Proline accumulation and metabolism-related genes expression profiles in Kosteletzkya virginica seedlings under salt stress

Frontiers in Plant Science

Volumn 6, Issue SEPTEMBER, 2015, Pages

  Wang, Hongyan ^a,b,c   Tang, Xiaoli ^a,c   Wang, Honglei ^b   Shao, Hong Bo ^a,d  

^a YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Expression profiles; Kosteletzkya virginica; Proline accumulation; Proline metabolism; Salt stress

Indexed keywords

EID: 84944222832     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00792     Document Type: Article

References (53)

1. Armengaud, P., Thiery, L., Buhot, N., Grenier-De March, G., and Savouré, A. (2004). Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol. Plant 120, 442-450. doi: 10.1111/j.0031-9317.2004.00251.x
2. Bates, L. S., Waldren, R. P., and Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant Soil 39, 205-207. doi: 10.1007/BF00018060
3. Blanchard, O. J. (2008). Innovations in Hibiscus and Kosteletzkya (Malvaceae. Hibisceae). Novon 18, 4-8. doi: 10.3417/2006125
4. Chaitanya, K. V., Rasineni, G. K., and Reddy, A. R. (2009). Biochemical responses to drought stress in mulberry (Morus alba L.): evaluation of proline, glycine betaine and abscisic acid accumulation in five cultivars. Acta Physiol. Plant. 31, 437-443. doi: 10.1007/s11738-008-0251-6
5. Fujiwara, T., Mitsuya, S., Miyake, H., Hattori, T., and Takabe, T. (2010). Characterization of a novel glycinebetaine/proline transporter gene expressed in the mestome sheath and lateral root cap cells in barley. Planta 232, 133-143. doi: 10.1007/s00425-010-1155-4
6. Gallagher, J. L. (1985). Halophytic crops for cultivation at seawater salinity. Plant Soil 89, 323-336. doi: 10.1007/BF02182251
7. Gallagher, J. L. (1995). “Biotechnology approaches for improving halophytic crops: somaclonal variation and genetic transformation,” in Biology of Salt-Tolerant Plants, eds M. A. Khan and I. A. Ungar (Karachi: University of Karachi), 397-406.
8. Grallath, S., Weimar, T., Meyer, A., Gumy, C., Suter-Grotemeyer, M., Neuhaus, J. M., et al. (2005). The AtProT family. Plant Physiol. 137, 117-126. doi: 10.1104/pp.104.055079
9. Hare, P. D., Cress, W. A., and Staden, J. (1999). Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J. Exp. Bot. 50, 413-434. doi: 10.1093/jexbot/50.333.413
10. Hu, C. A., Delauney, A., and Verma, D. S. (1992). A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc. Natl. Acad. Sci. U.S.A. 89, 9354-9358. doi: 10.1073/pnas.89.19.9354
11. Huang, Z., Zhao, L., Chen, D., Liang, M., Liu, Z., Shao, H., et al. (2013). Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS ONE 8:e62085. doi: 10.1371/journal.pone.0062085
12. Igarashi, Y., Yoshiba, Y., Takeshita, T., Nomura, S., Otomo, J., Yamaguchi-Shinozaki, K., et al. (2000). Molecular cloning and characterization of a cDNA encoding proline transporter in rice. Plant Cell Physiol. 41, 750-756. doi: 10.1093/pcp/41.6.750
13. Kavi-Kishor, P. B., Sangam, S., Amrutha, R. N., Sri Laxmi, P., Naidu, K. R., Rao, K. R. S. S., et al. (2005). Regulation of proline biosynthesis, degradation, uptakeand transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr. Sci. 88, 424-438.
14. Kavi-Kishor, P. B., and Sreenivasulu, N. (2014). Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ. 37, 300-311. doi: 10.1111/pce.12157
15. Kavi-Kishor, P. B. K., Hong, Z., Miao, G. H., Hu, C. A. A., and Verma, D. P. S. (1995). Overexpression of Δ1-pyrroline-5-carboxylate synthase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108, 1387-1394.
16. Khan, M. I. R., Iqbal, N., Masood, A., and Khan, N. A. (2012). Variation in salt tolerance of wheat cultivars: role of glycinebetaine and ethylene. Pedosphere 22, 746-754. doi: 10.1016/S1002-0160(12)60060-5
17. Kiyosue, T., Yoshiba, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1996). A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8, 1323-1335. doi: 10.1105/tpc.8.8.1323
18. Lehmann, S., Funck, D., Szabados, L., and Rentsch, D. (2010). Proline metabolism and transport in plant development. Amino Acids 39, 949-962. doi: 10.1007/s00726-010-0525-3
19. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using Real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
20. Miller, G., Honig, A., Stein, H., Suzuki, N., Mittler, R., and Zilberstein, A. (2009). Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. J. Biol. Chem. 284, 26482-26492. doi: 10.1074/jbc.M109.009340
21. Miller, G., Stein, H., Honig, A., Kapulnik, Y., and Zilberstein, A. (2005). Responsive modes of Medicago sativaproline dehydrogenase genes during salt stress and recovery dictate free proline accumulation. Planta 222, 70-79. doi: 10.1007/s00425-005-1518-4
22. Misra, N., and Gupta, A. K. (2005). Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci. 169, 331-339. doi: 10.1016/j.plantsci.2005.02.013
23. Mizoi, J., and Yamaguchi-Shinozaki, K. (2013). “Molecular approaches to improve rice abiotic stress tolerance,” in Rice Protocols, ed. Y. Yang (New York, NY: Humana Press), 269-283.
24. Molinari, H. B. C., Marur, C. J., Daros, E., De Campos, M. K. F., De Carvalho, J. F. R. P., Filho, J. C. B., et al. (2007). Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum sp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiol. Plant 130, 218-229. doi: 10.1111/j.1399-3054.2007.00909.x
25. Parida, A. K., Dagaonkar, V. S., Phalak, M. S., and Aurangabadkar, L. P. (2008). Differential responses of the enzymes involved in proline biosynthesis and degradation in drought tolerant and sensitive cotton genotypes during drought stress and recovery. Acta Physiol. Plant. 30, 619-627. doi: 10.1007/s11738-008-0157-3
26. Peng, Z., Lu, Q., and Verma, D. P. S. (1996). Reciprocal regulation of Δ 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol. Gen. Genet. 253, 334-341. doi: 10.1007/PL00008600
27. Rentsch, D., Hirner, B., Schmelzer, E., and Frommer, W. B. (1996). Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8, 1437-1446. doi: 10.2307/3870312
28. Ribarits, A., Abdullaev, A., Tashpulatov, A., Richter, A., Heberle-Bors, E., and Touraev, A. (2007). Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development. Planta 225, 1313-1324. doi: 10.1007/s00425-006-0429-3
29. Roosens, N. H., Thu, T. T., Iskandar, H. M., and Jacobs, M. (1998). Isolation of ornithine-d-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol. 117, 263-271. doi: 10.1104/pp.117.1.263
30. Saradhi, P. P., Alia, A., Arora, S., and Prasad, K. V. (1995). Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem. Biophys. Res. Commun. 209, 1-5. doi: 10.1006/bbrc.1995.1461
31. Savouré, A., Jaoua, S., Hua, X. J., Ardiles, W., Montagu, M. V., and Verbruggen, N. (1995). Isolation, characterization, and chromosomal location of a gene encoding the delta 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett. 372, 13-19. doi: 10.1016/0014-5793(95)00935-3
32. Sawahel, W. A., and Hassan, A. H. (2002). Generation of transgenic wheat plants producing high levels of the osmoprotectant proline. Biotechnol. Lett. 24, 721-725. doi: 10.1023/A:1015294319114
33. Schwacke, R., Grallath, S., Breitkreuz, K. E., Stransky, E., Stransky, H., and Fromme, W. B. (1999). LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. Plant Cell 11, 377-392. doi: 10.2307/3870867
34. Sharma, S., Villamor, J. G., and Verslues, P. E. (2011). Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol. 157, 292-304. doi: 10.1104/pp.111.183210
35. Silva-Ortega, C. O., Ochoa-Alfaro, A. E., Reyes-Agüerob, J. A., Aguado-Santacruz, G. A., and Jimenez-Bremont, J. F. (2008). Salt stress increases the expression of P5CS gene and induces proline accumulation in cactus pear. Plant Physiol. Biochem. 46, 82-92. doi: 10.1016/j.plaphy.2007.10.011
36. Siripornadulsil, S., Traina, S., Verma, D. P., and Sayre, R. T. (2002). Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14, 2837-2847. doi: 10.1105/tpc.004853
37. Su, J., and Wu, R. (2004). Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci. 166, 941-948. doi: 10.1016/j.plantsci.2003.12.004
38. Su, M., Li, X. F., Ma, X. Y., Peng, X. J., Zhao, A. G., Cheng, L. Q., et al. (2011). Cloning two P5CS genes from bioenergy sorghum and their expression profiles under abiotic stresses and MeJA treatment. Plant Sci. 181, 652-659. doi: 10.1016/j.plantsci.2011.03.002
39. Surabhi, G. K., Reddy, A. M., Kumari, G. J., and Sudhakar, C. (2008). Modulations in key enzymes of nitrogen metabolism in two high yielding genotypes of mulberry (Morus alba L.) with differential sensitivity to salt stress. Environ. Exp. Bot. 64, 171-179. doi: 10.1016/j.envexpbot.2008.04.006
40. Szabados, L., and Savouré, A. (2010). Proline: a multifunctional amino acid. Trends Plant Sci. 15, 89-97. doi: 10.1016/j.tplants.2009.11.009
41. Szekely, G., Abraham, E., Cselo, A., Rigo, G., Zsigmond, L., Csiszar, J., et al. (2008). Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53, 11-28. doi: 10.1111/j.1365-313X.2007.03318.x
42. Tang, X. L., Wang, H. Y., Shao, C. Y., and Shao, H-.B. (2015). Global gene expression of kosteletzkya virginica seedlings responding to salt stress. PLoS ONE 10:e0124421. doi: 10.1371/journal.pone.0124421
43. Tateishi, Y., Nakagawa, T., and Esaka, M. (2005). Osmotolerance and growth stimulation of transgenic tobacco cells accumulating free proline by silencing proline dehydrogenase expression with double-stranded RNA interference technique. Physiol. Plant. 125, 224-234. doi: 10.1111/j.1399-3054.2005.00553.x
44. Verbruggen, N., and Hermans, C. (2008). Proline accumulation in plants: a review. Amino Acids 35, 753-759. doi: 10.1007/s00726-008-0061-6
45. Wang, H. Y., Tang, X. L., Wang, H. L., and Shao, H-.B. (2015). Physiological responses of Kosteletzkya virginica to coastal wetland soil. Sci. World J. 2015:354581. doi: 10.1155/2015/354581
46. Xue, X. N., Liu, A. H., and Hua, X. J. (2009). Proline accumulation and transcriptional regulation of proline biothesynthesis and degradation in Brassica napus. BMB Rep. 42, 28-34. doi: 10.5483/BMBRep.2009.42.1.028
47. Yamaguchi-Shinozaki, K., and Shinoaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781-803. doi: 10.1146/annurev.arplant.57.032905.105444
48. Yoshiba, Y., Kiyosue, T., Katagiri, T. I., Ueda, H., Mizoguchi, T., Yamaguchi-Shinozaki, K., et al. (1995). Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J. 7, 751-760. doi: 10.1046/j.1365-313X.1995.07050751.x
49. Yoshiba, Y., Kiyosue, T., Nakashima, K., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1997). Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol. 38, 1095-1102. doi: 10.1093/oxfordjournals.pcp.a029093
50. Yoshiba, Y., Nanjo, T., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1999). Stress- responsive and developmental regulation of Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 261, 766-772. doi: 10.1006/bbrc.1999.1112
51. Zhang, C. S., Lu, Q., and Verma, D. P. S. (1995). Removal of feedback inhibition of Δ1-pyrroline- 5-carboxylate synthetase, a bifunctional enzymecatalyzing the first two steps of proline biosynthesis in plants. J. Biol. Chem. 270, 20491-20496. doi: 10.1074/jbc.270.35.20491
52. Zhang, M., Huang, H., and Dai, S. (2014). Isolation and expression analysis of proline metabolism-related genes in Chrysanthemum lavandulifolium. Gene 537, 203-213. doi: 10.1016/j.gene.2014.01.002
53. Zhou, G., Xia, Y., Ma, B., Feng, C., and Qin, P. (2010). Culture of seashore mallow under different salinity levels using plastic nutrient-rich matrices and transplantation. Agron. J. 102, 395-402. doi: 10.2134/agronj2009.0274