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γ-Aminobutyric Acid Regulates Grain Yield Formation in Different Fragrant Rice Genotypes Under Different Nitrogen Levels

  • Yuzhan Li
  • Rifang Lai
  • Wu Li
  • Jiaqi Liu
  • Mingzhi Huang
  • Yijing Tang
  • Xiangru Tang
  • Shenggang Pan
  • Meiyang Duan
  • Hua Tian
  • Longmei Wu
  • Shuli Wang
  • Zhaowen MoEmail author
Article
  • 28 Downloads

Abstract

The influences of γ-aminobutyric acid (GABA) and nitrogen on grain yield, yield-related traits, plant growth, grain–leaf ratio and NSC contents in different fragrant rice genotypes are not fully understood. A pot experiment was conducted with four nitrogen rates, i.e. 0, 0.87, 1.75, and 2.61 g pot−1, two GABA levels, i.e. 0 and 250 mg L−1, and three fragrant rice cultivars, i.e. Yuxiangyouzhan, Yungengyou 14 and Basmati. Results depicted that GABA treatment significantly increased the mean grain yield by 11.84% as a consequence of the increment of grain weight, spikelet per pot, grain weight per leaf area, stem sheath dry weight at HS, panicle dry weight at HS, panicle dry weight at MS and total dry weight at MS. Besides, significant effects of nitrogen and cultivar on yield and yield-related traits and some rice growth parameters were observed. Moreover, significant positive correlation relationships between yield and panicle number per pot, leaf area and dry weight for all the cultivars were observed. GABA application could alleviate the effects of nitrogen on grain yield in fragrant rice. These results suggest that GABA is feasible to increase grain yield and improve rice plant growth for fragrant rice varieties grown under different nitrogen conditions.

Keywords

Fragrant rice γ-Aminobutyric acid (GABA) Nitrogen Grain yield Plant growth 

Notes

Acknowledgements

The authors acknowledge the funding provided by the National Natural Science Foundation for Young Scientists (31601244), the Special Fund for National Natural Science Foundation of China (31271646), and the Key R&D Program of Guangdong (No. 2019B020221003).

Author contributions

ZM designed the experiments; YL, RL, JL, MH, and YT investigated the traits; ZW and WL analysed the data and wrote the manuscript; ZM, XT, SP, MD, HT, LW and SW revised and edited the manuscript. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interest

All the authors declare that there are no conflicts of interest.

References

  1. Aghdam MS, Naderi R, Jannatizadeh A, Sarcheshmeh MAA, Babalar M (2016) Enhancement of postharvest chilling tolerance of anthurium cut flowers by γ-aminobutyric acid (GABA) treatments. Sci Hortic 198:52–60Google Scholar
  2. An N, Wei WL, Qiao L, Zhang FS, Christie P, Jiang RF, Dobermann A, Goulding KWT, Fan JL, Fan MS (2018) Agronomic and environmental causes of yield and nitrogen use efficiency gaps in Chinese rice farming systems. Eur J Agron 93:40–49Google Scholar
  3. Barbosa JM, Singh NK, Cherry JH, Locy RD (2010) Nitrate uptake and utilization is modulated by exogenous ɤ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiol Biochem 48:443–450Google Scholar
  4. Batten GD, Blakeney AB, McGrath VB, Ciavarella S (1993) Non-structural carbohydrate: analysis by near infrared reflectance spectroscopy and its importance as an indicator of plant growth. Plant Soil 155(1):243–246Google Scholar
  5. Batushansky A, Kirma M, Grillich N, Toubiana D, Pham PA, Balbo I, Fromm H, Galili G, Fernie AR, Fait A (2014) Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic. Mol Plant 7(6):1065–1068Google Scholar
  6. Beuve N, Rispail N, Lainé P, Cliquet JB, Ourry A, Le Deunff E (2004) Putative role of γ-aminobutyric acid (GABA) as a long-distance signal in up-regulation of nitrate uptake in Brassica napus L. Plant Cell Environ 27(8):1035–1046Google Scholar
  7. Boling AA, Bouman BAM, Tuong TP, Konboon Y, Harnpichitvitaya D (2011) Yield gap analysis and the effect of nitrogen and water on photoperiod-sensitive Jasmine rice in north-east Thailand. NJAS-Wagening J Life Sci 58(1–2):11–19Google Scholar
  8. Browne RA, White EM, Burke JI (2006) Responses of developmental yield formation processes in oats to variety, nitrogen, seed rate and plant growth regulator and their relationship to quality. J Agric Sci 144(6):533–545Google Scholar
  9. Chen C, Wang Y, Yang B, Zhu ZK, Cao WY, Luo G, Zhou J, Wang XJ, Yu XF, Yuan QM, Zhong J, Yao YL, Huang JY, Wang YL, Dong GC (2015) Plant height affects nitrogen absorption and utilization in rice with similar genetic background. Sci Agric Sin 48(22):4450–4459Google Scholar
  10. Fageria NK, Santos AB (2015) Yield and yield components of lowland rice genotypes as influenced by nitrogen fertilization. Commun Soil Sci Plant Anal 46(14):1723–1735Google Scholar
  11. Fageria NK, Santos AD, Cutrim VA (2008) Dry matter and yield of lowland rice genotypes as influence by nitrogen fertilization. J Plant Nutr 31(4):788–795Google Scholar
  12. Fageria NK, Carvalho MCS, Dos Santos FC (2014) Response of upland rice genotypes to nitrogen fertilization. Commun Soil Sci Plant Anal 45(15):2058–2066Google Scholar
  13. 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(1):14–19Google Scholar
  14. Fait A, Nesi AN, Angelovici R, Lehmann M, Pham PA, Song LH, Haslam RP, Napier JA, Galili G, Fernie AR (2011) Targeted enhancement of glutamate-to-γ-aminobutyrate conversion in Arabidopsis seeds affects carbon-nitrogen balance and storage reserves in a development-dependent manner. Plant Physiol 157(3):1026–1042Google Scholar
  15. Fan MS, Shen JB, Yuan LX, Jiang RF, Chen XP, Davies WJ, Zhang FS (2011) Improving crop productivity and resource use efficiency to ensure food security and environmental quality in China. J Exp Bot 63(1):13–24Google Scholar
  16. Farooq M, Nawaz A, Chaudhry MAM, Indrasti R, Rehman A (2017) Improving resistance against terminal drought in bread wheat by exogenous application of proline and gamma-aminobutyric acid. J Agron Crop Sci 203(6):464–472Google Scholar
  17. Hu XH, Xu ZR, Xu WN, Li JM, Zhao N, Zhou Y (2015) Application of γ-aminobutyric acid demonstrates a protective role of polyamine and GABA metabolism in muskmelon seedlings under Ca(NO3)2 stress. Plant Physiol Biochem 92:1–10Google Scholar
  18. Inthapanya P, Sihavong P, Sihathep V, Chanphengsay M, Fukai S, Basnayake J (2000) Genotype differences in nutrient uptake and utilisation for grain yield production of rainfed lowland rice under fertilised and non-fertilised conditions. Field Crops Res 65(1):57–68Google Scholar
  19. Jia HS, Lu CM (2003) Effects of abscisic acid on photoinhibition in maize plants. Plant Sci 165(6):1403–1410Google Scholar
  20. Jia Y, Zou DT, Wang JG, Sha HJ, Liu HL, Inayat MA, Sun J, Zheng HL, Xia N, Zhao HW (2017) Effects of γ-aminobutyric acid, glutamic acid, and calcium chloride on rice (Oryza sativa L.) under cold stress during the early vegetative stage. J Plant Growth Regul 36(1):240–253Google Scholar
  21. Ju CX, Buresh RJ, Wang ZQ, Zhang H, Liu LJ, Yang JC, Zhang JH (2015) Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crops Res 175:47–55Google Scholar
  22. Kathiresan A, Miranda J, Chinnappa CC, Reid DM (1998) γ–aminobutyric acid promotes stem elongation in stellaria longipes: the role of ethylene. Plant Growth Regul 26(2):131–137Google Scholar
  23. Kinnersley AM, Lin F (2000) Receptor modifiers indicate that c-aminobutyric acid (GABA) is a potential modulator of ion transport in plants. Plant Growth Regul 32:65–76Google Scholar
  24. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19(6):479–509Google Scholar
  25. Knapp JS, Harms CL (1988) Nitrogen fertilization and plant growth regulator effects on yield and quality of four wheat cultivars. J Prod Agric 1(2):94–98Google Scholar
  26. 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 Plant 60(1):123–131Google Scholar
  27. Li M, Ashraf U, Tian H, Mo Z, Pan S, Anjum SA, Duan M, Tang XR (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 103:167–175Google Scholar
  28. Li S, Jiang H, Wang J, Wang Y, Pan S, Tian H, Duan M, Wang S, Tang X, Mo Z (2019) Responses of plant growth, physiological, gas exchange parameters of super and non-super rice to rhizosphere temperature at the tillering stage. Sci Rep 9:10618Google Scholar
  29. Li W, Liu JH, Ashraf U, Li GK, Li YL, Lu WJ, Gao L, Han FG, Hu JQ (2016c) Exogenous γ-aminobutyric acid (GABA) application improved early growth, net photosynthesis, and associated physio-biochemical events in maize. Front Plant Sci 7:919Google Scholar
  30. Li Z, Yu JJ, Peng Y, Huang BR (2016d) Metabolic pathways regulated by γ-aminobutyric acid (GABA) contributing to heat tolerance in creeping bentgrass (Agrostis stolonifera). Sci Rep 6:30338Google Scholar
  31. Li YF, Fan Y, Ma Y, Zhang Z, Yue HB, Wang LJ, Li J, Jiao Y (2017a) 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(2):436–449Google Scholar
  32. Li Z, Yu JJ, Peng Y, Huang BR (2017b) Metabolic pathways regulated by abscisic acid, salicylic acid and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera). Physiol Plant 159(1):42–58Google Scholar
  33. Liu K, Deng J, Lu J, Wang X, Lu B, Tian X, Zhang Y (2019a) High nitrogen levels alleviate yield loss of super hybrid rice caused by high temperatures during the flowering stage. Front Plant Sci 10:357Google Scholar
  34. Liu K, Yang R, Lu J, Wang X, Lu B, Tian X, Zhang Y (2019b) Radiation use efficiency and source-sink changes of super hybrid rice under shade stress during grain-filling stage. Agron J 111:1–11Google Scholar
  35. 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. China Agric Sci 44(4):753–761Google Scholar
  36. Luo DQ, Wang SH, Jiang XH, Li GH, Zhou WJ, Li M, Ji GM, Ding YF, Ling QH, Liu ZH (2014) Effects of accurate fertilizer model (AF) on yield and population quality of hybrid indica rice cultivars in guizhou highland area. Sci Agric Sin 47(11):2099–2108Google Scholar
  37. Ma XL, Zhu CH, Yang N, Gan LJ, Xia K (2016) γ-Aminobutyric acid addition alleviates ammonium toxicity by limiting ammonium accumulation in rice (Oryza sativa) seedlings. Physiol Plant 158(4):389–401Google Scholar
  38. Mahmud JA, Hasanuzzaman M, Nahar K, Rahman A, Hossain MS, Fujita M (2017) γ-Aminobutyric acid (GABA) confers chromium stress tolerance in Brassica juncea L. by modulating the antioxidant defense and glyoxalase systems. Ecotoxicology 26(5):675–690Google Scholar
  39. Mekonnen DW, Flügge UI, Ludewig F (2016) Gamma-aminobutyric acid depletion affects stomata closure and drought tolerance of Arabidopsis thaliana. Plant Sci 245:25–34Google Scholar
  40. Mo ZW, Lei S, Ashraf U, Khan I, Li Y, Pan SG, Duan MY, Tian H, Tang X (2017) Silicon fertilization modulates 2-acetyl-1-pyrroline content, yield formation and grain quality of aromatic rice. J Cereal Sci 75:17–24Google Scholar
  41. Palaniswamy KM, Gomez KA (1974) Length-width method for estimating leaf area of rice 1. Agron J 66(3):430–433Google Scholar
  42. Pan SG, Rasul F, Li W, Tian H, Mo ZW, Duan MY, Tang XR (2013) Roles of plant growth regulators on yield, grain qualities and antioxidant enzyme activities in super hybrid rice (Oryza sativa L.). Rice 6(1):9Google Scholar
  43. Pan JF, Liu YZ, Zhong XH, Lampayan RM, Singleton GR, Huang NR, Liang KM, Peng BL, Tian K (2017) Grain yield, water productivity and nitrogen use efficiency of rice under different water management and fertilizer-N inputs in South China. Agric Water Manag 184:191–200Google Scholar
  44. Peng SB (2014) Reflection on China’s rice production strategies during the transition period. Sci Sin Vitae 44(8):845–850Google Scholar
  45. Peng SB, Huang JL, Zhong XH, Yang JC, Wang GH, Zou YB, Zhang FS, Zhu QS, Buresh R, Witt C (2002) Challenge and opportunity in improving fertilizer-nitrogen use efficiency of irrigated rice in China. Agric Sci China 1(7):776–785Google Scholar
  46. Peng JW, Liu Q, Rong XM, Xie GX, Zhu HM (2003) Effects of plant growth regulator on accumulation and transportation of nitrogen and grain protein contents of rice. J Hunan Agric Univ 29(5):368–371Google Scholar
  47. Peng SB, Buresh RJ, Huang JL, Yang JC, Zou YB, Zhong XH, Wang GH, Zhang FS (2006) Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crops Res 96(1):37–47Google Scholar
  48. Peng SB, Buresh RJ, Huang JL, Zhong XH, Zou YB, Yang JC, Wang GH, Liu YY, Hu RF, Tang QY, Cui K, Zhang FS, Dobermann A (2010) Improving nitrogen fertilization in rice by site specific N management. A review. Agron Sustain Dev 30(3):649–656Google Scholar
  49. Ramesh SA, Tyerman SD, Gilliham M, Xu B (2017) γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74(9):1577–1603Google Scholar
  50. Renault H, El Amrani A, Berger A, Mouille G, Soubigou-Taconnat L, Bouchereau A, Deleu C (2013) γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 36(5):1009–1018Google Scholar
  51. 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 112:741–748Google Scholar
  52. Roberts MR (2007) Does GABA act as a signal in plants? Hints from molecular studies: hints from molecular studies. Plant Signal Behav 2(5):408–409Google Scholar
  53. 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 125:52–66Google Scholar
  54. Searchinger TD, Wirsenius S, Beringer T, Dumas P (2018) Assessing the efficiency of changes in land use for mitigating climate change. Nature 564(7735):249–253Google Scholar
  55. Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci 108(50):20260–20264Google Scholar
  56. Tirol-Padre A, Ladha JK, Singh U, Laureles E, Punzalan G, Akita S (1996) Grain yield performance of rice genotypes at suboptimal levels of soil N as affected by N uptake and utilization efficiency. Field Crops Res 46(1–3):127–143Google Scholar
  57. Valin H, Sands RD, Van der Mensbrugghe D, Nelson GC, Ahammad H, Blanc E, Bodirsky B, Fujimori S, Hasegawa T, Havlik P, Heyhoe E, Kyle P, Mason-D’Croz D, Paltsev S, Rolinski S, Tabeau A, Meijl HV, Lampe MV, Willenbockel D (2014) The future of food demand: understanding differences in global economic models. Agric Econ 45(1):51–67Google Scholar
  58. Vijayakumari K, Puthur JT (2016) γ-Aminobutyric acid (GABA) priming enhances the osmotic stress tolerance in Piper nigrum Linn. plants subjected to PEG-induced stress. Plant Growth Regul 78(1):57–67Google Scholar
  59. Wang F, Peng SB (2017) Yield potential and nitrogen use efficiency of China’s super rice. J Integr Agric 16(5):1000–1008Google Scholar
  60. Wu FB, Wu LH, Xu FH (1998) Chlorophyll meter to predict nitrogen sidedress requirements for short-season cotton (Gossypium hirsutum L.). Field Crops Res 56(3):309–314Google Scholar
  61. Xiong DL, Yu TT, Ling XX, Fahad S, Peng SB, Li Y, Huang JL (2015) Sufficient leaf transpiration and nonstructural carbohydrates are beneficial for high-temperature tolerance in three rice (Oryza sativa) cultivars and two nitrogen treatments. Funct Plant Biol 42(4):347–356Google Scholar
  62. Yamuangmorn S, Dell B, Rerkasem B, Prom-u-thai C (2018) Applying nitrogen fertilizer increased anthocyanin in vegetative shoots but not in grain of purple rice genotypes. J Sci Food Agric 98(12):4527–4532Google Scholar
  63. Yan W, Zhang XX, Yuan A (2011) Effects of two plant growth regulators on the growth and recovery of alfalfa seedlings exposed to aluminum stress. J Shanghai Jiaotong Univ (Agric Sci) 29:75–82Google Scholar
  64. Yang AP, Cao SF, Yang ZF, Cai YT, Zheng YH (2011) γ-Aminobutyric acid treatment reduces chilling injury and activates the defence response of peach fruit. Food Chem 129(4):1619–1622Google Scholar
  65. Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528(7580):51–59Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Yuzhan Li
    • 1
  • Rifang Lai
    • 1
  • Wu Li
    • 2
    • 3
  • Jiaqi Liu
    • 1
  • Mingzhi Huang
    • 1
  • Yijing Tang
    • 1
  • Xiangru Tang
    • 1
    • 4
  • Shenggang Pan
    • 1
    • 4
  • Meiyang Duan
    • 1
    • 4
  • Hua Tian
    • 1
    • 4
  • Longmei Wu
    • 5
  • Shuli Wang
    • 1
    • 4
  • Zhaowen Mo
    • 1
    • 2
    Email author
  1. 1.College of AgricultureSouth China Agricultural UniversityGuangzhouChina
  2. 2.Crop Research InstituteGuangdong Academy of Agricultural SciencesGuangzhouChina
  3. 3.Key Laboratory of Crops Genetics & Improvement of Guangdong ProvinceGuangzhouChina
  4. 4.Scientific Observing and Experimental Station of Crop Cultivation in South ChinaMinistry of Agriculture, P. R. ChinaGuangzhouChina
  5. 5.Rice Research InstituteGuangdong Academy of Agricultural SciencesGuangzhouChina

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