biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 60:459-468, 2016 | DOI: 10.1007/s10535-016-0619-1

Molecular cloning and expression of four phenylalanine ammonia lyase genes from banana interacting with Fusarium oxysporum

Z. Wang1, J.-Y. Li2, C.-H. Jia1, J.-P. Li1, B.-Y. Xu1,*, Z.-Q. Jin1,2
1 Key Laboratory of Tropical Crop Biotechnology, Ministry of Agriculture, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Hainan, P.R. China
2 Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Hainan, P.R. China

Phenylalanine ammonia lyase (PAL) is the first enzyme in the phenylpropanoid pathway. In this study, we describe the molecular characteristics of four PAL genes (MaPAL1, MaPAL2, MaPAL3, and MaPAL4) cloned from banana (Musa acuminata L. AAA group, cv. Cavendish) using a rapid amplification of cDNA ends and real time quantitative PCR. The predicted molecular masses of corresponding PALs ranged from 70.2 to 77.3 kDa and their isoelectric points were acidic. At the amino acid level, they shared a high sequence similarity with PALs in the banana DH-Pahang (AA group) genome. Phylogenetic analysis shows that the deduced amino acid sequences of MaPALs had also a high similarity with PALs of other plant species. Expression analysis by semi-quantitative reverse transcriptase PCR reveals that these genes were differentially expressed in various tissues. Enzyme activity of PAL and expression of MaPALs in bananas were induced after infection with Fusarium oxysporum f. sp cubense Tropical Race 4. Our findings suggest that MaPALs play important roles in banana resistance to F. oxysporum.

Keywords: disease resistance; gene expression; Musa acuminata; real time qPCR
Subjects: gene expression; phenylalanineammonia lyase; amino acid sequence; phylogenetic tree; fungal infection; banana

Received: January 21, 2015; Revised: October 21, 2015; Accepted: November 3, 2015; Published: September 1, 2016  Show citation

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Wang, Z., Li, J.-Y., Jia, C.-H., Li, J.-P., Xu, B.-Y., & Jin, Z.-Q. (2016). Molecular cloning and expression of four phenylalanine ammonia lyase genes from banana interacting with Fusarium oxysporum. Biologia plantarum60(3), 459-468. doi: 10.1007/s10535-016-0619-1
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References

  1. Alvarez, J.C., Rodriguez, H.A., Rodriguez-Arango, E., Monsalve, Z.I., Morales, O.J.G., Arango, I.R.E.: Characterization of a differentially expressed phenylalanine ammonia-lyase gene from banana induced during Mycosphaerella fijiensis infection. - J. Plant Studies 2: p35, 2013. Go to original source...
  2. Arnon, D.I., Hoagland D.R.: A comparison of water culture and soil as media for crop production. - Science 89: 512-514, 1939. Go to original source...
  3. Aurore, G., Parfait, B., Fahrasmane, L.: Bananas, raw materials for making processed food products. - Trends Food Sci. Technol. 20: 78-91, 2009. Go to original source...
  4. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. - Anal. Biochem. 72: 248-254, 1976. Go to original source...
  5. Chaman, M.E., Copaja, S.V., Argandona, V. H.: Relationships between salicylic acid content, phenylalanine ammonialyase (PAL) activity, and resistance of barley to aphid infestation. - J. Agr. Food Chem. 51: 2227-2231, 2003. Go to original source...
  6. Chang, A., Lim, M.H., Lee, S.W., Robb, E.J., Naza,r R.N.: Tomato phenylalanine ammonia-lyase gene family, highly redundant but strongly underutilized. - J. biol. Chem. 283: 33591-33601, 2008. Go to original source...
  7. Chen, J., He, L., Jiang, Y., Wang, Y., Joyce, D., Ji, Z., Lu, W.: Role of phenylalanine ammonia-lyase in heat pretreatmentinduced chilling tolerance in banana fruit. - Physiol. Plant. 132: 318-328, 2008. Go to original source...
  8. Cochrane, F.C., Davin, L.B., Lewis, N.G.: The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms. - Phytochemistry 65: 1557-1564, 2004. Go to original source...
  9. Cramer, C.L., Edwards, K., Dron, M., Liang, X., Dildine, S.L., Bolwell, G.P., Dixon, R.A., Lamb, C.J., Schuch, W.: Phenylalanine ammonia-lyase gene organization and structure. - Plant mol. Biol. 12: 367-383, 1989. Go to original source...
  10. Dixon, R.A., Paiva, N.L.: Stress-induced phenylpropanoid metabolism. - Plant Cell 7: 1085, 1995. Go to original source...
  11. Damodaran, T., Kumar, N., Kavino, M.: Breeding and evaluation of Musa hybrids resistant to Fusarium oxysporum f. sp. cubense race 1. - Fruits 64: 3-12, 2009. Go to original source...
  12. D'Hont, A., Denoeud, F., Aury, J.M., Baurens, F.C., Carreel, F., Garsmeur, O., Noel, B., Bocs, S., Droc, G., Rouard, M., Da Silva, C., Jabbari, K., Cardi, C., Poulain, J., Souquet, M., Labadie, K., Jourda, C., Lengellé, J., Rodier-Goud, M., Alberti, A., Bernard, M., Correa, M., Ayyampalayam, S., Mckain, M.R., Leebens-Mack, J., Burgess, D., Freeling, M., Mbeguie-A-Mbeguie, D., Chabannes, M., Wicker, T., Panaud, O., Barbosa, J., Hribova, E., Heslop-Harrison, P., Habas, R., Rivallan, R., Francois, P.: The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. - Nature 448: 213-217, 2012. Go to original source...
  13. Edwards, R., Kessmann, H.: Isoflavonoid phytoalexins and their biosynthetic enzymes. - In: Gurr, S.J., McPherson, M.J., Bowles, D.J. (ed.): Molecular Plant Pathology: a Practical Approach. Pp 45-62. Oxford University Press, Oxford 1992.
  14. El Modafar, C., El Boustani, E., Rahioui, B., El Meziane, A., El Alaoui-Talibi, Z.: Suppression of phenylalanine ammonialyase activity elicited in date palm by Fusarium oxysporum f. sp. albedinis hyphal wall elicitor. - Biol. Plant. 50: 697-700, 2006. Go to original source...
  15. Fishal, E.M.M, Meon, S., Yun, W.M.: Induction of tolerance to Fusarium wilt and defense-related mechanisms in the cultivar of susceptible berangan banana pre-inoculated with Pseudomonas sp. (UPMP3) and Burkholderia sp. (UPMB3). - Agr. Sci. China 9: 1140-1149, 2010. Go to original source...
  16. Gao, J., Zhang, S., Cai, F., Zheng, X., Lin, N., Qin, X., Ou, Y., Gu, X., Zhu, X., Xu, Y., Chen, F.: Characterization, and expression profile of a phenylalanine ammonia lyase gene from Jatropha curcas L. - Mol. Biol. Rep. 39: 3443-3452, 2012. Go to original source...
  17. Gunavathi, J., Kumar, N., Soorianathasundaram, K., Samiappan, R.: Reaction of synthetic diploids to Fusarium oxysporum f. sp. cubense (Race-1) and to a Fusarium-nematode complex. - In: Proceedings of the 2nd International Symposium on Fusarium Wilt on Banana. P. 22. Saverdor de Bahia 2003.
  18. Hahlbrock, K., Scheel, D.: Physiology and molecular biology of phenylpropanoid metabolism. - Annu. Rev. Plant Biol. 40: 347-369, 1989. Go to original source...
  19. Hou, X., Shao, F., Ma, Y., Lu, S.: The phenylalanine ammonialyase gene family in Salvia miltiorrhiza: genome-wide characterization, molecular cloning and expression analysis. - Mol. Biol. Rep. 40: 4301-4310, 2013. Go to original source...
  20. Hsieh, L.S., Hsieh, Y.L., Yeh, C.S., Cheng, C., Yang, C., Lee, P.: Molecular characterization of a phenylalanine ammonialyase gene (BoPAL1) from Bambusa oldhamii. - Mol. Biol. Rep. 38: 283-290, 2011. Go to original source...
  21. Hu, G.S., Jia, J.M., Hur, Y.J., Chung, Y., Lee, J., Yun, D., Chung, W., Yi, G., Kim, T., Kim, D.: Molecular characterization of phenylalanine ammonia lyase gene from Cistanche deserticola. - Mol. Biol. Rep. 38: 3741-3750, 2011. Go to original source...
  22. Huang, J., Gu, M., Lai, Z., Fan, B., Shi, K., Zhou, Y.H., Yu, J.Q., Chen, Z.: Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. - Plant Physiol. 153: 1526-1538, 2010. Go to original source...
  23. Hwang, S.C., Ko, W.H.: Cavendish banana cultivars resistant to Fusarium wilt acquired through somaclonal variation in Taiwan. - Plant Dis. 88: 580-588, 2004. Go to original source...
  24. Jiang, Y., Xia, N., Li, X., Shen, W., Liang, L., Wang, C., Wang, R., Peng, F., Xia, B.: Molecular cloning and characterization of a phenylalanine ammonia-lyase gene (LrPAL) from Lycoris radiata. - Mol. Biol. Rep. 38: 1935-1940, 2011. Go to original source...
  25. Jiang, Y., Xia, B., Liang, L., Li, X., Xu, S., Peng, F., Wang, R.: Molecular and analysis of a phenylalanine ammonia-lyase gene (LrPAL2) from Lycoris radiata. - Mol. Biol. Rep. 40: 2293-2300, 2013. Go to original source...
  26. Jorrin, J., Dixon, R.A.: Stress responses in alfalfa (Medicago sativa L.) II. Purification, characterization, and induction of phenylalanine ammonia-lyase isoforms from elicitor-treated cell suspension cultures. - Plant Physiol. 92: 447-455, 1990. Go to original source...
  27. Koenig, R.L., Ploetz, R.C., Kistler, H.C.: Fusarium oxysporum f. sp. cubense consists of a small number of divergent and globally distributed clonal lineages. - Phytopathology 87: 915-923, 1997. Go to original source...
  28. Kumar, A., Ellis, B.E.: The Phenylalanine ammonia-lyase gene family in raspberry: structure, expression, and evolution. - Plant Physiol. 127: 230-239, 2001. Go to original source...
  29. Leyva, A., Jarillo, J.A., Salinas, J., Martinez-Zapater, J.M.: Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. - Plant Physiol. 108: 39-46, 1995. Go to original source...
  30. Li, C., Deng, G., Yang, J., Viljoen, A., Jin, Y., Kuang, R., Zuo, C., Lv, Z., Yang, Q., Sheng, O., Wei, Y., Hu, C., Dong, T., Yi, G.: Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. - BMC Genomics 13: 374, 2012a. Go to original source...
  31. Li, M., Xu, B., Liu, J., Yang, X., Zhang, J., Jia, C., Ren, L., Jin, Z.: Identification and expression analysis of four 14-3-3 genes during fruit ripening in banana (Musa acuminata L. AAA group, cv. Brazilian). - Plant Cell Rep. 31: 369-378, 2012b. Go to original source...
  32. MacDonald, M.J., D'Cunha, G.B.: A modern view of phenylalanine ammonia lyase. - Biochem. Cell Biol. 85: 273-282, 2007. Go to original source...
  33. Mandal, S., Mallick, N., Mitra, A.: Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. - Plant Physiol. Biochem. 47: 642-649, 2009. Go to original source...
  34. Mauch-Mani, B., Slusarenko, A.J.: Production of salicylic acid precursors is a major function of phenylalanine ammonialyase in the resistance of Arabidopsis to Peronospora parasitica. - Plant Cell 8: 203-212, 1996. Go to original source...
  35. Morkunas, I., Bednarski, W., Kopyra, M.: Defense strategies of pea embryo axes with different levels of sucrose to Fusarium oxysporum and Ascochyta pisi. - Physiol. mol. Plant Pathology 72: 167-178, 2008. Go to original source...
  36. Morkunas, I., Gmerek, J.: The possible involvement of peroxidase in defense of yellow lupine embryo axes against Fusarium oxysporum. - J. Plant Physiol. 164: 185-194, 2007. Go to original source...
  37. Morkunas, I., Marczak, L., Stachowiak, J., Stobiecki, M.: Sucrose-induced lupine defense against Fusarium oxysporum: Sucrose-stimulated accumulation of isoflavonoids as a defense response of lupine to Fusarium oxysporum. - Plant Physiol. Biochem. 43: 363-373, 2005. Go to original source...
  38. Nugroho, L.H., Verberne, M.C., Verpoorte, R.: Activities of enzymes involved in the phenylpropanoid pathway in constitutively salicylic acid-producing tobacco plants. - Plant Physiol. Biochem. 40: 755-760, 2002. Go to original source...
  39. Ohl, S., Hedrick, S.A., Chory, J., Lamb, C.J.: Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. - Plant Cell 2: 837-848, 1990. Go to original source...
  40. Reichert A.I., He X.Z., Dixon R.A.: Phenylalanine ammonialyase (PAL) from tobacco (Nicotiana tabacum): characterization of the four tobacco PAL genes and active heterotetrameric enzymes. - Biochem. J. 424: 233-242, 2009. Go to original source...
  41. Robinson, J.C.: Bananas and Plantains. - CAB International, Oxford 1996.
  42. Schomburg, D., Salzmann, M.: Class 4: lyases, phenylalanine ammonia-lyase. - In: Schomburg, D., Salzmann, M. (ed.): Enzyme Handbook. Pp. 1-5. Springer-Verlag, Berlin 1990. Go to original source...
  43. Shadle, G.L., Wesley, S.V., Korth, K.L., Chen, F., Lamb, C., Dixon, R.A.: Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. - Phytochemistry 64: 153-161, 2003. Go to original source...
  44. Shang, Q.M., Li, L., Dong, C.J.: Multiple tandem duplication of the phenylalanine ammonia-lyase genes in Cucumis sativus L. - Planta 236: 1093-1105, 2012. Go to original source...
  45. Shi, R., Sun, Y.H., Li, Q., Heber, S., Sederoff, R., Chiang, V.L.: Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. - Plant Cell Physiol. 51: 144-163, 2010. Go to original source...
  46. Stover, R.H.: Fusarial Wilt (Panama Disease) of Bananas and Other Musa Species. - Commonwealth Mycological Institute, Kew - Surrey 1962.
  47. Tamura, K., Dudley, J., Nei, M., Kumar, S.: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. - Mol. Biol. Evol. 24: 1596e9, 2007. Go to original source...
  48. Thangavelu, R., Palaniswani, A., Doraiswamy, S., Velazhahan, R.: The effect of Pseudomonas fluorescens and Fusarium oxysporum f. sp. cubense on induction of defense enzymes and phenolics in banana. - Biol. Plant. 46: 107-112, 2003. Go to original source...
  49. Visser, M., Gordon, T., Fourie, G., Viljoen, A.: Characterisation of South African isolates of Fusarium oxysporum f. sp. cubense from Cavendish bananas. - South Afr. J. Sci. 106: 1-6, 2010. Go to original source...
  50. Wan, C.Y., Wilkins, T.A.: A modified hot borate method significantly enhance the yield of high-quality RNA from cotton (Gossypium hirsutum L.). - Anal. Biochem. 223: 7-12, 1994. Go to original source...
  51. Wang, X., Gong, M., Tang, L., Zheng, S., Lou, J., Ou, L., Gomes-Laranjo, J., Zhang, C.: Cloning, bioinformatics and the enzyme activity analyses of a phenylalanine ammonialyase gene involved in dragon's blood biosynthesis in Dracaena cambodiana. - Mol. Biol. Rep. 40: 97-107, 2013. Go to original source...
  52. Wang, Z., Zhang, J., Jia, C., Liu, J., Li, Y., Yin, X., Xu, B., Jin, Z.: De Novo characterization of the banana root transcriptome and analysis of gene expression under Fusarium oxysporum f. sp. cubense tropical race 4 infection. - BMC Genomics 13: 1-9, 2012. Go to original source...
  53. Ye, S., Zhou, Y., Sun, Y., Zou, L., Yu, J.: Cinnamic acid causes oxidative stress in cucumber roots, and promotes incidence of Fusarium wilt. - Environ.exp. Bot. 56: 255-262, 2006. Go to original source...
  54. Yin, X., Xu, B., Zheng, W., Wang, Z., Wang, B., Ha, W., Mao, H., Li, J., Sheng, Z., He, Y., Han, L., Chen, S., Zhang, J., Fu, Y., Wang, J., Jin, Z.: Characterization of early events in banana roots infected with green fluorescent protein-tagged Fusarium oxysporum f. sp. cubense. - Acta Hort. 897: 371-376, 2011. Go to original source...