Chromosomal Evolution and Apomixis in the Cruciferous Tribe Boechereae.

Terezie Mandáková,Michael D Windham,Thomas Mitchell-Olds,Bo Price,Petra Hloušková,Martin A Lysak,John Carman,Kaylynn Ashby

doi:10.3389/fpls.2020.00514

Abstract

The mustard family (Brassicaceae) comprises several dozen monophyletic clades usually ranked as tribes. The tribe Boechereae plays a prominent role in plant research due to the incidence of apomixis and its close relationship to Arabidopsis. This tribe, largely confined to western North America, harbors nine genera and c. 130 species, with >90% of species belonging to the genus Boechera. Hundreds of apomictic diploid and triploid Boechera hybrids have spurred interest in this genus, but the remaining Boechereae genomes remain virtually unstudied. Here we report on comparative genome structure of six genera (Borodinia, Cusickiella, Phoenicaulis, Polyctenium, Nevada, and Sandbergia) and three Boechera species as revealed by comparative chromosome painting (CCP). All analyzed taxa shared the same seven-chromosome genome structure. Comparisons with the sister Halimolobeae tribe (n = 8) showed that the ancestral Boechereae genome (n = 7) was derived from an older n = 8 genome by descending dysploidy followed by the divergence of extant Boechereae taxa. As tribal divergence post-dated the origin of four tribe-specific chromosomes, it is proposed that these chromosomal rearrangements were a key evolutionary innovation underlaying the origin and diversification of the Boechereae in North America. Although most Boechereae genera exhibit genomic conservatism, intra-tribal cladogenesis has occasionally been accompanied by chromosomal rearrangements (particularly inversions). Recently, apomixis was reported in the Boechereae genera Borodinia and Phoenicaulis. Here, we report sexual reproduction in diploid Nevada, diploid Sandbergia, and tetraploid Cusickiella and aposporous apomixis in tetraploids of Polyctenium and Sandbergia. In sum, apomixis is now known to occur in five of the nine Boechereae genera.

Highlights

Well-defined clades provide ideal study systems for understanding the role of whole-genome duplications (WGDs, polyploidy) and chromosomal rearrangements in speciation and diversification
Based on the Ancestral Crucifer Karyotype (ACK), and on previously analyzed Boechereae species (Mandáková et al, 2015a, 2020), detailed comparative cytogenetic maps were constructed by Comparative Chromosome Painting (CCP) for each of the 10 Boechereae species and for P. micrantha (Figure 2 and Supplementary Tables S2–S8)
Comparative chromosome painting in P. micrantha (2n = 16, Halimolobeae) was successful in identifying all 22 conserved genomic blocks (GBs) making up the eight chromosomes (Hal1–Hal8, Figures 2, 3 and Supplementary Table S2)

Summary

Introduction

Well-defined clades provide ideal study systems for understanding the role of whole-genome duplications (WGDs, polyploidy) and chromosomal rearrangements in speciation and diversification. With the advent of molecular phylogenetics, in many cases, the inferred monophyly of a group has confirmed its geographical determinant and helped to elucidate its origin as well as directionality of later migrations and dispersals (e.g., Cowie and Holland, 2008; Ogutcen and Vamosi, 2016; Huang et al, 2018; Carter et al, 2019; Kim et al, 2019). A geographically restricted clade might be supported by different synapomorphies, such as morphological traits, specific metabolic pathways, pollination syndromes, or a shared WGD, some falling in the category of rare genomic changes (RGCs, Rokas and Holland, 2000). Structural chromosomal changes may underlie incipient reproductive isolation inducing species splits and the evolution of separate gene pools, i.e., cladogenesis (Faria and Navarro, 2010). Some chromosomal rearrangements may precipitate lineage splitting yet occur within a monophyletic clade (Freyman and Höhna, 2017)

Methods

Results

Conclusion