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Plant-Environment Interactions

Exogenous γ-aminobutyric acid (GABA) application at different growth stages regulates 2-acetyl-1-pyrroline, yield, quality and antioxidant attributes in fragrant rice

, , , , , , , , , , & show all
Pages 139-152 | Received 19 Mar 2020, Accepted 06 May 2020, Published online: 01 Jun 2020

References

  • AL-Quraan NA, AL-Smadi ML, Swaleh AF. 2015. GABA metabolism and ROS induction in lentil (Lens culinaris Medik) plants by synthetic 1,2,3-Thiadiazole compounds. J Plant Interact. 10:185–194. doi:10.1080/17429145.2015.1056262.
  • Bao G, Ashraf U, Wang C, He L, Wei X, Zheng A, Mo Z, Tang X. 2018. Molecular basis for increased 2-acetyl-1-pyrroline contents under alternate wetting and drying (AWD) conditions in fragrant rice. Plant Physiol Biochem. 133:149–157. doi:10.1016/j.plaphy.2018.10.032.
  • Bates LS, Waldren RP, Teare ID. 1973. Rapid determination of free proline for water-stress studies. Plant Soil. 39:205–207. doi:10.1007/BF00018060.
  • Boontakham P, Sookwong P, Jongkaewwattana S, Wangtueai S, Mahatheeranont S. 2019. Comparison of grain yield and 2-acetyl-1-pyrroline (2AP) content in leaves and grain of two Thai fragrant rice cultivars cultivated at greenhouse and open-air conditions. Aust J Cereal Sci. 13:159–169. doi:10.21475/ajcs.19.13.01.p1431.
  • Bouché N, Fromm H. 2004. GABA in plants: just a metabolite? Trends Plant Sci. 9:110–115. doi:10.1016/j.tplants.2004.01.006.
  • Bradbury LM, Fitzgerald TL, Henry RJ, Jin Q, Waters DL. 2005. The gene for fragrance in rice. Plant Biotechnol J. 3:363–370. doi:10.1111/j.1467-7652.2005.00131.x.
  • Bradbury LM, Gillies SA, Brushett DJ, Waters DL, Henry RJ. 2008. Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Mol Biol. 68:439–449. doi:10.1007/s11103-008-9381-x.
  • Buttery RG, Ling LC, Juliano BO, Turnbaugh JG. 1983. Cooked rice aroma and 2-acetyl-1-pyrroline. J Agric Food Chem. 31:823–826. doi:10.1021/jf00118a036.
  • Chen S, Yang Y, Shi W, Ji Q, He F, Zhang Z, Cheng Z, Liu X, Xu M. 2008. Badh2, encoding betaine aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell. 20:1850–1861. doi:10.1105/tpc.108.058917.
  • Das B, Sengupta S, Kole B, Ghose TK. 2018. Elucidation of aroma levels within a set of rice landraces by means of aroma linked markers. J Pharmacogn Phytochem. 7:1756–1760.
  • Daygon VD, Calingacion M, Forster LC, De Voss JJ, Schwartz BD, Ovenden B, Alonso DE, McCouch SR, Garson MJ, Fitzgerald MA. 2017. Metabolomics and genomics combine to unravel the pathway for the presence of fragrance in rice. Sci Rep. 7:8767. doi:10.1038/s41598-017-07693-9.
  • Deng QQ, Ashraf U, Cheng SR, Sabir SR, Mo ZW, Pan SG, Tian H, Duan MY, Tang XR. 2018. Mild drought in interaction with additional nitrogen dose at grain filling stage modulates 2acetyl-1-pyrroline biosynthesis and grain yield in fragrant rice. Appl Ecol Environ Res. 16(6):7741–7758. doi:10.15666/aeer/1606_77417758.
  • Deng Y, Xu L, Zeng X, Li Z, Qin B, He N. 2010. New perspective of GABA as an inhibitor of formation of advanced lipoxidation end-products: it’s interaction with malondiadehyde. J Biomed Nanotechnol. 6:318–324. doi:10.1166/jbn.2010.1130.
  • Fait A, Fromm H, Walter D, Galili G, Fernie AR. 2008. Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 13:14–19. doi:10.1016/j.tplants.2007.10.005.
  • Ghosh P, Roychoudhury A. 2018. Differential levels of metabolites and enzymes related to aroma formation in aromatic indica rice varieties: comparison with non-aromatic varieties. 3 Biotech. 8:25. doi:10.1007/s13205-017-1045-6.
  • Giraud G. 2013. The world market of fragrant rice, main issues and perspectives. Inter Food Agribus Manag Rev. 16:1–20. doi:10.22004/ag.econ.148577.
  • Hashemi FG, Rafii MY, Ismail MR, Mahmud TMM, Rahim HA, Asfaliza R, Malek MA, Latif MA. 2013. Biochemical, genetic and molecular advances of fragrance characteristics in rice. Crit Rev Plant Sci. 32:445–457. doi:10.1080/07352689.2013.807716.
  • Huang ZL, Tang XR, Wang YL, Chen MJ, Zhao ZK, Duan MY, Pan SG. 2012. Effects of increasing aroma cultivation on aroma and grain yield of aromatic rice and their mechanism. Scientia Agricultura Sinica. 45:1054–1065 (in Chinese with English abstract). doi:10.3864/j.issn.0578-1752.2012.06.003.
  • Kaikavoosi K, Kad TD, Zanan RL, Nadaf AB. 2015. 2-Acetyl-1-pyrroline augmentation in scented indica rice (Oryza sativa L.) varieties through Δ 1-pyrroline-5-carboxylate synthetase (P5CS) gene transformation. Appl Biochem Biotechnol. 177:1466–1479. doi:10.1007/s12010-015-1827-4.
  • Kong L, Ashraf U, Cheng S, Rao G, Mo Z, Tian H, Pan S, Tang X. 2017. Short-term water management at early filling stage improves early-season rice performance under high temperature stress in South China. Eur J Agron. 90:117–126. doi:10.1016/j.eja.2017.07.006.
  • Li M, Ashraf U, Tian H, Mo Z, Pan S, Anjum SA, Duan M, Tang X. 2016b. Manganese-induced regulations in growth, yield formation, quality characters, rice aroma and enzyme involved in 2-acetyl-1-pyrroline biosynthesis in fragrant rice. Plant Physiol Biochem. 103:167–175. doi:10.1016/j.plaphy.2016.03.009.
  • Li Y, Fan Y, Ma Y, Zhang Z, Yue H, Wang L, Li J, Jiao Y. 2017. Effects of exogenous γ-aminobutyric acid (GABA) on photosynthesis and antioxidant system in pepper (Capsicum annuum L.) seedlings under low light stress. J Plant Growth Regul. 36:436–449. doi:10.1007/s00344-016-9652-8.
  • Li MF, Guo SJ, Yang XH, Meng QW, Wei XJ. 2016a. Exogenous gamma-aminobutyric acid increases salt tolerance of wheat by improving photosynthesis and enhancing activities of antioxidant enzymes. Biol Plantarum. 60:123–131. doi:10.1007/s10535-015-0559-1.
  • Li S, Jiang H, Wang J, Wang Y, Pan S, Tian H, Duan M, Wang S, Tang X, Mo Z. 2019a. Responses of plant growth, physiological, gas exchange parameters of super and non-super rice to rhizosphere temperature at the tillering stage. Sci Rep. 9:10618. doi:10.1038/s41598-019-47031-9.
  • Li Y, Lai R, Li W, Liu J, Huang M, Tang Y, Tang X, Pan S, Duan M, Tian H, et al. 2019b. γ-Aminobutyric acid regulates grain yield formation in different fragrant rice genotypes under different nitrogen levels. J Plant Growth Regul. 38:1–13. doi:10.1007/s00344-019-10016-z doi: 10.1007/s00344-018-9799-6
  • Li J, Tian Z, Wu X, Lv G, Ma W, Zhang Y, Gao H. 2018. Gamma-aminobutyric acid (GABA) modulates nitrate concentrations and metabolism in the leaves of Pakchoi (Brassica campestris ssp. chinensis Makino) treated with a nitrogen-rich solution. Plant Mol Biol Rep. 36:530–542. doi:10.1007/s11105-018-1092-0.
  • Luo HY, Gao HB, Xia QP, Gong BB, Wu XL. 2011. Effects of exogenous GABA on reactive oxygen species metabolism and chlorophyll fluorescence parameters in tomato under NaCl stress. Scientia Agricultura Sinica. 44:753–761 (in Chinese with English abstract). doi:10.3864/j.issn.0578-1752.2011.04.013.
  • Ma X, Zhu C, Yang N, Gan L, Xia K. 2016. γ-Aminobutyric acid addition alleviates ammonium toxicity by limiting ammonium accumulation in rice (Oryza sativa) seedlings. Physiol Plant. 158:389–401. doi:10.1111/ppl.12473.
  • Mahajan G, Sekhon NK, Singh N, Kaur R, Sidhu AS. 2010. Yield and nitrogen-use efficiency of aromatic rice cultivars in response to nitrogen fertilizer. J New Seeds. 11:356–368. doi:10.1080/1522886X.2010.520145.
  • Malekzadeh P, Khara J, Heydari R. 2014. Alleviating effects of exogenous Gamma-aminobutiric acid on tomato seedling under chilling stress. Physiol Mol Biol Plants. 20:133–137. doi:10.1007/s12298-013-0203-5.
  • Maraval I, Sen K, Agrebi A, Menut C, Morere A, Boulanger R, Gay F, Mestres C, Gunata Z. 2010. Quantification of 2-acetyl-1-pyrroline in rice by stable isotope dilution assay through headspace solid-phase microextraction coupled to gas chromatography–tandem mass spectrometry. Anal Chim Acta. 675:148–155. doi:10.1016/j.aca.2010.07.024.
  • Miller G, Honig A, Stein H, Suzuki N, Mittler R, Zilberstein A. 2009. Unraveling Δ1-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.
  • Mo Z, Fan P, Pan S, Wang Z, Tian H, Duan M, Tang X. 2016a. Effect of fertilizer types and fertilization methods on 2-acetyl-1-pyrroline content in aromatic rice. Acta Agriculturae Boreali-Sinica. 31:152–158 (in Chinese with English abstract). doi:10.7668/hbnxb.2016.05.023.
  • Mo Z, Huang J, Xiao D, Ashraf U, Duan M, Pan S, Tian H, Xiao L, Zhong K, Tang X. 2016b. Supplementation of 2-Ap, Zn and La improves 2-acetyl-1-pyrroline concentrations in detached aromatic rice panicles in vitro. PLoS ONE. 11:e0149523. doi:10.1371/journ al.pone.0149523 doi: 10.1371/journal.pone.0149523
  • Mo Z, Lei S, Ashraf U, Khan I, Li Y, Pan S, Duan M, Tian H, Tang X. 2017. Silicon fertilization modulates 2-acetyl-1-pyrroline content, yield formation and grain quality of aromatic rice. J Cereal Sci. 75:17–24. doi:10.1016/j.jcs.2017.03.014.
  • Mo Z, Li Y, Nie J, He L, Pan S, Duan M, Tian H, Xiao L, Zhong K, Tang X. 2019a. Nitrogen application and different water regimes at booting stage improved yield and 2-acetyl-1-pyrroline (2AP) formation in fragrant rice. Rice. 12:74. doi:10.1186/s12284-019-0335-5 doi: 10.1186/s12284-019-0328-4
  • Mo Z, Li W, Pan S, Fitzgerald TL, Xiao F, Tang Y, Wang Y, Duan M, Tian H, Tang X. 2015. Shading during the grain filling period increases 2-acetyl-1-pyrroline content in fragrant rice. Rice. 8:9. doi:10.1186/s12284-015-0040-y.
  • Mo Z, Tang Y, Ashraf U, Pan S, Duan M, Tian H, Wang S, Tang X. 2019b. Regulations in 2-acetyl-1-pyrroline contents in fragrant rice are associated with water-nitrogen dynamics and plant nutrient contents. J Cereal Sci. 88:96–102. doi:10.1016/j.jcs.2019.05.013.
  • Naliwajski MR, Skłodowska M. 2014. Proline and its metabolism enzymes in cucumber cell cultures during acclimation to salinity. Protoplasma. 251:201–209. doi:10.1007/s00709-013-0538-3.
  • Ncube B, Finnie JF, Van Staden J. 2013. Dissecting the stress metabolic alterations in in vitro Cyrtanthus regenerants. Plant Physiol Biochem. 65:102–110. doi:10.1016/j.plaphy.2013.01.001.
  • Pan S, Rasul F, Li W, Tian H, Mo Z, Duan M, Tang X. 2013. Roles of plant growth regulators on yield, grain qualities and antioxidant enzyme activities in super hybrid rice (Oryza sativa L.). Rice. 6:9. doi:10.1186/1939-8433-6-9.
  • Poonlaphdecha J, Maraval I, Roques S, Audebert A, Boulanger R, Bry X, Gunata Z. 2012. Effect of timing and duration of salt treatment during growth of a fragrant rice variety on yield and 2-acetyl-1-pyrroline, proline, and GABA levels. J Agric Food Chem. 60:3824–3830. doi:10.1021/jf205130y.
  • Priya M, Sharma L, Kaur R, Bindumadhava H, Nair RM, Siddique KHM, Nayyar H. 2019. GABA (γ-aminobutyric acid), as a thermo-protectant, to improve the reproductive function of heat-stressed mungbean plants. Sci Rep. 9:7788. doi:10.1038/s41598-019-44163-w.
  • Ramesh SA, Tyerman SD, Gilliham M, Xu B. 2017. γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci. 74:1577–1603. doi:10.1007/s00018-016-2415-7.
  • Ren Y, Ashraf U, He LX, Mo ZW, Wang F, Wan XC, Kong H, Ran XY, Tang XR. 2017. Irrigation and nitrogen management practices affect grain yield and 2-acetyl-1-pyrroline content in aromatic rice. Appl Ecol Environ Res. 15:1447–1460. doi:10.15666/aeer/1504_14471460.
  • Rezaei-Chiyaneh E, Seyyedi SM, Ebrahimian E, Moghaddam SS, Damalas CA. 2018. Exogenous application of gamma-aminobutyric acid (GABA) alleviates the effect of water deficit stress in black cumin (Nigella sativa L.). Ind Crops Prod. 112:741–748. doi:10.1016/j.indcrop.2017.12.067.
  • Routray W, Rayaguru K. 2018. 2-Acetyl-1-pyrroline: a key aroma component of aromatic rice and other food products. Food Rev Int. 34:539–565. doi:10.1080/87559129.2017.1347672.
  • Salvatierra A, Pimentel P, Almada R, Hinrichsen P. 2016. Exogenous GABA application transiently improves the tolerance to root hypoxia on a sensitive genotype of Prunus rootstock. Environ Exp Bot. 125:52–66. doi:10.1016/j.envexpbot.2016.01.009.
  • Sánchez E, Ruiz JM, Romero L. 2002. Proline metabolism in response to nitrogen toxicity in fruit of French Bean plants (Phaseolus vulgaris L. cv Strike). Sci Hortic. 93:225–233. doi:10.1016/S0304-4238(01)00342-9.
  • Sansenya S, Hua Y, Chumanee S. 2018. The correlation between 2-acetyl-1-pyrroline content, biological compounds and molecular characterization to the aroma intensities of Thai local rice. J Oleo Sci. 67:893–904. doi:10.5650/jos.ess17238.
  • Shang H, Cao S, Yang Z, Cai Y, Zheng Y. 2011. Effect of exogenous γ-aminobutyric acid treatment on proline accumulation and chilling injury in peach fruit after long-term cold storage. J Agric Food Chem. 59:1264–1268. doi:10.1021/jf104424z.
  • Song H, Xu X, Wang H, Wang H, Tao Y. 2010. Exogenous γ-aminobutyric acid alleviates oxidative damage caused by aluminium and proton stresses on barley seedlings. J Sci Food Agric. 90:1410–1416. doi:10.1002/jsfa.3951.
  • Su G, An Z, Zhang W, Liu Y. 2005. Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. J Plant Physiol. 162:1297–1303. doi:10.1016/j.jplph.2005.04.033.
  • Tang X, Wu M. 2006. Effects of application of Zinc, Iron and Lanthanum on contents of aroma in brown rice and proline in flag leaf of aromatic rice. Hybrid Rice. 21:69–72 (in Chinese with English abstract). doi:10.16267/j.cnki.1005-3956.2006.06.028.
  • Tripathi BN, Singh V, Ezaki B, Sharma V, Gaur JP. 2013. Mechanism of Cu-and Cd-induced proline hyperaccumulation in Triticum aestivum (wheat). J Plant Growth Regul. 32:799–808. doi:10.1007/s00344-013-9343-7.
  • Umair S, Leung YM, Bland RJ, Simpson HV. 2011. Enzymes of the ornithine–glutamate–proline pathway in the sheep abomasal nematode parasites Haemonchus contortus and Teladorsagia circumcincta. Exp Parasitol. 129:115–119. doi:10.1016/j.exppara.2011.07.006.
  • Wang P, Tang X, Tian H, Pan S, Duan M, Nie J, Luo Y, Xiao L. 2013. Effects of different irrigation modes on aroma content of aromatic rice at booting stage. Guangdong Agric Sci. 8:1–3. (in Chinese with English abstract).
  • Xie W, Ashraf U, Zhong D, Lin R, Xian P, Zhao T, Feng H, Wang S, Duan M, Tang X, et al. 2019. Application of γ-aminobutyric acid (GABA) and nitrogen regulates aroma biochemistry in fragrant rice. Food Sci Nutr. 7:3784–3796. doi:10.1002/fsn3.1240.
  • Xie W, Kong L, Ma L, Ashraf U, Pan S, Duan M, Tian H, Wu L, Tang X, Mo Z. 2020. Enhancement of 2-acetyl-1-pyrroline (2AP) concentration, total yield, and quality in fragrant rice through exogenous γ-aminobutyric acid (GABA) application. J Cereal Sci. 91:102900. doi:10.1016/j.jcs.2019.102900.
  • Yu GH, Sun MX. 2007. Deciphering the possible mechanism of GABA in tobacco pollen tube growth and guidance. Plant Signal Behav. 2:393–395. doi:10.4161/psb.2.5.4265.
  • Zhao D, Pu X, Zeng Y, Li B, Du J, Yang S. 2009. Determination of γ-aminobutyric acid in barley. J Triticeae Crops. 29:69–72 (in Chinese with English abstract).