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ESTUDIO DE LA MICOBIOTA ENDOFÍTICA ASOCIADA a LAS GRAMÍNEAS Dactylis Glomerata, Holcus Lanatus, Ammophila Arenaria Y Elymus Farctus

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ESTUDIO DE LA MICOBIOTA ENDOFÍTICA ASOCIADA a LAS GRAMÍNEAS Dactylis Glomerata, Holcus Lanatus, Ammophila Arenaria Y Elymus Farctus UNIVERSIDAD DE SALAMANCA FACULTAD DE BIOLOGÍA DEPARTAMENTO DE MICROBIOLOGÍA Y GENÉTICA ESTUDIO DE LA MICOBIOTA ENDOFÍTICA ASOCIADA A LAS GRAMÍNEAS Dactylis glomerata, Holcus lanatus, Ammophila arenaria y Elymus farctus Mª Salud Sánchez Márquez 2009 DR. ÍÑIGO ZABALGOGEAZCOA GONZÁLEZ, CIENTÍFICO TITULAR DEL CONSEJO SUPERIOR DE INVESTIGACIONES CIENTÍFICAS (CSIC), EN EL INSTITUTO DE RECURSOS NATURALES Y AGROBIOLOGÍA DE SALAMANCA, CERTIFICA Que la memoria titulada “ESTUDIO DE LA MICOBIOTA ENDOFÍTICA ASOCIADA A LAS GRAMÍNEAS Dactylis glomerata, Holcus lanatus, Ammophila arenaria y Elymus farctus”, presentada por Dña. Mª Salud Sánchez Márquez para optar al grado de Doctora en Ciencias Biológicas por la Universidad de Salamanca, ha sido realizada bajo mi dirección, en el Departamento de Estrés Abiótico del Instituto de Recursos Naturales y Agrobiología de Salamanca del Consejo Superior de Investigaciones Científicas (CSIC). Y para autorizar su presentación y evaluación por el tribunal correspondiente, expide y firma el presente certificado en Salamanca, a 20 de febrero de 2009. Fdo. Dr. Iñigo Zabalgogeazcoa González ÍNDICE Página 1. INTRODUCCIÓN ……………………………………………………………….. 7 1.1. Aspectos históricos de la investigación sobre hongos endofíticos …………... 10 1.2. Epichloë y Neotyphodium, los hongos endofíticos sistémicos de gramíneas .. 12 1.2.1. Ciclos de vida de Epichloë y Neotyphodium ………………………... 13 1.2.2. Efectos beneficiosos de Epichloë y Neotyphodium …………………. 16 1.2.3. Efectos perjudiciales de los endofitos en el ganado …………………. 18 1.3. Hongos endofíticos no Epichloë …………………………………………….. 19 1.3.1. Abundancia y diversidad taxonómica ………………………………... 20 1.3.2. Especificidad de tejidos ………………………………………………. 21 1.3.3. Especificidad por el hospedador ……………………………………… 22 1.3.4. Transmisión …………………………………………………………... 23 1.3.5. Tipos de interacción planta-hongo endofítico ………………………… 24 1.3.6. Interacciones mutualistas ……………………………………………… 26 1.4. Importancia del estudio de los hongos endofíticos …………………………… 28 1.5. Técnicas moleculares aplicadas a la identificación de hongos endofíticos …. 31 1.6. Las gramíneas ……………………………………………………………….. 33 1.6.1. Características generales ……………………………………………… 34 1.6.2. Distribución …………………………………………………………… 36 1.6.3. Importancia económica ……………………………………………….. 37 1.6.4. Especies de gramíneas analizadas …………………………………….. 39 1.6.4.1. Dactylis glomerata ……………………………………………….. 39 1.6.4.2. Holcus lanatus ……………………………………………………. 41 1.6.4.3. Ammophila arenaria ……………………………………………... 42 1.6.4.4. Elymus farctus ……………………………………………………. 43 2. OBJETIVOS ………………………………………………………………………. 45 3. MATERIALES Y MÉTODOS ……………………………………………………. 49 3.1. Recolección de muestras .…………………………………………………….. 51 3.2. Aislamiento de hongos .………………………………………………………. 53 3 Página 3.3. Identificación de los aislados .………………………………………………… 56 3.3.1. Morfológica .…………………………………………………………… 56 3.3.2. Molecular .……………………………………………………………... 57 3.4. Cuantificación de la diversidad fúngica .……………………………………… 60 3.4.1. Índices de diversidad .………………………………………………….. 60 3.4.2. Curvas de acumulación de especies .…………………………………... 61 3.4.3. Estimadores del número total de especies .……………………………. 63 3.4.4. Comparaciones de la micobiota entre hospedadores, tipos de tejidos y localidades .……………………………………………………………….. 65 4. RESULTADOS Y DISCUSIÓN ………………………………………………….. 67 4.1. Micobiota endofítica de Dactylis glomerata ...................................................... 69 4.1.1. Aislamiento de endofitos .……………………………………………… 69 4.1.2. Valor de las secuencias parciales para la identificación .……………… 70 4.1.3. Identificación de los aislados .………………………………………… 72 4.1.4. Abundancia y diversidad biológica .…………………………………… 81 4.1.5. Discusión .……………………………………………………………… 85 4.2. Micobiota endofítica de Holcus lanatus .…………………………………….. 91 4.2.1. Aislamiento de endofitos .……………………………………………... 91 4.2.2. Identificación de los aislados .…………………………………………. 92 4.2.3. Abundancia y diversidad biológica .…………………………………… 104 4.2.4. Comparación entre la micobiota de hojas y raíces .……………………. 105 4.2.5. Efectos geográficos en la composición de especies.……………………. 111 4.2.6. Discusión ……………………………………………………………… 113 4.3. Micobiota endofítica de Ammophila arenaria y Elymus farctus ...................... 117 4.3.1. Aislamiento de endofitos ……………………………………………… 117 4.3.2. Identificación de los aislados .…………………………………………. 118 4.3.3. Abundancia y diversidad biológica .…………………………………… 126 4.3.4. Comparación entre hospedadores .…………………………………….. 129 4.3.5. Comparación entre hojas y rizomas .…………………………………... 130 4.3.6. Efectos geográficos en la composición de especies .…………………... 132 4 Página 4.3.7. Discusión .……………………………………………………………… 136 5. DISCUSIÓN GENERAL ………………………………………………………….. 143 5.1. Patrones de diversidad biológica en la micobiota endofítica de gramíneas ….. 145 5.2. Problemas en la estimación del número total de especies endofíticas en gramíneas…………………………………………………………………………… 151 5.3. Composición taxonómica de la micobiota endofíticas .……………………… 152 5.4. Características de las especies únicas y dominantes .……………………….. 157 5.5. Especificidad de órganos .…………………………………………………… 161 5.6. Estacionalidad .……………………………………………………………… 163 5.7. Función ecológica de las especies endofíticas .………………………………. 165 6. CONCLUSIONES ………………………………………………………………… 173 7. APÉNDICE ……………………………………………………………………….. 177 8. BIBLIOGRAFÍA …………………………………………………………………. 197 9. PUBLICACIONES ……………………………………………………………….. 227 5 INTRODUCCIÓN Introducción El cultivo de gramíneas y su importancia para el ganado fue reconocido rápidamente durante el despertar de la civilización humana. No resultó complicado para aquellos primeros pueblos descubrir las ventajas que podía conferirles el hecho de domesticar unas pocas plantas y convertirse de este modo, de nómadas errantes a pueblos sedentarios. Aquella época fue el germen de la agricultura y el nacimiento de nuestros actuales cultivos de gramíneas (Figura 1). Figura 1. Campo sembrado con plantas de maíz, actualmente el cereal con mayor volumen de producción en el mundo. Esas gramíneas, y parece ser que el resto de las plantas que viven en la tierra establecen simbiosis con hongos. Estos hongos son importantes en la estructura, función, y salud de las comunidades de plantas (Giovannetti y Mosse, 1980; Petrini, 1986; Bacon y Hill, 1996; Gemma y Koske, 1997; van der Heijden et al., 1998; Clay y Holah, 1999). Además, la simbiosis con hongos contribuye, y puede ser responsable, de la adaptación de las plantas al estrés ambiental. De hecho, la mayoría, si no todas las plantas estudiadas en ecosistemas naturales, están infectadas por hongos que no causan síntomas visibles de enfermedad. Son los llamados hongos endofíticos. 9 Introducción 1.1. ASPECTOS HISTÓRICOS DE LA INVESTIGACIÓN SOBRE HONGOS ENDOFÍTICOS. Durante los últimos 30 años, el término endofito ha aparecido cada vez con más frecuencia en la literatura científica. Aunque el origen del término provenga del siglo XIX, cuando Antón de Bary lo utilizó para describir hongos que viven en el interior de las plantas (de Bary, 1866), su significado contemporáneo es diferente del original. Actualmente se usa este término para referirse a hongos capaces de infectar plantas aparentemente sanas sin causar síntomas (Large, 1940; Carroll, 1986). Es decir, en el más amplio de los sentidos, los hongos endofíticos son aquellos que colonizan tejidos vivos de plantas sin ocasionar ningún efecto negativo, inmediato o visible (Hirsch y Braun, 1992). Los primeros estudios de endofitos se realizaron en plantas de la familia de las gramíneas. A finales del siglo XIX, varios científicos europeos describieron la presencia de micelio fúngico en los carpelos y semillas de plantas sanas de Lolium arvense, Lolium linicolum, Lolium remotum y Lolium temulentum (Guerin, 1898a, 1898b; Hanausek, 1898; Nestler, 1898; Vogl, 1898; Neubauer y Remer, 1902). La cizaña (Lolium temulentum) ya era conocida como una mala hierba en cultivos de cereal en la antigüedad. Además, esta planta poseía propiedades tóxicas que con el descubrimiento de los endofitos fueron atribuídas al micelio fúngico (Font Quer, 1961). Estudios realizados por Freeman (1904) sobre el hongo endofítico de L. temulentum demostraron que este hongo se transmitía por semilla, ya que sus hifas penetraban en el embrión antes de que las semillas madurasen, y tras la germinación el hongo coordinaba su crecimiento con el de los tejidos de la planta, llegando a colonizar los meristemos laterales y después las inflorescencias. A principios de 1930 investigaciones realizadas en los Estados Unidos y Canadá demostraron la relación entre los endofitos y la toxicidad de L. temulentum para el ganado (Kingsbury, 1964). Una vez demostrada la relación, se especuló acerca de la posición taxonómica del endofito de esta gramínea. Freeman (1906), sugirió que eran Ustilaginales que habían perdido la capacidad de esporular en sus hospedadores, argumento basado en las similitudes de los ciclos de vida del endofito de L. temulentum y el del hongo patógeno Ustilago tritici en trigo; más tarde clasificó los endofitos de Lolium en el grupo de los Clavicipitales tras estudiar su transmisión. Muenscher (1939) y Kingsbury (1964) los 10 Introducción asociaron con el hongo Endoconidium temulentum, conocido por su toxicidad en semillas de plantas de L. temulentum. Sampson (1933, 1935) vio un paralelismo entre los endofitos de Lolium temulentum y Lolium perenne con algunas especies endofíticas del género Epichloë asociadas a plantas de Festuca rubra (Epichloë festucae) y Dactylis glomerata
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