γ-Aminobutyric Acid Imparts Partial Protection from Salt Stress Injury to Maize Seedlings by Improving Photosynthesis and Upregulating Osmoprotectants and Antioxidants

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Wang, Yongchao ^a   Gu, Wanrong ^a,b   Meng, Yao ^a,c   Xie, Tenglong ^a   Li, Lijie ^a   Li, Jing ^a,b   Wei, Shi ^a,b  

^a NORTHEAST AGRICULTURAL UNIVERSITY   (China)

^b Observation Experiment Station of Ministry of Agriculture for Crop Cultivation Science in Northeast Area   (China)

^c Institute of Animal Science and Veterinary Medicine   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ANTIOXIDANT; CHLOROPHYLL;

CHLOROPLAST; DRUG EFFECT; MAIZE; METABOLISM; MITOCHONDRION; OSMOREGULATION; OXIDATIVE STRESS; PHENOTYPE; PHOTOSYNTHESIS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; SALT TOLERANCE; SEEDLING;

ANTIOXIDANTS; CHLOROPHYLL; CHLOROPLASTS; GAMMA-AMINOBUTYRIC ACID; MITOCHONDRIA; OSMOREGULATION; OXIDATIVE STRESS; PHENOTYPE; PHOTOSYNTHESIS; PLANT LEAVES; SALT-TOLERANCE; SEEDLINGS; STRESS, PHYSIOLOGICAL; ZEA MAYS;

EID: 85014945315     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep43609     Document Type: Article

References (67)

1. Wang, W. X., Vinocur, B. & Altman, A. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta 218, 1-14 (2003).
2. Maas, E. V., Hofman, G. J., Chaba, G. D., Poss, J. A. & Shannon, M. C. Salt sensitivity of corn at various growth stages. Irrig. Sci. 4, 45-57 (1983).
3. Chinnusamy, V., Jagendorf, A. & Zhu, J. K. Understanding and improving salt tolerance in plants. Crop Sci. 45, 437-448 (2005).
4. Munns, R. Physiological processes limiting plant growth in saline soils: Some dogmas and hypotheses. Plant Cell Environ. 16, 15-24 (1993).
5. Szalai, G. & Janda, T. Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J. Agron. Crop Sci. 195, 165-171 (2009).
6. Spanswick, R. M. Electrogenic ion pumps. Annu. Rev. Plant Physiol. 32, 267-289 (1981).
7. Kaya, C., Tuna, A. L. & Okant, A. M. Effect of foliar applied kinetin and indole acetic acid on maize plants grown under saline conditions. Turk. J. Agric. For. 34, 529-538 (2010).
8. 4 photosynthesis of maize under salinity. J. Plant Physiol. 169, 469-477 (2012).
9. Hichem, H., Mounir, D. & Naceur, E. A. Diferential responses of two maize (Zea mays L.) varieties to salt stress: Changes on polyphenols composition of foliage and oxidative damages. Ind. Crops Prod. 30, 144-151 (2009).
10. Menezes-Benavente, L., Kernodle, S. P., Margis-Pinheiro, M. & Scandalios, J. G. Salt-induced antioxidant metabolism defenses in maize (Zea mays L.) seedlings. Redox Rep. 9, 29-36 (2004).
11. Breitkreuz, K. E. & Shelp, B. J. Subcellular compartmentation of the 4-aminobutyrate shunt in protoplasts from developing soybean cotyledons. Plant Physiol. 108, 99-103 (1995).
12. Su, Y. C., Wang, J. J., Lin, T. T. & Pan, T. M. Production of the secondary metabolites gamma-aminobutyric acid and monacolin K by Monascus. J Ind Microbiol Biotechnol. 30, 41-46 (2003).
13. Renault, H. et al. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10, 20 (2010).
14. Li, M. F., Guo, S. J., Yang, X. H., Meng, Q. W. & Wei, X. J. Exogenous gamma-aminobutyric acid increases salt tolerance of wheat by improving photosynthesis and enhancing activities of antioxidant enzymes. Biol. Plant. 60, 123-131 (2016).
15. Bouche, N. & Fromm, H. Gaba in plants: Just a metabolite? Trends Plant Sci. 9, 110-115 (2004).
16. Planamente, S. et al. A conserved mechanism of GABA binding and antagonism is revealed by structure-function analysis of the periplasmic binding protein Atu2422 in Agrobacterium tumefaciens. Journal of Biological Chemistry 285, 30294-30303 (2010).
17. Carapito, R. et al. Gene expression in fusarium graminearum grown on plant cell wall. Fungal Genet. Biol. 45, 738-748 (2008).
18. Fait, A., Fromm, H., Walter, D., Galili, G. & Fernie, A. R. Highway or byway: The metabolic role of the GABA shunt in plants. Trends Plant Sci. 13, 14-19 (2008).
19. 2 fxation in legumes? Plant Signal. Behav. 6, 32-36 (2011).
20. Renault, H. et al. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10, 20 (2010).
21. Kim, D. W. et al. Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol. Cells 24, 45-59 (2007).
22. Boonburapong, B., Laloknam, S. & Incharoensakdi, A. Accumulation of gamma-aminobutyric acid in the halotolerant cyanobacterium Aphanothece halophytica under salt and acid stress. J. Appl. Phycol. 28, 141-148 (2016).
23. Xing, S. G., Jun, Y. B., Hau, Z. W. & Liang, L. Y. Higher accumulation of gamma-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. Roots. Plant Physiol. Biochem. 45, 560-566 (2007).
24. Malekzadeh, P., Khara, J. & Heydari, R. Alleviating effects of exogenous gamma-aminobutiric acid on tomato seedling under chilling stress. Physiol. Mol. Biol. Plants 20, 133-137 (2014).
25. + antiporters of newly developed maize (Zea mays) hybrids contribute to salt resistance during the second phase of salt stress. J. Plant Nutr. Soil Sci. 176, 148-156 (2013).
26. Fortmeier, R. & Schubert, S. Salt tolerance of maize (Zea mays L.): The role of sodium exclusion. Plant Cell Environ. 18, 1041-1047 (1995).
27. Sümer, A., Zörb, C., Yan, F. & Schubert, S. Evidence of sodium toxicity for the vegetative growth of maize (Zea mays L.) during the first phase of salt stress. J. Appl. Bot. 78, 135-139 (2004).
28. Davenport, R., James, R. A., Zakrisson-Plogander, A., Tester, M. & Munns, R. Control of sodium transport in durum wheat. Plant Physiol. 137, 807-818 (2005).
29. + status. J. Plant Physiol. 164, 60-67 (2007).
30. Nayyar, H., Kaur, R., Kaur, S. & Singh, R. γ -aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J. Plant Growth Regul. 33, 408-419 (2014).
31. Mansour, M. M. F., Salama, K. H. A., Ali, F. Z. M. & Abou, H. A. F. Cell and plant responses to NaCl in Zea mays cultivars difering in salt tolerance. Gen Appl. Plant Physiol. 31, 29-41 (2005).
32. Chen, Z. et al. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J. Exp. Bot. 58, 4245-4255 (2007).
33. Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498 (2004).
34. Taulavuori, E., Hellström, E. K., Taulavuori, K. & Laine, K. Comparison of two methods used to analyse lipid peroxidation from vaccinium myrtillus (L.) during snow removal, reacclimation and cold acclimation. J. Exp. Bot. 52, 2375-2380 (2001).
35. Qiu, Z. B., Li, J. T., Zhang, M. M., Bi, Z. Z. & Li, Z. L. He-Ne laser pretreatment protects wheat seedlings against cadmium-induced oxidative stress. Ecotoxicol. Environ. Saf. 88, 135-141 (2013).
36. Lu, J. et al. Effect of hydrogen peroxide on seedling growth and antioxidants in two wheat cultivars. Biol. Plant. 57, 487-494 (2013).
37. Zhu, Z. J., Wei, G. Q., Li, J., Qian, Q. Q. & Yu, J. Q. Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (Cucumis sativus L.). Plant Sci. 167, 527-533 (2004).
38. Li, Y., Bai, Q., Jin, X., Wen, H. & Gu, Z. Effects of cultivar and culture conditions on γ -aminobutyric acid accumulation in germinated fava beans (Vicia faba L.). J. Sci. Food Agric. 90, 52-57 (2010).
39. Zörb, C. et al. The biochemical reaction of maize (Zea mays L.) to salt stress is characterized by a mitigation of symptoms and not by a specific adaptation. Plant Sci. 167, 91-100 (2004).
40. Zhang, Z. P., Miao, M. M. & Wang, C. L. Effects of ALA on photosynthesis, antioxidant enzyme activity, and gene expression, and regulation of proline accumulation in tomato seedlings under NaCl stress. J. Plant Growth Regul. 34, 637-650 (2015).
41. Li, Z. et al. Exogenously applied spermidine improves drought tolerance in creeping bentgrass associated with changes in antioxidant defense, endogenous polyamines and phytohormones. Plant Growth Regul. 76, 71-82 (2015).
42. Vijayakumari, K. & Jos, T. P. γ -aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum L. Plants subjected to PEG-induced stress. Plant Growth Regul. 78, 57-67 (2016).
43. Turano, F. J., Thakkar, S. S., Fang, T. & Weisemann, J. M. Characterization and expression of NAD(H)-dependent glutamate dehydrogenase genes in Arabidopsis. Plant Physiol. 113, 1329-1341 (1997).
44. Beuve, N. et al. Putative role of γ -amino butyric acid (GABA) as a long distance signal in upregulation of nitrate uptake in Brassica napus L. Plant Cell Environ. 27, 1035-1046 (2004).
45. Buttery, B. R. & Buzzell, R. I. The relationship between chlorophyll content and rate of photosynthesis in soybeans. Can. J. Plant Sci. 57, 1-5 (1977).
46. Wu, H. L., Wu, X. L., Li, Z. H., Duan, L. S. & Zhang, M. C. Physiological evaluation of drought stress tolerance and recovery in caulifower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. J. Plant Growth Regul. 31, 113-123 (2012).
47. Sharkey, T. D. & Zhang, R. High temperature effects on electron and proton circuits of photosynthesis. J. Integr. Plant Biol. 52, 712-722 (2010).
48. Hajiboland, R., Aliasgharzadeh, N., Laiegh, S. F. & Poschenrieder, C. Colonization with arbuscular mycorrhizal fungi improves salinity tolerance of tomato (Solanum lycopersicum L.) plants. Plant Soil 331, 313-327 (2010).
49. Naumann, J. C., Young, D. R. & Anderson, J. E. Linking leaf chlorophyll fuorescence properties to physiological responses for detection of salt and drought stress in coastal plant species. Physiol. Plant. 131, 422-433 (2007).
50. Steponkus, P. L. & Lanphear, F. O. Refnement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol. 42, 1423-1426 (1967).
51. Misra, A. N., Srivastava, A. & Strasser, R. J. Utilization of fast chlorophyll a fuorescence technique in assessing the salt/ion sensitivity of mung bean and brassica seedlings. J. Plant Physiol. 158, 1173-1181 (2001).
52. Jiang, Q., Roche, D., Monaco, T. A. & Hole, D. Stomatal conductance is a key parameter to assess limitations to photosynthesis and growth potential in barley genotypes. Plant Biol. 8, 515-521 (2006).
53. Karaba, A. et al. Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc. Natl. Acad. Sci. USA 104, 15270-15275 (2007).
54. Cao, S. F., Cai, Y. T., Yang, Z. F. & Zheng, Y. H. MeJA induces chilling tolerance in loquat fruit by regulating proline and γ -aminobutyric acid contents. Food Chem. 133, 1466-1470 (2012).
55. Almeselmani, M., Deshmukh, P. S. & Sairam, R. K. High temperature stress tolerance in wheat genotypes: Role of antioxidant defence enzymes. Acta Agron. Hung. 57, 1-14 (2009).
56. Saito, T. et al. Screening for γ -aminobutyric acid (GABA)-rich tomato varieties. J. Jpn Soc. Hortic. Sci. 77, 242-250 (2008).
57. Najeeb, U., Atwell, B. J., Bange, M. P. & Tan, D. K. Y. Aminoethoxyvinylglycine (AVG) ameliorates waterlogging-induced damage in cotton by inhibiting ethylene synthesis and sustaining photosynthetic capacity. Plant Growth Regul. 76, 83-98 (2015).
58. Premchandra, G. S., Sameoka, H. & Ogata, S. Cell osmotic membrane-stability, an indication of drought tolerance, as afected by applied nitrogen in soil. J. Agric. Res. 115, 63-66 (1990).
59. Barrs, H. D. & Weatherley, P. E. A re-examination of the relative turgidity technique for estimating water defcits in leaves. Aust. J. Biol. Sci. 15, 413-428 (1962).
60. Giannopolitis, C. N. & Ries, S. K. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 59, 309-314 (1977).
61. Hernández, J. A., Jiménez, A., Mullineaux, P. & Sevilia, F. Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ. 23, 853-862 (2000).
62. Change, B. & Maehly, A. C. Assay of catalases and peroxidase. Methods Enzymol. 2, 764-775 (1955).
63. Nakano, Y. & Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22, 867-880 (1981).
64. Kuk, Y. I. et al. Antioxidative enzymes ofer protection from chilling damage in rice plants. Crop Sci. 43, 2109-2117 (2003).
65. Xie, Z. et al. Coronatine alleviates salinity stress in cotton by improving the antioxidative defense system and radical-scavenging activity. J. Plant Physiol. 165, 375-384 (2008).
66. Monreal, J. A. et al. Proline content of sugar beet storage roots: Response to water defcit and nitrogen fertilization at feld conditions. Environ. Exp. Bot. 60, 257-267 (2007).
67. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254 (1976).