Biologia plantarum 62:663-670, 2018 | DOI: 10.1007/s10535-018-0807-2

Abscisic acid biosynthesis under water stress: anomalous behavior of the 9-cis-epoxycarotenoid dioxygenase1 (NCED1) gene in rice

S. S. Changan1, K. Ali1, V. Kumar2, N. K. Garg1, A. Tyagi1,*
1 Division of Biochemistry, Indian Agricultural Research Institute, New Delhi, India
2 Division of Basic Sciences, Indian Institute of Pulse Research, Kanpur, India

The gene NCED1 encodes 9-cis-epoxycarotenoid dioxygenase, which catalyzes oxidative cleavage of 9-cis-epoxycarotenoids neoxanthin and violaxanthin to xanthoxin, a key step in the biosynthesis of abscisic acid in higher plants. In the present study, the complete NCED1 of 1 917 bp was cloned and characterized from rice (Oryza sativa L. cv. N22) as no earlier reports were available for its characterization from indica cultivar. The NCED1 had no intron and encoded a protein of 639 amino acids with a predicted molecular mass of 68.62 kD and pI of 6.07. The aliphatic index and grand average of hydropathicity were found to be 77.04 and -0.148, respectively. Multiple alignment analysis revealed that the sequence shared a high identity with the Oryza sativa japonica group (100 %) followed by Triticum aestivum (90 %), Hordeum vulgare (90 %), and Zea mays (89 %). The enzyme had a RPE65 domain of 476 amino acid residues. The RPE65 domain requires Fe(II) as a cofactor coordinated with 4 histidine residues and 3 glutamic acid residues. The phylogenic tree shows that NCED1 of japonica rice and NCED1 of indica rice were in the same group. They might have been evolved from a common ancestor. Analysis with a PSORT III tool shows that NCED is a chloroplastic protein. The real-time quantitative PCR and RNA-sequencing studies show that the expression of NCED1 was progressively reduced with increasing water stress, and a negative correlation between expression of OsNCED1 and severity of stress was established. Further, NCED1 expression negatively correlated with abscisic acid (ABA) accumulation under water stress whereas in some other species its expression increased along with ABA accumulation. This might be due to feedback inhibition of the ABA biosynthesis in rice.

Keywords: carotenoids; membrane stability index; phylogenetic tree; relative water content
Subjects: abscisic acid; 9-cis-epoxycarotenoid dioxygenase; carotenoids; water stress; relative water content; cell membrane stability; phylogenetic tree; gene expression; rice
Species: Oryza sativa

Received: May 8, 2017; Revised: November 29, 2017; Accepted: December 4, 2017; Published: August 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Changan, S.S., Ali, K., Kumar, V., Garg, N.K., & Tyagi, A. (2018). Abscisic acid biosynthesis under water stress: anomalous behavior of the 9-cis-epoxycarotenoid dioxygenase1 (NCED1) gene in rice. Biologia plantarum62(4), 663-670. doi: 10.1007/s10535-018-0807-2.
Download citation

Supplementary files

Download filebpl-201804-0006_S1.pdf

File size: 497.33 kB

References

  1. Alet, A.I., Sanchez, D.H., Cuevas, J.C., Del Valle, S., Altabella, T., Tiburcio, A.F., Marco, F., Ferrando, A., Espasandín, F.D., González, M.E., Ruiz, O.A., Carrasco, P.: Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. - Plant Signal. Behav. 6: 278-286, 2011. Go to original source...
  2. Alexandre, M.S., Vandré, G.L., Morganna, P.N., Janivan, F., Liziane, M., Pedro, D. F.: Expression of NCED gene in colored cotton genotypes subjected to water stress. - Rev. bras. Eng. Agr. ambient. 20: 692-696, 2016.
  3. Ali, K., Gujjar, R.S., Niwas, R., Gopal, M., Tyagi, A.: A rapid method for estimation of abscisic acid and characterization of aba regulated gene in response to water deficit stress from rice. - Amer. J. Plant Physiol. 6: 144-156, 2011.
  4. Barr, H.D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves. - Aust. J. biol. Sci. 15: 413-428, 1962. Go to original source...
  5. Boneh, U., Biton, I., Zheng, C., Schwartz, A., Ben-Ari, G.: Characterization of potential ABA receptors in Vitis vinifera. - Plant Cell Rep. 31: 311-321, 2012. Go to original source...
  6. Burbidge, A., Grieve, T., Jackson, A., Thompson, A., Taylor, I.: Structure and expression of a cDNA encoding a putative neoxanthin cleavage enzyme (NCE), isolated from a wiltrelated tomato (Lycopersicon esculentum Mill.) library. - J. exp. Bot. 47: 2111-2112, 1997. Go to original source...
  7. Chai, Y.M., Jia, H.F., Li, C.L., Dong, Q.H., Shen, Y.Y.: FaPYR1 is involved in strawberry fruit ripening. - J. exp. Bot. 62: 5079-5089, 2011. Go to original source...
  8. Chernys, J.T., Zeevaart, J.A.: Characterization of the 9-cisepoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. - Plant Physiol. 124: 343-353, 2000. Go to original source...
  9. Cutler, A.J., Krochko, J.E.: Formation and breakdown of ABA. - Trends Plant Sci. 4: 472-478, 1999. Go to original source...
  10. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., Abrams, S.R.: Abscisic acid: emergence of a core signaling network. - Annu. Rev. Plant Biol. 61: 651-679, 2010. Go to original source...
  11. Estrada-Melo, A.C. Ma, C., Reid, M.S., Jiang, C.-Z.: Overexpression of an ABA biosynthesis gene using a stressinducible promoter enhances drought resistance in petunia. - Hort. Res. 2: 15013, 2015. Go to original source...
  12. Hwang, S.G., Chen, H.C., Huang, W.Y., Chu, Y.C., Shii, C.T., Cheng, W.H.: Ectopic expression of rice OsNCED3 in Arabidopsis increases ABA level and alters leaf morphology. - Plant Sci. 178: 12-22, 2010. Go to original source...
  13. Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., Shinozaki, K.: Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. - Plant J. 27: 325-333, 2001. Go to original source...
  14. Iuchi, S., Kobayashi, M., Yamaguchi-Shinozaki, K., Shinozaki, K.: A stress inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. - Plant Physiol. 123: 553-652, 2000. Go to original source...
  15. Kim, H., Hwang, H., Hong, J.W., Lee, Y.N., Ahn, I.P., Yoon, I.S., Yoo, S.D., Lee, S., Lee, S.C., Kim, B.G.: A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. - J. exp. Bot. 63: 1013-1024, 2012. Go to original source...
  16. Lambers, H., Chapin, F. S., III, Pons, T.: Photosynthesis. - In: Lambers, H. (ed.: - Plant Physiology and Ecology. Pp. 11-99. Springer-Verlag, New York 2008. Go to original source...
  17. Leung, J.M., Giraudat, J.: Abscisic acid signal transduction. - Annu. Rev. Plant Physiol. Plant mol. Biol. 49: 199-222, 1998. Go to original source...
  18. Liang, J., Yang, L., Chen, X., Li, L., Guo, D., Li, H., Zhang, B.: Cloning and characterization of the promoter of the 9-cis-epoxycarotenoid dioxygenase gene in Arachis hypogaea L. - Biosci. Biotechnol. Biochem. 73: 2103-2106, 2009. Go to original source...
  19. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔC(T) method. - Methods 25: 402-408, 2001. Go to original source...
  20. Mansouri, H., Asrar, Z.: Effects of abscisic acid on content and biosynthesis of terpenoids in Cannabis sativa at vegetative stage. - Biol. Plant. 56: 153-156, 2012. Go to original source...
  21. Mawlong, I., Ali, K., Kurup, D., Yadav, S., Tyagi, A.: Isolation and characterization of an AP2/ERF-type drought stress inducible transcription factor encoding gene from rice. - J. Plant Biochem. Biotechnol. 23: 42-51, 2014. Go to original source...
  22. Mawlong, I., Ali, K., Srinivasan, R., Rai, R.D., Tyagi, A.: Functional validation of a drought-responsive AP2/ERF family transcription factor-encoding gene from rice in Arabidopsis. - Mol. Breed. 35: 163-177, 2015. Go to original source...
  23. Muñoz-Espinoza, V.A., López-Climent, M.F., Casaretto, J.A., Gómez-Cadenas, A.: Water stress responses of tomato mutants impaired in hormone biosynthesis reveal abscisic acid, jasmonic acid and salicylic acid interactions. - Front. Plant Sci. 6: 997, 2015. Go to original source...
  24. Nambara, E., Marion-Poll, A.: Abscisic acid biosynthesis and catabolism. - Annu. Rev. Plant Biol. 56: 165-185, 2005. Go to original source...
  25. Pena-Cortes, H., Sanchez-Serrano, J.J., Mertens, R., Willmitzer, L., Prat, S.: Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato. - Proc. nat. Acad. Sci. USA 86: 9851-9855, 1989. Go to original source...
  26. Premachandra, G.S., Saneoka, H., Ogata, S.: Cell membrane stability, an indicator of drought tolerance, as affected by applied nitrogen in soybean. - J. agr. Sci. 115: 63-66, 1990. Go to original source...
  27. Qin, X., Zeevaart, J.A.D.: The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. - Proc. nat. Acad. Sci. USA 96: 15354-15361, 1999. Go to original source...
  28. Qin, X., Zeevaart, J.A.D.: Overexpression of a 9-cisepoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. - Plant Physiol. 128: 544-551, 2002. Go to original source...
  29. Rogers, S.O., Bendich, A.J.: Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. - Plant mol. Biol. 5: 69-76, 1985. Go to original source...
  30. Saika, H., Okamoto, M., Miyoshi, K., Kushiro, T., Shinoda, S., Jikumaru, Y., Fujimoto, M., Arikawa, T., Takahashi, H., Ando, M., Arimura, S., Miyao, A., Hirochika, H., Kamiya, Y., Tsutsumi, N., Nambara, E., Nakazono, M.: Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8-hydroxylase in rice. - Plant Cell Physiol. 48: 287-298, 2007.
  31. Sairam, R.K., Deshmukh, P.S., Shukla, D.S.: Tolerance to drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. - J. Agron. Crop Sci. 178: 171-177, 1997. Go to original source...
  32. Santner, A., Calderon-Villalobos, L.I., Estelle, M.: Plant hormones are versatile chemical regulators of plant growth. - Nat. Chem. Biol. 5: 301-307, 2009. Go to original source...
  33. Schwartz, S.H., Qin, X., Zeevaart, J.A.D.: Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. - Plant Physiol. 131: 1591-1601, 2003. Go to original source...
  34. Seo, M., Koshiba, T.: Complex regulation of ABA biosynthesis in plants. - Trends Plant Sci. 7: 41-48, 2002. Go to original source...
  35. Singh, N.K., LaRosa, P.C., Handa, A.K., Hasegawa, P.M., Bressan, R.A.: Hormonal regulation of protein synthesis associated with salt tolerance in plant cells. - Proc. nat. Acad. Sci. USA 84: 739-743, 1987. Go to original source...
  36. Sun, L., Wang, Y.P., Chen, P., Ren, J., Ji, K., Li, Q., Li, P., Dai, S.J., Leng, P.: Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. - J. exp. Bot. 62: 5659-5669, 2011. Go to original source...
  37. Taylor, I.B., Burbidge, A., Thompson, A.J.: Control of abscisic acid synthesis. - J. exp. Bot. 51: 1563-1574, 2000. Go to original source...
  38. Thompson, A.J., Jackson, A.C., Symonds, R.C., Mulholland, B.J., Dadswell, A.R., Blake, P.S., Burbidge, A., Taylor, I.B.: Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. - Plant J. 23: 363-374, 2000. Go to original source...
  39. Tian, L., DellaPenna, D., Zeevaart, J.A.D.: Effects of hydroxylated carotenoid deficiency on ABA accumulation in Arabidopsis. - Physiol. Plant. 122: 314-320, 2004. Go to original source...
  40. Tong, S.-M., Xi, H.-X., Ai, K.-J., Hou, H.-S.: Overexpression of wheat TaNCED gene in Arabidopsis enhances tolerance to drought stress and delays seed germination. - Biol. Plant. 61: 64-72, 2017. Go to original source...
  41. Xiong, L., Zhu, J.K.: Regulation of abscisic acid biosynthesis. - Plant Physiol. 133: 29-36, 2003. Go to original source...
  42. Yamaguchi-Shinozaki, K., Shinozaki, K.: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. - Annu. Rev. Plant Biol. 57: 781-803, 2006. Go to original source...
  43. Yang, J., Guo, Z.: Cloning of a 9-cis-epoxycarotenoid dioxygenase gene (SgNCED1) from Stylosanthes guianensis and its expression in response to abiotic stresses. - Plant Cell Rep. 26: 1383-1390, 2007. Go to original source...
  44. Ye, N., Zhu, G., Liu, Y., Li, Y., Zhang, J.: ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. - Plant Cell Physiol. 52: 689-698, 2011. Go to original source...
  45. Zeevaart, J.A.D.: Abscisic acid metabolism and its regulation. - In: Hooykaas, P.P.J., Hall, M.A., Libbenga, K.R. (ed.: Biochemistry and Molecular Biology of Plant Hormones. Pp. 189-207. Elsevier, Amsterdam 1999. Go to original source...
  46. Zhu, G., Ye, N., Zhang, J.: Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. - Plant Cell Physiol. 50: 644-651, 2009. Go to original source...