Analysis of plant diversity with retrotransposon-based molecular markers

Heredity (2011) 106, 520–530 & 2011 Macmillan Publishers Limited All rights reserved 0018-067X/11 REVIEW www.nature.com/hdy Analysis of plant diversity with retrotransposon-based molecular markers R Kalendar1, AJ Flavell2, THN Ellis3, T Sjakste4, C Moisy1 and AH Schulman1,5 MTT/BI Plant Genomics Laboratory, Institute of Biotechnology, University of Helsinki, Helsinki, Finland; 2Division of Plant Sciences, University of Dundee at SCRI, Dundee, UK; 3John Innes Centre, Colney Lane, Norwich, UK; 4Genomics and Bioinformatics Laboratory, Institute of Biology of the University of Latvia, Salaspils, Latvia and 5Biotechnology and Food Research, MTT Agrifood Research Finland, Jokioinen, Finland 1 Retrotransposons are both major generators of genetic diversity and tools for detecting the genomic changes associated with their activity because they create large and stable insertions in the genome. After the demonstration that retrotransposons are ubiquitous, active and abundant in plant genomes, various marker systems were developed to exploit polymorphisms in retrotransposon insertion patterns. These have found applications ranging from the mapping of genes responsible for particular traits and the management of backcrossing programs to analysis of population structure and diversity of wild species. This review provides an insight into the spectrum of retrotransposon-based marker systems developed for plant species and evaluates the contributions of retrotransposon markers to the analysis of population diversity in plants. Heredity (2011) 106, 520–530; doi:10.1038/hdy.2010.93; published online 4 August 2010 Keywords: molecular marker; phylogeny; retrotransposon; IRAP and REMAP; SSAP; RBIP Introduction Markers have a key role in the study of genetic variability and diversity, in the construction of linkage maps and in the tracking of individuals or lines carrying particular genes. The emergence of marker systems has closely followed developments in biochemistry and molecular biology for the past 40 years (Hubby and Lewontin, 1966). The shortcomings of biochemically derived markers, such as isozymes, drove the development of markers based on DNA polymorphisms (Kan and Dozy, 1978). A DNA molecular marker in essence detects nucleotide sequence variation at a particular location in the genome. The variation must be found between the parents of the chosen cross for the marker to be informative among their offspring and to allow its pattern of inheritance to be analyzed. DNA markers can generate ‘fingerprints,’ which are distinctive patterns of DNA fragments resolved by electrophoresis and detected by staining or labeling. The advent of the PCR was a breakthrough for molecular marker technologies, and made possible many fingerprinting methods. These fall into two broad categories, namely methods that detect single loci and multiplex methods that detect multiple loci simultaneously. The first multiplex methods to be developed were named randomly amplified polymorphic DNA (Williams et al., 1990; Welsh and McClelland, 1990) and DNA Correspondence: Professor AH Schulman, MTT/BI Plant Genomics Laboratory, Institute of Biotechnology, University of Helsinki, PO Box 65, Viikinkaari 1, Helsinki, FIN-00014, Finland. E-mail: Received 25 February 2010; revised 26 May 2010; accepted 8 June 2010; published online 4 August 2010 amplification fingerprinting (Caetano-Anollés et al., 1991), respectively, and involve amplification of random repetitious sites in the genome using short primers, typically 8–12 nt in length. The approaches involve quick and easy reaction set-up and no genome sequence information is needed to design the primers. However, problems in reproducibility due to the presence of many potential priming sites in the genome and the low annealing temperatures in the reactions, because of the nature of the primers themselves, have led to the disappearance of these systems from the molecular marker toolkit today. The amplified fragment length polymorphism (AFLP) method, introduced in the mid1990s, also generates anonymous markers. It detects restriction sites by amplifying a subset of all the sites for a given enzyme pair in the genome by PCR between ligated adapters (Vos et al., 1995). Interspersed repetitive sequences comprise a large fraction of the genome of many eukaryotic organisms and they predominantly consist of transposable elements (TEs). It is therefore not surprising that many DNA marker techniques that are based on these repeats have been devised. In an early example, restriction fragment length polymorphism (RFLP) probes derived from repetitive sequences were hybridized to Southern blots of restriction-digested genomic DNA to produce a highly variable pattern (Lee et al., 1990). The RFLP technique was used extensively in the past, but has been replaced by PCR-based methods because of the slowness of Southern blotting. Nucleotide sequences matching repetitive sequences showing polymorphism in RFLP analyses have also been used as PCR primers for the inter-repeat amplification polymorphism marker method (Meyer et al., 1993; Salimath et al., 1995). Such repetitive sequences include Diversity analysis with retrotransposon markers R Kalendar et al 521 microsatellites, such as (TG)n or (AC)n, which are distributed throughout the genome. A derived approach was developed to generate PCR markers based on amplification of microsatellites near the 30 end of the Alu (short interspersed repetitive element (SINE)) TEs, called Alu-PCR or SINE-PCR (Chariieu et al., 1992). TEs are divided into two major classes. Class II transposons, which were first discovered by McClintock (1984), move by a cut-and-paste mechanism as doublestranded DNA. In contrast, Class I retrotransposons transpose through an RNA intermediate, and hence the original copy remains in the genome (Finnegan, 1989). Retrotransposons are separated into two major subclasses that differ in their structure and transposition cycle. These are the long terminal repeat (LTR) retrotransposons and the non-LTR retrotransposons (LINE and SINE elements), which are distinguished by the respective presence or absence of LTRs) at their ends. All groups are complemented by their respective nonautonomous forms that lack one or more of the genes essential for transposition: MITEs (miniature invertedrepeat terminal elements) for class II, SINEs for non-LTR retrotransposons and TRIMs (terminal-repeat retrotransposons in miniature) and LARDs (large retrotransposon derivatives) for LTR retrotransposons. transposons are dispersed throughout the genome, at least in the cereals and citrus they are often locally nested one into another and in extensive domains that have been referred to as ‘retrotransposon seas’ surrounding gene islands (SanMiguel et al., 1996; Shirasu et al., 2000; Ramakrishna et al., 2002; Bernet and Asins, 2004; Gu et al., 2004; Kong et al., 2004; Sabot et al., 2005). Bertioli et al. (2009) have shown that retrotransposo (...truncated)