Journal of Plant Biology

, Volume 61, Issue 6, pp 401–409 | Cite as

Heat Shock Proteins atHSP93-III and atHSP93-V Affect ABA Response and Leaf Senescence

  • Min Young Park
  • Soo Young KimEmail author
Original Article


We carried out activation tagging screen to isolate ABA signaling components and isolated an ABAhypersensitive mutant, ahs716 (ABA-hypersensitive 716). TDNA was inserted in the 5’ flanking region of the atHSP93-III gene in the mutant, and the atHSP93-III transcript level was barely detectable, indicating that it is a knockdown mutant. The mutant exhibited poor viability, and, therefore, we prepared and analyzed its overexpression (OX) lines to study its function. Plants overexpressing atHSP93-III were hypersensitive to ABA, and several ABA-regulated genes were up-regulated in the transgenic plants. We also investigated the role of atHSP93-V in ABA response. atHSP93-V is a paralog of atHSP93-III and encodes an isoform of HSP93. Although it is highly homologous to atHSP93-III, atHSP93-V OX did not affect ABA sensitivity. However, the atHSP93-V OX lines displayed early senescence phenotype, and changes in the expression levels of several senescence-related genes were observed in the transgenic lines. Collectively, our data suggest that, whereas atHSP93-V is involved in leaf senescence, atHSP93-III is involved in ABA response. Considering that HSP93 is a molecular chaperone essential for chloroplast biogenesis and function, the resuls provide evidence that chloroplast function is important for normal ABA response.


Abscisic acid (ABA) Chaperone Hsp93 Senescence 


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Supplementary material

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  1. Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell A, Zheng B, Vallon O, Rodermel SR, Shinozaki K, Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol 125: 1912–1918Google Scholar
  2. Bechtold N, and Pelletier, G (1998) In planta Agrobacteriummediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266Google Scholar
  3. Constan D, Froehlich JE, Rangarajan S, Keegstra K (2004) A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 136:3605–3615CrossRefGoogle Scholar
  4. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679CrossRefGoogle Scholar
  5. Finkelstein R (2013) Abscisic Acid synthesis and response. The Arabidopsis book /American Society of Plant Biologists 11: e0166CrossRefGoogle Scholar
  6. Flores-Perez U, Bedard J, Tanabe N, Lymperopoulos P, Clarke AK, Jarvis P (2016) Functional Analysis of the Hsp93/ClpC Chaperone at the Chloroplast Envelope. Plant Physiol 170:147–162CrossRefGoogle Scholar
  7. Flores-Perez U, Jarvis P (2013) Molecular chaperone involvement in chloroplast protein import. Biochim Biophys Acta 1833:332–340CrossRefGoogle Scholar
  8. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124:509–525CrossRefGoogle Scholar
  9. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 20:3901–3907CrossRefGoogle Scholar
  10. Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357CrossRefGoogle Scholar
  11. Kovacheva S, Bedard J, Patel R, Dudley P, Twell D, Rios G, Koncz C, Jarvis P (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 41:412–428CrossRefGoogle Scholar
  12. Kovacheva S, Bedard J, Wardle A, Patel R, Jarvis P (2007) Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 50:364–379CrossRefGoogle Scholar
  13. Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116CrossRefGoogle Scholar
  14. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628CrossRefGoogle Scholar
  15. Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient Isolation and Mapping of Arabidopsis thaliana T-DNA Insert Junctions by Thermal Asymmetric Interlaced PCR. Plant J 8:457–463CrossRefGoogle Scholar
  16. Park MY, Kang JY, Kim SY (2011) Overexpression of AtMYB52 confers ABA hypersensitivity and drought tolerance. Mol Cells 31:447–454CrossRefGoogle Scholar
  17. Park S, Rodermel SR (2004) Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis. Proc Natl Acad Sci USA 101:12765–12770CrossRefGoogle Scholar
  18. Schippers JHM, Schmidt R, Wagstaff C, Jing H-C (2015) Living to die and dying to live: the survival strategy behind leaf senescence. Plant Physiol 169:914–930CrossRefGoogle Scholar
  19. Shanklin J, DeWitt ND, Flanagan JM (1995) The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: an archetypal two-component ATP-dependent protease. Plant Cell 7:1713–1722Google Scholar
  20. Sjogren LL, MacDonald TM, Sutinen S, Clarke AK (2004) Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol 136:4114–4126CrossRefGoogle Scholar
  21. Sjogren LL, Tanabe N, Lymperopoulos P, Khan NZ, Rodermel SR, Aronsson H, Clarke AK (2014) Quantitative analysis of the chloroplast molecular chaperone ClpC/Hsp93 in Arabidopsis reveals new insights into its localization, interaction with the Clp proteolytic core, and functional importance. J Biol Chem 289: 11318–11330CrossRefGoogle Scholar
  22. Sokolenko A, Lerbs-Mache S, Altschmied L, Herrmann RG (1998) Clp protease complexes and their diversity in chloroplasts. Planta 207:286–295CrossRefGoogle Scholar

Copyright information

© Korean Society of Plant Biologists and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Molecular Biotechnology & Kumho Life Science Laboratory, College of Agriculture & Life SciencesChonnam National UniversityGwangjuKorea

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