Abstract
Glutamate decarboxylase (GAD) is an enzyme that catalyses the conversion of l-glutamate into γ-aminobutyric acid (GABA), which is a four-carbon non-protein amino acid present in all organisms. Although plant GAD plays important roles in GABA biosynthesis, our knowledge concerning GAD gene family members and their evolutionary relationship remains limited. Therefore, in this study, we have analysed the evolutionary mechanisms of soybean GAD genes and suggested that these genes expanded in the soybean genome partly due to segmental duplication events. The approximate dates of duplication events were calculated using the synonymous substitution rate, and we suggested that the segmental duplication of GAD genes in soybean originated 9.47 to 11.84 million years ago (Mya). In addition, all segmental duplication pairs (GmGAD1/3 and GmGAD2/4) are subject to purifying selection. Furthermore, GmGAD genes displayed differential expression either in their transcript abundance or in their expression patterns under abiotic stress conditions like salt, drought, and cold. The expression pattern of paralogous pairs suggested that they might have undergone neofunctionalization during the subsequent evolution process. Taken together, our results provide valuable information for the evolution of the GAD gene family and represent the basis for future research on the functional characterization of GAD genes in higher plants.
Similar content being viewed by others
References
Baum G, Chen Y, Arazi T, Takatsuji H and Fromm H 1993 A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence, and functional analysis. J. Biol. Chem. 268 19610–19617
Ben-Ari Y, Khalilov I, Kahle KT and Cherubini E 2012 The GABA excitatory/inhibitory shift in brain maturation and neurological disorders. Neuroscientist 18 467–486
Beuve NRN, Laine P, Cliquet J-B, Ourry A and 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 1035–1046
Bouche N and Fromm H 2004 GABA in plants: just a metabolite? Trends Plant Sci. 9 110–115
Bouché N, Lacombe B and Fromm H 2003 GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol. 13 607–610
Bown AW, Macgregor KB and Shelp BJ 2006 Gamma-aminobutyrate: defense against invertebrate pests? Trends Plant Sci. 11 424–427
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, et al. 2002 Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14 559–574
Flagel LE and Wendel JF 2009 Gene duplication and evolutionary novelty in plants. New Phytol. 183 557–564
Hyun TK, Eom SH, Jeun YC, Han SH and Kim J-S 2013 Identification of glutamate decarboxylases as a γ-aminobutyric acid (GABA) biosynthetic enzyme in soybean. Ind. Crop. Prod. 49 864–870
Jiang SY, González JM and Ramachandran S 2013 Comparative genomic and transcriptomic analysis of tandemly and segmentally duplicated genes in rice. PLoS One 8 e63551
Kumar V, Rani A, Pandey V and Chauhan GS 2006 Changes in lipoxygenase isozymes and trypsin inhibitor activity in soybean during germination at different temperatures. Food Chem. 99 565–568
Lancien M and Roberts MR 2006 Regulation of Arabidopsis thaliana 14-3-3 gene expression by γ-aminobutyric acid. Plant Cell Environ. 29 1430–1436
Lestari P, Van K, Lee J, Kang YJ and Lee SH 2013 Gene divergence of homeologous regions associated with a major seed protein content QTL in soybean. Front. Plant Sci. 4 176
Ling Y, Chen T, Jing Y, Fan L, Wan Y and Lin J 2013 γ-Aminobutyric acid (GABA) homeostasis regulates pollen germination and polarized growth in Picea wilsonii. Planta 238 831–843
Luo H, Song F, Goodman RM and Zheng Z 2005 Up-regulation of OsBIHD1, a rice gene encoding BELL homeodomain transcriptional factor, in disease resistance responses. Plant Biol. (Stuttg.) 7 459–468
Lynch M and Conery JS 2000 The evolutionary fate and consequences of duplicate genes. Science 290 1151–1155
Matsuyama A, Yoshimura K, Shimizu C, Murano Y, Takeuchi H and Ishimoto M 2009 Characterization of glutamate decarboxylase mediating gamma-amino butyric acid increase in the early germination stage of soybean (Glycine max [L.] Merr). J. Biosci. Bioeng. 107 538–543
Molina-Rueda JJ, Pascual MB, Canovas FM and Gallardo F 2010 Characterization and developmental expression of a glutamate decarboxylase from maritime pine. Planta 232 1471–1483
Nogata Y and Nagamine T 2009 Production of free amino acids and gamma-aminobutyric acid by autolysis reactions from wheat bran. J. Agric. Food Chem. 57 1331–1336
Oh CH and Oh SH 2004 Effects of germinated brown rice extracts with enhanced levels of GABA on cancer cell proliferation and apoptosis. J. Med. Food 7 19–23
Oh SH, Soh JR and Cha YS 2003 Germinated brown rice extract shows a nutracetical effect in the recovery of chronic alchol-related symptoms. J. Med. Food 6 115–121
Park HC, Kim ML, Kang YH, Jeon JM, Yoo JH, Kim MC, Park CY, Jeong JC et al. 2004 Pathogen- and NaCl-induced expression of the SCaM-4 promoter is mediated in part by a GT-1 box that interacts with a GT-1-like transcription factor. Plant Physiol. 135 2150–2161
Queiroz HM, Sodek L and Haddad CRB 2012 Effect of salt on the growth and metabolism of Glycine max. Braz. Arch. Biol. Technol. 55 809–817
Reddy UK, Almeida A, Abburi VL, Alaparthi SB, Unselt D, Hankins G, Park M, Choi D, et al. 2014 Identification of gene-specific polymorphisms and association with capsaicin pathway metabolites in Capsicum annuum L. collections. PLoS One 9 e86393
Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A and Deleu C 2010 The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biol. 10 20
Roberts MR 2007 Does GABA Act as a signal in plants?: Hints from molecular studies. Plant Signal. Behav. 2 408–409
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, et al. 2010 Genome sequence of the palaeopolyploid soybean. Nature 463 178–183
Schneider KT, van de Mortel M, Bancroft TJ, Braun E, Nettleton D, Nelson RT, Frederick RD, Baum TJ, et al. 2011 Biphasic gene expression changes elicited by Phakopsora pachyrhizi in soybean correlate with fungal penetration and haustoria formation. Plant Physiol. 157 355–371
Severin AJ, Cannon SB, Graham MM, Grant D and Shoemaker RC 2011 Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. Plant Cell 23 3129–3136
Shelp BJ, Bown AW and McLean MD 1999 Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 4 446–452
Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL and Brikis CJ 2012 Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci. 193-194 130–135
Shi H, Nam PK and Ma Y 2010a Comprehensive profiling of isoflavones, phytosterols, tocopherols, minerals, crude protein, lipid, and sugar during soybean (Glycine max) germination. J. Agric. Food Chem. 58 4970–4976
Shi SQ, Shi Z, Jiang ZP, Qi LW, Sun XM, Li CX, Liu JF, Xiao WF, et al. 2010b Effects of exogenous GABA on gene expression of Caragana intermedia roots under NaCl stress: regulatory roles for H2O2 and ethylene production. Plant Cell Environ. 33 149–162
Snedden WA, Arazi T, Fromm H and Shelp BJ 1995 Calcium/calmodulin activation of soybean glutamate decarboxylase. Plant Physiol. 108 543–549
Tajima F 1993 Simple methods for testing molecular clock hypothesis. Genetics 135 599–607
Takeshima K, Yamatsu A, Yamashita Y, Watabe K, Horie N, Masuda K and Kim M 2014 Subchronic toxicity evaluation of γ-aminobutyric acid (GABA) in rats. Food Chem. Toxicol. 68 128–134
Tamura K, Dudley J, Nei M and Kumar S 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 1596–1599
Wang Q, Ge X, Tian X, Zhang Y, Zhang J and Zhang P 2013 Soy isoflavones: the multipurpose phytochemical (review). Biomed. Rep. 1 697–701
von Schantz M, Jenkins A and Archer SN 2006 Evolutionary history of the vertebrate period genes. J. Mol. Evol. 62 701–707
Xing SG, Jun YB, Hau ZW and Liang LY 2007 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
Xu J-G and Hu Q-P 2014 Changes in γ-aminobutyric acid content and related enzyme activities in Jindou 25 soybean (Glycine max L.) seeds during germination. LWT Food Sci. Technol. 55 341–346
Yang R, Guo Q and Gu Z 2013 GABA shunt and polyamine degradation pathway on γ-aminobutyric acid accumulation in germinating fava bean (Vicia faba L.) under hypoxia. Food Chem. 136 152–159
Yang Z 2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24 1586–1591
Yang Z and Nielsen R 2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17 32–43
Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y and Hu Y 2013 The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biol. 13 148
Yoshimura M, Toyoshi T, Sano A, Izumi T, Fujii T, Konishi C, Inai S, Matsukura C, et al. 2010 Antihypertensive effect of a gamma-aminobutyric acid rich tomato cultivar 'DG03-9' in spontaneously hypertensive rats. J. Agric. Food Chem. 58 615–619
Zhou Y and Danbolt NC 2013 GABA and glutamate transporters in brain. Front. Endocrinol. (Lausanne) 4 165
Acknowledgements
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2014R1A1A2004432), Republic of Korea
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: Rajeev Kumar Varshney
[Hyun TK, Eom SH, Han X and Kim J-S 2014 Evolution and expression analysis of the soybean glutamate decarboxylase gene family. J. Biosci. 39 1–9] DOI 10.1007/s12038-014-9484-2
Supplementary materials pertaining to this article are available on the Journal of Biosciences Website at http://www.ias.ac.in/jbiosci/dec2014/supp/Hyun.pdf
Tae Kyung Hyun and Seung Hee Eom contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 212 kb)
Rights and permissions
About this article
Cite this article
Hyun, T.K., Eom, S.H., Han, X. et al. Evolution and expression analysis of the soybean glutamate decarboxylase gene family. J Biosci 39, 899–907 (2014). https://doi.org/10.1007/s12038-014-9484-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-014-9484-2