Cyclic nucleotide-gated ion channel 6 mediates thermotolerance in Arabidopsis seedlings by regulating nitric oxide production via cytosolic calcium ions.

Publisher: BioMed Central Country of Publication: England NLM ID: 100967807 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2229 (Electronic) Linking ISSN: 14712229 NLM ISO Abbreviation: BMC Plant Biol Subsets: MEDLINE

Original Publication: London : BioMed Central, [2001-

Thermotolerance*; Arabidopsis/*metabolism ; Arabidopsis Proteins/*metabolism ; Calcium/*metabolism ; Cyclic Nucleotide-Gated Cation Channels/*metabolism ; Nitric Oxide/*metabolism; Arabidopsis/genetics ; Arabidopsis Proteins/genetics ; Calcium Channels/metabolism ; Cyclic Nucleotide-Gated Cation Channels/genetics ; Cytosol/metabolism ; Heat-Shock Proteins/genetics ; Heat-Shock Proteins/metabolism ; Heat-Shock Response ; Mutation ; Nitrate Reductase/genetics ; Nitrate Reductase/metabolism ; Nitric Oxide Synthase/genetics ; Nitric Oxide Synthase/metabolism ; Seedlings/genetics ; Seedlings/metabolism

Background: We previously reported the involvement of nitric oxide (NO) and cyclic nucleotide-gated ion channel 6 (CNGC6) in the responses of plants to heat shock (HS) exposure. To elucidate their relationship with heat tolerance in Arabidopsis thaliana, we examined the effects of HS on several groups of seedlings: wild type, cngc6, and cngc6 complementation and overexpression lines.
Results: After HS exposure, the level of NO was lower in cngc6 seedlings than in wild-type seedlings but significantly elevated in the transgenic lines depending on CNGC6 expression level. The treatment of seeds with calcium ions (Ca ²⁺ ) enhanced the NO level in Arabidopsis seedlings under HS conditions, whereas treatment with EGTA (a Ca ²⁺ chelator) reduced it, implicating that CNGC6 stimulates the accumulation of NO depending on an increase in cytosolic Ca ²⁺ ([Ca ²⁺ ] cyt ). This idea was proved by phenotypic observations and thermotolerance testing of transgenic plants overexpressing NIA2 and NOA1, respectively, in a cngc6 background. Western blotting indicated that CNGC6 stimulated the accumulation of HS proteins via NO.
Conclusion: These data indicate that CNGC6 acts upstream of NO in the HS pathway, which improves our insufficient knowledge of the initiation of plant responses to high temerature.

Plant J. 1998 Dec;16(6):735-43. (PMID: 10069079)
Biochem J. 2001 Aug 1;357(Pt 3):593-615. (PMID: 11463332)
Plant Physiol. 2002 Feb;128(2):379-87. (PMID: 11842142)
Trends Plant Sci. 2003 Jun;8(6):286-93. (PMID: 12818663)
Science. 2003 Oct 3;302(5642):100-3. (PMID: 14526079)
Cell Calcium. 2005 Sep-Oct;38(3-4):161-9. (PMID: 16076488)
Biochem Biophys Res Commun. 2005 Nov 4;336(4):1259-67. (PMID: 16181612)
Trends Plant Sci. 2006 Jan;11(1):15-9. (PMID: 16359910)
J Exp Bot. 2006;57(6):1341-51. (PMID: 16531462)
Free Radic Biol Med. 2006 Apr 15;40(8):1369-76. (PMID: 16631527)
Methods Mol Biol. 2006;323:307-27. (PMID: 16739587)
Plant Cell Environ. 2007 Feb;30(2):156-64. (PMID: 17238907)
New Phytol. 2007;176(3):550-9. (PMID: 17953540)
Annu Rev Plant Biol. 2008;59:21-39. (PMID: 18031216)
Plant Cell. 2008 Mar;20(3):786-802. (PMID: 18326829)
Plant J. 2008 Sep;55(5):760-73. (PMID: 18466301)
Plant Cell. 2008 May;20(5):1303-15. (PMID: 18469163)
Plant Physiol. 2009 Apr;149(4):1773-84. (PMID: 19211698)
Plant Physiol. 2010 Aug;153(4):1895-906. (PMID: 20576787)
Plant Physiol. 2011 Feb;155(2):1023-36. (PMID: 21139086)
Plant J. 2012 Feb;69(4):689-700. (PMID: 22007900)
Plant J. 2012 Jun;70(6):1056-69. (PMID: 22372427)
Plant Cell. 2012 Aug;24(8):3333-48. (PMID: 22904147)
Plant Physiol. 2013 Feb;161(2):1010-20. (PMID: 23370720)
Plant Physiol. 2013 Oct;163(2):459-70. (PMID: 23749853)
Plant Physiol. 2014 Apr;164(4):2184-96. (PMID: 24510762)
Plant Cell Physiol. 2014 Nov;55(11):1873-83. (PMID: 25149227)
J Exp Bot. 2016 Feb;67(3):809-19. (PMID: 26608645)
Curr Biol. 2015 Dec 7;25(23):3119-25. (PMID: 26752079)
Front Plant Sci. 2016 Jan 21;6:1161. (PMID: 26834755)
Proc Natl Acad Sci U S A. 2016 Mar 15;113(11):3096-101. (PMID: 26929345)
Front Plant Sci. 2016 Mar 31;7:398. (PMID: 27066042)
Front Plant Sci. 2016 Apr 12;7:471. (PMID: 27148300)
Cell Physiol Biochem. 2016;39(1):341-9. (PMID: 27352220)
Curr Genomics. 2016 Aug;17(4):315-29. (PMID: 27499681)
Sci Rep. 2016 Oct 12;6:35246. (PMID: 27731387)
Biomed Pharmacother. 2017 Feb;86:8-15. (PMID: 27936394)
Bio Protoc. 2016 Jul 20;6(14):. (PMID: 28491909)
Front Plant Sci. 2017 Sep 13;8:1582. (PMID: 28955368)
Curr Opin Plant Biol. 2018 Oct;45(Pt B):212-217. (PMID: 29673612)
Cell Stress Chaperones. 2019 Mar;24(2):295-308. (PMID: 30758704)
Anal Biochem. 1976 May 7;72:248-54. (PMID: 942051)
Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10328-33. (PMID: 9707647)

Keywords: Arabidopsis; Cyclic nucleotide-gated ion channel 6; Heat shock; Heat shock protein; Nitric oxide

0 (Arabidopsis Proteins)
0 (CNGC6 protein, Arabidopsis)
0 (Calcium Channels)
0 (Cyclic Nucleotide-Gated Cation Channels)
0 (Heat-Shock Proteins)
31C4KY9ESH (Nitric Oxide)
EC 1.14.13.39 (NOA1 protein, Arabidopsis)
EC 1.14.13.39 (Nitric Oxide Synthase)
EC 1.7.1.1 (NIA2 protein, Arabidopsis)
EC 1.7.99.4 (Nitrate Reductase)
SY7Q814VUP (Calcium)

Date Created: 20190821 Date Completed: 20190827 Latest Revision: 20200225

20240105

PMC6702746

10.1186/s12870-019-1974-9

31429706