Fusarium oxysporum Tolerance assay in Strawberry (Fragaria x ananassa) Varieties and Analysis of FaPAL Gene Expression in an In vitro System
DOI:
https://doi.org/10.29356/jmcs.v69i2.2162Keywords:
Beta-aminobutyric acid, chitosan, FaPAL genes, flavonoids, Fragaria x ananassa NiktéAbstract
Abstract. Strawberry (Fragaria x ananassa) is one of the most commercially important fruits worldwide, and produces nutraceuticals flavonoids as pelargonidin, and other important antioxidants like quercetin and kaempferol. In Mexico, several strawberry varieties have been developed looking for more resistant plants to different pathogens like Fusarium oxysporum. Phenolics and flavonoids have been recognized as part of the defense mechanism of plants. These compounds arise from phenylalanine ammonia lyase (PAL) enzyme activity and strawberry contains several FaPAL genes; however, most publications don’t specify which one is being analyzed, or they are used interchangeably. Although FaPAL1, FaPAL2 and FaPAL6 have been isolated, no expression differences nor analysis of their promoters have been done. In this work we use an in vitro system to analyze the putative Fusarium oxysporum tolerance of ‘Camino Real’ and ‘Nikté’ strawberry cultivars grown in Mexico. Phenotypical traits, phenolics and flavonoids from control and infected plants were analyzed. We also made a bioinformatic analysis of the FaPAL genes from complete and partial cDNAs, and genomics comparisons. The two FaPAL gene families were recognized. Cis-active elements were analyzed in the promotor regions of both FaPAL gene families and the specific expression of FaPAL1 and FaPAL2 genes was analyzed in comparison with defensive genes like FaMBL1, FaWRKY1, FaCyf1, FaChi3, and FaPR1, upon the application of chitosan and beta-aminobutyric acid (BABA) as elicitors. Specific responses were related to FaEF1-alfa and FaGAPDH2 as optimal reference genes. We found that FaPAL1 and FaPAL2 responded strongly to chitosan, and BABA response suggest a downregulation of FaPAL1.
Resumen. La fresa (Fragaria x ananassa) es una de las frutas de mayor importancia comercial a nivel mundial, y produce flavonoides nutracéuticos como la pelargonidina y otros importantes antioxidantes como la quercetina y el kaempferol. En México se han desarrollado diversas variedades de fresa buscando plantas más resistentes a diferentes patógenos como Fusarium oxysporum. Los fenólicos y flavonoides han sido reconocidos como parte del mecanismo de defensa de las plantas. Estos compuestos surgen de la actividad de la enzima fenilalanina amonio liasa (PAL) y la fresa contiene varios genes FaPAL; sin embargo, la mayoría de las publicaciones no especifican cuál se está analizando o se usan indistintamente. Aunque se han aislado FaPAL1, FaPAL2 y FaPAL6, no se han realizado análisis de diferencias de expresión ni de sus promotores. En este trabajo utilizamos un sistema in vitro para analizar la supuesta tolerancia a Fusarium oxysporum de los cultivares de fresa ‘Camino Real’ y ‘Nikté’ cultivados en México. Se analizaron rasgos fenotípicos, fenólicos y flavonoides de plantas control e infectadas. También realizamos un análisis bioinformático de los genes FaPAL a partir de ADNc completos y parciales, y comparaciones genómicas. Se reconocieron las dos familias de genes FaPAL. Se analizaron elementos activos cis en las regiones promotoras de las dos familias de FaPAL1 y se analizó la expresión específica de los genes FaPAL1 y FaPAL2 en comparación con genes defensivos como FaMBL1, FaWRKY1, FaCyf1, FaChi3 y FaPR1, tras la aplicación de quitosano y ácido beta-aminobutírico (BABA) como inductores. Las respuestas específicas se relacionaron con FaEF1α y FaGAPDH2 como genes de referencia óptimos. Encontramos que FaPAL1 y FaPAL2 respondieron fuertemente al quitosano, y la respuesta de BABA sugiere una regulación negativa de FaPAL1.
Downloads
References
Duchesne, A. N. Histoire naturelle des fraisiers. Printed by Michel Lambeet, rue des Cord, Collége de Bourgogne, Paris, France 1766.
Liston, A.; Cronn, R.; Ashman, T. L. Am. J. Bot. 2014, 101, 1686-1699. DOI: https://doi.org/10.3732/ajb.1400140.
León-López, L.; Guzmán-Ortíz, D. L.; García-Berumen, J. A.; Chávez-Marmolejo, C. G.; Peña-Cabriales, J. J. Rev. Mex. Cienc. Agríc. 2014, 5, 673-686. DOI: https://doi.org/10.29312/remexca.v5i4.929.
Garrido, C.; Carbú, M.; Fernández-Acero, F. J.; González-Rodríguez, V. E.; Cantoral, J. M., in: New Insights in the Study of Strawberry Fungal Pathogens. In Genomics, Transgenics, Molecular Breeding Biotechnology of Strawberry. Global Science Books, UK. 2011, 24-39.
Dávalos-Gonzalez, P.A.; Jofre-Garfias, A.E.; Hernandez-Razo, A.R.; Narro-Sanchez, J.; Castro-Franco, J.; Vazquez-Sanchez, N. Bujanos-Muniz, R. Acta Hortic. 2006, 708, 547-552. DOI: https://doi.org/10.17660/ActaHortic.2006.708.97.
Dávalos-González, P.; Narro-Sanchez, J.; Jofre-Garfias, A.; Vazquez-Sanchez, M. Int. Soc. Hortic. Sci. 2014, 1049, 263-266. DOI: https://doi.org/10.17660/ActaHortic.2014.1049.33.
Mejía-Ramírez, E., in: Asimilación de carbono, partición de biomasa y producción de fruto en variedades de fresa. MSc Thesis, Colegio de Postgraduados. Campus Montecillo. 2015.
Valencia-Juárez, M. C.; Escobedo-López, D.; Díaz-Espino, L. F.; González-Pérez, E. Rev. Mex. Cienc. Agríc. 2019, 10, 91-100. DOI: https://doi.org/10.29312/remexca.v10i1.1633.
Dávalos-González, P.; Jofre-Garfias, A.; Díaz-Espino, L.; Mariscal-Amaro, L.; López-Pérez, M. Int. Soc. Hortic. Sci. 2017, 1156, 159-166. DOI: https://doi.org/10.17660/ActaHortic.2017.1156.23.
Guevara-Domínguez, P., in: Biosíntesis in vitro de fructooligosacáridos en el sistema Agave tequilana – Fragaria x ananassa. MSc Thesis, CINVESTAV-IPN Irapuato Unit, 2017
Guerrero-Ramírez, E., in: Calidad de vida y postcosecha del fruto de variedades mexicanas de fresa (Fragaria x ananassa Duch.) MSc Thesis, Colegio de Postgraduados. Campus Montecillo, 2017.
Koike, S. T.; Gordon, T. R. Crop Prot. 2015, 73, 67-72. DOI: https://doi.org/10.1016/j.cropro.2015.02.003.
Castro, F. J.; Dávalos-González, P. Rev. Mex. Fitopat. 1990, 8, 80-86. DOI: https://doi.org/10.18781/r.mex.fit.1904-5.
Ceja-Torres, L.; Mora-Aguilera, G.; Téliz, D.; Mora-Aguilera, A.; Sánchez-García, P.; Muñoz-Ruíz, C.; Tlapal-Bolaños, B.; De La Torre-Almaraz, R. Agrociencia. 2008, 42, 451-461. https://www.redalyc.org/articulo.oa?id=30211241008.
Bárcenas-Santana, D.; Guillén-Sánchez, D.; Yazmín-Basaldua, C.; Ramos-García, M. D.; Valle-de la Paz, M. Rev. Mex. Fitopatol. 2019, 37, 454-463. DOI: https://doi.org/10.18781/R.MEX.FIT.1904-5.
Quintero-Arias, G.; Vargas, J.; Acuña-Caita, J. F.; Valenzuela, J. L., in: Strawberry. In Temperate Fruits. Production, Processing, Marketing. New York, Apple Academic Press. 2021, 449-489. DOI: https://doi.org/10.1201/9781003045861.
Pastrana, A. M.; Borrero, C.; Pérez, A. G.; Avilés, M. Plant Sci. 2022, 111533. DOI: https://doi.org/10.1016/j.plantsci.2022.111533.
Amil-Ruiz, F.; Blanco-Portales, R.; Munoz-Blanco, J.; Caballero, J. L. Plant. Cell. Physiol. 2011, 52, 1873-1903. DOI: https://doi.org/10.1093/pcp/pcr136.
Capocasa, F.; Scalzo, J.; Mezzetti, B. Battino, M. Food Chem. 2008, 111, 872– 878. DOI: https://doi.org/10.1016/j.foodchem.2008.04.068.
Dong, N.‐Q.; Lin, H.‐X. J. Integ. Develop. Plant–Envir. Interac. 2020, 63, 180-209. DOI: https://doi.org/10.1111/jipb.13054.
Ghasemzadeh, A.; Ghasemzadeh, N. Acad. J. 2011, 5, 6697-6703. DOI: https://doi.org/10.5897/JMPR11.1404.
Skadhauge, B.; Thomsen, K. K.; Von Wettstein, D. Hereditas. 1997, 126, 147-160. DOI: https://doi.org/10.1111/j.1601- 5223.1997.00147.x.
Mierziak, J.; Kostyn, K.; Kulma, A. Molecules. 2014, 19, 16240-16265. DOI: https://doi.org/10.3390/molecules191016240.
Chen, X.; Wang, P.; Gu, M.; Hou, B.; Zhang, C.; Zheng, Y.; Sun, Y.; Jin, S. Ye, N. Hortic. Plant J. 2022, 8, 381-394. DOI: https://doi.org/10.1016/j.hpj.2021.12.005.
Landi, L.; Feliziani, E. Romanazzi, G. J. Agric. Food Chem. 2014, 62, 3047-3056. DOI: https://doi.org/10.1021/jf404423x.
Crognale, S.; Russo, C.; Petruccioli, M.; D’annibale, A. Fermentation. 2022, 8, 76. DOI: https://doi.org/10.3390/fermentation8020076.
Suresh, P. V.; Sakhare, P. Z.; Sachindra, N. M.; Halami, P. M. J. Food Sci. Technol. 2014, 51, 1594-1599. DOI: https://doi.org/10.1007/s13197-012-0676-1.
Al‐Hetar, M. Y.; Zainal Abidin, M. A.; Sariah, M.; Wong, M. Y. J. Appl. Polym. Sci. 2011, 120, 2434-2439. DOI: https://doi.org/10.1002/app.33455.
Massoud, M. A.; Kordy, A. M.; Abdel-Mageed, A. A.; Heflish, A. I. A.; Sehier, M. M. J. Adv. Agric. Res. 2020, 25, 176-196. DOI: http://doi.org/10.21608/JALEXU.2020.161766.
Benhamou, N.; Lafontaine, P. J.; Nicole, M. Phytopathology. 1994, 84, 1432-1444. DOI: https://doi.org/10.1094/Phyto-84-1432.
Stasińska-Jakubas, M.; Hawrylak-Nowak, B. Molecules. 2022, 27, 2801. DOI: https://doi.org/10.3390/molecules27092801.
Papavizas, G. C., in: Greenhouse control of Aphanomyces root rot of peas with aminobutyric acid and methylaspartic acid. In The Plant Disease Reporter. USDA. Beltsville, Maryland. 1964, 537-541.
Jakab, G.; Cottier, V.; Toquin, V.; Rigoli, G.; Zimmerli, L.; Métraux, J. P. Mauch-Mani, B. Eur. J. Plant Pathol. 2001, 107,29–37. DOI: https://doi.org/10.1023/A:1008730721037.
Cohen, Y. R. Plant Dis. 2002, 86, 448–457. DOI: https://doi.org/10.1094/PDIS.2002.86.5.448.
Huang, T.; Jander, G. de Vos, M. Phytochemistry. 2011, 72, 1531–1537. DOI: https://doi.org/10.1016/j.phytochem.2011.03.019.
Balmer, A.; Pastor, V.; Gamir, J.; Flors, V. Mauch-Mani, B. Trends Plant Sci. 2015, 20, 443–452. DOI: https://doi.org/10.1016/j.tplants.2015.04.002.
Hegedűs, G.; Nagy, Á.; Decsi, K.; Kutasy, B.; Virág, E. Data Brief. 2022, 41, 107983. DOI: https://doi.org/10.1016/j.dib.2022.107983.
Murashige, T.; Skoog, F. Physiol. Plant. 1962, 15, 473-497. DOI: https://doi.org/10.1111/j.1399-3054.1962.tb08052.x.
Fang, X. L.; Phillips, D.; Li, H.; Sivasithamparam, K.; Barbetti, M. J. Australas. Plant Pathol. 2011, 40, 109–119. DOI: https://doi.org/10.1007/s13313-010-0019-5.
Giusti, M. Wrolstad, M. J. Food Sci. 1996, 61, 688-694. DOI: https://doi.org/10.1111/j.1365-2621.1996.tb12182.x.
Slinkard, K, Singleton, V. J. Enol. Vitic. 1977, 28, 49-55. DOI: htpp://doi.org/10.5344/ajev.1977.28.1.49.
Woisky, RG. Salatino, A. J. Apic. Res. 1998, 37, 99-105. DOI: https://doi.org/10.1080/00218839.1998.11100961.
Liu, J.; Wang, J.; Wang, M.; Zhao, J.; Zheng, Y.; Zhang, T. Front. Plant Sci. 2021, 12, 702160. DOI: http://doi.org/10.3389/fpls.2021.702160.
Chen, C.; Chen, H.; Zhang, Y.; Thomas, H. R.; Frank, M. H.; He, Y.; Xia, R. Molec. Plant. 2020, 13, 1194-1202. DOI: https://doi.org/10.1016/j.molp.2020.06.009.
Rombauts, S.; Déhais, P.; Van Montagu, M.; Rouzé, P. Nucleic Acid Res. 1999, 27, 295-296. DOI: https://doi.org/10.1093/nar/27.1.295.
Amil-Ruiz, F.; Garrido-Gala, J.; Blanco-Portales, R.; Folta, K. M.; Muñoz-Blanco, J. Caballero, J. L. PLoS ONE, 2013, 8, e70603. DOI: https://doi.org/10.1371/journal.pone.0070603.
Martínez, M.; Abraham, Z.; Gambardella, M.; Echaide, M.; Carbonero, P. Diaz, I. J. Exp. Bot. 2005, 56, 1821-1829. DOI: https://doi.org/10.1093/jxb/eri172.
Guidarelli, M.; Zoli, L.; Orlandini, A.; Bertolini, P.; Baraldi, E. Mol. Plant Pathol. 2014, 15, 832-840. DOI: https://doi.org/10.1111/mpp.12143.
Zhou, Y.; Xiong, J.; Shu, Z.; Dong, C.; Gu, T.; Sun, P.; He, S.; Jiang, M.; Xia, Z.; Xue, J.; Khan, W. U.; Chen, F. Cheng, Z-M. Horticult. Res. 2023, 10, uhad027. DOI: https://doi.org/10.1093/hr/uhad027.
Tzanetakis, I. E.; Halgren, A.; Mosier, N.; Martin, R. R. Virus Res. 2007, 127, 26-33. DOI: https://doi.org/10.1016/j.virusres.2007.03.010.
Rott, M. E.; Jelkmann, W. Eur. J. Plant Pathol. 2001, 107, 411-420. DOI: https://doi.org/10.1023/A:1011264400482.
Livak, K. J. Schmittgen, T. D. Methods. 2001, 5, 402−408. DOI: https://doi.org/10.1006/meth.2001.1262.
Mariscal-Amaro, L.; Rivera-Yerena, A.; Dávalos-González, P.; Ávila-Martínez, D. México. Agrociencia, 2017, 51, 673-61. http://www.redalyc.org/articulo.oa?id=30252708007
Gill, U. S.; Uppalapati, S. R.; Gallego‐Giraldo, L.; Ishiga, Y.; Dixon, R. A.; Mysore, K. S. Plant Cell Environ. 2017, 41, 1997- 2007. DOI: https://doi.org/10.1111/pce.13093.
Lee, J. H.; Lee, S. J.; Park, S.; Jeong, S. W.; Kim, C. Y.; Jin, J. S.; Shin, S. C. Food Chem. 2012, 133, 1653-1657. DOI: https://doi.org/10.1016/j.foodchem.2012.02.063.
Wojtasik, W.; Kulma, A.; Dymińska, L.; Hanuza, J.; Czemplik, M.; Szopa, J. BMC Plant Biol. 2016, 75, 1-16. DOI: https://doi.org/10.1186/s12870-016-0762-z.
Romero-Rincón, A.; Martínez, S. T.; Higuera, B. L.; Coy-Barrera, E.; Duban, A. H. Phytochemistry. 2021, 192, 1-14. DOI: https://doi.org/10.1016/j.phytochem.2021.112933.
Galdino, A. C.; de Freitas, M. B.; de Borba, M. C.; Stadnik, M. J. Trop. Plant Pathol. 2021, 46, 553–558. DOI: https://doi.org/10.1007/s40858-021-00440-6.
Nagpala, E. G.; Guidarelli, M.; Gasperotti, M.; Masuero, D.; Bertolini, P.; Vrhovsek, U.; Elena, B. Agric. Food Chem. 2016, 64, 1869–1878. DOI: https://doi.org/10.1021/acs.jafc.5b06005.
Mikulic-Petkovsek, M.; Schmitzer, V.; Slatnar, A.; Weber, N.; Veberic, R.; Stampar, F.; Munda, A.; Koron, D. J. Agric. Food Chem. 2013, 61, 5987−5995. DOI: https://doi.org/10.1021/jf402105g.
Haile, Z. M.; Nagpala-De Guzman, E. G.; Moretto, M.; Sonego, P.; Engelen, K.; Zoli, L.; Baraldi, E. Front. Plant Sci. 2019, 10, 1-17. DOI: https://doi.org/10.3389/fpls.2019.01131.
Hano, C.; Addi, M.; Fliniaux, O.; Bensaddek, L.; Duverger, E.; Mesnard, F.; Lainé, E. Plant Physiol. Biochem. 2008, 46, 590- 600. DOI: https://doi.org/10.1016/j.plaphy.2008.02.004.
Weber, N.; Veberic, R.; Mikulic-Petkovsek, M.; Stampar, F.; Koron, D.; Munda, A.; Jakopic, J. Physiol. Molec. Plant Pathol. 2015, 92, 119-129. DOI: http://dx.doi.org/10.1016/j.pmpp.2015.10.003.
Pombo, M. A.; Rosli, H. G.; Martínez, G. A. Civello, P. M. Postharv. Biol. Technol. 2011, 59, 94-102. DOI: https://doi.org/10.1016/j.postharvbio.2010.08.003.
Li, G.; Wang, H.; Cheng, X.; Su, X.; Zhao, Y.; Jiang, T.; Jin, Q.; Lin, Y. Cai, Y. PeerJ, 2019, 7, e8064. DOI: https://doi.org/10.7717/peerj.8064.
Parra-Palma, C.; Morales-Quintana, L.; Ramos, P. Agronomy, 2020, 10, 588. DOI: https://doi.org/10.3390/agronomy10040588
Pillet, J.; Yu, H.-W.; Chambers, A.H.; Whitaker, V.M.; Folta, K.M. J. Exp. Bot. 2015, 66, 4455–4467. DOI: https://doi.org/10.1093/jxb/erv205.
Liu, Y.; Ye, Y.; Wang, Y.; Jiang, L.; Yue, M.; Tang, L.; Tang, H. Int. J. Molec. Sci. 2022, 23, 7757. DOI: https://doi.org/10.3390/ijms23147757.
Martínez‐Rivas, F. J.; Blanco‐Portales, R.; Serratosa, M. P.; Ric‐Varas, P.; Guerrero‐Sánchez, V.; Medina‐Puche, L.; Molina‐ Hidalgo, F. J. Plant J. 2023, 114, 683-698. DOI: https://doi.org/10.1111/tpj.16166.
Gaete-Eastman, C.; Stappung, Y.; Molinett, S.; Urbina, D.; Moya-Leon, M. A.; Herrera, R. Front. Plant Sci. 2022, 13, 976901. DOI: https://doi.org/10.3389/fpls.2022.976901.
Ma, C.; Xiong, J.; Liang, M.; Liu, X.; Lai, X.; Bai, Y.; Cheng, Z. Agronomy. 2021, 11, 2377. DOI: https://doi.org/10.3390/agronomy11122377.
Khan, A. A.; Shih, D. S. Plant Sci. 2004, 166, 753-762. DOI: https://doi.org/10.1016/j.plantsci.2003.11.015.
Manning, K. Planta. 1998, 205, 622–631. DOI: https://doi.org/10.1007/s004250050365.
Ma, L.; Haile, Z.; Sabbadini, S.; Mezzetti, B.; Negrini, F.; Baraldi, E. J. Exp. Bot. 2022, 74, 149-161. DOI: https://doi.org/10.1093/jxb/erac396.
Mo, F.; Luo, Y.; Ge, C.; Mo, Q.; Ling, Y.; Luo, S.; Tang, H., in: Cloning and expression analysis of FaPR-1 gene in strawberry. 1956, 26-28 September, 2017; Trincone, A.; Azevedo, J. L. Gong, M. (Eds.), AIP Publishing, Offenburg, Germany, 2018, 020009. DOI: https://doi.org/10.1063/1.5034261.
Liang, W.; Wang, M.; Du, B.; Ling, L.; Bi, Y.; Zhang, J.; Sun, Y.; Zhou, S.; Zhang, L.; Ma, X.; Ma, J.; Wu, L. Guo, C. Biotechnol. Biotechnol. Equip. 2022, 36, 684-696. DOI: https://doi.org/10.1080/13102818.2022.2106886.
Encinas-Villarejo, S.; Maldonado, A. M.; Amil-Ruiz, F.; de los Santos, B.; Romero, F.; Pliego-Alfaro, F.; Muñoz-Blanco, J.; Caballero, J. L. J. Exp. Bot. 2009, 60, 3043-3065. DOI: https://doi.org/10.1093/jxb/erp152.
Wang, Y.; Zhao, F.; Zhang, G.; Jia, S.; Yan, Z. Sci. Hortic. 2021, 279, 109893. DOI: https://doi.org/10.1016/j.scienta.2020.109893.
Gambardella, M.; Ríos, R.; Aballay, E.; Cambra, I.; Diaz, I.; Acta Hortic. 2010, 926, 113-117. DOI: https://doi.org/10.17660/ActaHortic.2012.926.15.
Zimmerli, L.; Jakab, G.; Métraux, J. P.; Mauch-Mani, B. PNAS. 2000, 97, 12920-12925. DOI: https://doi.org/10.1073/pnas.230416897.
Yi-Lan, J.; Shi-Long, J.; Xuan-Li, J. Arch. Microbiol. 2021, 203, 3623-3632. DOI: https://doi.org/10.1007/s00203-021-02350-2.
Almoneafy, A. A.; Ojaghian, M. R.; Seng-fu, X.; Ibrahim, M.; Guan-Lin, X.; Yu, S.; Wen-Xiao, T. Bin, L. Trop. Plant Pathol. 2013, 38, 102-113. DOI: https://doi.org/10.1590/S1982-56762013000200003.
Baccelli, I. Mauch-Mani, B. Plant Mol. Biol. 2016, 91, 703–711. DOI: https://doi.org/10.1007/s11103-015-0406-y.
Cai, J.; Aharoni, A. Curr. Opin. Plant Biol. 2022, 69, 102288. DOI: https://doi.org/10.1016/j.pbi.2022.102288.
Khan, W.; Prithiviraj, B.; Smith, D. L. J. Plant Physiol. 2003, 160, 859-863. DOI: https://doi.org/10.1078/0176-1617-00905.
Rahman, M.; Mukta, J. A.; Sabir, A. A.; Gupta, D. R.; Mohi-Ud-Din, M.; Hasanuzzaman, M.; Islam, M. T. PLoS ONE, 2018, 13, e0203769. DOI: https://doi.org/10.1371/journal.pone.0203769.
Wang, K.; Liao, Y.; Xiong, Q.; Kan, J.; Cao, S. Zheng, Y. J. Agric. Food Chem. 2016, 64, 5855-5865. DOI: https://doi.org/10.1021/acs.jafc.6b00947.
Jannatizadeh, A.; Aghdam, M. S.; Farmani, B.; Maggi, F. Morshedloo, M. R. Sci. Hortic. 2018, 240, 249-257. DOI: https://doi.org/10.1016/j.scienta.2018.06.048.
Li, S.; Wang, G.; Chang, L.; Sun, R.; Wu, R.; Zhong, C.; Sun, J. Int. J. Mol. Sci. 2022, 23, 11961. DOI: https://doi.org/10.3390/ijms231911961.
Fatima, S.; Cheema, K.; Shafiq, M.; Manzoor, M.; Ali, Q.; Haider, M.; Shahid, M. Bull. Biol. Alli. Sci. Res. 2023, 2023, 38-38. DOI: https://doi.org/10.54112/bbasr.v2023i1.3.
Sánchez-Gómez, C.; Posé, D.; Martín-Pizarro, C. Front. Plant Sci. 2022, 13, 1022369. DOI: https://doi.org/10.3389/fpls.2022.1022369.
Wanner, L. A.; Li, G.; Ware, D.; Somssich, I. E. Davis, K. R. Plant Mol. Biol. 1995, 27, 327-338. DOI: https://doi.org/10.1007/BF00020187.
Huang, J.; Gu, M.; Lai, Z.; Fan, B.; Shi, K.; Zhou, Y. H.; Yu, J. Q. Chen, Z. Plant Physiol. 2010, 153, 1526-1538. DOI: https://doi.org/10.1104/pp.110.157370.
Dong, C. J. Shang, Q. M. Planta. 2013, 238, 35-49. DOI: https://doi.org/10.1007/s00425-013-1869-1
de Jong, F.; Hanley, S. J.; Beale, M. H. Karp, A. Phytochemistry. 2015, 117, 90-97. DOI: https://doi.org/10.1016/j.phytochem.2015.06.005.
Dong, C. J.; Ning, C.; Zhang, Z. G. Shang, Q. M. J. Integr. Agric. 2016, 15, 1239-1255. DOI: https://doi.org/10.1016/S2095-3119(16)61329-1.
Yan, F.; Li, H. Zhao, P. Genes. 2019, 10, 46. DOI: https://doi.org/10.3390/genes10010046.
Ren, W.; Wang, Y.; Xu, A. Zhao, Y. Legume Res. 2019, 42, 461-466. DOI: https://doi.org/10.18805/LR-431.
Gho, Y. S.; Kim, S. J. Jung, K. H. Genes Genom. 2020, 42, 67-76. DOI: https://doi.org/10.1007/s13258-019-00879-7.
Jiang, L.; Yue, M.; Liu, Y.; Ye, Y.; Zhang, Y.; Lin, Y.; Wang, X.; Chen, Q. Tang, H. Int. J. Mol. Sci. 2022, 23, 7375. DOI: https://doi.org/10.3390/ijms23137375.
Pant, S.; Huang, Y. Sci. Rep. 2022, 12, 22537. DOI: https://doi.org/10.1038/s41598-022-25214-1.
Zhang, F.; Wang, J.; Li, X.; Zhang, J.; Liu, Y.; Chen, Y.; Yu, Q.; Li, N. Front. Plant Sci. 2023, 14, 1204990. DOI: https://doi.org/10.3389/fpls.2023.1204990.
Kariñho-Betancourt, E.; Carlson, D.; Hollister, J.; Fischer, A.; Greiner, S.; Johnson, M. T. PLoS ONE, 2022, 17, e0269307. DOI: https://doi.org/10.1371/journal.pone.0269307.
Downloads
Additional Files
Published
Issue
Section
License
Copyright (c) 2025 Yazmín García-Canales, Alba Estela Jofre-y-Garfias, Silvia Edith Vales-Rodríguez, José Luis Hernández-Flores, Jesús Alonso Garduño-Hernández, Quiahuitl María Guadalupe Zavala-Navarro, Edmundo Lozoya-Gloria
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
