Display options
Share it on

Hortic Res. 2015 Nov 11;2:15051. doi: 10.1038/hortres.2015.51. eCollection 2015.

Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components.

Horticulture research

Ying Hu, Qingyu Wu, Stuart A Sprague, Jungeun Park, Myungmin Oh, C B Rajashekar, Hisashi Koiwa, Paul A Nakata, Ninghui Cheng, Kendal D Hirschi, Frank F White, Sunghun Park

Affiliations

  1. Department of Horticulture, Forestry, and Recreation Resources, Kansas State University , Manhattan, KS 66506, USA.
  2. Department of Horticultural Science, Texas A&M University , College Station, TX 77843, USA.
  3. United States Department of Agriculture/Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine , Houston, TX 77030, USA.
  4. Department of Plant Pathology, Kansas State University , Manhattan, KS 66506, USA.

PMID: 26623076 PMCID: PMC4641303 DOI: 10.1038/hortres.2015.51

Abstract

Chilling stress is a production constraint of tomato, a tropical origin, chilling-sensitive horticultural crop. The development of chilling tolerant tomato thus has significant potential to impact tomato production. Glutaredoxins (GRXs) are ubiquitous oxidoreductases, which utilize the reducing power of glutathione to reduce disulfide bonds of substrate proteins and maintain cellular redox homeostasis. Here, we report that tomato expressing Arabidopsis GRX gene AtGRXS17 conferred tolerance to chilling stress without adverse effects on growth and development. AtGRXS17-expressing tomato plants displayed lower ion leakage, higher maximal photochemical efficiency of photosystem II (Fv/Fm) and increased accumulation of soluble sugar compared with wild-type plants after the chilling stress challenge. Furthermore, chilling tolerance was correlated with increased antioxidant enzyme activities and reduced H2O2 accumulation. At the same time, temporal expression patterns of the endogenous C-repeat/DRE-binding factor 1 (SlCBF1) and CBF mediated-cold regulated genes were not altered in AtGRXS17-expressing plants when compared with wild-type plants, and proline concentrations remained unchanged relative to wild-type plants under chilling stress. Green fluorescent protein -AtGRXS17 fusion proteins, which were initially localized in the cytoplasm, migrated into the nucleus during chilling stress, reflecting a possible role of AtGRXS17 in nuclear signaling of chilling stress responses. Together, our findings demonstrate that genetically engineered tomato plants expressing AtGRXS17 can enhance chilling tolerance and suggest a genetic engineering strategy to improve chilling tolerance without yield penalty across different crop species.

References

  1. Biotechniques. 2005 Sep;39(3):301-2, 304 - PubMed
  2. Plant Cell. 2005 Jul;17(7):1866-75 - PubMed
  3. Nat Biotechnol. 1999 Mar;17(3):287-91 - PubMed
  4. New Phytol. 2012 Sep;195(4):737-51 - PubMed
  5. Methods Biochem Anal. 1954;1:357-424 - PubMed
  6. Biochim Biophys Acta. 2008 Nov;1780(11):1304-17 - PubMed
  7. J Plant Physiol. 2008 May 26;165(8):813-24 - PubMed
  8. J Cell Sci. 2001 May;114(Pt 9):1643-53 - PubMed
  9. Plant Cell. 2015 Jan;27(1):104-20 - PubMed
  10. Plant Cell. 2008 Aug;20(8):2117-29 - PubMed
  11. Annu Rev Plant Biol. 2008;59:143-66 - PubMed
  12. Plant Physiol. 2015 Apr;167(4):1643-58 - PubMed
  13. Annu Rev Plant Biol. 2007;58:459-81 - PubMed
  14. Plant Physiol. 2002 Oct;130(2):618-26 - PubMed
  15. Plant Cell Rep. 2011 Oct;30(10):1949-57 - PubMed
  16. Physiol Plant. 2010 Apr;138(4):405-13 - PubMed
  17. Arch Biochem Biophys. 1986 May 15;247(1):1-11 - PubMed
  18. Science. 1988 Jun 3;240(4857):1302-9 - PubMed
  19. Antioxid Redox Signal. 2003 Feb;5(1):15-22 - PubMed
  20. Nat Protoc. 2006;1(4):2019-25 - PubMed
  21. Cryobiology. 1987 Aug;24(4):324-31 - PubMed
  22. Antioxid Redox Signal. 2005 Mar-Apr;7(3-4):348-66 - PubMed
  23. Plant Cell. 2009 Feb;21(2):429-41 - PubMed
  24. Mol Gen Genet. 1978 Jul 11;163(2):181-7 - PubMed
  25. Annu Rev Plant Biol. 2004;55:373-99 - PubMed
  26. J Biol Chem. 2002 Apr 19;277(16):13609-14 - PubMed
  27. Plant Biotechnol J. 2011 Feb;9(2):230-49 - PubMed
  28. Annu Rev Genet. 2009;43:335-67 - PubMed
  29. Plant Biotechnol J. 2007 Sep;5(5):591-604 - PubMed
  30. Planta. 2010 Jan;231(2):361-9 - PubMed
  31. Mol Plant Microbe Interact. 2004 Apr;17 (4):343-50 - PubMed
  32. Arch Biochem Biophys. 1994 Jul;312(1):52-8 - PubMed
  33. Plant Cell. 2002 Aug;14(8):1675-90 - PubMed
  34. DNA Res. 2010 Dec;17(6):353-67 - PubMed
  35. J Biol Chem. 1987 Jul 15;262(20):9895-901 - PubMed
  36. Eur J Biochem. 2000 Aug;267(16):4928-44 - PubMed
  37. J Biochem. 1997 May;121(5):842-8 - PubMed
  38. J Plant Physiol. 2011 Oct 15;168(15):1804-12 - PubMed
  39. Trends Plant Sci. 2002 May;7(5):193-5 - PubMed
  40. Biochim Biophys Acta. 2001 Sep 3;1514(1):100-16 - PubMed
  41. Anal Biochem. 1987 Mar;161(2):559-66 - PubMed
  42. Trends Plant Sci. 2007 Oct;12(10):444-51 - PubMed
  43. J Integr Bioinform. 2010 Mar 25;7(3):null - PubMed
  44. Trends Plant Sci. 2014 Apr;19(4):256-65 - PubMed
  45. J Exp Bot. 2004 Jan;55(395):225-36 - PubMed
  46. Free Radic Biol Med. 2012 Aug 15;53(4):936-50 - PubMed
  47. J Plant Physiol. 2009 Jan 30;166(2):180-91 - PubMed
  48. J Cell Sci. 2006 Nov 1;119(Pt 21):4554-64 - PubMed
  49. J Biol Chem. 2006 Sep 8;281(36):26280-8 - PubMed
  50. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:249-279 - PubMed
  51. Antioxid Redox Signal. 2009 Apr;11(4):861-905 - PubMed
  52. Plant J. 2011 Nov;68(3):507-19 - PubMed
  53. Biochem J. 1954 Jul;57(3):508-14 - PubMed
  54. Plant Physiol. 2010 Oct;154(2):571-7 - PubMed
  55. J Biol Chem. 2011 Jun 10;286(23):20398-406 - PubMed
  56. Trends Plant Sci. 2004 Oct;9(10):490-8 - PubMed
  57. FEBS J. 2011 Jul;278(14):2525-39 - PubMed
  58. Plant Physiol. 2001 Nov;127(3):910-7 - PubMed
  59. J Exp Bot. 2006;57(3):449-59 - PubMed
  60. J Exp Bot. 2011 Jul;62(11):3807-19 - PubMed
  61. Plant Physiol. 2005 Jan;137(1):317-27 - PubMed
  62. J Exp Bot. 2012 Jan;63(1):503-15 - PubMed
  63. Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9873-8 - PubMed
  64. Plant Physiol Biochem. 2010 Dec;48(12):909-30 - PubMed
  65. Anal Biochem. 2009 Apr 15;387(2):238-42 - PubMed
  66. Plant Biotechnol J. 2012 Oct;10(8):945-55 - PubMed
  67. Plant Cell Environ. 2009 Jul;32(7):851-8 - PubMed
  68. Methods Mol Biol. 2010;639:317-31 - PubMed
  69. Plant Cell. 2015 Jan;27(1):121-31 - PubMed
  70. J Plant Physiol. 2003 Oct;160(10):1253-7 - PubMed
  71. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47:509-540 - PubMed
  72. Antioxid Redox Signal. 2005 Jul-Aug;7(7-8):919-29 - PubMed
  73. PLoS One. 2011 Mar 08;6(3):e17603 - PubMed
  74. J Appl Genet. 2009;50(4):311-9 - PubMed
  75. Plant J. 2004 Sep;39(6):905-19 - PubMed
  76. Plant J. 2006 Sep;47(6):851-63 - PubMed

Publication Types