Kuraklık Stresi ve Bitki Proteomiği

Yıl 2020, Cilt: 10 Sayı: 1, 286 - 297, 15.01.2020

Mustafa Yıldız , Fadimana Kaya Hakan Terzi

https://doi.org/10.17714/gumusfenbil.568384

Cited By: 2

Öz

Hayatta kalabilmek için bitkilerin stresle sürekli başa çıkmaları
gerekir. Kuraklık bitki büyümesini, gelişimini ve ürün verimliliğini etkileyen
ana abiyotik streslerden biridir. Bitki ıslahı çalışmaları kapsamında, kuraklık
stresine karşı dayanıklı ve yüksek besin değerine sahip tarımsal bitki
türlerinin geliştirilmesi genomik, transkriptomik, proteomik ve metabolomik
gibi “omik” teknolojileri ile sağlanabilecektir. Proteomik, kuraklık stresi
koşullarında bir hücredeki proteinlerin tanımlanması, ifade seviyelerinin
belirlenmesi, translasyon sonrası modifikasyonların ortaya konulması ve
protein-protein etkileşimlerinin anlaşılması için güçlü bir yöntemdir. Farklı
streslere maruz kalan bitkilerde protein ifade seviyesinde önemli değişiklikler
meydana geldiğinden, proteomik yaklaşım stres koşulları altında proteinlerin
stres toleransı ile ilişkisini aydınlatmak için oldukça önemlidir. Kuraklık
stresi genellikle fotosentez, enerji metabolizması, stres savunma, protein
metabolizması ve sinyal iletimi gibi yolaklarda fonksiyon gören proteinlerin
ifade seviyelerinde değişime neden olmaktadır. Bitkilerde proteomik
çalışmalarda fizyolojik ve moleküler sonuçların beraber değerlendirilmesi
kuraklık toleransı için bazı potansiyel proteinler ya da metabolik yolakların keşfedilmesine
olanak tanımaktadır. Bu derlemede, bitkilerin kuraklık stresine vermiş
oldukları protein seviyesindeki tepkiler hakkındaki son bilgiler
tartışılmıştır.

Anahtar Kelimeler

Kuraklık stresi, Kuraklık toleransı, Proteomik, Savunma mekanizmaları

Drought Stress and Plant Proteomics

Öz

Plant need to overcome with stress to survive permanently. Drought is one
of the major abiotic stresses that affect growing and developing of plants and
productivity of crops. Within the scope of plant breeding studies, development
of agricultural plant species which are resistant to drought stress and have
high nutritional value will be provided by omics technologies such as genomics,
transcriptomics, proteomics and metabolomics. Proteomics is a strong method for
identification of proteins in a cell under drought stress conditions,
determination of expression levels, introducing post-translational
modifications, and understanding protein-protein interactions. Since there is a
significant change in protein expression level in plants exposed to different
stresses, the proteomics approach is quite important to elucidate the
relationship of proteins to stress tolerance. Drought stress usually causes
changes in expression levels of proteins that function in pathways such as
photosynthesis, energy metabolism, stress defense, protein metabolism and
signal transduction. Combination of physiological and molecular results in
proteomic studies in plants allows the discovery of some potential proteins or
metabolic pathways for drought tolerance. In this review, we discussed recent
information on plant responses to drought stress at protein level.

Anahtar Kelimeler

Drought stress, Drought tolerance, Proteomics, Defense mechanisms

Kaynakça

• Abreu, I., Farinha, A., Negrao, S., Goncalves, N., Fonseca, C., Rodrigues, M., Batista, R., Saibo, N. ve Oliveira, M., 2013. Coping with abiotic stress, proteome changes for crop improvement. Journal of Proteomics, 93, 145–168.
• Alam, I., Sharmin, S. A., Kim, K., Yang, J. K., Choi, M. S. ve Lee, B., 2010. Proteome analysis of soybean roots subjected to short-term drought stress. Plant and Soil, 333, 491–505.
• Babita, M., Maheswari, M., RaoL, M., Shanker, A.K. ve Rao, D.G., 2010. Osmotic adjustment, drought tolerance and yield in castor (Ricinus communis L.) hybrids. Environmental and Experimental Botany, 69, 243–249.
• Baier, M. ve Dietz, K.J., 1997. The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. The Plant Journal, 12, 179–190.
• Baldoni, E., Genga, A. ve Cominelli, E., 2015. Plant MYB transcription factors: their role in drought response mechanisms. International Journal of Molecular Sciences, 16, 15811–15851.
• Barkla, B.J., Vera-Estrella, R. ve Raymond, C., 2016. Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins. BMC Plant Biology, 16, 110.
• Batlang, U., Baisakh, N., Ambavaram, M.M. ve Pereira, A., 2013. Phenotypic and physiological evaluation for drought and salinity stress responses in rice. Methods in Molecular Biology, 956, 209–225.
• Bilal, T., Bisma, P. ve Reiaz, M., 2014. Signaling in response to cold stress, in: I. Tahir, R.U. Rehman, K.R. Hakeem (Eds.), Plant Signaling: Understanding the Molecular Crosstalk, Springer India, pp. 193–226.
• Boudet, J., Buitink, J., Hoekstra, F. A., Rogniaux, H., Larré, C. ve Satour, P., 2006. Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiology, 140, 1418–1436.
• Chaves, M.M., Flexas, J. ve Pinheiro, C., 2009. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany, 103, 551–560.
• Chen, F., Zhang, S., Jiang, H., Ma, W., Korpelainen, H. ve Li, C., 2011. Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. Journal of Proteome Research, 10(9), 3944–3958.
• Chintakovid, N., Maipoka, M., Phaonakrop, N., Mickelbart, M.V., Roytrakul, S. ve Chadchawan, S., 2017. Proteomic analysis of drought-responsive proteins in rice reveals photosynthesis-related adaptations to drought stress. Acta Physiologiae Plantarum, 39(10), 1–13.
• Chmielewska, K., Rodziewicz, P., Swarcewicz, B., Sawikowska, A., Krajewski, P., Marczak, Ł., Ciesiołka, D., Kuczynska, A., Mikołajczak, K., Ogrodowicz, P., Krystkowiak, K., Surma, M., Adamski, T., Bednarek, P. ve Stobiecki, M., 2016. Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Frontiers in Plant Science, 7, 1–14.
• Clement, M., Leonhardt, N., Droillard, M. J. ve Reiter, I., 2011. The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiology, 156, 1481–1492.
• Faghani, E., Gharechahi, J., Komatsu, S., Mirzaei, M., Khavarinejad, R.A., Najafi, F., Farsad, L.K. ve Salekdeh, G.H., 2015. Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. Journal of Proteomics, 114, 1–15.
• Faize, M., Burgos, L., Faize, L.V., Piqueras, A., Nicolas, E., Barba-Espin, G., Clemente-Moreno, M.J., Alcobendas, R., Artlip, T. ve Hernandez, J.A., 2011. Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. Journal of Experimental Botany, 62, 2599–2613.
• Frydman, J., 2001. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annual Review of Biochemistry, 70, 603–647.
• Gao, S., Zhang, Y.L., Yang, L., Song, J.B. ve Yang, Z.M., 2014. AtMYB20 is negatively involved in plant adaptive response to drought stress. Plant and Soil, 376, 433–443.
• González, J.C., Banerjee, R.V., Huang, S., Sumner, J.S. ve Matthews, R.G., 1992. Comparison of cobalamin-independent and cobalamin-dependent methionine synthases from Escherichia coli: two solutions to the same chemical problem. Biochemistry, 31, 6045–6056.
• Hao, P., Zhu, J., Gu, A., Lv, D., Ge, P. ve Chen, G., 2015. An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery. Proteomics, 15, 1544–1563.
• Hossain, Z., Khatoon, A. ve Komatsu, S., 2013. Soybean proteomics for unraveling abiotic stress response mechanism. Journal of Proteome Research, 12, 4670–4684.
• Ji, K., Wang, Y., Sun, W., Lou, Q., Mei, H. ve Shen, S., 2012. Drought-responsive mechanisms in rice genotypes with contrasting drought tolerance during reproductive stage. Journal of Plant Physiology, 169, 336–344.
• Johnová, P., Skalák, J., Saiz-Fernández, I. ve Brzobohatý, B., 2016. Plant responses to ambient temperature fluctuations and water-limiting conditions: a proteome-wide perspective. Biochimica et Biophysica Acta, 1864, 916–931.
• Joshi, R., Karan, R., Singla-Pareek, S.L. ve Pareek, A., 2016. Ectopic expression of Pokkali phosphoglycerate kinase-2 (OsPGK2-P) improves yield in tobacco plants under salinity stress. Plant Cell Reports, 35, 27–41.
• Katam, R., Sakata, K., Suravajhala, P., Pechan, T., Kambiranda, D.M., Naik, K.S. ve Basha, S.M., 2016. Comparative leaf proteomics of drought-tolerant and -susceptible peanut in response to water stress. Journal of Proteomics, 143, 209–226.
• Kausar, R., Arshad, M., Shahzad, A. ve Komatsu, S., 2013. Proteomics analysis of sensitive and tolerant barley genotypes under drought stress. Amino Acids, 44, 345–359.
• Khodadadi, E., Fakheri, B. A., Aharizad, S., Emamjomeh, A., Norouzi, M. ve Komatsu, S., 2017. Leaf proteomics of drought-sensitive and -tolerant genotypes of fennel. Biochimica et Biophysica Acta - Proteins and Proteomics, 1865(11), 1433–1444.
• Komatsu, S., Makino, T. ve Yasue, H., 2013. Proteomic and biochemical analyses of the cotyledon and root of flooding-stressed soybean plants. PLoS ONE, 8, e65301.
• Konopka-Postupolska, D., Clark, G., Goch, G., Debski, J., Floras, K. ve Cantero, A., 2009. The role of annexin 1 in drought stress in Arabidopsis. Plant Physiology, 150, 1394–410.
• Kosma, D. K., Murmu, J., Razeq, F. M., Santos, P., Bourgault, R. ve Molina, I., 2014. AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. The Plant Journal, 80, 216–229.
• Kosova, K., Vitamvas, P., Prasil, I.T. ve Renaut, J., 2011. Plant proteome changes under abiotic stress – contribution of proteomics studies to understanding plant stress response. Journal of Proteomics, 74, 1301–1322.
• Kosová, K., Vítámvás, P., Urban, M.O., Prášil, I.T. ve Renaut, J., 2018. Plant abiotic stress proteomics: The major factors determining alterations in cellular proteome. Frontiers in Plant Science, 9, 1–22.
• Kumari, S., Roy, S., Singh, P., Singla-Pareek, S.L. ve Pareek, A., 2013. Cyclophilins: proteins in search of function. Plant Signaling and Behavior, 8(1), e22734.
• Larkindale, J. ve Vierling, E., 2008. Core genome responses involved in acclimation to high temperature. Plant Physiology, 146, 748–761.
• Li, J.W., Chen, X.D., Hu, X.Y., Ma, L. ve Zhang, S.B., 2018. Comparative physiological and proteomic analyses reveal different adaptive strategies by Cymbidium sinense and C. tracyanum to drought. Planta, 247(1), 69–97.
• Limami, A.M., Glevarec, G., Ricoult, C., Cliquet, J.B. ve Planchet, E., 2008. Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. Journal of Experimental Botany, 59, 2325–2335.
• Liu, L., Hu, X., Song, J., Zong, X., Li, D. ve Li, D., 2009. Over-expression of a Zea mays L. protein phosphatase 2C gene (ZmPP2C) in Arabidopsis thaliana decreases tolerance to salt and drought. Journal of Plant Physiology, 166, 531–542.
• Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S. ve Gruissem, W., 2002. Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell, 14, 389–400.
• Luo, D., Niu, X., Yu, J., Yan, J., Gou, X., Lu, B.R. ve Liu, Y., 2012. Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). Plant Cell Reports, 31,1625–1635.
• Marrs, K.A., 1996. The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 127–158.
• Meyer, E., Aspinwall, M.J., Lowry, D.B., Palacio-Mejia, J.D., Logan, T.L., Fay, P.A. ve Juenger, T.E., 2014. Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.). BMC Genomics, 15, 527.
• Mhawech, P., 2005. 14–3–3 proteins—an update. Cell Research, 15, 228–236.
• Michaletti, A., Naghavi, M. R., Toorchi, M., Zolla, L. ve Rinalducci, S., 2018. Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Scientific Reports, 8(1), 1–18.
• Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410.
• Mohammadi, P.P., Moieni, A. ve Komatsu, S., 2012. Comparative proteome analysis of drought-sensitive and drought-tolerant rapeseed roots and their hybrid F1 line under drought stress. Amino Acids, 43, 2137–2152.
• Moschen, S., Di Rienzo, J. A., Higgins, J., Tohge, T., Watanabe, M., González, S. ve Heinz, R. A., 2017. Integration of transcriptomic and metabolic data reveals hub transcription factors involved in drought stress response in sunflower (Helianthus annuus L.). Plant Molecular Biology, 94(4–5), 549–564.
• Nakashima, K., Yamaguchi-Shinozaki, K. ve Shinozaki, K., 2014. The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Frontiers in Plant Science, 5, 1–7.
• Negi, N.P., Shrivastava, D.C., Sharma, V. ve Sarin, N.B., 2015. Overexpression of CuZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Reports, 34(7), 1109–1126.
• Nemati, N., Piro, A., Norouzi, M., Vaheda, M.M., Nisticò, D.M. ve Mazzuca, S., 2019. Comparative physiological and leaf proteomic analyses revealed the tolerant and sensitive traits to drought stress in two wheat parental lines and their F6 progenies. Environmental and Experimental Botany, 158, 223–237.
• Onaga, G. ve Wydra, K., 2016. Advances in plant tolerance to abiotic stresses, in: Abdurakhmonov, I.Y. (Ed.), Plant Genomics, IntechOpen, pp. 167–228.
• Piterkova, J., Luhova, L., Mieslerova, B., Lebeda, A. ve Petrivalsky, M., 2013. Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Science, 207, 57–65.
• Pitzschke, A., Forzani, C. ve Hirt, H., 2006. Reactive oxygen species signaling in plants. Antioxidants and Redox Signaling, 8, 1757–1764. Prasad, P.V.V., Pisipati, S.R., Momčilović, I. ve Ristic, Z., 2011. Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. Journal of Agronomy and Crop Science, 197, 430–441.
• Pitzschke, A., Forzani, C. ve Hirt, H., 2006. Reactive oxygen species signaling in plants. Antioxidants and Redox Signaling, 8, 1757–1764.
• Prasad, P.V.V., Pisipati, S.R., Momčilović, I. ve Ristic, Z., 2011. Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. Journal of Agronomy and Crop Science, 197, 430–441.
• Rasheed, S., Bashir, K., Matsui, A., Iida, K., Tanaka, M. ve Seki, M., 2016. Transcriptomic analysis of soil-grown Arabidopsis thaliana roots and shoots in response to a drought stress. Frontiers in Plant Science, 7, 1–21.
• Ravanel, S., Block, M.A., Rippert, P., Jabrin, S., Curien, G., Reeille, F. ve Douce, R., 2004. Methionine metabolism in plants: chloroplasts are autonomous for de novo methionine synthesis and can import S-adenosylmethionine from the cytosol. Journal of Biological Chemistry, 279, 22548–22557.
• Reggiani, R., Nebuloni, M., Mattana, M. ve Brambilla, I., 2000. Anaerobic accumulation of amino acids in rice roots: role of the glutamine synthetase/glutamate synthase cycle. Amino Acids, 18, 207–217.
• Rocha, M., Sodek, L., Licausi, F., Hameed, M.W., Dornelas, M.C. ve van Dongen, J.T., 2010. Analysis of alanine aminotransferase in various organs of soybean (Glycine max) and in dependence of different nitrogen fertilisers during hypoxic stress. Amino Acids, 39, 1043–1053.
• Shi, H., Ye, T. ve Chan, Z., 2014. Comparative proteomic responses of two bermudagrass (Cynodon dactylon (L). Pers.) varieties contrasting in drought stress resistance. Plant Physiology and Biochemistry, 82, 218–228.
• Sobhanian, H., Razavizadeh, R., Nanjo, Y., Ehsanpour, A. A., RastgarJazii, F. ve Motamed, N., 2010. Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Science, 8, 1–15.
• Song, H., Zhao, R., Fan, P., Wang, X., Chen, X. ve Li, Y., 2009. Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta, 229, 955–964.
• Sun, G., Xie, F. ve Zhang, B., 2011. Transcriptome-wide identification and stress properties of the 14-3-3 gene family in cotton (Gossypium hirsutum L.). Functional and Integrative Genomics, 11, 627–636.
• Takahashi, Y., Kinoshita, T. ve Shimazaki, K., 2007. Protein phosphorylation and binding of a 14-3-3 protein in Vicia guard cells in response to ABA. Plant and Cell Physiology, 48, 1182–1191.
• Tripathi, B.N., Bhatt, I. ve Dietz, K.J., 2009. Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma, 235, 3–15.
• Urban, M.O., Vašek, J., Klíma, M., Krtková, J., Kosová, K., Prášil, I.T. ve Vítámvás, P., 2017. Proteomic and physiological approach reveals drought-induced changes in rapeseeds: Water-saver and water-spender strategy. Journal of Proteomics, 152, 188–205.
• Vítámvás, P., Prášil, I. T., Kosová, K., Planchon, S. ve Renaut, J., 2012. Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics, 12, 68–85.
• Vitamvas, P., Urban, M.O., Skodacek, Z., Kosova, K., Pitelkova, I., Vitamvas, J., Renaut, J. ve Prasil, I.T., 2015. Quantitative analysis of proteome extracted from barley crowns grown under different drought conditions. Frontiers in Plant Science, 6, 479.
• Wang, W., Vinocur, B., Shoseyov, O. ve Altman, A., 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science, 9, 244–252.
• Wang, X., Cai, X., Xu, C., Wang, Q. ve Dai, S., 2016. Drought-responsive mechanisms in plant leaves revealed by proteomics. International Journal of Molecular Sciences, 17, 1706.
• Wang, Y., Fan, K., Wang, J., Ding, Z. tang, Wang, H., Bi, C. ve Sun, H., 2017. Proteomic analysis of Camellia sinensis (L.) reveals a synergistic network in the response to drought stress and recovery. Journal of Plant Physiology, 219, 91–99.
• Wei, W., Huang, J., Hao, Y.-J., Zou, H.-F., Wang, H.-W. ve Zhao, J.-Y., 2009. Soybean GmPHD-type transcription regulators improve stress tolerance in transgenic Arabidopsis plants. PLoS ONE, 4, e7209.
• Xin, L., Zheng, H., Yang, Z., Guo, J., Liu, T., Sun, L. ve Guo, L., 2018. Physiological and proteomic analysis of maize seedling response to water deficiency stress. Journal of Plant Physiology, 228, 29–38.
• Xu, Y.-H., Liu, R., Yan, L., Liu, Z.-Q., Jiang, S.-C., Shen, Y.-Y., Wang, X.-F. ve Zhang, D.-P., 2012. Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. Journal of Experimental Botany, 63, 1095–1106.
• Xu, J., Xing, X.J., Tian, Y.S., Peng, R.H., Xue, Y., Zhao, W. ve Yao, Q.H., 2015. Transgenic Arabidopsis plants expressing tomato glutathione S-transferase showed enhanced resistance to salt and drought stress. PLoS ONE, 10(9), e0136960.
• Yan, J., He, C., Wang, J., Mao, Z., Holaday, S.A. ve Allen, R.D., 2004. Overexpression of the Arabidopsis 14-3-3 protein GF14 lambda in cotton leads to a “stay-green” phenotype and improves stress tolerance under moderate drought conditions. Plant and Cell Physiology, 45, 1007–1014.
• Yan, S.P., Zhang, Q.Y., Tang, Z.C., Su, W.A. ve Sun, W.N., 2006. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Molecular and Cellular Proteomics, 5, 484–496.
• Zadražnika, T., Hollung, K., Egge-Jacobsen, W., Meglič, V. ve Šuštar-Vozlič, J., 2013. Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). Journal of Proteomics, 78, 254–272.
• Zhang, J., Tan, W., Yang, X.-H. ve Zhang, H.-X., 2008. Plastid-expressed choline monooxygenase gene improves salt and drought tolerance through accumulation of glycine betaine in tobacco. Plant Cell Reports, 27, 1113.
• Zhang, S., Li, C. ve Cao, J., 2009. Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by TLD1/ OsGH3.13 activation. Plant Physiology, 151(4), 1889–1901.
• Zhang, H., Zhang, L., Lv, H. ve Yu, Z., 2014. Identification of changes in Triticum aestivum L. leaf proteome in response to drought stress by 2D-PAGE and MALDI-TOF/TOF mass spectrometry. Acta Physiologiae Plantarum, 36, 1385–1398.
• Zhang, H., Ni, Z., Chen, Q., Guo, Z., Gao, W., Su, X. ve Qu, Y., 2016. Proteomic responses of drought-tolerant and drought-sensitive cotton varieties to drought stress. Molecular Genetics and Genomics, 291(3), 1293–1303.
• Zhou, Y., Cai, H., Xiao, J., Li, X., Zhang, Q. ve Lian, X., 2009. Over-expression of aspartate aminotransferase genes in rice resulted in altered nitrogen metabolism and increased amino acid content in seeds. Theoretical and Applied Genetics, 118, 1381–1390.