Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 19, 2015, Pages 6212-6217

  Walley, Justin ^a,e   Xiao, Yanmei ^b   Wang, Jin Zheng ^b   Baidoo, Edward E ^c   Keasling, Jay D ^c,d   Shen, Zhouxin ^a   Briggs, Steven P ^a   Dehesh, Katayoon ^b  

^a SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d University of California at Berkeley   (United States)

^e IOWA STATE UNIVERSITY   (United States)

Author keywords

Endoplasmic reticulum; Interorgannellar communication; Methylerythritol cyclodiphosphate; Retrograde signaling; Unfolded protein response

Indexed keywords

ISOPRENOID; METHYLERYTHRITOL CYCLODIPHOSPHATE; PROTEIN DISULFIDE ISOMERASE; PROTEOME; TRANSCRIPTOME; UNCLASSIFIED DRUG; ERYTHRITOL; METHYL-D-ERYTHRITOL 2,4-CYCLODIPHOSPHATE; VEGETABLE PROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENVIRONMENTAL STRESS; GENE EXPRESSION; GENE INDUCTION; HOMEOSTASIS; INTRACELLULAR SIGNALING; LONG TERM CARE; LONG TERM EXPOSURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN ISOLATION; PROTEOMICS; ROOT GROWTH; ROOT LENGTH; TRANSGENE; UNFOLDED PROTEIN RESPONSE; ANALOGS AND DERIVATIVES; ARABIDOPSIS; CHEMISTRY; CHLOROPLAST; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; MICROARRAY ANALYSIS; PLASTID; SIGNAL TRANSDUCTION;

EUKARYOTA;

ARABIDOPSIS; CHLOROPLASTS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ERYTHRITOL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOMEOSTASIS; MICROARRAY ANALYSIS; PLANT PROTEINS; PLASTIDS; PROTEIN FOLDING; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; TRANSCRIPTOME; UNFOLDED PROTEIN RESPONSE;

EID: 84929208100     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504828112     Document Type: Article

References (37)

1. Walter P, Ron D (2011) The unfolded protein response: From stress pathway to homeostatic regulation. Science 334(6059):1081-1086.
2. Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22(9):2930-2942.
3. Howell SH (2013) Endoplasmic reticulum stress responses in plants. Annu Rev Plant Biol 64:477-499.
4. Iwata Y, Koizumi N (2012) Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci 17(12):720-727.
5. Toulmay A, Prinz WA (2011) Lipid transfer and signaling at organelle contact sites: The tip of the iceberg. Curr Opin Cell Biol 23(4):458-463.
6. Stefan CJ, Manford AG, Emr SD (2013) ER-PM connections: Sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25(4):434-442.
7. Andersson MX, Goksör M, Sandelius AS (2007) Membrane contact sites: Physical attachment between chloroplasts and endoplasmic reticulum revealed by optical manipulation. Plant Signal Behav 2(3):185-187.
8. Andersson MX, Goksör M, Sandelius AS (2007) Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. J Biol Chem 282(2):1170-1174.
9. Kaneko Y, Keegstra K (1996) Plastid biogenesis in embryonic pea leaf cells during early germination. Protoplasma 195(1-4):59-67.
10. Xiao Y, et al. (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149(7):1525-1535.
11. Bouvier F, Rahier A, Camara B (2005) Biogenesis, molecular regulation and function of plant isoprenoids. Prog Lipid Res 44(6):357-429.
12. Phillips MA, León P, Boronat A, Rodríguez-Concepción M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13(12):619-623.
13. Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5(2):318-333.
14. Xiao Y, Wang J, Dehesh K (2013) Review of stress specific organelles-to-nucleus metabolic signal molecules in plants. Plant Sci 212:102-107.
15. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414(6863):562-565.
16. Moreno AA, et al. (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS ONE 7(2): e31944.
17. Nagashima Y, Iwata Y, Ashida M, Mishiba K, Koizumi N (2014) Exogenous salicylic acid activates two signaling arms of the unfolded protein response in Arabidopsis. Plant Cell Physiol 55(10):1772-1778.
18. Wright LP, et al. (2014) Deoxyxylulose 5-Phosphate Synthase Controls Flux through the Methylerythritol 4-Phosphate Pathway in Arabidopsis. Plant Physiol 165(4): 1488-1504.
19. Deng Y, 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(17):7247-7252.
20. 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(48):19633-19638.
21. Mishiba K, 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(14):5713-5718.
22. Nagashima Y, et al. (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 1:29.
23. 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(14):5280-5285.
24. Lu DP, Christopher DA (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol Genet Genomics 280(3):199-210.
25. Humbert S, Zhong S, Deng Y, Howell SH, Rothstein SJ (2012) Alteration of the bZIP60/ IRE1 pathway affects plant response to ER stress in Arabidopsis thaliana. PLoS ONE 7(6):e39023.
26. Martínez IM, Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15(2): 561-576.
27. Deng Y, Srivastava R, Howell SH (2013) Endoplasmic Reticulum (ER) Stress Response and Its Physiological Roles in Plants. Int J Mol Sci 14(4):8188-8212.
28. Kalinski A, et al. (1995) Binding-protein expression is subject to temporal, developmental and stress-induced regulation in terminally differentiated soybean organs. Planta 195(4):611-621.
29. Lu DP, Christopher DA (2008) Light enhances the unfolded protein response as measured by BiP2 gene expression and the secretory GFP-2SC marker in Arabidopsis. Physiol Plant 134(2):360-368.
30. Schattat M, Barton K, Mathur J (2011) Correlated behavior implicates stromules in increasing the interactive surface between plastids and ER tubules. Plant Signal Behav 6(5):715-718.
31. Schattat MH, Klösgen RB, Mathur J (2012) New insights on stromules: Stroma filled tubules extended by independent plastids. Plant Signal Behav 7(9):1132-1137.
32. Walley JW, et al. (2007) Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genet 3(10):1800-1812.
33. Walley JW, et al. (2008) The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathog 4(12):e1000237.
34. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139(1):5-17.
35. O'Brien RN, Shen Z, Tachikawa K, Lee PA, Briggs SP (2010) Quantitative proteome analysis of pluripotent cells by iTRAQ mass tagging reveals post-transcriptional regulation of proteins required for ES cell self-renewal. Mol Cell Proteomics 9(10): 2238-2251.
36. Katari MS, et al. (2010) VirtualPlant: A software platform to support systems biology research. Plant Physiol 152(2):500-515.
37. Baidoo EEKXY, Dehesh K, Keasling JD (2014) Metabolite profiling of Plastidial Deoxyxylulose-5-phosphate pathway intermediates by liquid chromatography and mass spectrometry. Methods Mol Biol 1153:57-76.