Genome Structure of the Heavy Metal Hyperaccumulator Noccaea caerulescens and Its Stability on Metalliferous and Nonmetalliferous Soils

Abstract

Noccaea caerulescens (formerly known as Thlaspi caerulescens), an extremophile heavy metal hyperaccumulator model plant in the Brassicaceae family, is a morphologically and phenotypically diverse species exhibiting metal tolerance and leaf accumulation of zinc, cadmium, and nickel. Here, we provide a detailed genome structure of the approximately 267-Mb N. caerulescens genome, which has descended from seven chromosomes of the ancestral proto-Calepineae Karyotype (n = 7) through an unusually high number of pericentric inversions. Genome analysis in two other related species, Noccaea jankae and Raparia bulbosa, showed that all three species, and thus probably the entire Coluteocarpeae tribe, have descended from the proto-Calepineae Karyotype. All three analyzed species share the chromosome structure of six out of seven chromosomes and an unusually high metal accumulation in leaves, which remains moderate in N. jankae and R. bulbosa and is extreme in N. caerulescens. Among these species, N. caerulescens has the most derived karyotype, with species-specific inversions on chromosome NC6, which grouped onto its bottom arm functionally related genes of zinc and iron metal homeostasis comprising the major candidate genes NICOTIANAMINE SYNTHASE2 and ZINC-INDUCED FACILITATOR-LIKE1. Concurrently, copper and organellar metal homeostasis genes, which are functionally unrelated to the extreme traits characteristic of N. caerulescens, were grouped onto the top arm of NC6. Compared with Arabidopsis thaliana, more distal chromosomal positions in N. caerulescens were enriched among more highly expressed metal homeostasis genes but not among other groups of genes. Thus, chromosome rearrangements could have facilitated the evolution of enhanced metal homeostasis gene expression, a known hallmark of metal hyperaccumulation.

Frequency, Origins, and Evolutionary Role of Chromosomal Inversions in Plants

“…Such approaches are most powerful in groups such as the Brassicaceae and Solanaceae, in which virtually repeat-free BAC contigs covering much of the genome are available for use as probes, permitting "comparative chromosome mapping" (Lysak and Lexer, 2006). Successful application of this method has led to the discovery of numerous inversions across various clades of the Brassicaceae, but especially Arabidopsis and Brassica (Lysak et al, , 2007Mandakova and Lysak, 2008;Mandakova et al, 2015;Lee et al, 2017), as well as among and within species in Solanum (Szinay et al, 2012). However, suitable sets of chromosome-specific painting probes are needed for the broader application of this approach in other plant groups.…”

“…Likewise, Coughlan and Willis (2019) showed that key life history QTLs mapping to an inversion differentiating annual and perennial Mimulus guttatus mapped to the same region in a population involving annual M. guttatus and a collinear perennial species, M. tilingii, thereby showing that loci contributing to local adaptation predate the inversion in this system as well. Inversions on chromosome NC6 of Noccaea caerulescens are found to group pre-existing metal homeostasis genes, which may explain their fixation and role in speciation (Mandakova et al, 2015).…”

Lessons on Evolution from the Study of Edaphic Specialization

“…Serpentine ( , (Macnair & Christie, 1983;Wright et al, 2013) Granite (Peterson et al, 2013) Serpentine and other metal-enriched soils (Mandáková et al, 2015) Sandy dunes and rocky headlands (Melo et al, 2014) Serpentine (Bratteler et al, 2006, b); Copper soils (van Hoof et al, 2001) Copper tolerance (Macnair, 1983; Drought tolerance (Peterson et al, 2013) Enhanced metal homeostasis gene expression (Mandáková et al, 2015) Salinity tolerance, potassium transport (Roda et al, 2013) Nickel tolerance (Bratteler et al, 2006); Copper tolerance (van Hoof et al, 2001) Self-compatibility, flowering time differences, hybrid lethality (Christie & Macnair, 1984, 1987Macnair et al, 1989;Friedman & Willis, 2013;Wright et al, 2013) Flowering time differences (Ferris et al, 2016) Possible role of inversion polymorphism (Mandáková et al, 2015); lower selfing rates in metallicolous populations…”

Monophyletic Origin and Evolution of the Largest Crucifer Genomes

“…All the inferred ancestral genomes in Brassicaceae have descended from a common post-At-a genome, which later diversified into an ancestral clade F genome and an ancestral genome (n = 8) shared by all crowngroup clades (A-E). The evolution of the latter genome is still rather elusive due to the lack of genomic data on clades C (except for Biscutelleae; Geiser et al, 2016) and D. Comparisons of structurally characterized modern genomes of clades A, B, C, and E plus Arabideae suggest that the ancestral crown-group genome further evolved into ACK (n = 8;Schranz et al, 2006) and another n = 8 genome shared by Arabideae and clade E. ACK either remained conserved in clade A (Lysak et al, 2006(Lysak et al, , 2016Mandáková et al, 2013), was altered by a reciprocal translocation in clade C (pre-PCK of Biscutelleae; Geiser et al, 2016), or underwent descending dysploidy toward the PCK genome of clade B (n = 7; Mandáková and Lysak, 2008;Cheng et al, 2013;Mandáková et al, 2015). Although CEK of clade E and KAA of Arabideae (Willing et al, 2015) share some unique genomic features (Fig.…”