Karyotype Evolution in Apomictic Boechera and the Origin of the Aberrant Chromosomes
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The Plant Journal (2015) 82, 785–793 doi: 10.1111/tpj.12849 Karyotype evolution in apomictic Boechera and the origin of the aberrant chromosomes Terezie Mandakov a1, M. Eric Schranz2, Timothy F. Sharbel3, Hans de Jong4 and Martin A. Lysak1,* 1CEITEC – Central European Institute of Technology, Masaryk University, Brno, CZ-62500 Czech Republic, 2Plant Systematics Group, Wageningen University (WU), Droevendaalsesteeg 1, Wageningen, 6708 PB The Netherlands, 3Apomixis Research Group, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, D-06466 Germany, and 4Laboratory of Genetics, Wageningen UR PSG, P.O. Box 16, Wageningen, 6700 AA The Netherlands Received 17 February 2015; revised 24 March 2015; accepted 1 April 2015; published online 10 April 2015. *For correspondence (e-mail [email protected]). SUMMARY Chromosome rearrangements may result in both decrease and increase of chromosome numbers. Here we have used comparative chromosome painting (CCP) to reconstruct the pathways of descending and ascend- ing dysploidy in the genus Boechera (tribe Boechereae, Brassicaceae). We describe the origin and structure of three Boechera genomes and establish the origin of the previously described aberrant Het and Del chro- mosomes found in Boechera apomicts with euploid (2n = 14) and aneuploid (2n = 15) chromosome number. CCP analysis allowed us to reconstruct the origin of seven chromosomes in sexual B. stricta and apomictic B. divaricarpa from the ancestral karyotype (n = 8) of Brassicaceae lineage I. Whereas three chromosomes (BS4, BS6, and BS7) retained their ancestral structure, five chromosomes were reshuffled by reciprocal translocations to form chromosomes BS1-BS3 and BS5. The reduction of the chromosome number (from x = 8tox= 7) was accomplished through the inactivation of a paleocentromere on chromosome BS5. In apomictic 2n = 14 plants, CCP identifies the largely heterochromatic chromosome (Het) being one of the BS1 homologues with the expansion of pericentromeric heterochromatin. In apomictic B. polyantha (2n = 15), the Het has undergone a centric fission resulting in two smaller chromosomes – the submeta- centric Het0 and telocentric Del. Here we show that new chromosomes can be formed by a centric fission and can be fixed in populations due to the apomictic mode of reproduction. Keywords: Boechera, Brassicaceae, apomixis, chromosome fission, karyotype evolution, heterochromatin, centromere inactivation. INTRODUCTION The genus Boechera (Bocher’s€ rock cress, formerly Arabis, as geographically and genetically distinct populations Brassicaceae) is a member of the tribe Boechereae (127 (Sharbel and Mitchell-Olds, 2001; Sharbel et al., 2005). species in nine genera, Al-Shehbaz, 2012) distributed The genus Boechera is an ideal model system to com- throughout North America and Greenland (Koch et al., pare sexual and apomictic reproduction and associated life 1999, 2003; Kiefer et al., 2009). The genus with 110 species history traits, as it is characterized by naturally-occurring is monophyletic (Alexander et al., 2013), has a basic chro- diploid sexual and diploid apomictic forms (Bocher,€ 1951; mosome number x = 7 (Koch et al., 1999), and is character- Aliyu et al., 2010; Rushworth et al., 2011). Using high ized by diploid sexual (2n = 2x = 14), as well as diploid, throughput seed screening methods, in conjunction with aneuploid, and mostly triploid (2n = 3x = 21) apomictic custom-made high-density microarrays for tissue-targeted forms (Bocher,€ 1951; Schranz et al., 2005; Alexander et al., expression analyses, a single candidate factor each for 2015). Extensive morphological variations and correspond- meiotically unreduced egg (APOLLO; Corral et al., 2013) ing problematic taxonomy of the genus are due to rampant and pollen (UPGRADE-2; Mau et al., 2013) production hybridization among diploid species resulting in the origin in apomictic Boechera have been identified. More than of apomictic diploid and aneuploid hybrids. Triploids have 95% of seeds produced by diploid apomictic Boechera are arisen multiple times through hybridization between sex- characterized by a diploid embryo (100% maternally ual and apomictic diploid species (Alexander et al., 2015) derived) and a hexaploid endosperm (four maternal ge- © 2015 The Authors 785 The Plant Journal © 2015 John Wiley & Sons Ltd 786 Terezie Mandakov a et al. nomes and two paternal genomes); less frequent are seeds bidopsis lyrata (Hu et al., 2011) and Capsella rubella with a diploid embryo and a pentaploid endosperm (Aliyu (Slotte et al., 2013). Results of comparative genetic map- et al., 2010). In plants producing seeds with a hexaploid ping and chromosome painting analyses in crucifer spe- endosperm, it is hypothesized that both maternal and cies have been integrated to establish a set of 24 parental factors are required in order to stabilize apomixis conserved genomic blocks (GBs) building up eight chro- through the combined effects of producing a meiotically mosomes of the Ancestral Crucifer Karyotype (ACK; Sch- unreduced ovule with balanced (2 maternal:1 paternal) ranz et al., 2006a). These GBs have been used as the endosperm formation. Recent data on these candidates basis to elucidate chromosome rearrangements associ- have demonstrated that both factors are highly correlated ated with descending dysploidies (reductions of chromo- in apomictic Boechera from genetically (i.e. different taxa) some number) across the Brassicaceae. For the and geographically (i.e. 1000s of kms) divergent genotypes Boechereae, Schranz et al. (2007) created a comparative (Mau et al., 2015). genetic map of the diploid sexual B. stricta and outlined Apomictic Boechera plants with 15 chromosomes were a tentative scenario of its evolution from the ACK. How- already described as early as 1951 in the elaborate study of ever, as the centromeres were only tentatively mapped Tyge Bocher€ (Bocher,€ 1951), the cytologist whose name onto Boechera chromosomes, neither the exact nature of was later given to the genus. Later studies investigated the chromosome rearrangements can be attained, nor it can nature of supernumerary chromosomes in aneuploid dip- be concluded if the genome of B. stricta is likely to repre- loid (2n = 15) and triploid (2n = 22) apomicts more closely sent an ancestral genome of the genus. (Sharbel et al., 2004, 2005). But the findings from those In this paper, we used comparative chromosome paint- studies failed to explain the nature and the origin of the ing (CCP) with A. thaliana chromosome-specific BAC con- additional, B-like chromosomes. Sharbel et al. (2004, 2005) tigs representing 24 GBs of the ACK to resolve several described the chromosomes as being heterochromatic, questions about genome evolution in the genus Boecher- often smaller than all the remaining chromosomes and of a. First, we used CCP to verify and specify the order and a different length in different populations. As these chro- orientation of the GBs in B. stricta identified in our initial mosomes were absent in the sexual diploids and present F2 genetic mapping, and characterize chromosome in the diploid (2n = 15) and triploid (2n = 22) apomictic cy- regions, such as the centromeres and chromosome BS1, totypes it was argued that the chromosomes may contain not resolved by genetic mapping due to a lack of recom- genetic elements associated with the apomictic trait (Shar- bination (Schranz et al., 2007). Second, in comparison bel et al., 2005; Lovell et al., 2013). Comparative analyses with the ACK, we reconstructed the origin of the seven of the mitotic and meiotic cell complements of the sexual chromosomes in B. stricta and B. divaricarpa from the and apomictic accessions demonstrated that all diploid eight ancestral chromosomes. Third, in the apomictic dip- apomicts have a variable and highly heterochromatic (Het) loid B. divaricarpa (2n = 14) and the aneuploid apomictic chromosome with pericentromeric heterochromatin B. polyantha (2n = 15) we elucidated the origin of aber- repeats from Boechera stricta, which suggests that this rant chromosomes that have previously been referred to chromosome originated from this species. An additional as the Het and Del chromosomes (Kantama et al., 2007). smaller chromosome, referred to as Del (as presumed a The results of this study will contribute to better under- deletion chromosome), was found in the 2n = 15 and standing of chromosome fissions in plants and may pro- 2n = 22 apomicts (Kantama et al., 2007). Whereas GISH vide an invaluable comparative framework needed for (genomic in situ hybridization) in diploid as well as aneu- high-quality genome assemblies in sequenced Boechera ploid apomicts revealed the hybrid origin of these ge- species. nomes, the nature of Het and Del chromosomes was not explained (Kantama et al., 2007). RESULTS The tribe Boechereae is one of the 49 well defined CCP analysis confirms close phylogenomic relationship monophyletic tribes in Brassicaceae (Al-Shehbaz, 2012). between the ACK n = 8 and the n = 7 Boechera genome The Boechereae along with tribes Cardamineae, Desc- urainieae, Halimolobeae, Lepidieae, Microlepidieae, Phys- Based on the published genetic map of B. stricta (Schranz arieae, Smelowskieae, and the paraphyletic Camelineae et al., 2007) we have designed BAC painting probes to ver- form one of the three major crucifer lineages – lineage I ify the position and orientation of all 24 GBs on the seven (Franzke et al., 2011; Al-Shehbaz, 2012; Heenan et al., chromosomes of B. stricta (accessions ES06) and B. divari- 2012).