Brassicales: an Update on Chromosomal Evolution and Ancient Polyploidy
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Plant Systematics and Evolution (2018) 304:757–762 https://doi.org/10.1007/s00606-018-1507-2 ORIGINAL ARTICLE Brassicales: an update on chromosomal evolution and ancient polyploidy Martin A. Lysak1 Received: 24 January 2018 / Accepted: 5 March 2018 / Published online: 7 April 2018 © Springer-Verlag GmbH Austria, part of Springer Nature 2018 Abstract Brassicales comprise 17 families, c. 400 genera and more than 4600 species. Despite the mustard family (crucifers, Bras- sicaceae) continuing to be the subject of intensive research, the remaining 16 families are largely under studied. Here I sum- marize the available data on chromosome number and genome size variation across Brassicales in the context of a robust phylogenetic framework. This analysis has revealed extensive knowledge gaps in karyological data for non-crucifer and species-rich families in particular (i.e., Capparaceae, Cleomaceae, Resedaceae and Tropaeolaceae). A parsimonious inter- pretation of the combined chromosomal and phylogenetic data set suggests that the ancestral pre-Brassicales genome had 9 or 14 chromosome pairs, later multiplied by the At-β (beta) whole-genome duplication (WGD) to n = 18 or 28. This WGD was followed by post-polyploid diploidization marked by diversifcation to 12 or 13 families and independent decreases in chromosome numbers. Family-specifc WGDs are proposed to precede the diversifcation of Capparaceae, Resedaceae and Tropaeolaceae. Keywords Ancestral genome evolution · Chromosome number evolution · Paleogenomics · Paleopolyploidy · Post- polyploid diversifcation · Whole-genome duplications Introduction and importance of Brassicaceae, the largest Brassicales fam- ily comprising of 3997 species in 341 genera (BrassiBase The Brassicales order, despite its name referring to crucifer accessed on January 18, 2018), over shadow the remaining species (Brassicaceae) primarily dominating the northern sixteen families. The exceptions are the papaya tree (Carica Hemisphere, is an eco-geographically and morphologically papaya, Caricaceae), commonly grown for its feshy berries diverse clade spread over all continents except Antarctica. in tropical and subtropical regions of the world; the caper Brassicales comprise 17 families and some 400 genera and c. bush (Capparis spinosa, Capparaceae), cultivated for edi- 4700 species (Christenhusz and Byng 2016; Cardinal-McTe- ble fower buds (capers) and fruits (caper berries); and the ague et al. 2016; Edger et al. 2018). Due to the pivotal role lesser-known but multi-purpose drumstick tree or moringa of Arabidopsis thaliana and other Brassicaceae species as (Moringa oleifera, Moringaceae). model organisms in various research disciplines, Brassicales The recently published phylogenetic analyses of Brassi- made their way into contemporary textbooks. The diversity cales (Cardinal-McTeague et al. 2016; Rockinger et al. 2016; Edger et al. 2018) show a renewed interest in evolution of this group. The robust phylogenetic frameworks permit Handling editor: Karol Marhold. the reinterpretation of existing data sets, identifcation of Electronic supplementary material The online version of this knowledge gaps and formulation of new hypotheses. Here I article (https://doi.org/10.1007/s00606-018-1507-2) contains am reassessing what is currently known about chromosome supplementary material, which is available to authorized users. number and genome size variation across Brassicales and how these data can be used to reconstruct chromosomal and * Martin A. Lysak [email protected] genome evolution patterns in this order. Furthermore, three family-specifc whole-genome duplication (WGD) events 1 CEITEC – Central European Institute of Technology, are inferred, and chromosome numbers of an ancestral Masaryk University, Kamenice 5, 625 00 Brno, Czech Republic Vol.:(0123456789)1 3 758 M. A. Lysak pre-Brassicales genome and the paleotetraploid genome four bispecifc families—Akaniaceae, Bataceae, Koeber- shared by the core Brassicales are discussed. liniaceae and Tovariaceae. Chromosome number varia- tion is relatively well characterized in smaller Brassicales families, such as Caricaceae (all 6 genera, c. 21 out of 35 Chromosome number and genome size data: species), Gyrostemonaceae (3 out of 4 genera, 3 out of 20 knowledge gaps spp.), Limnanthaceae (all 8 spp.), Moringaceae (5 out of 13 spp.) and Salvadoraceae (2 out of 3 genera, 4 out of Chromosome numbers for Brassicaceae species are continu- 11 spp.). ously updated in BrassiBase (Kiefer et al. 2014; Koch et al. Among the species-rich families, Brassicaceae is the best 2018), and several new counts for Caricaceae were published researched Brassicales family. Warwick and Al-Shehbaz by Rockinger et al. (2016). The Chromosome Counts Data- (2006) reported chromosome counts for 232 out of 338 base (CCDB, Rice et al. 2015) represents the most compre- genera (69%) and for 1558 out of 3709 species (42%). Since hensive chromosome number data resource for Brassicales 2006, the number of known chromosome counts for Bras- species, and CCDB was explored to draw the conclusions sicaceae species has further increased (cf. BrassiBase and detailed on the following lines (see also Online Resource 1 CCDB). On the other hand is Tropaeolaceae, with counts and Fig. 1). for only eight species (8% of species); Capparaceae, with Chromosome number data are lacking for three mono- records for 38 species (12% of species) in 13 out of 30 gen- specific Brassicales families, namely Emblingiaceae, era; Cleomaceae, with 49 (14%) species counted; and Rese- Pentadiplandraceae and Setchellanthaceae. Chromosome daceae, with chromosome number counts for c. 39 species numbers are known for only one of the two species in in fve genera (36% of species). At-α 4, 5 - 8 - 21, 28, 29, 35, ... Brassicaceae (328/3 628) [157 - 4 626] Cs-α 9 - 12, 15 -18, 20, 28, 29, 35 Cleomaceae (1/346) [303] 7 - 13 -16, 18 - 22 Capparaceae (30/324) 14 Tovariaceae (1/2) 14 Gyrostemonaceae (4/20) [636] 6, 10, 12 - 17, 20, 24, 28, 30 Resedaceae (12/107) [342 - 499] ? Pentadiplandraceae (1/1) ? Emblingiaceae (1/1) 22 Koeberliniaceae (1/2) At-β 11 Bataceae (1/2) [445] 18 / 28 10 - 12 Salvadoraceae (3/11) [411] 5 Limnanthaceae (2/8) [1 359] ? Setchellanthaceae (1/1) 7 - 9 Caricaceae (6/35) [318 - 968] 9 / 14 14 Moringaceae (1/13) [596] 14 Tropaeolaceae (1/94) [1 300] 9 Akaniaceae (2/2) Fig. 1 Phylogeny of Brassicales with plotted chromosome numbers the uncertainty of its phylogenetic placement (Edger et al. 2018). and genome sizes for each family. Known haploid chromosome num- Three red stars symbolize WGDs purported at the base of Cappa- bers, number of genera/number of species and genome sizes (Mb, in raceae, Resedaceae and Tropaeolaceae. Note that Cleomaceae can square brackets) are given for each family (the most frequent chro- be treated as containing only Cleome species or 18 diferent genera mosome numbers are underlined in three families). Inferred ancestral (Patchell et al. 2014). The plastid phylogeny was adopted from Edger haploid chromosome numbers are marked in black. A star represents et al. (2018), the number of taxa follows Christenhusz and Byng a whole-genome duplication; two stars for the At-β duplication refect (2016) and karyological records are based on Online Resource 1 1 3 Chromosomal and genome evolution in Brassicales 759 At least one genome size record is available for ten out Limnanthes douglasii (Limnanthaceae) having its 1360-Mb of 17 Brassicales families (Online Resource 1 and Fig. 1). genome divided among only fve chromosomes (Fig. 2). Not surprisingly, Brassicaceae is the family with the most extensive genome size variation knowledge. Genome sizes in other species-rich families remain largely unexplored. Ancient WGDs in Brassicales Kew’s Plant DNA C-values database (Bennett and Leitch 2012, accessed on January 20, 2018) contains only a single The frst ancient WGD in Brassicales was detected during C-value for Cleomaceae and Tropaeolaceae, and only two the Arabidopsis genome sequencing and assembly, when entries for Resedaceae. Not a single value is available for several genome regions were found to be duplicated on the Capparaceae, harboring more than 300 species. same or diferent chromosomes (Arabidopsis Genome Ini- This statistics summary reveals that the least known are tiative 2000). This paleotetraploid event was referred to as chromosome numbers for three monospecifc families (i.e., 3R or α (alpha), or alternatively as At-α duplication (e.g., Emblingiaceae, Pentadiplandraceae and Setchellanthaceae) Bowers et al. 2003; Maere et al. 2005; Barker et al. 2009). and that four species-rich Brassicales families (i.e., Cappar- The At-α is shared by all Brassicaceae tribes including aceae, Cleomaceae, Resedaceae and Tropaeolaceae) remain Aethionemeae (Schranz et al. 2012), the tribe sister to all largely understudied. The knowledge gap on genome size other Brassicaceae tribes. Similarly, Cleomaceae, the second variation in Brassicales is even more evident, with genome largest Brassicales family (Christenhusz and Byng 2016), sizes either unknown or reported only for c. 1% of species in experienced a WGT referred to as Cs-α or Th-α duplication all families, except Brassicaceae and Caricaceae. To expe- (Schranz and Mitchell-Olds 2006; Cheng et al. 2013). Both dite and navigate future comparative phylogenomic studies Brassicaceae and Cleomaceae, but not Caricaceae, share an in Brassicales, a collaborative efort should be undertaken older WGD, called At-β (beta) (Ming et al. 2008; Barker to compile basic