Efecto de CLas en genotipos de limón mexicano con diferente nivel de ploidía

Autores

  • Silvia Heréndira Carrillo Medrano
  • Serafín Cruz Izquierdo
  • Miguel Ángel Manzanilla Ramírez
  • Marciano Manuel Robles González
  • Ricardo Lobato Ortiz
  • José Alfredo Carrillo Salazar

DOI:

https://doi.org/10.34188/bjaerv9n3-295

Palavras-chave:

Citrus aurantifolia, HLB, híbridos de limón mexicano, Índice SPAD, Candidatus Liberibacter asiaticus

Resumo

“Candidatus Liberibacter asiaticus” (CLas), reportada como la causante de la enfermedad huanglongbing (HLB) y responsable de importantes pérdidas económicas en las regiones citrícolas de todo el mundo. En limón mexicano [Citrus aurantifolia (christm) swingle], se presenta una disminución de la producción a causa de la presencia de CLas. Se há reportado tolerancia en genótipos poliploides de algunos cítricos. En este estudio se evaluaron los efectos en el crecimiento de genótipos de limón mexicano con diferente nível de ploidia infectados con CLas. Las plantas se establecieron en contenedores de 27 L-1 dentro de una estrutura cubierta con malla antiáfidos. Los tratamentos evaluados fueron plantas de los genótipos: Colimex diploide (2x), Mestizo triploide (3x) y Mex 13 tetraploide (4x), injertadas en C. macrophylla Wester con y sin presencia de CLas. Se determinó el crecimiento e índice SPAD. El mayor crecimiento, lo presentó Mestizo 3x independientemente de la presencia de CLas. En el índice SPAD, Mestizo 3x obtuvo los mayores valores en plantas libres de CLas. En este estudio se mostró que los genotipos de limón mexicano con diferente nivel de ploidía infectados con CLas, disminuyeron su nivel de clorofila (índice SPAD), redujeron la longitud de brotes, el número de brotes por planta y número de hojas por brote, pero, aun así, continuaron su crecimiento. Se confirmó que el genotipo Mestizo 3x, aun en presencia de CLas, presentó mejor crecimiento que Colimex 2x, determinando una mayor tolerancia. Se requiere continuar con investigaciones que esclarezcan los mecanismos de tolerancia que este genotipo pudiera tener ante la infección con CLas.

Referências

ACHOR, D. et al. Citrus affected with huanglongbing disease. Plant Pathology Journal, v. 9, n. 2, p. 56-64, 2010.

ALBRECHT, U.; BOWMAN, K. D. Gene expression in Citrus sinensis (L.) Osbeck following infection with the bacterial pathogen Candidatus Liberibacter asiaticus causing Huanglongbing in Florida. Plant Science, v. 175, n. 3, p. 291-306, 2008.

ALBRECHT, U.; BOWMAN, K. D. Transcriptional response of susceptible and tolerant citrus to infection with Candidatus Liberibacter asiaticus. Plant Science, v. 185–186, p. 118–130, 2012. DOI: https://doi.org/10.1016/j.plantsci.2011.09.008.

ALEZA, P. et al. Tetraploidization events by chromosome doubling of nucellar cells are frequent in apomictic citrus and are dependent on genotype and environment. Annals of Botany, v. 108, n. 1, p. 37–50, 2011. DOI: https://doi.org/10.1093/aob/mcr099.

ALLARIO, T. et al. Large changes in anatomy and physiology between diploid Rangpur lime (Citrus limonia) and its autotetraploid are not associated with large changes in leaf gene expression. Journal of Experimental Botany, v. 62, n. 8, p. 2507–2519, 2011. DOI: https://doi.org/10.1093/jxb/erq467.

ARCE-LEAL, Á. P. et al. Gene expression profile of Mexican lime (Citrus aurantifolia) trees in response to huanglongbing disease caused by Candidatus Liberibacter asiaticus. Microorganisms, v. 8, n. 4, art. 528, 2020. DOI: https://doi.org/10.3390/microorganisms8040528.

BOJÓRQUEZ-OROZCO, A. M. et al. Differential Expression of MiRNAs Involved in Response to Candidatus Liberibacter Asiaticus Infection in Mexican Lime at Early and Late Stages of Huanglongbing Disease. Plants, v. 12, n. 5, art. 1039, 2023. DOI: https://doi.org/10.3390/plants12051039.

BOVÉ, J. M. Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, v. 88, n. 1, p. 7–37, 2006. DOI: https://doi.org/10.4454/jpp.v88i1.828.

BONFIG, K. B.; SCHREIBER, U.; GABLER, A. La infección con cepas virulentas y avirulentas de P. syringae afecta de manera diferencial la fotosíntesis y el metabolismo de los sumideros en hojas de Arabidopsis. Planta, v. 225, n. 1, p. 1–12, 2006. DOI: https://doi.org/10.1007/s00425-006-0303-3.

BROCHMANN, C. et al. Polyploidy in arctic plants. Biological Journal of the Linnean Society, v. 82, n. 4, p. 521–536, 2004. DOI: https://doi.org/10.1111/j.1095-8312.2004.00337.x.

CHEN, Z. J. Molecular mechanisms of polyploidy and hybrid vigor. Trends in Plant Science, v. 15, n. 2, p. 57–71, 2010. DOI: https://doi.org/10.1016/j.tplants.2009.12.003.

CIMO, G. et al. Carbohydrate and nutritional responses to stem girdling and drought stress with respect to understanding symptoms of Huanglongbing in citrus. HortScience, v. 48, n. 7, p. 920-928, 2013.

DA GRAÇA, J. V. et al. Huanglongbing in Texas: Report on the first detections in commercial citrus. Journal of Citrus Pathology, v. 2, n. 1, p. 1-6, 2015.

DENG, H. et al. Phloem regeneration is a mechanism for huanglongbing-tolerance of “bearss” lemon and “LB8-9” sugar belle® mandarin. Frontiers in Plant Science, v. 10, art. 277, 2019. DOI: https://doi.org/10.3389/fpls.2019.00277.

ESTRELLA-MALDONADO, H. et al. Insights into the Molecular Basis of Huanglongbing Tolerance in Persian Lime (Citrus latifolia Tan.) through a Transcriptomic Approach. International Journal of Molecular Sciences, v. 24, n. 8, art. 7497, 2023. DOI: https://doi.org/10.3390/ijms24087497.

ETXEBERRIA, E. et al. Anatomical distribution of abnormally high levels of starch in HLB-affected Valencia orange trees. Physiological and Molecular Plant Pathology, v. 74, n. 1, p. 76-83, 2009.

EVANS, E. A.; BALLEN, F. H.; CRANE, J. H. Economic potential of producing tahiti limes in southern Florida in the presence of citrus canker and citrus greening. HortTechnology, v. 24, n. 1, p. 99–106, 2014. DOI: https://doi.org/10.21273/HORTTECH.24.1.99.

FAN, J. et al. Differential anatomical responses of tolerant and susceptible citrus species to the infection of ‘Candidatus Liberibacter asiaticus’. Physiological and Molecular Plant Pathology, v. 83, p. 69–74, 2013.

FAN, J. et al. Changes in carbohydrate metabolism in Citrus sinensis infected with ‘Candidatus Liberibacter asiaticus’. Plant Pathology, v. 59, n. 6, p. 1037-1043, 2010.

FOLIMONOVA, S. Y. et al. Examination of the responses of different genotypes of citrus to huanglongbing (citrus greening) under different conditions. Phytopathology, v. 99, n. 12, p. 1346–1354, 2009. DOI: https://doi.org/10.1094/PHYTO-99-12-1346.

GMITTER, F. G. Jr.; CASTLE, W. S.; GROSSER, J. W. Mandarin Tree Named ‘LB8-9’. U.S. Patent Application No. 12/313,081, 2010.

GONZÁLEZ, M. M. R. et al. Experiencias con huanglonbing en limón mexicano en el Estado de Colima, México. Citrus Research & Technology, v. 39, p. 1-12, 2018.

GONZALEZ, P.; REYES-DE-CORCUERA, J.; ETXEBERRIA, E. Characterization of leaf starch from HLB-affected and unaffected-girdled citrus trees. Physiological and Molecular Plant Pathology, v. 79, p. 71-78, 2012.

GRAHAM, J. et al. Presymptomatic fibrous root decline in citrus trees caused by huanglongbing and potential interaction with Phytophthora spp. Plant Disease, v. 97, n. 9, p. 1195-1199, 2013.

GROSSER, J. W.; GMITTER, F. G. Fusión de protoplastos para la producción de tetraploides y triploides: aplicaciones para el mejoramiento de injertos y portainjertos en cítricos. Plant Cell, Tissue and Organ Culture, v. 104, p. 343–357, 2011.

GROSSER, J. et al. Salinity tolerance of ‘Valencia’ orange trees on allotetraploid rootstocks. Proceedings of the Florida State Horticultural Society, v. 125, p. 50–55, 2012.

GUZMÁN OTALVAREZ, M. V. Relación entre daño foliar y los rasgos funcionales foliares en plantas de especies con estrategias adquisitivas y conservativas en un bosque alto-andino colombiano Bogotá - Torca. 2020. Trabalho de Conclusão de Curso (Graduação em Biologia) – Universidad de La Salle, Bogotá, 2020. Disponível em: https://ciencia.lasalle.edu.co/biologia/100. Acesso em: 21 set. 2026.

HAMIDO, S. A.; MORGAN, K. T.; KADYAMPAKENI, D. M. The Effect of Huanglongbing on Young Citrus Tree Water Use. HortTechnology, v. 27, n. 5, p. 659–665, 2017.

HUANG, X.; WANG, Y.; WANG, N. Base editors for citrus gene editing. Frontiers in Genome Editing, v. 4, art. 852867, 2022.

INTRIGLIOLO, F. et al. SPAD as an indicator of nitrogen status in Citrus. In: INTERNATIONAL CITRUS CONGRESS, 9., 2000, Orlando. Proceedings... Orlando, FL: IOCV, 2000. p. 665-667.

HE, J. et al. A general formula for calculating surface area of the similarly shaped leaves: Evidence from six Magnoliaceae species. Global Ecology and Conservation, v. 23, e01129, 2020.

KHALID, M. F. et al. Better salinity tolerance in tetraploid vs diploid volkamer lemon seedlings is associated with robust antioxidant and osmotic adjustment mechanisms. Journal of Plant Physiology, v. 244, art. 153071, 2020. DOI: https://doi.org/10.1016/j.jplph.2019.153071.

KWAKYE, S.; KADYAMPAKENI, D. M. Micronutrients Improve Growth and Development of HLB-Affected Citrus Trees in Florida. Plants, v. 12, n. 1, art. 73, 2023.

KILLINY, N. et al. Metabolically speaking: possible reasons behind the tolerance of ‘Sugar Belle’ mandarin hybrid to huanglongbing. Plant Physiology and Biochemistry, v. 116, p. 36–47, 2017. DOI: https://doi.org/10.1016/j.plaphy.2017.05.001.

KOIZUMI, M. et al. Field evaluation of citrus cultivars for greening disease resistance in Thailand. In: INTERNATIONAL ORGANIZATION OF CITRUS VIROLOGISTS CONFERENCE, 12., 1993. Proceedings... Riverside: IOCV, 1993. v. 12.

KUCHARIK, C. J.; NORMAN, J. M.; GOWER, S. T. Measurements of branch area and adjusting leaf area index indirect measurements. Agricultural and Forest Meteorology, v. 91, n. 1-2, p. 69-88, 1998.

LI, J. et al. Residue Dynamics of Streptomycin in Citrus Delivered by Foliar Spray and Trunk Injection and Effect on 'Candidatus Liberibacter asiaticus' Titer. Phytopathology, v. 111, n. 7, p. 1095-1103, 2021. DOI: https://doi.org/10.1094/PHYTO-09-20-0427-R.

LI, J. et al. Developing Citrus Huanglongbing (HLB) Management Strategies Based on the Severity of Symptoms in HLB-Endemic Citrus-Producing Regions. Phytopathology, v. 109, n. 4, p. 582-592, 2019. DOI: https://doi.org/10.1094/PHYTO-08-18-0287-R.

LOURKISTI, R. et al. Triploidy in citrus genotypes improves leaf gas exchange and antioxidant recovery from water deficit. Frontiers in Plant Science, v. 11, art. 2311, 2021. DOI: https://doi.org/10.3389/fpls.2020.615335.

LOURKISTI, R. et al. Triploid citrus genotypes have a better tolerance to natural chilling conditions of photosynthetic capacities and specific leaf volatile organic compounds. Frontiers in Plant Science, v. 11, art. 330, 2020. DOI: https://doi.org/10.3389/fpls.2020.00330.

MACHADO, R. et al. Exploring the Genetic Networks of HLB Tolerance in Citrus: Insights Across Species and Tissues. Plants, v. 14, n. 12, art. 1792, 2025. DOI: https://doi.org/10.3390/plants14121792.

MANJUNATH, K. L. et al. Detection of “Candidatus Liberibacter asiaticus” in Diaphorina citri and its importance in the management of Citrus huanglongbing in Florida. Phytopathology, v. 98, n. 4, p. 387–396, 2008.

MANZANILLA RAMÍREZ, M. Á. Cambios fisiológicos en árboles de limón mexicano (Citrus aurantifolia) infectados con huanglongbing. 2019. Tese (Doutorado) – Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Colima, 2019. p. 103.

MANZANILLA RAMÍREZ, M. Á. et al. Manejo Integral del cultivo de limón mexicano en un escenario de alta incidencia de HLB. Tecomán: INIFAP, 2018. (Folleto técnico).

MARTINELLI, F. et al. Transcriptome profiling of citrus fruit response to huanglongbing disease. PLoS ONE, v. 7, n. 5, e38039, 2012.

MASAOKA, Y. et al. Lower Concentrations of Microelements in Leaves of Citrus Infected with ‘Candidatus Liberibacter Asiaticus’. Japan Agricultural Research Quarterly, v. 45, n. 3, p. 269–275, 2011.

MILES, G. P. et al. Apparent tolerance to huanglongbing in citrus and citrus-related germplasm. HortScience, v. 52, n. 1, p. 31–39, 2017. DOI: https://doi.org/10.21273/HORTSCI11374-16.

NEUPANE, A. et al. Poor shoot and leaf growth in Huanglongbing-affected sweet orange is associated with increased investment in defenses. Frontiers in Plant Science, v. 14, art. 1305815, 2023. DOI: https://doi.org/10.3389/fpls.2023.1305815.

PITINO, M.; ARMSTRONG, C. M.; DUAN, Y. Molecular Mechanisms behind the Accumulation of ATP and H2O2 in Citrus Plants in Response to “Candidatus Liberibacter Asiaticus” Infection. Horticulture Research, v. 4, art. 17040, 2017.

RAMADUGU, C. et al. Long-term field evaluation reveals huanglongbing resistance in Citrus relatives. Plant Disease, v. 100, n. 9, p. 1858–1869, 2016. DOI: https://doi.org/10.1094/PDIS-03-16-0271-RE.

REN, B. et al. Genome-wide location and function of DNA binding proteins. Science, v. 290, n. 5500, p. 2306–2309, 2000. DOI: https://doi.org/10.1126/science.290.5500.2306.

ROBLES-GONZÁLEZ, M. M. et al. Síntomas del Huanglongbing (HLB) en árboles de limón mexicano [Citrus aurantifolia (Christm) Swingle] y su dispersión en el estado de Colima, México. Revista Chapingo Serie Horticultura, v. 19, n. 1, p. 15-31, 2013.

RUIZ, M. et al. Synthetic polyploidy in grafted crops. Frontiers in Plant Science, v. 11, art. 540894, 2020. DOI: https://doi.org/10.3389/fpls.2020.540894.

SIVAGER, G. et al. Specific Physiological and Anatomical Traits Associated with Polyploidy and Better Detoxification Processes Contribute to Improved Huanglongbing Tolerance of the Persian Lime Compared With the Mexican Lime. Frontiers in Plant Science, v. 12, art. 685679, 2021. DOI: https://doi.org/10.3389/fpls.2021.685679.

SOLTIS, P. S.; SOLTIS, D. E. The role of hybridization in plant speciation. Annual Review of Plant Biology, v. 60, p. 561–588, 2009. DOI: https://doi.org/10.1146/annurev.arplant.043008.092039.

STOVER, E. et al. Growth, health and Liberibacter asiaticus titer in diverse citrus scions on mandarin versus trifoliate hybrid rootstocks in a field planting with severe huanglongbing. Proceedings of the Florida State Horticultural Society, v. 127, p. 53–59, 2014.

SU, M.-X. et al. Compensatory Growth and Physiological Protective Mechanisms of Populus talassica Kom. Populus euphratica Oliv. In Response to Leaf Damage. Forests, v. 14, n. 9, art. 1713, 2023. DOI: https://doi.org/10.3390/f14091713.

SUH, J. H. et al. Metabolomic Analysis Provides New Insight Into Tolerance of Huanglongbing in Citrus. Frontiers in Plant Science, v. 12, art. 710598, 2021.

SWARBRICK, P. J.; SCHULZE-LEFERT, P.; SCHOLES, J. D. Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant, Cell & Environment, v. 29, n. 6, p. 1061–1076, 2006. DOI: https://doi.org/10.1111/j.1365-3040.2005.01472.x.

THAKURIA, D. et al. Huanglongbing de los cítricos (HLB): Opciones de diagnóstico y manejo. Patología Vegetal Fisiológica y Molecular, v. 125, art. 102016, 2023.

THOMA, I. et al. Los isoprostanos de ciclopentenona inducidos por especies reactivas de oxígeno desencadenan la activación de genes de defensa y la acumulación de fitoalexinas en plantas. El Diario de la Planta, v. 34, n. 3, p. 363-375, 2003. DOI: https://doi.org/10.1046/j.1365-313X.2003.01730.x.

WANG, N.; TRIVEDI, P. Citrus huanglongbing: a newly relevant disease presents unprecedented challenges. Phytopathology, v. 103, n. 7, p. 652-665, 2013.

WEBER, K. C. et al. Insights into the mechanism of Huanglongbing tolerance in the Australian finger lime (Citrus australasica). Frontiers in Plant Science, v. 13, art. 1019295, 2022. DOI: https://doi.org/10.3389/fpls.2022.1019295.

WU, F. et al. Physiological Variables Influenced by ‘Candidatus Liberibacter Asiaticus’ Infection in Two Citrus Species. Plant Disease, v. 107, n. 6, p. 1769–1776, 2023.

YU, Q. et al. Reprogramming of a defense-signaling pathway in rough lemon and sweet orange is a critical element of the early response to ‘Candidatus Liberibacter asiaticus’. Horticulture Research, v. 4, art. 17063, 2017. DOI: https://doi.org/10.1038/hortres.2017.63.

ZHAO, H. et al. Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease. Molecular Plant, v. 6, n. 1, p. 301-310, 2013.

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Publicado

2026-09-21

Como Citar

Medrano, S. H. C., Izquierdo, S. C., Ramírez, M. Ángel M., González, M. M. R., Ortiz, R. L., & Salazar, J. A. C. (2026). Efecto de CLas en genotipos de limón mexicano con diferente nivel de ploidía. Brazilian Journal of Animal and Environmental Research, 9(3), e89371. https://doi.org/10.34188/bjaerv9n3-295

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v. 9 n. 3 (2026)

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