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Ultraviolet-Absorbing Compounds in Bryophytes: Phylogeny, Ecology and Biomonitorization

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Ultraviolet-Absorbing Compounds in Bryophytes: Phylogeny, Ecology and Biomonitorization TESIS DOCTORAL Título Ultraviolet-absorbing compounds in bryophytes: phylogeny, ecology and biomonitorization Autor/es Laura Monforte López Director/es Javier Martínez Abaigar y Encarnación Núñez Olivera Facultad Facultad de Ciencias, Estudios Agroalimentarios e Informática Titulación Departamento Agricultura y Alimentación Curso Académico 2013-2014 Ultraviolet-absorbing compounds in bryophytes: phylogeny, ecology and biomonitorization, tesis doctoral de Laura Monforte López, dirigida por Javier Martínez Abaigar y Encarnación Núñez Olivera (publicada por la Universidad de La Rioja), se difunde bajo una Licencia Creative Commons Reconocimiento-NoComercial-SinObraDerivada 3.0 Unported. Permisos que vayan más allá de lo cubierto por esta licencia pueden solicitarse a los titulares del copyright. © El autor © Universidad de La Rioja, Servicio de Publicaciones, 2014 publicaciones.unirioja.es E-mail: [email protected] ྛ UNIVERSIDAD DE LA RIOJA DEPARTAMENTO DE AGRICULTURA Y ALIMENTACIÓN Ultraviolet-absorbing compounds in bryophytes: phylogeny, ecology and biomonitorization Memoria presentada por: LAURA MONFORTE LÓPEZ para optar al Grado de Doctor por la Universidad de La Rioja (Programa de Doctorado “Ecosistemas Agrícolas Sostenibles”) Fdo. LAURA MONFORTE LÓPEZ 2014 UNIVERSIDAD DE LA RIOJA DEPARTAMENTO DE AGRICULTURA Y ALIMENTACIÓN LOS DOCTORES JAVIER MARTÍNEZ ABAIGAR Y ENCARNACIÓN NÚÑEZ OLIVERA, CATEDRÁTICOS DE BOTÁNICA Y DE FISIOLOGÍA VEGETAL DE LA UNIVERSIDAD DE LA RIOJA, INFORMAN: Que la Memoria titulada “Ultraviolet-absorbing compounds in bryophytes: phylogeny, ecology and biomonitorization” ha sido realizada en las Áreas de Fisiología Vegetal y Botánica de la Universidad de La Rioja bajo nuestra dirección por LAURA MONFORTE LÓPEZ, Licenciada en Ciencias Ambientales. Considerando que se encuentra concluida, autorizamos su presentación para ser juzgada por el tribunal correspondiente. Y para que conste, expedimos el presente informe en Logroño, a 18 de Junio de dos mil catorce. Fdo. Javier Martínez Abaigar Fdo. Encarnación Núñez Olivera A mis padres INDEX Chapter 1. Introduction .......................................................................... 1 Bryophytes ........................................................................................................ 3 Ultraviolet radiation and its effects on photosynthetic organisms ....................... 5 Bryophytes and UV radiation ............................................................................ 7 UV-absorbing compounds and their use as biomonitors of UV in bryophytes . 22 Chapter 2. Objectives ............................................................................. 25 Chapter 3. Compartmentation of ultraviolet-absorbing compounds in liverworts and mosses: linking UV, phylogeny and ecology ............ 29 3.1. Abstract ................................................................................................... 31 3.2. Introduction ............................................................................................. 33 3.3. Materials and Methods ............................................................................. 36 3.4. Results and Discussion.............................................................................. 48 3.5. Conclusions ............................................................................................. 83 Chapter 4. Ultraviolet-absorbing compounds in herbarium samples of the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia and their use as a proxy in the reconstruction of past levels of UV radiation: a case study in Spain ............................................................. 85 4.1. Abstract ................................................................................................... 87 4.2. Introduction ............................................................................................. 89 4.3. Materials and Methods ............................................................................. 93 4.4. Results and Discussion ........................................................................... 105 4.5. Conclusions ........................................................................................... 126 Chapter 5. Environmental factors determining UV-absorbing compounds and physiology in the aquatic liverwort Jungermannia exsertifolia subsp. cordifolia across a wide latitudinal and altitudinal gradient ................................................................................................ 129 5.1. Abstract ................................................................................................. 131 5.2. Introduction ........................................................................................... 133 5.3. Materials and Methods ........................................................................... 138 5.4. Results and Discussion ........................................................................... 144 5.5. Conclusions ........................................................................................... 165 Chapter 6. Conclusions ....................................................................... 167 Chapter 7. References ......................................................................... 175 Chapter 8. Acknowledgements ........................................................... 189 Chapter 1 1.- INTRODUCTION Bryophytes Bryophytes are photosynthetic organisms with a diplobiontic life-cycle characterized by a marked alternation of generations in which a haploid phase gives rise, following fertilization, to a diploid phase that eventually undergoes meiosis to regenerate haploid cells. The transition from haploid to diploid generation is characterized by fusion of gametes, yielding a zygote. The reverse transition is marked by meiosis, resulting in spore formation. The gametophyte bears the sex organs and the sporophyte holds the sporangium. However, unlike tracheophytes, in which the dominant life cycle stage is the diploid sporophyte, bryophytes are characterized by dominant, perennial gametophytic stages, with relatively small, unbranched, monosporangiate sporophytes, that remain permanently attached to the maternal gametophytes. Bryophytes can be either dioecious or monoecious. In dioecious bryophytes, male and female sex organs are borne on different gametophyte plants. In monoecious bryophytes, both are borne on the same plant. Traditionally, bryophytes comprise three main lineages (Shaw & Goffinet, 2000): liverworts (Division Marchantiophyta), mosses (Bryophyta), and hornworts (Anthocerotophyta). The major bryophyte lineages differ from one another in a variety of attributes, most conspicuously in the architecture of the vegetative gametophyte body and the sporophyte. The sporophytes of many moss species do not continue to grow after spore production and are essentially annual. Liverwort sporophytes are especially short-lived and generally persist for weeks to months. The sporophytes of hornworts are potentially indeterminate in life span, but in nature they rarely persist for more than a year (Shaw et al., 2011). Bryophytes lack typical organs of vascular plants (root, stem, leaf), thick cuticle, epidermis, functional stomata, and trichomes, although exhibit a wide range of structural complexity. Attachment of a bryophyte to the substrate is by simple filaments called rhizoids. Likewise, many bryophytes have an axial structure with expansions resembling stems and leaves, but not comparable in complexity to these organs, and are called caulidia and phyllidia, respectively. 3 Introduction Liverworts have been divided according to gametophyte growth form: complex thalloids, where the thallus typically has both photosynthetic and storage tissues, with dorsal pores (not stomata); simple thalloids, that lack significant tissue differentiation; and the leafy liverworts, typically with two rows of lateral leaves and a row of ventral amphigastria (often lacking). Several smaller groups fall outside this simple classification (Crandall-Stotler, 2009). In mosses, gametophytes are always leafy. Their growth forms (orthotropic, with major axes perpendicular to the substrate, and plagiotropic, with principal axes parallel to the substrate) are associated with two major moss types. The acrocarpous mosses are characterized by sparsely or unbranched stems, grow upright and the archegonia are formed terminally on the main stems. Pleurocarpous, in contrast, have archegonia borne on short lateral branches, so that sporophytes occur laterally along the gametophyte stems. All hornworts have thalloid gametophytes that harbor endosymbiotic cyanobacteria of the genus Nostoc (Villarreal et al., 2010). Despite their relatively limited species diversity, hornworts are of particular phylogenetic interest because they appear to be the sister group to tracheophytes (Qiu et al., 2006). Bryophytes lack a fully developed vascular system for the transport of water and nutrients, which drastically limits their size. In addition, they cannot develop complex supporting or conducting tissues because, unlike tracheophytes, bryophytes always lack lignin (Popper, 2008) although can produce lignans (Ligrone et al., 2008). Physiologically, bryophytes are poikilohydrous. This characteristic represents not only a limitation but also a successful life strategy, since bryophytes combine poikilohydry with the capacity of maintaining latent life after desiccation (Oliver et al., 2005). Thus, typically, bryophytes are able to tolerate desiccation
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