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TESIS DOCTORAL Felix Antonio Plasencia Martinez Combinado.Pdf UNIVERSIDAD DE MURCIA FACULTAD DE BIOLOGÍA Identificación y Caracterización de Mutantes Alterados en la Tolerancia a la Salinidad en Especies de Tomate. Papel del Gen SICBL10 en los Mecanismos de Respuesta a Salinidad Señalizados por Ca² en Tomate. D. Félix Antonio Plasencia Martínez = 2015 UNIVERSIDAD DE MURCIA FACULTAD DE BIOLOGÍA Identificación y caracterización de mutantes alterados en la tolerancia a la salinidad en especies de tomate. Papel del gen SlCBL10 en los mecanismos de respuesta a salinidad señalizados por Ca 2+ en tomate. D. Félix Antonio Plasencia Martínez 2015 Identificación y caracterización de mutantes alterados en la tolerancia a la salinidad en especies de tomate. Papel del gen SlCBL10 en los mecanismos de respuesta a salinidad señalizados por Ca 2+ en tomate. Tesis Doctoral D. Félix Antonio Plasencia Martínez Directores de la Tesis Dra. María del Carmen Bolarín Jiménez Dra. María Isabel Egea Sánchez 2015 A mis padres, a mis hermanas y a Silvia. Resumen RESUMEN La salinidad está considerada como uno de los principales factores limitantes de la producción agrícola. Ante las predicciones del aumento de la población a nivel mundial con el consiguiente incremento de la demanda de alimentos, y los efectos negativos del cambio climático sobre la productividad de los cultivos de interés agronómico, como tomate (Solanum lycopersicum ), un objetivo prioritario en la investigación en biología vegetal en la actualidad es avanzar en el conocimiento de los mecanismos y genes implicados en la tolerancia a la salinidad. Una de las estrategias más interesantes para abordar el anterior objetivo es el análisis de mutantes. Esta tesis se enmarca dentro del programa de mutagénesis insercional llevado a cabo por los grupos de investigación del IBMCP (Valencia), UAL (Almería) y CEBAS (Murcia), donde se han generado colecciones de mutantes de tomate cultivado y silvestre. Uno de los objetivos de este trabajo ha sido la identificación y caracterización de mutantes de la especie silvestre Solanum pennellii . La identificación de mutantes en una especie filogenéticamente relacionada con tomate, y que presenta características morfológicas muy diferentes al tomate cultivado y altos niveles de tolerancia al estrés abiótico, puede ser la mejor elección para identificar genes y procesos determinantes de la tolerancia a la salinidad. Respecto a los mutantes de S. pennellii , los cambios morfológicos y fisiológicos observados en el mutante sl-1 (succulent leaves-1) en ausencia de estrés están asociados a una menor perdida de agua por transpiración, y a un mantenimiento de la homeostasis de Na + y K + frente al estrés salino. Por el contrario, el mutante hipersensible a sal shp-1 (salt hypersensitive pennellii-1) experimentaba una mayor pérdida de agua por transpiración y una elevada acumulación de Na + en las hojas durante el periodo de exposición a la sal. La caracterización de ambos mutantes ha puesto de manifiesto que la regulación de la pérdida de agua es un mecanismo clave en la tolerancia a la salinidad. En este trabajo también se ha abordado la caracterización de mutantes de tomate generados a partir del cultivar Moneymaker. A nivel fenotípico y fisiológico, el mutante hipersensible a la salinidad she-1 (salt hypersensitive esculentum-1) mostraba una respuesta similar a la observada en el mutante shp-1 de S. Pennellii, con alta acumulación de Na + en sus hojas. Sin embargo, la sensibilidad a la sal del mutante she-1 parece estar relacionado con la alteración en los niveles de expresión de los genes SlHKT1s implicados en el transporte de Na + a la parte aérea. Además, mediante injertos recíprocos se observó que la raíz es el órgano responsable de la sensibilidad a la sal del mutante she-1. I Resumen Finalmente, se ha abordado la caracterización de un mutante que tiene anulada la expresión del gen CBL10 (CALCINEURIN B-LIKE PROTEIN 10 ) de tomate. El mutante cbl10 es hipersensible al estrés salino a pesar de que la acumulación de Na + en las plantas del mutante es menor que en las plantas no transformadas de Moneymaker y mantiene mayores niveles de K + con la salinidad, lo que sugiere que la capacidad de acumular Na + en vacuolas está alterada en el mutante y por tanto se alcanzan antes niveles citotóxicos del ion en el citoplasma. Además, el mutante tiene alterada la distribución de Na + entre hojas jóvenes y adultas, produciéndose un mayor transporte de Na + a los tejidos en desarrollo, que puede causar el colapso apical detectado en el mutante tras su exposición a la salinidad. Otra alteración fisiológica provocada por la anulación del gen SlCBL10 es una reducción de la pérdida de agua vía transpiración en condiciones de estrés. Además, la menor transpiración está asociada a una alteración en la homeostasis de Ca 2+ y a cambios en el perfil de expresión del transportador de Ca 2+ vacuolar SlCAX1 , tanto en condiciones salinas como en ausencia de las mismas. Mediante injertos se ha demostrado que el principal órgano responsable de la sensibilidad del mutante cbl10 al estrés salino es la parte aérea, ya que solo muestran sensibilidad a sal las plantas injertadas con el mutante cbl10 como esqueje, pero no cuando éste es utilizado como portainjerto. Este resultado sugiere que SlCBL10 podría tener una función diferente en parte aérea y raíz, siendo su función en la parte aérea la implicada en la tolerancia a la salinidad en tomate. Además, la alteración de la homeostasis de Ca 2+ en la parte aérea nos lleva a proponer como papel del gen SlCBL10 su participación en la regulación de la homeostasis de Ca 2+ , siendo esta función crucial para la tolerancia del tomate al estrés salino. II Abstract ABSTRACT Salinity is considered as one of the major limiting effects on agriculture production. Keeping in mind the predictions about the rise of world population resulting in an increase in food demand, and the negative effects of climate change on the productivity of plants of agronomic interest, such tomato ( Solanum lycopersicum ), one current critical aim in plant biology research is to advance in the knowledge of genes and mechanisms involved in salt tolerance in plants. One of the most interesting strategies to approach this goal is the analysis of mutants. This PhD thesis is framed within the insertional mutagenesis programme carried out by the Spanish research groups from IBMCP (Valencia), UAL (Almeria) and CEBAS (Murcia), where mutant collections have been generated in domesticated tomato and in wild-related species. One of the objectives of this research work has been the identification and characterization of mutants of the tomato wild species Solanum pennellii . The identification of mutants in a species phylogenetically related with tomato that exhibits so different morphological characteristics and high levels of tolerance to abiotic stress could be the best choice to identify genes and processes determining tolerance to salinity. Regarding S. pennellii mutants, the morphological and physiological alterations observed in the sl-1 (succulent leaves-1) mutant in absence of stress are associated to a lower transpirational water loss and a better maintenance of Na + and K + homeostasis when confronted to salt stress. On the contrary, the salt hypersensitive shp-1 (salt hypersensitive pennellii-1) mutant suffered a higher transpirational water loss and an elevated accumulation of Na + in leaves during the period of exposition to salt stress. The characterization of both mutants has revealed that regulation of water loss is a key mechanism in salt stress tolerance. In this research work it has also been approached the characterization of tomato mutants generated in Moneymaker commercial cultivar. At phenotypical as well as physiological level the salt hypersensitive she-1 (salt hypersensitive esculentum-1) mutant showed a similar response to the one observed in shp-1 S. pennellii mutant: a remarkable increase in Na + accumulation in leaves. However, the susceptibility to salt of she-1 mutant seems to be related to the alteration in the levels of expression of SlHKT1 genes involved in the Na + transport from root to shoot. Moreover, it was observed by reciprocal grafting that the root was the responsible organ for the salt sensitivity of she-1 mutant. Finally, it has been approached the characterization of a mutant that exhibits a knock-out expression of CBL10 (CALCINEURIN B-LIKE PROTEIN 10 ) tomato gene. The cbl10 mutant is hypersensitive to salt stress in spite of III Abstract the fact that Na + accumulation in mutant plants is lower than in untransformed WT ones and it upholds higher levels of K + in salt stress condition. These observations suggest that ability to accumulate Na + in vacuoles is compromised in the mutant and therefore cytotoxic levels of the ion in the cytoplasm are reached earlier in cbl10 than in WT. What is more, the distribution of Na + between young and adult leaves is altered in the mutant, since a higher transport of the ion to developing tissues occurred in cbl10 . This behavior could be the cause of the apical meristem collapse detected in the mutant plant after exposition to salt stress. Another physiological alteration induced by knocking out SlCBL10 gene is the reduction of water loss via transpiration in stressful conditions. Moreover, the lower transpiration is associated with a perturbation in Ca 2+ homeostasis and with changes in the gene expression profile of the vacuolar Ca 2+ carrier SlCAX1 , in salt stress as well as in non-stressful conditions. Grafting experiments demonstrated that the main responsible organ for the salt stress sensitivity in cbl10 mutant is the shoot, as only grafted plants using cbl10 as scion exhibited such sensitivity, which is not observed when cbl10 is used as rootstock. This result suggests that SlCBL10 could have a different function in shoot and in root, being the function in shoot the one involved in salt tolerance in tomato. Also the alteration of the Ca 2+ homeostasis in the shoot of cbl10 mutant lead us to propose a role for SlCBL10 in the regulation of Ca 2+ homeostasis, being this potential function a crucial one for tolerance of tomato to salt stress.
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