Expression of gene involved in the response to abiotic factors in Capsicum annuum
DOI:
https://doi.org/10.21640/ns.v12i25.2283Keywords:
Capsicum annuum, WRKY transcription factors, gibberellins, FT proteins, LEA proteins, abiotic stress, phytohormones, cold stress, hydric stress, agricultural crops, chili, cellular processes, biochemistry of plants, gene expressionAbstract
Introduction: Abiotic stress caused by cold or water-deficit alters many cellular processes that modificate the physiology and biochemistry of plants, which reduces yield of agricultural crops. Gibberellins are phytohormones that can induce growth and development of the plants. There are many genes whose transcription is modified during abiotic stress or by exogenous-gibberellins application; some of them encode for proteins such as LEA that confer protection against low temperature and dehydration, WRKY and FT that take part in the response to abiotic stress, FT that regulates the flowering time, and GA20ox1 that synthesized gibberellins. The understanding of molecular mechanism that regulates the plant responses to abiotic stress or exogenous gibberellins application is essential for Capsicum annuum (pepper) agriculture improvement. To this aim, we have proceeded to study the effect of biotic stress and exogenous phytohormones on C. annuum development, mainly in fruit (chili) production and expression of genes involved in the response to these conditions.
Method: The genome of Capsicum annuum contains homologues to the proteins LEA, WRKY, FT and GA20oxy, so we estimate by Real-Time PCR (qPCR) and phenotype analysis, the gene expression and fruits production in plants grown under abiotic stress and after treatment with exogenous gibberellins.
Results: The transcripts of CaLea73 and CaWRKY40 increased by cold stress in leaves. While, CaGA20ox1 expression was down-regulated by cold stress, GA3, and hydric stress-GA3 in leaves. This effect was also observed in flower buds of plants grown under water-deficit, treated with gibberellins or hydric stress-GA3; curiously, the transcripts from this gene became slightly abundant in plants grown under water-deficit. CaFT transcription was induced by cold stress and GA3 in leaves and flower buds, respectively; however, transcription of this gene was almost abolished by hydric stress and GA3–hydric stress in both tissues. Cold stress and exogenous phytohormones raised the fruits production.
Conclusion: According with these results, we propose that cold treatment induces the plant defense mechanisms through activation of transcription factors like WRKYs and LEA proteins and increases the plant development through induction of signaling pathway of FT. Our study contributes to understanding on molecular mechanisms governing the responses to abiotic stress and the participation of the gibberellins in C. annuum development and to improve the yield of the chili crop.
Downloads
References
Acosta-García, G., Chapa-Oliver, A.M., Millán-Almaraz, J.R., Guevara-González, R.G., Cortez-Baheza, E., Rangel-Cano, R.M., Ramírez-Pimentel, J.G., Cruz-Hernández, A., Guevara-Olvera, L., Aguilera-Bibian, J.E., Hernández-Salazar, M. & Torres-Pacheco, I. (2014). CaLEA 73 gene from Capsicum annuum L. enhances drought and osmotic tolerance modulating transpiration rate in transgenic Arabidopsis thaliana. Canadian Journal of Plant Science, 95(2), 227-235. DOI: https://doi.org/10.1139/CJPS-2014-281
Banerjee, A. & Roychoudhury, A. (2015). WRKY proteins: signaling and regulation of expression during abiotic stress responses. The Scientific World Journal, 2015, 807560. DOI: https://doi.org/10.1155/2015/807560
Beck, E.H., Fettig, S., Knake, C., Hatrtig K. & Bhattrai, T. (2007). Specific and unspecific responses of plants to cold and drought stress. Journal of Biosciences, 32(3), 501-510. DOI: 10.1007/s12038-007-0049-5
Binenbaum, J., Weinstain, R. & Shani, E. (2018). Gibberellin localization and transport in plants. Trends in Plant Science, 23(5), 410-421. DOI: https://doi.org/10.1016/j.tplants.2018.02.005
Bonhomme, L., Valot, B., Tardieu, F. & Zivy, M. (2012). Phosphoproteome dynamics upon changes in plant water status reveal early events associated with rapid growth adjustment in maize leaves. Molecular and Cellular Proteomics, 11(10), 957-972. DOI: https://doi.org/10.1074/mcp.M111.015867
Bravo, L.A, Gallardo, J., Navarrete, A., Olave, N., Martínez, J., Alberdi, M., Close, T.J. & Corcuera, L.J. (2003). Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiologia Plantarum, 118(2), 262-269. DOI: https://doi.org/10.1034/j.1399-3054.2003.00060.x
Cai, H., Yang, S., Yan, Y., Xiao, Z., Cheng, J., Wu, J., Qiu, A., Lai, Y., Mou, S., Guan, D., Huang, R. & He, S. (2015). CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper. Journal of Experimental Botany, 66(11), 3163-3174. DOI: https://doi.org/10.1093/jxb/erv125
Cai, M., Qiu, D., Yuan, T., Ding, X., Li, H., Duan, L., Xu, C., Li, X. & Wang, S. (2008). Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant, Cell & Environment 31(1), 86-96. DOI: https://doi.org/10.1111/j.1365-3040.2007.01739.x
Chen, L., Song, Y., Li, S., Zhang, L., Zou, C. & Yu, D. (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta (BBA) – Gene Regulatory Mechanisms, 1819(2), 120-128. DOI: https://doi.org/10.1016/j.bbagrm.2011.09.002
Chomczynski, P. & Mackey, K. (1995). Modification of the TRIZOL reagent procedure for isolation of RNA from Polysaccharide-and proteoglycan-rich source. Biotechniques, 19(6), 942-950.
Corbesier, L., Vincent, C., Jang, S., Fornara, F., Fan, Q., Searle, I., Giakountis, A., Farrona, S., Gissot, L., Turnbull, C. & Coupland, G. (2007). FT Protein Movement Contributes to Long-Distance Signaling in Floral Induction of Arabidopsis. Science, 316(5821), 1030-1033. DOI: 10.1126/science.1141752
Cortez-Baheza, E., Cruz-Fernández, F., Hernández-Álvarez, M.I., Peraza-Luna, F., Aguado-Santacruz, G.A., Serratos-Arévalo, J.C., Posos-Ponce, P., González-Chavira, M.M., Torres-Pacheco, I., Guevara-Olvera, L. & Guevara-González, R.G. (2008). A new Lea gene induced during osmopriming of Capsicum annuum L. seeds. International Journal of Botany, 4(1), 77-84.
Cortez-Baheza, E., Peraza-Luna, F., Hernández-Álvarez, M.I., Aguado-Santacruz, G.A., Torres-Pacheco, I., González-Chavira, M.M., Guevara-Olvera, L. & Guevara-González, R.G. (2007). Profiling the transcriptome in Capsicum annuum L. seeds during osmopriming. American Journal of Plant Physiology, 2(2): 77-84. DOI: 10.3923/ajpp.2007.99.106
Dang, F.F., Wang, Y.N., Yu, L., Eulgem, T., Lai, Y., Liu, Z.Q., Wang, X., Qiu, A.L., Zhang, T.X., Lin, J., Chen, Y.S., Guan, D.Y., Cai, H.Y., Mou, S.L. & He, S.L. (2013). CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant, Cell & Environment, 36(4), 757-774. DOI: https://doi.org/10.1111/pce.12011
Danilevskaya, O.N., Meng, X., Hou, Z., Ananiev, E. V. & Simmons, C.R. (2008). A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiology, 146(1), 250-264. DOI: DOI: 10.1104/pp.107.109538
de Jong, M., Wolters-Arts, M., Feron, R., Mariani, C. & Vriezen, W.H. (2009). The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. The Plant Journal, 57(1) 160-170. DOI: https://doi.org/10.1111/j.1365-313X.2008.03671.x
FAOSTAT. (2018). World food and agriculture statistical book. Food and Agriculture Organization of the United Nations. Rome, Italy.
Gupta, D.B., Rai, Y., Gayali, S., Chakraborty, S. & Chakraborty, N. (2016). Plant organellar proteomics in response to dehydration: Turning Protein Repertoire into Insights. Frontiers in Plant Science, 7, 460. DOI: https://doi.org/10.3389/fpls.2016.00460
Hong-Bo, S., Zong-Suo, L. & Ming-An, S. (2005) LEA proteins in higher plants: structure, function, gene expression and regulation. Colloids and Surfaces B: Biointerfaces, 45(3-4),131-135. DOI: https://doi.org/10.1016/j.colsurfb.2005.07.017
Hsu, C.Y., Adams, J.P., Kim, H., No, K., Ma, C., Strauss, S.H., Drnevich, J., Vandervelde, L., Ellis, J.D., Rice, B.M., Wickett, N., Gunter, L. E., Tuskan, G. A., Brunner, A. M., Page, G. P., Barakat, A., Carlson, J. E., DePamphilis, C. W., Luthe, D. S & Yuceer, C. (2011). FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proceedings of the National Academy of Sciences of the United States of America, 108(26), 10756-10761. DOI: https://doi.org/10.1073/pnas.1104713108
Hundertmark, M. & Hincha, D. K. (2008). LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics, 9, 1.
Jeknić, Z., Pillman, K.A., Dhillon, T., Skinner, J.S., Veisz, O., Cuesta-Marcos, A, Hayes, P.M., Jacobs, A.K., Chen, T.H. & Stockinger, E.J. (2014). Hv-CBF2A overexpression in barley accelerates COR gene transcript accumulation and acquisition of freezing tolerance during cold acclimation. Plant Molecular Biology, 84(1-2), 67-82. DOI: 10.1007/s11103-013-0119-z
Josine, T.L., Ji, J., Wang, G. & Guan, C.F. (2011). Advances in genetic engineering for plants abiotic stress control. African Journal of Biotechnology, 10(28), 5402-5413.
Kardailsky, I., Shukla, V.K., Ahn, J.H., Dagenais, N., Christensen, S.K., Nguyen, J.T., Chory, J., Harrison M.J. & Weigel, D. (1999). Activation tagging of the floral inducer FT. Science, 286, 1962-1965.
Kim, S., Park, M., Yeom, S.I., Kim, Y.M., Lee, J.M., Lee, H.A., Seo, E., Choi, J., Cheong, K., Kim, K.T., Jung, K., Lee, G.W., Oh, S.K., Bae, C., Kim, S.B., Lee, H.Y., Kim, S.Y., Kim, M.S., Kang, B.C., Jo, Y.D., Yang, H.B., Jeong, H.J., Kang, W.H., Kwon, J.K., Shin, C., Lim, J.Y., Park, J.H., Huh, J.H., Kim, J.S., Kim, B.D., Cohen, O., Paran, I., Suh, M.C., Lee, S.B., Kim, Y.K., Shin, Y., Noh, S.J., Park, J., Seo, Y.S., Kwon, S.Y., Kim, H.A., Park, J.M., Kim, H.J., Choi, S.B., Bosland, P.W., Reeves, G., Jo, S.H., Lee, B.W., Cho, H.T., Choi, H.S., Lee, M.S., Yu, Y., Do Choi, Y., Park, B.S., van Deynze, A., Ashrafi, H., Hill, T., Kim, W.T., Pai, H.S., Ahn, H.K., Yeam, I., Giovannoni, J.J., Rose, J.K., Sørensen, I., Lee, S.J., Kim, R.W., Choi, I.Y., Choi, B.S., Lim, J.S., Lee, Y.H. & Choi, D. (2014). Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nature Genetics, 46(3), 270-278. DOI: https://doi.org/10.1038/ng.2877
Komatsu, S., Wada, T., Abaléa, Y., Nouri, M.-Z., Nanjo, Y., Nakayama, N., Shimamura, S., Yamamoto, R., Nakamura, T. & Furukawa, K. (2009). Analysis of plasma membrane proteome in soybean and application to flooding stress response. Journal of Proteome Research, 8(10), 4487-4499. DOI: https://doi.org/10.1021/pr9002883
Koornneef, M., Hanhart, C.J. & Veen, J.H. (1991). A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular and General Genetics MGG, 229, 57-66. DOI: https://doi.org/10.1007
Lee, R., Baldwin, S., Kenel, F., McCallum, J. & Macknight, R. (2013). FLOWERING LOCUS T genes control onion bulb formation and flowering. Nature Communications, 4, 2884. DOI: https://doi.org/10.1038/ncomms3884
Martínez, C., Pons, E., Prats, G. & León, J. (2004). Salicylic acid regulates flowering time and links defence responses and reproductive development. The Plant Journal, 37(2), 209-217. DOI: https://doi.org/10.1046/j.1365-313X.2003.01954.x
Mertens, J., Aliyu, H. & Cowana, D.A. (2018). LEA Proteins and the evolution of the WHy domain. Applied and Environmental Microbiology, 84(15), e00539-18. DOI: 10.1128/AEM.00539-18
Moscone, E., Scaldaferro, M., Grabiele, M., Cecchini, N., Sánchez-García, Y., Jarret, R., Daviña, J., Ducasse, D., Barboza, B. & Ehrendorfer, F. (2007). The evolution of chili peppers (Capsicum-solanaceae): a cytogenetic perspective. ISHS Acta horticulturae, 745. 1-7. DOI: 10.17660/ActaHortic.2007.745.5
Navarro, C., Abelenda, J.A., Cruz-Oro´, E., Cuéllar, C.A., Tamaki, S., Silva, J., Shimamoto, K. & Prat, S. (2011). Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature, 478, 119-122.
Nishikawa, F., Endo, T., Shimada, T., Fujii, H., Shimizu, T., Omura, M. & Ikoma, Y. (2007). Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). Journal of Experimental Botany, 58(14), 3915-3927. DOI: https://doi.org/10.1093/jxb/erm246
Ouzounidou, G., Ilias, I., Giannakaoula, A. & Papadopoulou, P. (2010). Comparative study on the effects of various plant growth regulators on growth, quality, and physiology of Capsicum annuum L. Pakistan Journal of Botany, 42, 805-814.
Pearce, S., Vanzetti, L.S. & Dubcovsky, J. (2013). Exogenous gibberellins induce wheat spike development under short days only in the presence of vernalization. Plant Physiology, 163(3), 1433-1445. DOI: https://doi.org/10.1104/pp.113.225854
Phukan, U.J., Jeena, G.S. and Shukla, R.K. (2016). WRKY Transcription Factors: Molecular regulation and stress responses in plants. Frontiers in Plant Science, 7, 760. DOI: https://doi.org/10.3389/fpls.2016.00760
Pichardo-González, J.M., Guevara-Olvera, L., Couoh-Uicab, Y.L., González-Cruz, L., Bernardino-Nicanor, A., Medina, H.R., González-Chavira, M.M. & Acosta-García, G. (2018) Efecto de las giberelinas en el rendimiento de chile jalapeño (Capsicum annuum L.). Revista Mexicana de Ciencias Agrícolas, 9(5), 925-934. DOI: https://doi.org/10.29312/remexca.v9i5.1502
Putterill, J., Robson, F., Lee, K., Simon, R. & Coupland, G. (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell, 80(6), 847–857. DOI: https://doi.org/10.1016/0092-8674(95)90288-0
Reyes, J.L., Rodrigo, M.J., Colmenero-Flores, J.M., Gil, J.V., Garay-Arroyo, A., Campos, F., Salamini, F., Bartels, D. & Covarrubias, A.A. (2005). Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant, Cell & Environment, 28(6), 709-718. DOI: https://doi.org/10.1111/j.1365-3040.2005.01317.x
Reyes-Escogido, M., Gonzalez-Mondragon, E. G. & Vazquez-Tzompantzi, E. (2011). Chemical and pharmacological aspects of capsaicin. Molecules (Basel, Switzerland), 16(2), 1253-1270. DOI: https://doi.org/10.3390/molecules16021253
Rihan, H.Z., Al-Issawi, M. & Fuller, M.P. (2018) Advances in physiological and molecular aspects of plant cold tolerance. Journal of Plant Interactions, 12(1), 143-157. DOI: https://doi.org/10.1080/17429145.2017.1308568
Rushton, P. J., Somssich, I. E., Ringler, P. & Shen, Q. J. (2010). WRKY transcription factors. Trends in plant science, 15(5), 247–258. DOI: https://doi.org/10.1016/j.tplants.2010.02.006
Sandoval-Oliveros, R., Guevara-Olvera, L., Beltrán, J. P., Gómez-Mena, C., & Acosta-García, G. (2017). Developmental landmarks during floral ontogeny of jalapeño chili pepper (Capsicum annuum L.) and the effect of gibberellin on ovary growth. Plant reproduction, 30(3), 119-129. DOI: https://doi.org/10.1007/s00497-017-0307-0
Sanghera, G. S., Wani, S. H., Hussain, W. & Singh, N. B. (2011). Engineering cold stress tolerance in crop plants. Current genomics, 12(1), 30–43. DOI: https://doi.org/10.2174/138920211794520178
Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y. & Shinozaki, K. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. The Plant journal: for cell and molecular biology, 31(3), 279-292. DOI: https://doi.org/10.1046/j.1365-313x.2002.01359.x
Sharma, A., Kumar, D., Kumar, S., Rampuria, S., Reddy, A.R. & Kirti, P.B. (2016). Ectopic expression of an atypical hydrophobic group 5 LEA protein from wild peanut Arachis diogoi confers abiotic stress tolerance in tobacco. PLoS One, 11, e0150609.
Suárez-López, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F. & Coupland, G. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature, 410, 1116-1120.
Taoka, K., Ohki, I., Tsuji, H., Furuita, K., Hayashi, K., Yanase, T., Yamaguchi, M., Nakashima, C., Purwestri, Y.A., Tamaki, S., Ogaki, Y., Shimada, C., Nakagawa, A., Kojima, C. & Shimamoto, K. (2011). 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature, 476, 332-335.
Thomashow, M. F. (1998). Role of cold-responsive genes in plant freezing tolerance. Plant physiology, 118(1), 1-8. DOI: https://doi.org/10.1104/pp.118.1.1
Thomashow, M. F. (1999). PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annual review of plant physiology and plant molecular biology, 50, 571-599. DOI: https://doi.org/10.1146/annurev.arplant.50.1.571
Varkonyi-Gasic, E., Moss, S.M.A., Voogd, C., Wang, T., Putterill, J. & Hellens, R.P. (2013). Homologs of FT, CEN and FD respond to developmental and environmental signals affecting growth and flowering in the perennial vine kiwifruit. The New Phytologist, 198(3), 732-746. DOI: 10.1111/nph.12162
Wang, F., Chen, H.W., Li, Q.T., Wei, W., Li, W., Zhang, W.K., Ma, B., Bi, Y.D., Lai, Y.C., Liu, X.L., Man, W.Q., Zhang, J.S., Chen, S.Y. (2015). GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. The Plant journal: for cell and molecular biology, 83(2), 224-236. DOI: https://doi.org/10.1111/tpj.12879
Published
How to Cite
Issue
Section
License
Copyright (c) 2020 Nova Scientia
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Conditions for the freedom of publication: the journal, due to its scientific nature, must not have political or institutional undertones to groups that are foreign to the original objective of the same, or its mission, so that there is no censorship derived from the rigorous ruling process.
Due to this, the contents of the articles will be the responsibility of the authors, and once published, the considerations made to the same will be sent to the authors so that they resolve any possible controversies regarding their work.
The complete or partial reproduction of the work is authorized as long as the source is cited.
