Abstract
Main conclusion
Despite AtJ3 and AtJ2 sharing a high protein-sequence identity and both being substrates of protein farnesyltransferase (PFT), AtJ3 but not AtJ2 mediates in Arabidopsis the heat-dependent phenotypes derived from farnesylation modification.
Abstract
Arabidopsis HEAT-INTOERANT 5 (HIT5)/ENHANCED RESPONSE TO ABA 1 (ERA1) encodes the β-subunit of the protein farnesyltransferase (PFT), and the hit5/era1 mutant is better able to tolerate heat-shock stress than the wild type. Given that Arabidopsis AtJ2 (J2) and AtJ3 (J3) are heat-shock protein 40 (HSP40) homologs, sharing 90% protein-sequence identity, and each contains a CaaX box for farnesylation; atj2 (j2) and atj3 (j3) mutants were subjected to heat-shock treatment. Results showed that j3 but not j2 manifested the heat-shock tolerant phenotype. In addition, transgenic j3 plants that expressed a CaaX- abolishing J3C417S construct maintained the same capacity to tolerate heat shock as j3. The basal transcript levels of HEAT-SHOCK PROTEIN 101 (HSP101) in hit5/era1 and j3 were higher than those in the wild type. Although the capacities of j3/hsp101 and hit5/hsp101 double mutants to tolerate heat-shock stress declined compared to those of j3 and hit5/era1, they were still greater than that of the wild type. These results show that a lack of farnesylated J3 contributes to the heat-dependent phenotypes of hit5/era1, in part by the modulation of HSP101 activity, and also indicates that (a) mediator(s) other than J3 is (are) involved in the PFT-regulated heat-stress response. In addition, because HSP40s are known to function in dimer formation, bimolecular fluorescence complementation experiments were performed, and results show that J3 could dimerize regardless of farnesylation. In sum, in this study, a specific PFT substrate was identified, and its roles in the farnesylation-regulated heat-stress responses were clarified, which could be of use in future agricultural applications.
Similar content being viewed by others
Abbreviations
- BiFC:
-
Bi-molecular fluorescence complementation
- ERA1:
-
Enhanced response to aba 1
- EYFP:
-
Enhanced yellow fluorescence protein
- HIT5:
-
Heat-intolerant 5
- HSP (40, 70, 101):
-
Heat-shock protein (40, 70, 101)
- HSR:
-
Heat-stress response
- J2/J3:
-
AtJ2/AtJ3 (Arabidopsis thaliana DnaJ homologue 2/3)
- PFT:
-
Protein farnesyltransferase
References
Barghetti A, Siögren L, Floris M, Paredes EB, Wenkel S, Brodersen P (2017) Heat-shock protein 40 is the key farnesylation target in meristem size control, abscisic acid signaling, and drought resistance. Genes Dev 31:2282–2295. https://doi.org/10.1101/gad.301242.117
Blanvillain R, Boavida LC, McCormick S, Ow DW (2008) EXPORTIN1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. Genetics 180:1493–1500. https://doi.org/10.1534/genetics.108.094896
Caplan AJ, Tsai J, Casey PJ, Douglas MG (1992) Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J Biol Chem 267:18890–18895. http://www.jbc.org/content/267/26/18890.long
Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P (1996) A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science 273:1239–1241. https://doi.org/10.1126/science.273.5279.1239
Cyr DM, Ramos CH (2015) Specification of Hsp70 function by type I and type II Hsp40. Subcell Biochem 78:91–102. https://doi.org/10.1007/978-3-319-11731-7_4
Dutilleul C, Ribeiro I, Blanc N, Nezames CD, Deng XW, Zglobicki P, Barrera AMP, Atehortùa L, Courtois M, Labas V, Giolioli-Guivarc’h N, Ducos E (2016) ASG2 is a farnesylated DWD protein that acts as ABA negative regulator in Arabidopsis. Plant, Cell Environ 39:185–198. https://doi.org/10.1111/pce.12605
Galichet A, Gruissem W (2003) Protein farnesylation in plants—conserved mechanisms but different targets. Curr Opin Plant Biol 6:530–535. https://doi.org/10.1016/j.pbi.2003.09.005
Goritschnig S, Weihmann T, Zhang Y, Fobert P, McCourt P, Li X (2008) A novel role for protein farnesylation in plant innate immunity. Plant Physiol 148:348–357. https://doi.org/10.1104/pp.108.117663
Ham BK, Park JM, Lee SB, Kim MJ, Lee IJ, Kim KJ, Kwon CS, Paek KH (2006) Tobacco Tsip1, a DnaJ-type Zn finger protein, is recruited to and potentiates Tsi1-mediated transcriptional activation. Plant Cell 18:2005–2020. https://doi.org/10.1105/tpc.106.043158
Hashiguchi A, Komatsu S (2017) Posttranslational modifications and plant-environment interaction. Methods Enzymol 586:97–113. https://doi.org/10.1016/bs.mie.2016.09.030
Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci USA 97:4392–4397. https://doi.org/10.1073/pnas.97.8.4392
Hu C, Lin SY, Chi WT, Charng YY (2012) Recent gene duplication and subfunctionalization produced a mitochondrial GrpE, the nucleotide exchange factor of the Hsp70 complex, specialized in thermotolerance to chronic heat stress in Arabidopsis. Plant Physiol 158:747–758. https://doi.org/10.1104/pp.111.187674
Huang HY, Chang KY, Wu SJ (2018) High irradiance sensitive phenotype of Arabidopsis hit2/xpo1a mutant is caused in part by nuclear confinement of AtHsfA4a. Biol Plantarum 62:69–79. https://doi.org/10.1007/s10535-017-0753-4
Jalakas P, Huang YC, Yeh YH, Zimmerli L, Merilo E, Kollist H, Brosché M (2017) The role of ENHANCED RESPONSES TO ABA1(ERA1) in Arabidopsis stomatal responses is beyond ABA signaling. Plant Physiol 174:665–671. https://doi.org/10.1104/pp.17.00220
Jiang H, Zhang X, Chen X, Aramsangtienchai P, Tong Z, Lin H (2018) Protein lipidation: occurrence, mechanisms, biological functions and enabling technologies. Chem Rev 118:919–988. https://doi.org/10.1021/acs.chemrev.6b00750
Lee CF, Pu HY, Wang LC, Sayler RJ, Yeh CH, Wu SJ (2006) Mutation in a homolog of yeast Vps53p accounts for the heat and osmotic hypersensitive phenotypes in Arabidopsis hit1-1 mutant. Planta 224:330–338. https://doi.org/10.1007/s00425-005-0216-6
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529:84–87. https://doi.org/10.1038/nature16467
Liberek K, Marszalek J, Ang D, Georgopoulos C, Zylicz M (1991) Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci USA 88:2874–2878. https://doi.org/10.1073/pnas.88.7.2874
Liu HT, Gao F, Li GL, Han JL, Liu DL, Sun DY, Zhou RG (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55:760–773. https://doi.org/10.1111/j.1365-313X.2008.03544.x
Liu HC, Liao HT, Charng YY (2011) The role of class A1 heat shock factors (HSFA1 s) in response to heat and other stresses in Arabidopsis. Plant, Cell Environ 34:738–751. https://doi.org/10.1111/j.1365-3040.2011.02278.x
Manavalan LP, Chen X, Clarke J, Salmeron J, Nguyen HT (2012) RNAi-mediated disruption of squalene synthase improves drought tolerance and yield in rice. J Exp Bot 63:163–175. https://doi.org/10.1093/jxb/err258
Manmathan H, Shaner D, Snelling J, Tisserat N, Lapitan N (2013) Virus-induced gene silencing of Arabidopsis thaliana gene homologous in wheat identifies genes conferring improved drought tolerance. J Exp Bot 64:1381–1392. https://doi.org/10.1093/jxb/ert003
Morgner N, Schmidt C, Beilsten-Edmands V, Ebong IO, Patel NA, Clerico EM, Kierschke E, Daturpalli S, Jackson SE, Agard D, Robinson CV (2015) Hsp70 forms antiparallel dimers stabilized by post-translational modifications to position clients form transfer to Hsp90. Cell Rep 11:759–769. https://doi.org/10.1016/j.celrep.2015.03.063
Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282:287–290. https://doi.org/10.1126/science.282.5387.287
Pulido P, Leister D (2018) Novel DNAJ-related proteins in Arabidopsis thaliana. New Phytol 217:480–490. https://doi.org/10.1111/nph.14827
Rajan VBV, D’Silva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genomics 9:433–446. https://doi.org/10.1007/s10142-009-0132-0
Reindl A, Schoffl F, Schell J, Koncz C, Bako L (1997) Phosphorylation by a cyline-dependent kinase modulates DNA binding of the Arabidopsis heat-shock-transcription factor HSF1 in vitro. Plant Physiol 115:93–100. https://doi.org/10.1104/pp.115.1.93
Running MP (2014) The role of lipid post-translational modification in plant developmental processes. Front Plant Sci 5:50. https://doi.org/10.3389/fpls.2014.00050
Running MP, Fletcher JC, Meyerowitz EM (1998) The WIGGUM gene is required for proper regulation of floral meristem size in Arabidopsis. Development 125: 2545–2553. http://dev.biologists.org/content/125/14/2545.full.pdf
Sable A, Agarwal SK (2018) Plant heat shock protein families: essential machinery for development and defense. J Biol Sci Med 4:51–64. http://jbscim.com/index.php/jbsm/article/view/82
Sarbeng EB, Liu Q, Tian X, Yang J, Hongtao Li, Wong JL, Zhou L, Liu QL (2015) A functional DnaK dimer is essential for the efficient interaction with Hsp40 heat shock protein. J Biol Chem 290:8849–8862. https://doi.org/10.1074/jbc.M114.596288
Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta 1819:104–119. https://doi.org/10.1016/j.bbagrm.2011.10.002
Shi YY, Hong XG, Wang CC (2005) The C-terminal (331-376) sequence of Escherichia coli DnaJ is essential for dimerization and chaperone activity: a small angle X-ray scattering study in solution. J Biol Chem 280:22761–22768. https://doi.org/10.1074/jbc.M503643200
Uchida T, Kanemori M (2018) Two J domains ensure high cochaperone activity of DnaJ, Escherichia coli heat shock protein 40. J Biochem 164:153–163. https://doi.org/10.1093/jb/mvy038
Venne AS, Kollipara L, Zahedi RP (2014) The next level of complexity: crosstalk of posttranstrational modification. Proteomics 14:513–524. https://doi.org/10.1002/pmic.201300344
Wang M, Casey PJ (2016) Protein prenylation: unique fats make their mark on biology. Nat Rev Mol Boil Cell Biol 17:110–122. https://doi.org/10.1038/nrm.2015.11
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252. https://doi.org/10.1016/j.tplants.2004.03.006
Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT, McCourt P, Huang Y (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43:413–424. https://doi.org/10.1111/j.1365-313X.2005.02463.x
Wang LC, Tsai MC, Chang KY, Fan YS, Yeh CH, Wu SJ (2011) Involvement of the Arabidopsis HIT1/AtVPS53 tethering protein homologue in the acclimation of plasma membrane to heat stress. J Exp Bot 62:3609–3620. https://doi.org/10.1093/jxb/err060
Wang LC, Wu JR, Chang WL, Yeh CH, Ke YT, Lu CA, Wu SJ (2013) Arabidopsis HIT4 encodes a novel chromocentre-localized protein involved in the heat reactivation of transcriptionally silent loci and is essential for heat tolerance in plants. J Exp Bot 64:1689–1701. https://doi.org/10.1093/jxb/ert030
Wu YK, Li JZ, Jin ZM, Fu ZQ, Sha BD (2005) The crystal structure of the c-terminal fragment of Yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. J Mol Biol 346:1005–1011. https://doi.org/10.1016/j.jmb.2004.12.040
Wu FH, Shen SC, Lee LY, Lee SH, Chan MT, Lin CS (2009) Tape-Arabidopsis sandwich–a simpler Arabidopsis protoplast isolationmethod. Plant Methods 5:16. https://doi.org/10.1186/1746-4811-5-16
Wu SJ, Wang LC, Yeh CH, Lu CA, Wu SJ (2010) Isolation and characterization of Arabidopsis heat-intolerant 2 (hit2) mutant reveal the essential role of the nuclear export receptor EXPORTIN1A (XPO1A) in plant heat tolerance. New Phytol 186:833–842. https://doi.org/10.1111/j.1469-8137.2010.03225.x
Wu JR, Wang LC, Lin YR, Weng CP, Yeh CH, Wu SJ (2017) The Arabidopsis heat-intolerant 5 (hit5)/enhanced response to aba 1 (era1) mutant reveals the crucial role of protein farnesylation in plant responses to heat stress. New Phytol 213:1181–1193. https://doi.org/10.1111/nph.14212
Yamada K, Fukao Y, Hayashi M, Fukazawa M, Suzuki I, Nishimura M (2007) Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J Biol Chem 282:37794–37804. https://doi.org/10.1074/jbc.M707168200
Yeh CH, Kaplinsky NJ, Catherine Hu, CHarng YY (2012) Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci 195:10–23. https://doi.org/10.1016/j.plantsci.2012.06.004
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protoc 2:1565–1572. https://doi.org/10.1038/nprot.2007.199
Yoshida T et al (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 268:321–332. https://doi.org/10.1007/s00438-011-0647-7
Zhu JK, Bressan RA, Hasegawa PM (1993) Isoprenylaiton of the plant molecular chaperone ANJ1 facilitates membrane association and function at high temperature. Proc Natl Acad Sci USA 90:8557–8561. https://doi.org/10.1073/pnas.90.18.8557
Acknowledgements
The authors are very grateful to Dr. Peter Brodersen for providing the J3C417S transgenic line. This work was funded by the Ministry of Science and Technology, Taiwan (MOST 105-2311-B-008-004-MY3 and 108-2311-B-008-004-MY3 to S-JW).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wu, JR., Wang, TY., Weng, CP. et al. AtJ3, a specific HSP40 protein, mediates protein farnesylation-dependent response to heat stress in Arabidopsis. Planta 250, 1449–1460 (2019). https://doi.org/10.1007/s00425-019-03239-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-019-03239-7