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Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response


Plant growth requires continuous signal transduction in response to ever-changing environment. Phosphoinositides represent primary lipid-derived signals that are involved in various plant responses to surrounding environment. However, enzymes that determine the complex phosphoinositide molecular profiles remained elusive due to the existence of a number of candidate genes for each step. Here, in Arabidopsis thaliana, we found AtPLC2 as the enzyme that is decisive in phosphoinositide metabolism by analytical lipidomics of the gene knockout study. Functional characterization of AtPLC2 knockout plant enabled us to find two novel roles of phosphoinositides: requirement in seedling growth and ER stress tolerance. Because economically important environmental stresses such as salinity and temperature upshift cause ER stress, our findings may open up a new avenue in addressing ER stress responses via phosphoinositide signaling.


Vyšlo v časopise: Arabidopsis AtPLC2 Is a Primary Phosphoinositide-Specific Phospholipase C in Phosphoinositide Metabolism and the Endoplasmic Reticulum Stress Response. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005511
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005511

Souhrn

Plant growth requires continuous signal transduction in response to ever-changing environment. Phosphoinositides represent primary lipid-derived signals that are involved in various plant responses to surrounding environment. However, enzymes that determine the complex phosphoinositide molecular profiles remained elusive due to the existence of a number of candidate genes for each step. Here, in Arabidopsis thaliana, we found AtPLC2 as the enzyme that is decisive in phosphoinositide metabolism by analytical lipidomics of the gene knockout study. Functional characterization of AtPLC2 knockout plant enabled us to find two novel roles of phosphoinositides: requirement in seedling growth and ER stress tolerance. Because economically important environmental stresses such as salinity and temperature upshift cause ER stress, our findings may open up a new avenue in addressing ER stress responses via phosphoinositide signaling.


Zdroje

1. Boss WF, Im YJ. Phosphoinositide signaling. Annu Rev Plant Biol. 2012;63: 409–429. doi: 10.1146/annurev-arplant-042110-103840 22404474

2. Arisz SA, Testerink C, Munnik T. Plant PA signaling via diacylglycerol kinase. Biochim Biophys Acta. 2009;1791: 869–875. doi: 10.1016/j.bbalip.2009.04.006 19394438

3. Nakamura Y, Awai K, Masuda T, Yoshioka Y, Takamiya K, Ohta H. A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J Biol Chem. 2005;280: 7469–7476. doi: 10.1074/jbc 15618226

4. Gaude N, Nakamura Y, Scheible WR, Ohta H, Dörmann P. Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J. 2008;56: 28–39. doi: 10.1111/j.1365-313X.2008.03582.x 18564386

5. Mueller-Roeber B, Pical C. Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol. 2002;130: 22–46. doi: 10.1104/Pp.004770 12226484

6. Hunt L, Otterhag L, Lee JC, Lasheen T, Hunt J, Seki M, et al. Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. New Phytol. 2004;162: 643–654. doi: 10.1111/J.1469-8137.2004.01069.X

7. Tasma IM, Brendel V, Whitham SA, Bhattacharyya MK. Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem. 2008;46: 627–637. doi: 10.1016/j.plaphy.2008.04.015 18534862

8. Hirayama T, Ohto C, Mizoguchi T, Shinozaki K. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci USA. 1995;92: 3903–3907. doi: 10.1073/pnas.92.9.3903 7732004

9. Sanchez JP, Chua NH. Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell. 2001;13: 1143–1154. doi: 10.1105/tpc.13.5.1143 11340187

10. Zheng SZ, Liu YL, Li B, Shang ZL, Zhou RG, Sun DY. Phosphoinositide-specific phospholipase C9 is involved in the thermotolerance of Arabidopsis. Plant J. 2012;69: 689–700. doi: 10.1111/j.1365-313X.2011.04823.x 22007900

11. Gao K, Liu YL, Li B, Zhou RG, Sun DY, Zheng SZ. Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. Plant Cell Physiol. 2014;55: 1873–1883. doi: 10.1093/pcp/pcu116 25149227

12. Hirayama T, Mitsukawa N, Shibata D, Shinozaki K. AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana. Plant Mol Biol. 1997;34: 175–180. doi: 10.1023/A:1005885230896 9177324

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

14. Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH. 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. 2011;108: 7247–7252. doi: 10.1073/pnas.1102117108 21482766

15. Cox JS, Walter P. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell. 1996;87: 391–404. doi: 10.1016/S0092-8674(00)81360-4 8898193

16. Mori K, Ma WZ, Gething MJ, Sambrook J. A transmembrane protein with a Cdc2+/Cdc28-related kinase-activity is required for signaling from the ER to the nucleus. Cell. 1993;74: 743–756. doi: 10.1016/0092-8674(93)90521-Q 8358794

17. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8: 519–529. doi: 10.1038/nrm2199 17565364

18. Brodsky JL, McCracken AA. ER-associated and proteasome-mediated protein degradation: How two topologically restricted events came together. Trends Cell Biol. 1997;7: 151–156. doi: 10.1016/S0962-8924(97)01020-9 17708933

19. Tsai B, Ye Y, Rapoport TA. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nat Rev Mol Cell Biol. 2002;3: 246–255. doi: 10.1038/nrm780 11994744

20. Kanehara K, Kawaguchi S, Ng DT. The EDEM and Yos9p families of lectin-like ERAD factors. Semin Cell Dev Biol. 2007;18: 743–50. doi: 10.1016/j.semcdb.2007.09.007 17945519

21. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell. 2000;5: 897–904. doi: 10.1016/S1097-2765(00)80330-5 10882126

22. Brodsky JL, Skach WR. Protein folding and quality control in the endoplasmic reticulum: Recent lessons from yeast and mammalian cell systems. Curr Opin Cell Biol. 2011;23: 464–475. doi: 10.1016/j.ceb.2011.05.004 21664808

23. Iwata Y, Fedoroff NV, Koizumi N. Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell. 2008;20: 3107–3121. doi: 10.1105/tpc.108.061002 19017746

24. Su W, Liu Y, Xia Y, Hong Z, Li J. Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proc Natl Acad Sci U S A. 2010;108: 870–875. doi: 10.1073/pnas.1013251108 21187394

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

26. Howell SH. Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol. 2013;64: 477–499. doi: 10.1146/annurev-arplant-050312-120053 23330794

27. Fagone P, Jackowski S. Membrane phospholipid synthesis and endoplasmic reticulum function. J Lipid Res. 2009;50 Suppl:S311–316. doi: 10.1194/jlr.R800049-JLR200 18952570

28. Otterhag L, Sommarin M, Pical C. N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana. FEBS Lett. 2001;497: 165–170. doi: 10.1016/S0014-5793(01)02453-X 11377433

29. Liu JX, Srivastava R, Che P, Howell SH. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell. 2007;19: 4111–4119. doi: 10.1105/tpc.106.050021 18156219

30. Martinez IM, Chrispeels MJ. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell. 2003;15: 561–576. doi: 10.1105/tpc.007609 12566592

31. Noh SJ, Kwon CS, Oh DH, Moon JS, Chung WI. Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene. 2003;311: 81–91. doi: 10.1016/S0378-1119(03)00559-6 12853141

32. Cao Z, Zhang J, Li Y, Xu X, Liu G, Bhattacharrya MK, et al. Preparation of polyclonal antibody specific for AtPLC4, an Arabidopsis phosphatidylinositol-specific phospholipase C in rabbits. Protein Expr Purif. 2007;52: 306–312. doi: 10.1016/j.pep.2006.10.007 17142056

33. Zhong R, Burk DH, Morrison WH, Ye ZH. FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells. Plant Cell. 2004;16: 3242–3259. doi: 10.1105/tpc.104.027466 15539468

34. Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH III, Ye ZH. Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell. 2005;17: 1449–1466. doi: 10.1105/tpc.105.031377 15805481

35. Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, et al. VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development. 2005;132: 1699–1711. doi: 10.1242/dev.01716 15743878

36. Carland FM, Nelson T. COTYLEDON VASCULAR PATTERN2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell. 2004;16: 1263–1275. doi: 10.1105/tpc.021030 15100402

37. Naramoto S, Sawa S, Koizumi K, Uemura T, Ueda T, Friml J, et al. Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. Development. 2009;136: 1529–1538. doi: 10.1242/dev.030098 19363154

38. Kim DH, Eu YJ, Yoo CM, Kim YW, Pih KT, Jin JB, et al. Trafficking of phosphatidylinositol 3-phosphate from the trans-Golgi network to the lumen of the central vacuole in plant cells. Plant Cell. 2001;13: 287–301. doi: 10.1105/tpc.13.2.287 11226186

39. Thibault G, Shui G, Kim W, McAlister GC, Ismail N, Gygi SP, et al. The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network. Mol Cell. 2012;48: 16–27. doi: 10.1016/j.molcel.2012.08.016 23000174

40. van der Sanden MH, Houweling M, van Golde LM, Vaandrager AB. Inhibition of phosphatidylcholine synthesis induces expression of the endoplasmic reticulum stress and apoptosis-related protein CCAAT/enhancer-binding protein-homologous protein (CHOP/GADD153). Biochem J. 2003;369: 643–650. doi: 10.1042/BJ20020285 12370080

41. Yasuda E, Nagasawa K, Nishida K, Fujimoto S. Decreased expression of phospholipase C-beta 1 protein in endoplasmic reticulum stress-loaded neurons. Biol Pharm Bull. 2008;31: 719–721. doi: 10.1248/bpb.31.719 18379069

42. Sriburi R, Jackowski S, Mori K, Brewer JW. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J Cell Biol. 2004;167: 35–41. doi: 10.1083/Jcb.200406136 15466483

43. Winnay JN, Boucher J, Mori MA, Ueki K, Kahn CR. A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat Med. 2010;16: 438–445. doi: 10.1038/nm.2121 20348923

44. Thakur PC, Stuckenholz C, Rivera MR, Davison JM, Yao JK, Amsterdam A, et al. Lack of de novo phosphatidylinositol synthesis leads to endoplasmic reticulum stress and hepatic steatosis in cdipt-deficient zebrafish. Hepatology. 2011;54: 452–462. doi: 10.1002/hep.24349 21488074

45. Thakur PC, Davison JM, Stuckenholz C, Lu L, Bahary N. Dysregulated phosphatidylinositol signaling promotes endoplasmic-reticulum-stress-mediated intestinal mucosal injury and inflammation in zebrafish. Dis Model Mech. 2014;7: 93–106. doi: 10.1242/dmm.012864 24135483

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

47. Kim YJ, Guzman-Hernandez ML, Balla T. A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev Cell. 2011;21: 813–824. doi: 10.1016/j.devce1.2011.09.005 22075145

48. Wang PW, Hawkins TJ, Richardson C, Cummins I, Deeks MJ, Sparkes I, et al. The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr Biol. 2014;24: 1397–1405. doi: 10.1016/J.Cub.2014.05.003 24909329

49. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plantarum. 1962;15: 473–497. doi: 10.1111/J.1399-3054.1962.Tb08052.X

50. Karimi M, De Meyer B, Hilson P. Modular cloning in plant cells. Trends Plant Sci. 2005;10: 103–105. doi: 10.1016/j.tplants.2005.01.008 15749466

51. Sawano A, Miyawaki A. Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res. 2000;28: E78. doi: 10.1093/nar/28.16.e78 10931937

52. Drobak BK, Brewin NJ, Hernandez LE. Extraction, separation, and analysis of plant phosphoinositides and complex glycolipids. Methods Mol Biol. 2000;141: 157–174. doi: 10.1385/1-59259-067-5:157 10820743

53. Nasuhoglu C, Feng S, Mao J, Yamamoto M, Yin HL, Earnest S, et al. Nonradioactive analysis of phosphatidylinositides and other anionic phospholipids by anion-exchange high-performance liquid chromatography with suppressed conductivity detection. Anal Biochem. 2002;301: 243–254. doi: 10.1006/abio.2001.5489 11814295

54. Nakamura Y, Teo NZW, Shui GH, Chua CHL, Cheong WF, Parameswaran S, et al. Transcriptomic and lipidomic profiles of glycerolipids during Arabidopsis flower development. New Phytol. 2014;203: 310–322. doi: 10.1111/Nph.12774 24684726

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