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

Abstract

Chromosomal inversions have the potential to play an important role in evolution by reducing recombination between favorable combinations of alleles. Until recently, however, most evidence for their likely importance derived from dipteran flies, whose giant larval salivary chromosomes aided early cytogenetic studies. The widespread application of new genomic technologies has revealed that inversions are ubiquitous across much of the plant and animal kingdoms. Here we review the rapidly accumulating literature on inversions in the plant kingdom and discuss what we have learned about their establishment and likely evolutionary role. We show that inversions are prevalent across a wide range of plant groups. We find that inversions are often associated with locally favored traits, as well as with traits that contribute to assortative mating, suggesting that they may be key to adaptation and speciation in the face of gene flow. We also discuss the role of inversions in sex chromosome formation, and explore possible parallels with inversion establishment on autosomes. The identification of inversion origins, as well as the causal variants within them, will advance our understanding of chromosomal evolution in plants.

Keywords: comparative genetic mapping; comparative genomics; inversions; reduced recombination model; secondary contact.

FIGURE 1

Effective reduction in recombination of inversion by selection against recombinant gametes in meiosis. (A) In individuals that are heterozygous for a pericentric inversion, a single crossover within the inversion generates unbalanced gametes that contain a duplication and a deletion. (B) In individuals that are heterozygous for a paracentric inversion, a single crossover within the inversion produces a dicentric bridge and an acentric fragment. The acentric fragment is lost because it cannot be drawn to either end and the chromosomal bridge breaks at random point during segregation, resulting in two deletion products. Lines of blue and orange colors represent homologous chromosomes and small circles indicate centromeres.

FIGURE 2

Models for the establishment of inversions. (A) Kirkpatrick and Barton (2006) model. At the starting point, population 1 and 2 occur in different environments, but are connected by gene flow (maroon arrows). Different alleles (red and green colors) at multiple genes underlying the same locally adapted trait (deep color and light color triangles) are favored in local environments (green and gray backgrounds). The ancestral chromosome carries mixtures of adapted and maladapted alleles in the face of gene flow, while a new inversion carries only the locally adapted alleles (yellow bars). The inversion is therefore favored and rises to high frequency in population 2. (B) Inversions become established through a process similar to (A) but by carrying a combination of alleles at two loci that are adapted to different aspects of the local environment (triangles and squares in different colors). For example, in a dune ecotype of the prairie sunflower (Helianthus petiolaris), larger seed size and tolerance to low nutrient soils were found to map to the same inversions (Huang et al., 2019; Todesco et al., 2019). (C) Mixed geographic model proposed by Feder et al. (2011). At the starting point, population 1 and 2 are allopatric. Multiple locally adapted alleles (triangles and squares in different colors) are fixed due to lack of gene flow, and an inversion carrying a full complement of these alleles is present at low frequency in population 2 through mutation-purifying selection balance or genetic drift. At secondary contact, the reduction in recombination caused by the inversion results in a selective advantage over collinear regions, leading to rise of inversion frequency. Red crosses indicate that chromosomes carrying maladaptive combinations of alleles are eliminated in each environment.

FIGURE 3

Results of local population structure analyses in (A) Helianthus petiolaris (data from Huang et al., 2019), (B) H. bolanderi (data from Owens et al., 2016), and (C) H. niveus (data from Zhang et al., 2019). Variant calling and multidimensional scaling (MDS) follow the same methods described in Huang et al. (2019). Only the first MDS coordinate is plotted. Clusters of MDS outliers, which indicate putative inversions (and have been confirmed with other methods), are identified in H. petiolaris (indicated with dotted circles) but not in the other two species.

FIGURE 4

The model for the role of inversions in speciation proposed by Trickett and Butlin (1994). An inversion facilitates speciation by suppressing recombination between genes involved in local adaptation (red and green triangles) and those underlying assortative mating traits, as such flowering time (black and white asterisks). The ancestral chromosome carries mixtures of adapted and maladapted alleles due to recombination. Individuals that are locally adapted to the environment of population 2, but carries the white assortative mating allele, will tend to mate with individuals adapted to the other environment and produce maladaptive offspring in population 2. Individuals with a new inversion that captures only the locally adapted alleles and black assortative mating allele do not suffer the reproductive cost from recombination. The inversion is therefore favored and contributes to further divergence between populations. Red crosses indicate that chromosomes carrying maladaptive combinations of alleles are eliminated in each environment.