The Cyanobacterial: Cycad Symbiosis

Abstract

THE CYANOBACTERJAL- CYCAD SYMBIOSIS P. Lindblad and J.-L. Costa P Lindblad (corresponding author, e-mailpeterlindblad@ ebc uu se) and J -L Costa,Department of Physiological Botany, Evolutionary Biology Centre, Uppsala University, Villavagen 6, SE-752 36 Uppsala, Sweden INTRODUCTION Cycads are an ancient group of gymnosperms occurring naturally in tropical and subtropical re gions. They have a unique capacity to form symbi otic associations with heterocystous cyanobacteria (Nostoc) within apogeotropical coralloid roots This is the only example of a symbiosis between a gymnosperm and a nitrogen-fixing organism In this paper we present an overview of the location, establishment, charactenstics and specificity of the symbioses, aswell as information on the transfer of metabolites between the two partners. Cycads first appeared in the Pennsylvanian pernod and have existed for approximately 300 million years. Nearly 100 million years ago, cycads had a wide geographical distribution, extending from Alaska and Siberia to the Antarctic Today they are found on every continent except Europe and Antarctica but are restricted to small popula tions in the tropics and subtropics of both henm spheres. Moreover, many are facing possible extinction in nature The approximately 160 spe cies of cycads are distributed in three familles Cycadaceae, with a single genus, Cycas; Stangerl aceae, with two genera, Stangeria and Bowenia, and Zamiaceae, with eight genera, Ceratozamia, Chigua, Dioon, Encephalartos, Lepidozamia, Macrozamia, Microcycas and Zamia Cycads are mostly terrestrial and arborescent, except for at least one species (Zamia pseudoparasitica Yates), which is truly epi phytic, and can grow in a number of different habitats. Some species may be found in forests (both rainforest and seasonally dry forest), and others grow in open stands in grasslands Struc turally, cycads have a stem, normally columnar and woody, with the exception of Zamia pygmaea Sims ,which has a subterranean stem The aerial stem, which may be branched, is covered by persistent leaf bases In general, the vegetative shoots of cycads produce two types of leaves: scale leaves (called cataphylls) and foliage leaves The leaves are born terminally and are mainly pinnate, with the exception of the genus Bowenia, which has bipinnate leaves. Reproductively, cycads are dioecious, producing either pollen-bearing or ovule-beanng modified leaves called sporophylls The ovules, like those of true gymnosperms, are naked Cycads produce three types of root (1) a taproot equivalent to the primary root system found inmost plants (restricted to the genus Cycas, it is adventitious, arises from the lower side of trunk offsets and grows downwards close to the trunk); (ni) lateral roots, and (1ii) highly speciallsed lateral roots usually termed 'corallold roots' WHERE ARE THE SYMBIOTIC CYANOBACTERIA LOCATED? Corallold roots have been known to exist for a long time and have been recorded in all genera and all cycad species examined The ability to form this type of root is encoded by genes in the cycad, and the roots are formed before being invaded by symbiotic cyanobacterna Instead of themore com mon downward growth pattern, these roots show a marked negative geotropism and grow laterally and upwards toward the surface of the soil In seedlings of Macrozamia, the process of corallold root development begins with the initiation of paplllose roots called 'pre-corallold'. The first 'pre corallold' roots are adventitious and emerge from the hypocotyl immediately under the cotyledonary petioles Their subsequent development involves phases of maturation, cyanobactenal invasion, corallold formation, senescence and regeneration. When they are infected, the cyanobacteria are present in a specific cortical layer inside the root (the cyanobacterial zone) The presence of cyanobacteria inside the root induces irreversible modifications to the growth and development of the root The growth in length of these roots is much retarded compared with normal roots of the same age, but growth in diameter increases notice ably. Furthermore, the cells in the cyanobactenal zone undergo marked differentiation and elongate radially to connect the two adjacent cortical layers It has been suggested that these elongated cells are speciallsed cells responsible for the transfer of metabolhtes between the partners (Lindblad et al 1991; Pate et at 1988; Costa et a[ 1999, Adams 2000). ESTABLISHMENT OF THE SYMBIOSIS The process of infection is still unclear Invasion may occur at any stage of development of the root, but...