Arabidopsis thaliana. Autophagy 14: 1562–1573. doi: 10.1080/15548627.2018.1462426 29940799

39. Chen Y, Brandizzi F (2012) AtIRE1A/AtIRE1B and AGB1 independently control two essential unfolded protein response pathways in Arabidopsis. Plant J 69: 266–277. doi: 10.1111/j.1365-313X.2011.04788.x 21914012

40. Qi H, Xia FN, Xie LJ, Yu LJ, Chen QF, et al. (2017) TRAF family proteins regulate autophagy dynamics by modulating AUTOPHAGY PROTEIN6 stability in Arabidopsis. Plant Cell 29: 890. doi: 10.1105/tpc.17.00056 28351989

41. Zhang SS, Yang H, Ding L, Song ZT, Ma H, et al. (2017) Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. Plant Cell 29: 1007–1023. doi: 10.1105/tpc.16.00916 28442596