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

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.