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Genetic Diversity and Evolution in Lactuca L. (Asteraceae)

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Genetic Diversity and Evolution in Lactuca L. (Asteraceae) Genetic diversity and evolution in Lactuca L. (Asteraceae) from phylogeny to molecular breeding Zhen Wei Thesis committee Promotor Prof. Dr M.E. Schranz Professor of Biosystematics Wageningen University Other members Prof. Dr P.C. Struik, Wageningen University Dr N. Kilian, Free University of Berlin, Germany Dr R. van Treuren, Wageningen University Dr M.J.W. Jeuken, Wageningen University This research was conducted under the auspices of the Graduate School of Experimental Plant Sciences. Genetic diversity and evolution in Lactuca L. (Asteraceae) from phylogeny to molecular breeding Zhen Wei Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Monday 25 January 2016 at 1.30 p.m. in the Aula. Zhen Wei Genetic diversity and evolution in Lactuca L. (Asteraceae) - from phylogeny to molecular breeding, 210 pages. PhD thesis, Wageningen University, Wageningen, NL (2016) With references, with summary in Dutch and English ISBN 978-94-6257-614-8 Contents Chapter 1 General introduction 7 Chapter 2 Phylogenetic relationships within Lactuca L. (Asteraceae), including African species, based on chloroplast DNA sequence comparisons* 31 Chapter 3 Phylogenetic analysis of Lactuca L. and closely related genera (Asteraceae), using complete chloroplast genomes and nuclear rDNA sequences 99 Chapter 4 A mixed model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce* 129 Chapter 5 Allele-specific expression of Lactuca HKT1;1 genes correlates with divergence of promoter regions and whole-plant Na+/K+ homeostasis 153 Chapter 6 General discussion 187 Summary 199 Samenvatting 201 Acknowledgements 205 About the author 207 *Manuscript published Chapter 1 General introduction Zhen Wei Biosystematics Group, Wageningen University and Research Centre, 6708 PB Wageningen, The Netherlands Chapter 1 Lettuce (Lactuca sativa L.) is an economically important vegetable crop. The total value of world lettuce sales in 2007 was US $1,934,983,000. The world production of lettuce and the related chicory (Cichorium intybus) has been increasing yearly and the total yield reached 23,733,803 metric tons in 2009 (U.S.D.A. 2011). The edible parts of domesticated lettuce include the leaves and/or stems and are usually consumed as fresh or cooked products. Due to its economic importance, most current studies of the genus Lactuca have focused on lettuce cultivars and the species that can be easily crossed to domesticated lettuce (Koopman et al. 1998; Zohary 1991), including studies of phylogeny and trait breeding. However, the broader phylogenetic relationships of domesticated lettuce and wild lettuce species remain unclear, including the taxonomic boundary of the genus Lactuca L. itself. In lettuce breeding, quantitative trait loci (QTLs) related to biotic (Christopoulou et al. 2015; Jeuken et al. 2008; Simko et al. 2013; Simko et al. 2009) and abiotic stresses have been identified (Hartman et al. 2014; Jenni et al. 2013a; Uwimana et al. 2012a), providing the possibilities to improve the tolerance of lettuce to different stresses. In this thesis, I will provide the most extensive phylogenetic reconstruction of Lactuca domesticated and wild species, based on chloroplast genes, genome and nuclear DNA (Internal Transcribe Spacer, ITS) sequences. A QTL analysis of the responses to salinity in a recombinant inbred line population, derived from a cross between cultivated lettuce (L. sativa ‘Salinas’) and wild lettuce (L. serriola), will also be presented and the potential candidate gene associated with salinity stress will be tested. Therefore, in this introduction, I will provide an overview of lettuce cultivars and uses, its hypothesized domestication history, the taxonomic position of the genus Lactuca, the current status of lettuce molecular breeding and mechanisms of salinity tolerance in plants, especially the High-affinity K+ Transporter (HKT) gene family. Overview of domesticated lettuce According to different leaf shape and size, degree of rosette and head formation and less so on colour, stem type and other traits, lettuce cultivars have been classified into seven types: Butterhead, Crisphead, Cos, Cutting, Stalk, Latin, and Oilseed (De Vries and Van Raamsdonk 1994; Křístková et al. 2008; Ryder 1999; Vries 1997). Butterhead lettuce is a head type lettuce with soft and tender broad leaves, originating from Europe. Crisphead lettuce with a large firm head has two subtypes: the iceberg subtype, larger in weight and volume with a dense head, the Batavia subtype, smaller with a less dense head (Ryder 1999; Vries 1997). Cos lettuce has an erect, elongated or loaf-shaped head, with a predominant midrib running almost to the apex (Lindqvist 1960b). The leaf colour ranges from yellowish to dark green (Lebeda et al. 2007; Ryder 1999). Cutting lettuce normally doesn’t form a head or have an enclosure stage. The leaves vary in leaf margin (entire, frilled), shapes (broad, elongated, lobed, curled), sizes, texture (crisp, soft), and colours (red, green; dark, light) (Křístková et al. 2008; Lebeda et al. 2007; Ryder 1999). The stalk lettuce has a thick elongated stalk and narrow leaves. The stalk is tender and consumed raw in Egypt and cooked in China (Lindqvist 8 General introduction 1960b). There are two stalk lettuce types: one type is represented by the Chinese cultivars with light grey leaves and the leaves can be as broad as Cos type. The other type has long lanceolate leaves with pointed apex (Lindqvist 1960b). Latin, or grassé, lettuce forms a loose head and has thick leathery leaves of dark green colour. It is of European origin, but also grown around the Mediterranean including North Africa, in South America and on small areas in the U.S. (Křístková et al. 2008; Rodenburg 1960). Oilseed lettuce is a primitive type of L. sativa with larger seeds than those of other lettuces. The seeds are crushed to produce oil for cooking. This group has not yet been fully domesticated (Boukema 1990; Křístková et al. 2008; Lebeda et al. 2007; Ryder 1999; Ryder 1986). Different regions and countries produce different types of lettuce cultivars. Butterhead and Crisphead lettuces are overwhelmingly popular in the United States, the United Kingdom, France, the Netherlands, Belgium, Germany and other European countries (Ryder 1999; Vries 1997). Cos lettuce came from the Greek island Cos (Kos) (Helm 1954) and remains popular in the Mediterranean Basin, northern Africa, southwest Asia, and southern Europe (Lebeda et al. 2007; Ryder 1999). The Greeks and Romans cultivated cutting lettuce (Křístková et al. 2008). More recently, Cos and Cutting lettuces have been increasingly used in the U.S. and in other countries (Lebeda et al. 2007; Vries 1997). Stalk lettuce is found in Egypt and Middle Eastern countries, and is also very common in China and India (Ryder 1999; Vries 1997). The ancient practice of making oil from Oilseed lettuce has continued to the present time in Egypt (Ryder 1999). In ancient Egypt, lettuce was considered as an aphrodisiac and played an important role in the yearly festival of Min, God of fertility and procreation. A long-leafed lettuce type was depicted on walls of Egyptian tombs (Harlan 1986). Lindqvist (1960b) referred some primitive forms of L. sativa in Egypt and considered them as in a semi-wild state, rather than cultivated. Whitaker (1969) concluded that the ancestors of cultivated lettuce is indigenous to the eastern Mediterranean Basin, probably Egypt. Zeven & De Wet (1982) mentioned part of the European-Siberian region (the Middle East) as the primary centre of origin of L. sativa. Rulkens (1987) presumed cultivated lettuce originated in the Kurdistan-Mesopotamia area instead of in Egypt. Boukema et al. (1990) indicated that the domestication of lettuce happened in South-West Asia in the region between Egypt and Iran. De Vries (1997) deemed that the cultivated lettuces originated in South-West Asia, from the area around the Euphrates and Tigris rivers. In his point of view, there were two main reasons: 1. the highest number of related wild species can be found between the Euphrates and Tigris rivers, whereas only one related wild species - L. serriola is found in the Nile Valley. 2. Cereal-growing cultures in Kurdistan-Mesopotamia were known long before the first known Egyptian-grown cereals (Rulkens 1987), indicating a more ancient origin of agriculture. Taxonomic position of Lactuca 9 Chapter 1 The Mediterranean basin, South-Western Asia and Africa comprise centres of diversity of wild Lactuca species and can be considered as hot-spots for lettuce conservation (Lebeda et al. 2008; Lebeda et al. 2004; Lebeda et al. 2009). Lactuca species are distributed in temperate and warm regions of the northern hemisphere (Europe, Asia, Indonesia, North and Central America, Africa) (Feráková and Májovský 1977; Lebeda et al. 2004). Most of them are xerophytes except for some scandent, liana-like endemic species in the central African mountains (Stebbins 1937). Taxonomic and phylogenetic analyses place the genus Lactuca in the subtribe Lactucinae, tribe Lactuceae (Cichorieae), subfamily Cichorioideae of the family Asteraceae (Compositae) (Judd et al. 2007; Kadereit and Jeffrey 2007). This genus was established by Linné in 1753 (Linné 1753). However, since it was first proposed, the circumscription and delimitation of Lactuca has remained obscure,
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