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. 2021 Sep 17;10(9):1939. doi: 10.3390/plants10091939

Table 4.

Exogenous GABA modifies GABA, antioxidant, phytohormone and secondary pathways, and improves tolerance to abiotic stresses.

Plant Species Abiotic Stress Biochemical, Molecular and Physiological Responses References
Arabidopsis
(Arabidopsis thaliana (L.) Heyhn.)
Drought for up to 7 d
  • ↓ light-stimulated increase in stomatal conductance

  • ↑ WUE

[40]
Tomato
(Solanum lycopersicum L.)
2 °C for 2 d
  • ↑ GABA; ↓ Pro, soluble sugars, MDA and EL

[150]
75 mM NaCl for 6 d
  • ↑ growth rate, DM, Chl

  • ↑ GABA, Glu, Pro, activities of GAD, SOD, POD and CAT, expression of GAD1-3, especially GAD1

  • ↓ ROS, MDA, Na+, Na+ flux from roots to leaves

[151]
Creeping bentgrass (Agrostis stolonifera L.) 35/30 °C or drought for 20–35 d
  • ↑ Chl, RWC, cell membrane stability

  • ↑ Pro

  • ↓ ROS, MDA, EL

  • ↑ expression of ABF3, POD, APX, HSP90, DHN3 and MT1 during heat

  • ↑ expression of CDPK26, MAPK1, ABF3, WRKY75, MYB13, HSP70, MT1, 14-3-3, SOD, CAT, POD, APX and DHAR during drought

[152,153]
35/30 °C D:N for 35 d
  • ↑ stomatal conductance, WUE, osmotic adjustment

  • ↑ amino acids (GABA), organic acids, sugars, ASC, GSH, GSSG, activities of SOD, APX, DHAR and GR

  • ↓ H2O2, MDA

[154]
Drought for 25 d
  • ↑ turf quality, RWC, osmotic adjustment, Chl, photochemical efficiency, amino acids (GABA), organic acids

  • ↓ EL

[155]
38/33 °C D:N for 12 d
  • ↑ Chl, PN

  • ↑ GABA, expression of CAD3, ACS, AER and many HSPs

  • ↓ MDA, EL

[156]
PEG (−0.52 MPa) for 12 d
  • ↑ RWC, WUE, Chl, PN

  • ↑ GABA, NO, activities of NR, GS, GOGAT, GDH, SOD, CAT, MDHAR and GR

  • ↓ Glu, GAD activity

  • ↓ photoinhibition, ROS, MDA, EL

[157]
Rice
(Oryza sativa L.)
42/37 °C D:N for 10 d
  • ↑ growth, survival, RWC, stomatal conductance

  • ↑ GABA, Pro, ASC, GSH, activities of CAT and APX

  • ↓ H2O, MDA, EL

[158]
100 μM As3+ (pH 4.4) for 22 d
  • ↑ FM, shoot height, PN, WUE

  • ↑ GABA, expression of GAD2,3, GABA-T1,2 and SSADH (shoot)

  • ↓ activities of CAT, APX, POD, SOD and GR (shoot)

  • ↓ H2O2, GSH:GSSG (shoot)

  • ↓ expression of GAD3, GABA-T2 and SSADH (roots)

[159]
25 μM As3+ (pH 4.4) for 7 d
  • ↑ Pro, Glu, linolenic acid, Put, expression of ADC and SAMDC, activities of MDHAR, GPX and POD (shoot)

  • ↓ Spd, Spm, ROS (shoot)

  • ↑ length, Put, expression of ADC and SAMDC (roots)

  • ↓ Spd, Spm, ROS

[160]
30% PEG or/and 150 mM NaCl or 1 wk
  • ↑ germination percent, vigor index, seedling growth, PN, Chl, RWC, WUE

  • ↑ GABA, sugars, protein, starch

  • ↓ Pro, Na+, H2O2, O2•−, •OH, MDA

  • ↑ K+, activities or/and expression of GR, SOD, CAT, APX, PAL, PPO, SKDH, CAD, GST, CHI, expression of many CIPKs,

[161]
White clover
(Trifolium repens L.)
15% PEG for 17 d
  • ↑ RWC, activities of GABA-T, OGDH, P5CS, PDH, ADC, ODC and SAMDC, GAD expression

  • ↑ GABA; transient ↑ Pro

  • ↓ EL, MDA, wilt

  • ↓ Glu, activities of GAD, PAO, CuAO and OAT

  • transient ↑ and ↓ in expression of ADC, ODC, SAMDC, PAO and CuAO

  • modifies free and conjugated PAs

[162]
100 mM NaCl for 1 wk
  • ↑ germination percentage, shoot DM and height.

  • ↑ GABA, activities of amylase, CAT, APX, POX, SOD, GR. DHAR and MDHR

  • ↑ expression of CuZnSOD, MnSOD, FeSOD, CAT, APX, MDHR, GST, GPX, HKT1, HKT8, HAL2, H+-ATPase, SOS1 and genes encoding dehydrins

  • ↓ starch, soluble sugars, amino acids (including Pro)

  • ↓ H2O2, MDA, EL

[163]
Melon
(Cucumis melo L. var. reticulatus)
2 mg L−1 O2 for 8 d
  • ↑ GABA, Glu, expression and activities of ADC, ODC and SAMDC (roots)

  • ↓ expression and activities of DAO and PAO (roots)

  • modifies free and conjugated PAs (roots)

[164]
50–80 mM Ca(NO3)2 (pH 8.6) for 1 wk
  • ↑ leaf area, PN, chloroplast ATPase activities, ALA and improves chloroplast structure (seedling)

  • ↑ GABA, ASC, GSH (seedling)

  • ↑ activities of GAD, GABA-T, PAO, SOD, APX, GR, MDAR and DHAR, expression of RBOHD (seedling)

  • ↓ DAO activity, H2O2, MDA, Chl and its precursors (seedling)

  • ↑ Spd, Spm, activities of ADC, ODC and SAMDC, but ↓ Put (leaves and roots)

  • ↑ GABA-T activity (roots)

  • ↓ activities of GAD, PAO and DAO (roots)

  • Modifies levels of free and conjugated PAs

[165,166,167]
75 mM NaCl/Na2SO4/NaHCO3/Na2CO3 (1:9:9:1 molar ratio, pH 8.6) for 24 h
  • ↑ plant growth, NO and activities of NR, NOS, SOD, CAT, APX and GR

  • ↓ MDA, restores Na+/K+ balance

[168]
Mungbean
(Vigna radiata (L.) R. Wilczek)
45/30 °C D:N for 30 d until maturity
  • ↑ pod number, pod yield, seed yield, PN

  • ↑ sugars, Pro, ASC, GSH

  • ↑ activities of Rubisco, P5CS, PDH, SOD, CAT, APX and GR

  • ↓ H2O2, MDA

[169]
Caragana intermedia Kuang et H.C. Fu 300 mM NaCl for 3 d
  • ↑ GABA; ↓ H2O2 (roots)

  • transient ↑ in expression of RBOHB, ACO1,2 and ABA receptor, ethylene production (roots)

  • CuAO expression (roots)

[170]
Wheat
(Triticum aestivum L.)
100–200 mM NaCl for 21 d; 300 mM NaCl for 24 h
  • ↑ germination, shoot DM, Chl, PN, activities of SOD and CAT

  • ↓ MDA, EL

[171]
Corn
(Zea mays L.)
300 mM NaCl for 48 h
  • ↑ shoot height, leaf DM, area per plant, mitochondrial function.

  • ↑ GABA, Pro, sugars, activities of SOD and CAT activities.

  • ↓ GAD activity

  • ↓ MDA

[172]
waterlogging for 14 d
  • ↑ shoot and root DM, PN, Chl, number of grana per chloroplast, GABA, activities of SOD, POD, CAT, GR and APX

  • ↓ MDA, H2O2, O2•−

[173]
Lettuce
(Latuca sativa L.)
80 mM NaCl for 2 wk
  • ↓ germination time

  • ↑ shoot and root DM, photosynthetic electron flow, activities of CAT, APX and SOD

  • ↓ Pro, H2O2, EL

[174]
Poplar
(Populus tomentosa Carr.)
200 mM NaCl for 1 d
  • ↓ H2O2, C2H4 (leaves)

  • ↑ ABA (leaves)

  • ↑ H2O2 (roots)

  • differential expression of various ABA/ethylene biosynthesis and receptor genes

[175]
Perennial ryegrass
(Lolium perenne L.)
Drought for 14 d
  • ↑ RWC, canopy temperature, turf quality, POD activity

  • ↓ wilt rating, MDA, EL

[176]
Black pepper (Piper nigrum L.) 10% PEG (w/v) for 15 d
  • ↑ RWC, SOD activity

  • ↓ wilting %, Pro, MDA, impact on mitochondrial activity

[177]
Prunus rootstock (Prunus avium L.) 4 mg L−1 O2 for 14 d
  • transient ↓ and ↑ in H2O2 in roots and leaves, respectively.

  • ↑ PN, stomatal conductance, Chl, Ala (leaves)

  • ↓ Glu (leaves)

  • transient ↑ in Glu, Ala, GAD2,4 expression (roots)

[178]
Barley
(Hordeum vulgare L.)
20 μM Al3+ (pH 4.5) for 1 d
  • ↑ elongation, activities of SOD, CAT and POD (roots)

  • ↓ protein carbonylation, MDA, ROS

[179]
20 mM NaCl for 6 d
  • ↑ total phenolics and flavonoids (gallic acid, protocatechic acid, caffeic acid, quercetin), ABTS and DPPH radical scavenging activities

  • ↑ activities or expression of PAL, C4H, 4CL

  • ↓ MDA

[180]
Mustard
(Brassica juncea L.)
0.15 or 0.3 mM CrVI for 5 d
  • ↑ shoot height and DM, RWC, Chl, GSH, ASC, GSH/GSSG, ASC/DHA, activities of MDHAR, DHAR, GR, GPX, SOD and CAT

  • ↓ Pro, ROS, MDA, DHA, GSSG, MG, LOX activity

[181]
Tobacco
(Nicotiana tabaccum L.)
200 μM Cd for 7 d
  • ↑ Pro, GSH, stability of O2-evolving complex, electron transfer rate in PSII, stomatal conductance, expression of P5CS and P5CR

  • ↓ H2O2, MDA

[182]
Sunflower
(Helianthus annuus L.)
38 °C or drought 55 d
  • ↑ shoot height and FM, root FM, Chl, transpiration, Pro and TSS

  • ↓ H2O2, MDA, EL

  • may ↑ activities of SOD and POD, expression of Hsp70, MDHAR, Osmotin, GR and Aquaporin

[183]
Carrot
(Daucus carota L.)
Drought for 2 wk
  • ↑ leaf and root growth, RWC, amino acids, CAT activity

  • ↓ MDA, EL

[184]

Symbols: ↑, increases/improves; ↓, decreases. Abbreviations: 14-3-3, regulatory protein; ABA, abscisic acid; ABF, transcription factor; ACS, acetyl-coenzyme A synthetase; AER, NADPH-dependent alkenal reductase P2; As3+, arsenic; ASC, ascorbate; ADC, arginine decarboxylase; ALA, δ-aminolevulinic acid; Al3+, aluminum; APX, ascorbate peroxidase; CAD3, cinnamyl alcohol dehydrogenase 3; CAT, catalase; Cd, cadmium; CDPK, calcium-dependent protein kinase; CrVI, chromium; CuAO, copper amine oxidase; D, day; DAO, diamine oxidase; DHA, dehydroascorbate; DHAR, dehydroascorbate reductase; DHN, dehydrin; DM/FM, dry/fresh mass; EL, electrolyte leakage; GABA, γ-aminobutyric acid; GABA-TP or GABA-TOG, pyruvate- or 2-oxoglutarate-dependent GABA transaminase; GAD, glutamate decarboxylase; Glu, glutamate; GOGAT, glutamate synthase; GPX, glutathione peroxidase; GR, glutathione reductase; GS, glutamine synthetase; GSH, reduced glutathione; GST, glutathione S-transferase; H2O2, hydrogen peroxide; HSP, heat shock protein; LOX, lipoxygenase; MAPK, mitogen-activated protein kinase; MDA, malondialdehyde; MDHAR, monodehydroascorbate reductase; miRNA, microRNA; MSI, membrane stability index; MT, metallothionein; MYB, transcription factor; N, night; NO, nitric oxide; NOS, NO synthase; NR, nitrate reductase; OAT, ornithine δ-aminotransferase; ODC, ornithine decarboxylase; P5CR, Δ1-pyrroline-5-carboxylate reductase; P5CS, Δ1-pyrroline-5-carboxylate synthetase; PA, polyamine; PAO, polyamine oxidase; PEG, polyethyleneglycol 6000; PN, net photosynthesis; POD, peroxide dismutase; PPO, polyphenol oxidase; POX, peroxide oxidase; PP, phenylpropanoid; Pro, proline; Put, putrescine; PYL, pyrabactin resistance 1-like; RBOHD, respiratory burst oxidase homologue D/NADPH oxidase; ROS, reactive oxygen species; RuBisCo, ribulose bisphosphate carboxylase oxygenase; RWC, relative water content; SAMDC, S-adenosylmethionine decarboxylase; Spd, spermidine; Spm, spermine; SSADH, succinic semialdehyde dehydrogenase; TSS, total soluble sugars; WRKY, transcription factor; WUE, water use efficiency.