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Evolution of Flowering Time in the Tetraploid Capsella Bursa-Pastoris (Brassicaceae)

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Evolution of Flowering Time in the Tetraploid Capsella Bursa-Pastoris (Brassicaceae) Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 367 Evolution of Flowering Time in the Tetraploid Capsella bursa-pastoris (Brassicaceae) TANJA SLOTTE ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6214 UPPSALA ISBN 978-91-554-7024-1 2007 urn:nbn:se:uu:diva-8311 ! " #$$" $%$$ & & & ' ( ) * ( + )( #$$"( & ! * ) ) ,-( . ( /0"( 1$ ( ( 2+ 3" 4345514"$#14( . 6 & &* & * ( 2 2 & & * * & * & ( ! * & ( . 7 & * . * & & & & & * ( & & * & * 8 & ( ) & & * * ( . 4 4& * && * * && & * ( + * 9) ,9 ) - & & * : ( ) !"!#$% ,%- & 9) &!'$()* &! ,&- * & * ( && & * & * & ; ( ) % & * & && & * ( 2 8 & & * +, - & * 8 9) . / $ / * / $ * / ) %0/ / $ 12345 / , < ) 6 + #$$" 2++ 0540#1 2+ 3" 4345514"$#14 % %%% 4 / , %== (:(= > ? % %%% 4 /- looking carefully, a shepherd’s purse is blooming under the fence Bash List of papers This thesis is based on the following papers, which are referred to by their Roman numerals: I Slotte, T., Ceplitis, A., Neuffer, B., Hurka, H., and M. Lascoux. 2006. Intrageneric phylogeny of Capsella (Brassicaceae) and the origin of the tetraploid C. bursa-pastoris based on chloroplast and nuclear DNA sequences. American Journal of Botany 93: 1714-1724 II Slotte, T., Huang, H., Lascoux, M. and A. Ceplitis. Polyploid speci- ation did not confer instant reproductive isolation in Capsella (Bras- sicaceae). (Manuscript) III Slotte, T., Holm, K., McIntyre, L. M., Lagercrantz, U. and M. Las- coux. 2007. Differential expression of genes important for adapta- tion in Capsella bursa-pastoris (Brassicaceae). Plant Physiology 145: 160-173 IV Ceplitis, A., Slotte, T., Neuffer, B., Linde, M., Kraft, T, and M. Las- coux. QTL mapping of flowering time using AFLP and candidate gene markers in the tetraploid Capsella bursa-pastoris (Brassica- ceae). (Manuscript) V Slotte, T., Huang, H., Ceplitis, A., Chen, J., and M. Lascoux. The role of introgressed alleles for flowering time variation in the tetraploid Capsella bursa-pastoris (Brassicaceae). (Manuscript) Papers I and III are reprinted with kind permission from the Botanical Soci- ety of America and the American Society for Plant Biology, respectively. Contents Introduction.....................................................................................................9 Polyploid speciation ...................................................................................9 The model system Capsella .....................................................................11 Genetic basis of flowering time variation ................................................12 Finding the genes that matter for quantitative variation...........................13 Aims .........................................................................................................16 Specific aims........................................................................................16 Results and Discussion .................................................................................17 Polyploid speciation in Capsella..............................................................17 Intrageneric phylogeny of Capsella (Paper I)......................................17 Multiple origins or introgression (Paper II).........................................20 Genetic basis of flowering time variation in C. bursa-pastoris ...............23 Differential gene expression and flowering time variation (Paper III)23 QTL mapping (Paper IV).....................................................................25 Association mapping (Paper V)...........................................................26 Conclusions...................................................................................................30 Svensk sammanfattning ................................................................................31 Acknowledgements.......................................................................................33 References.....................................................................................................34 Abbreviations AFLP Amplified fragment length polymor- phism cpDNA Chloroplast DNA FDR False discovery rate GA Gibberellic acid ka Years before present, thousands QTL Quantitative trait locus SNP Single nucleotide polymorphism Introduction “Natural selection merely modified, while redundancy created” The above quote summarizes Ohno’s (1970) view of gene duplication as a major source of evolutionary novelty. It has since become clear that gene duplication can play a role in the evolution of new gene function and in speciation. What is less well known is what role gene and genome duplica- tion plays for the evolution of quantitative traits, and whether this could pro- vide an adaptive benefit in polyploids. Up to now, studies of the genetics of quantitative traits in polyploids have mostly been confined to crops. Here, we study the genetic basis of flowering time variation and the evolutionary history of the wild tetraploid crucifer Capsella bursa-pastoris. Almost a century ago, the prominent American geneticist Shull (1929) conducted ex- tensive studies on speciation and genetic variation in C. bursa-pastoris and its relatives. The conceptual and experimental toolbox available today is very different from that available to Shull. However, our aims are similar: to carry genetic analysis “beyond the field of domesticated plants and animals into the realm of wild nature”. Polyploid speciation Polyploidization, the duplication of entire genomes, is common in flowering plants, where an estimated 47 to 70% of all species have gone through poly- ploidization at some point in their history (Masterson 1994). Polyploid spe- cies include major crops such as wheat, sugarcane, cotton and coffee, to name a few. Even species possessing “streamlined genomes” such as Arabi- dopsis thaliana exhibit signs of polyploidy in their genomes (Arabidopsis Genome Initiative 2000; Simillon et al. 2002; Bowers et al. 2003), and the number of such cryptic paleopolyploids can be expected to increase with the rapid increase in whole genome sequences. According to their mode of origin, polyploids can be classified as autopolyploids, which form by genome doubling within a single species, and allopolyploids, which form by interspecific hybridization and genome dou- bling (Ramsey and Schemske 1998). When orthologous chromosomes from different species come together in one nucleus, as in allopolyploid species, 9 these chromosomes are termed homoeologous (or homeologous), and this term can be used for genes or regions on such chromosomes as well (Fig. 1). Figure 1. Modes of polyploid formation (modified from Chen 2007). A. Autopoly- ploid formation occurs through genome doubling within a species. B. Allopolyploids form by interspecific hybridization and genome doubling. There are several ways for this to occur, e.g. by genome doubling in a first generation hybrid, by the union of unreduced (2n) gametes or by hybridization between two autopolyploids (not shown). Polyploid speciation is likely to be a predominant mode of sympatric speci- ation in plants (Otto and Whitton 2000) and can also contribute to allopatric speciation (Lynch and Conery 2000). Of all speciation processes in flower- ing plants, polyploidy has been estimated to account for 2-4% (Otto and Whitton 2000). It is less common among animals, but polyploids can still be found in many animal lineages (Otto and Whitton 2000). Unlike other speci- ation processes, polyploidization is often assumed to constitute a special form of “instant speciation” whereby the newly formed polyploid is immedi- ately and completely reproductively isolated from its progenitor species (Coyne and Orr 2004; Linder and Rieseberg 2004; Mallet 2007). This is expected to occur because hybrids between a polyploid and its ancestors have an uneven number of chromosome sets, potentially leading to meiotic non-disjunction and infertility in hybrids. However, not all hybrids are com- pletely sterile, and it has been shown that hybridization between polyploids and their ancestors can constitute a “bridge” that allows gene flow across ploidy levels (Ramsey and Schemske 1998; Petit et al. 1999; Husband 2004; Henry et al. 2005; Henry et al. 2007). Although this process can lead to shared polymorphism across ploidy levels, such observations have more often been interpreted as signs of multiple origins of the polyploid, and the consensus in the field is that most polyploids originated more than once (Soltis and Soltis 1993; 1999; 2000). Exceptions include the peanut Arachis hypogaea (Kochert et al. 1996), the salt marsh grass Spartina anglica (Ainouche et al. 2004), and Arabidopsis suecica (Jakobsson et al. 2006), all of which appear to have had a single origin. The fact that so many extant plant species are polyploids implies that ge- nome duplication may have been an important source of evolutionary nov- 10 elty, as hypothesized by Ohno (1970). Although our knowledge on the ge- netic and epigenetic changes accompanying polyploid formation is rapidly increasing (Chen 2007), the genetic basis of quantitative
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