Abstract
Phenylalanine ammonia-lyase (PAL) is one of the principle enzymes involved in plant’s secondary metabolism. Expression of individual isogene from the PAL gene family is variable with species of plants in responses to different stresses. In this study, transcriptome analysis of the PAL gene family in rice seedlings exposed to potassium chromate Cr(VI) or chromium nitrate Cr(III) was conducted using Agilent 44K rice microarray and real-time quantitative RT-PCR. Uptake and accumulation of both Cr species by rice seedlings and their effect on PAL activity were also determined. Three days of Cr exposure led to significant accumulation of Cr in plant tissues, but majority being in roots rather than shoots. Changes of PAL activities in rice tissues were evident from both Cr treatments. Individual isogene from the rice PAL gene family was expressed differentially in response to both Cr variants. Comparing gene expression between two Cr treatments, only osPAL2 and osPAL4 genes were expressed in similar patterns. Also, gene expression pattern was inconsistent in both plant tissues. Results indicated that expression of individual isoform from the rice PAL gene family is tissue, and stimulus specific under different Cr exposure, suggesting their different detoxification strategies for decreasing or eliminating Cr stresses.
Similar content being viewed by others
References
Achnine L, Blancaflor EB, Rasmussen S, Dixon RA (2004) Colocalization of L-phenylalanine ammonina-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16:3098–3109
Anterola AM, Lewis NG (2002) Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61:221–294
Appert C, Logemann E, Hahlbrock K, Schmid J, Amrhein N (1994) Structural and catalytic proteries of the fore phenylalanine ammonia-lyase isoenzymes form parsley (Petroselinum cripum Nym.). Eur J Biochem 225:491–499
Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162
Chen YA, Chi WC, Trinh NN, Huang LY, Chen YC, Cheng TL, Lin CY, Huang HJ (2014) Transcriptome profiling and physiological studies reveal a major role for aromatic amino acids in mercury stress tolerance in rice seedlings PLoS ONE 9:e95163
Cochrane FC, Davin LB, Lewis NG (2004) The Arabidopsis phenylalanine ammonia-lyase gene family: kinetic characterization of the four PAL isoforms. Phytochemistry 65:1557–1564
Ebbs SD, Piccinin RC, Goodger JQD, Kolev SD, Woodrow IE, Baker AJM (2008) Transport of ferrocyanide by two eucalypt species and sorghum. Int J Phytorem 10:343–357
Fang CX, Wang QS, Luo MR, Huang LK, Xiong J, Shen LH, Lin WX (2011) Differential expression of PAL multigene family in allelopathic rice and it counterpart exposed to stressful condition. Acta Ecol Sin 31:4760–4767. (in Chinese)
Gao S, Ouyang C, Wang S, Xu Y, Tang L, Chen F (2008a) Effects of salt stress on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. Seedlings. Plant Soil Environ 54:374–381
Gao S, Yan R, Cao M, Yang W, Wang S, Chen F (2008b) Effects of copper on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. Seedlings. Plant Soil Environ 54:117–121
Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–1538
Hussain S, Yin H, Peng S, Khan FA, Khan F, Sameeullah M, Hussain HA, Huang J, Cui K, Nie L (2016) Comparative transcriptional profiling of primed and non-primed rice seedlings under submergence stress. Front Plant Sci 7:1125
Hsieh LS, Hsieh YL, Yeh CH, Cheng CY, Yang CC, Lee PD (2011) Molecular characterization of a phenylalanine ammonia-lyase gene (BOPAL1) from Bambusa oldhamii. Mol Biol Rep 130:796–807
Jiang LL, Li RW, Mao YQ, Zhou M (2013) Present processing technology and comprehensive utilization of chromium slag. Environ Sci Technol 36:480–483. (in Chinese)
Kale RA, Lokhande VH, Ade AB (2015) Investigation of chromium phytoremediation and tolerance capacity of a weed, Portulaca oleracea L. in a hydroponic system. Water Environ J 29:236–242
Kao YL, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalaninie ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 38:283–290
Kumar A, Ellis B (2001) The phenylalanine ammonia-lyase gene family in raspberry; structure, expression, and evolution. Plant Physiol 127:230–239
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Lea U, Slimestad R, Smedvig P, Lillo C (2007) Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway. Planta 225:1245–1253
Liang X, Dron M, Cramer CL, Dixon RA, Lamb CJ (1989) Differential regulation of phenylalanine ammonia-lyase genes during plant development and by environmental cues. J Biol Chem 264:14486–14492
Lillo C, Lea US, Ruoff P (2008) Nutrient depletion as a key factor for manipulating gene expression and product formation in different branches of the flavonoid pathway. Plant Cell Environ 31:587–601
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Neumann G, Schwemmle B (1993) Flavonoids from Oenothera-seedlings: identification and extranuclear control of their biosynthesis. J Plant Physiol 142:135–143
Ohl S, Hedrick SA, Chory J, Lamb CJ (1990) Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Plant Cell 2:837–848
Olsen KM, Lea US, Slimestad RS, Verheul M, Lillo C (2008) Differential expression of four Arabidopsis PAL genes; PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis. J Plant Physiol 165:1491–1499
Raes J, Rohde A, Holst CJ, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071
Ren JH, Ma LQ, Sun HJ, Cai F, Luo J (2014) Antimony uptake, translocation and speciation in rice plants exposed to antimonite and antimonate. Sci Total Environ 475:83–89
Rosler J, Krekel F, Amrhein N, Schmid J (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity. Plant Physiol 113:175–179
Sarma AD, Sarma R (1999) Purification and characterization of UV-B induced phenylalanine ammonia-lyase from rice seedlings. Phytochemistry 50:729–737
Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udverdi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499
Shufflebottom D, Edwards K, Schich W, Bevan M (1993) Transcription of two members of a gene encoding phenylalanine ammonia-lyase leads to remarkably different cell specificities and induction patterns. Plant J 3:835–845
Wang JY, Su HJ, Tan TW (2007) Study on reuse and treatment of tannery chromium effluents. Chin J Environ Eng 1:23–27. (in Chinese)
Wanner LA, Li G, Ware D, Somssich IE, Davis KR (1995) The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol Biol 27:327–338
Xiong J, Wang HB, Fang CX, Qiu L, Wu WX, He HB, Lin WX (2007) The differential expression of the genes of the key enzymes involved in phenolic compound metabolism in rice (Oryza sativa L.) under different nitrogen supply. J Plant Physiol Mol Biol 33:387–394. (in Chinese)
Yu XZ, Zhang XH (2016) Determination of the Michaelis-Menten kinetics and the genes expression involved in phyto-degradation of cyanide and ferri-cyanide. Ecotoxicology 25:888–899
Yu XZ, Feng YX, Liang YP (2016) Kinetics of phyto-accumulation of hexavalent and trivalent chromium in rice seedlings. Int Biodeter Biodegra. https://doi.org/10.1016/j.ibiod.2016.09.003
Yu XZ, Zhang FF, Liu W (2017a) Chromium-induced depression of 15N content and nitrate reductase activity in rice seedlings. Int J Environ Sci Technol 14:29–36
Yu XZ, Lin YJ, Fan WJ, Lu MR (2017b) The role of exogenous proline in amelioration of lipid peroxidation in rice seedlings exposed to Cr(VI). Int Biodeter Biodegra 123:106–112
Yu XZ, Lin YJ, Lu CJ, Zhang XH (2017c) Identification and expression analysis of CYS-A1, CYS-C1, NIT4 genes in rice seedlings exposed to cyanide. Ecotoxicology 26:956–965
Zar JH (1999) Biostatistical analysis. 4th edn, Prentice Hall, New Jersey, pp 231–261
Zayed AM, Terry N (2003) Chromium in the environment: factors affecting biological remediation. Plant Soil 249:139–156
Zeng F, Zhou W, Qiu B, Ali S, Wu F, Zhang G (2011) Subcellular distribution and chemical forms of chromium in rice plants suffering from different levels of chromium toxicity. J Plant Nutr Soil Sci 174:249–256
Zhang FF (2017) Response of phenolic compounds to Cr stress during secondary metabolism of rice seedlings. Master Thesis at Guilin University of Technology, Guilin
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632
Acknowledgements
This work was financially supported by the National Natural Science Foundation of China (No. 41761094) and The Guangxi Talent Highland for Hazardous Waste Disposal Industrialization.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
X-Z Yu has received the grants from the National Natural Science Foundation of China. The remaining authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Yu, XZ., Fan, WJ., Lin, YJ. et al. Differential expression of the PAL gene family in rice seedlings exposed to chromium by microarray analysis. Ecotoxicology 27, 325–335 (2018). https://doi.org/10.1007/s10646-018-1897-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-018-1897-5