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Phylogeny, Detection, and Mating Behaviour of Mycosphaerella Spp

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Phylogeny, Detection, and Mating Behaviour of Mycosphaerella Spp Phylogeny, detection, and mating behaviour of Mycosphaerella spp. occurring on banana Mahdi Arzanlou Promotoren: Prof. dr. P.W. Crous Hoogleraar in de Evolutionaire Fytopathologie Wageningen Universiteit Prof. dr. ir. P.J.G.M. de Wit Hoogleraar in de Fytopathologie Wageningen Universiteit Co-promotoren: Dr. L.-H. Zwiers Onderzoeker, CBS Fungal Biodiversity Centre Dr. ir. G.H.J. Kema Senior onderzoeker, Plant Research International Promotiecommissie Prof. dr. R.F. Hoekstra (Wageningen Universiteit) Prof. dr. H.A.B. Wösten (Utrecht Universiteit) Dr. F.T. Bakker (Wageningen Universiteit) Dr. ir. A.J. Termorshuizen (Blgg, Wageningen) Dit onderzoek is uitgevoerd binnen de onderzoekschool Experimental Plant Sciences Phylogeny, detection, and mating behaviour of Mycosphaerella spp. occurring on banana Mahdi Arzanlou Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof. dr. M.J. Kropff in het openbaar te verdedigen op woensdag 28 mei 2008 des voormiddags te 11:00 in de Aula Mahdi Arzanlou (2008) Phylogeny, detection, and mating behaviour of Mycosphaerella spp. occurring on banana PhD thesis Wageningen University, The Netherlands With summaries in English and Dutch ISBN 978-90-8504-800-8 To my Father, Mother and my brothers, Mohammad and Mohsen “In generosity and helping others be like a river In compassion and grace be like the sun In concealing other’s faults be like a night In anger and fury be like the dead In modesty and humility be like the earth In tolerance be like a sea Either exist as you are or be as you look” Mevlana Jalaluddin Rumi (1207- 1273) CONTENTS Chapter 1 General introduction 9 Chapter 2 Multiple gene genealogies and phenotypic characters differentiate several novel species of Mycosphaerella and related anamorphs on banana 23 Chapter 3 Molecular diagnostics in the Sigatoka disease complex of banana 55 Chapter 4 Phylogenetic and morphotaxonomic revision of Ramichloridium and allied genera 71 Chapter 5 Evolution of heterothallism in three major Mycosphaerella species associated with the Sigatoka disease complex of banana 129 Chapter 6 General discussion 151 Appendix Summary in English 162 Samenvatting (Summary in Dutch) 163 Acknowledgements 164 About the Author 167 List of Publications 168 Education Certificate of the EPS Graduate School 170 CHAPTER 1 GENERAL INTRODUCTION 9 Chapter 1 Speciation AND SPECIES RECOGNITION IN FUNGI Evolution is the consequence of mutation, selection, and intraspecies or interspecies gene flow between populations. Speciation can be considered the ultimate outcome of evolutionary forces, and is defined as the splitting of an existing species into two or several new taxa, or even replacing the old species by a new one. New species emerge from ancestral species when genetic differences have accumulated among subpopulations at a level that prevent them from reproducing successfully (Zhan et al. 2002, Kohn 2005). The two main mechanisms of speciation are classified as allopatric or sympatric. In allopatric speciation the geographical isolation of populations is the main driving force for the emergence of new species. This is the main mechanism for speciation in macro-biota. Sympatric speciation involves accumulation of genetic polymorphisms within a population of a given species and is the most common mechanism among micro-biota. Evolutionary changes, which may ultimately lead to speciation among eukaryotic micro- organisms like fungi occur either by routine or by episodic selection. Routine selection is defined as the sum of selection factors, which favours the maintenance of a stable population structure over time (Brasier 1995, 2000). Populations with (i) sexual reproduction, (ii) highly polymorphic vegetative compatibility loci and (iii) many variable structural characters are considered to be subject to routine selection (Brasier 1995, 2000, McDonald et al. 2002). Episodic selection is defined as any sudden environmental disturbance that is likely to lead to a significant alteration in the population of a species; it presumably acts as a cause of sudden evolutionary developments in fungi (Brasier 1995). Disturbances, such as changes in availability of resources, exposure to a new host, arrival of a new competitor, and geographical transposition are considered as likely causes of episodic selection (Brasier 1995, 2000, Newcombe et al. 2000, 2001). There are two major routes along which episodic selection might occur among fungi. The first involves selection based on strong differences in fitness, the second involves build-up of increased variation based by interspecific hybridisation or horizontal gene transfer. Typical characteristics such as small sizes, simple structures, diverse life styles, short generation times, frequent occurrence of haploidy and asexual reproduction, anastomosis, and inter-species mycelial interactions, make fungi particularly suitable to study their microevolution (Brasier 1995). This holds also for species within the genus Mycosphaerella. Moreover, multiple species of the genus Mycosphaerella commonly co-occur on a single host (Crous et al. 2004, Chapter 2, this thesis). The goal of biological systematics is to recognise and describe natural groups of organisms at species and higher levels. Species recognition and determination of boundaries in fungal taxonomy are crucial in order to group as many as 1.5 million fungal species (Hawksworth 1991, 2001), of which we assume that less than 10 percent have been described. Currently, there are several theoretical and operational species concepts (Mayden 1997). While theoretical species concepts are not helpful in species recognition or diagnosis, operational species concepts have both diagnostic and recognition values (Taylor et al. 2000). The main theoretical species concept is the Evolutionary Species Concept (ESC) and is defined as “…a single lineage of ancestor-descendent populations which maintains its identity from other such lineages and which has its own evolutionary fate” (Wiley 1978, Taylor et al. 2000). ESC by itself represents not a recognition criterion, and as such cannot be used for species recognition. Morphological Species Concept (MSC), Biological Species Concept (BSC) and Phylogenetic Species Concept (PSC) represent the more commonly used operational species concepts. All three are compatible with the ESC, as each one tries to define evolutionary species (Mayden 1997). The terms ‘species concept’ and ‘species recognition’ have often been used as equivalent to the theoretical 10 General introduction and outline of thesis and operational species concepts, respectively (Taylor et al. 2000). Defining morphologically distinct units is the basis for MSR (Seifert 1993, Taylor et al. 2000). The foundation for BSR is interbreeding populations, which are reproductively isolated from other groups, regardless of the absence of morphological differences (Taylor et al. 2000). PSR uses DNA sequence data to build a ‘relationship tree’ of organisms. With fungi, PSR recognises species as “… the smallest aggregation of populations with a common lineage that shares unique, diagnosable phenotypic characters” (Harrington & Rizzo 1999). Evolution is an ongoing process and it is impossible to recognise the moment that individuals in an ancestral species have splitted into progeny, using the methods of species recognition, because time is needed for changes in morphology, mating behaviour and gene sequences to occur. PSR performs more consistent with ESC than MSR and BSR, because development of a new evolutionary species out of an ancestor requires changes in gene sequences to occur before the resulting morphological traits (Taylor et al. 2000). However, it is unclear how to draw a limit for species boundaries when a gene is polymorphic within the species, or fixed for alternative alleles in more than one species. This can be avoided by applying concordance of more than one gene genealogy (Taylor et al. 2000). To avoid subjectivity, the Genealogical Concordance Phylogenetic Species Recognition (GCPSR) model was proposed, which defines a species as “a basal, exclusive group of organisms all of whose genes coalesce more recently with each other than with those of any organism outside the group, and that contains no exclusive group within it” (Baum & Donoghue, 1995, Taylor et al. 2000). When conflict occurs among lineages, the transition from concordance to conflict determines the limits of species (Taylor et al. 2000). Sequence data from various protein-coding and non-coding genes have been applied to assess levels of phylogenetic relationship among different groups of fungi. Sequence analysis of 28S nrDNA and 18S nrDNA is routinely used to resolve higher- order phylogenetic relationships within the fungal kingdom. Internal transcribed spacer (ITS) areas of the rDNA operon and housekeeping genes like the actin, translation elongation factor 1-α, β-tubulin and histone H3 genes are routinely applied to resolve phylogenetic relationships among species (Crous et al. 2001, 2004, 2006, Banke et al. 2004, Verkley & Starink-Willemse 2004, Feau et al. 2006). MYCOSPHAERELLA, A GENUS OF SUCCESSFUL PLANT pathogens The genus Mycosphaerella The genus Mycosphaerella belongs to the Mycosphaerellaceae (Capnodiales, Dothideomyce- tidae) (Schoch et al. 2006) and is one of the largest genera of ascomycetes, comprising several thousands of species (Crous 1998, Crous et al. 2001, Aptroot 2006). Species in this genus have a wide range of lifestyles, ranging from saprobes, plant
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