On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)

Abstract

Polyploidy, or whole-genome duplication, is a common speciation mechanism in plants. An important barrier to polyploid establishment is a lack of compatible mates. Because self-compatibility alleviates this problem, it has long been hypothesized that there should be an association between polyploidy and self-compatibility (SC), but empirical support for this prediction is mixed. Here, we investigate whether the molecular makeup of the Brassicaceae self-incompatibility (SI) system, and specifically dominance relationships among S-haplotypes mediated by small RNAs, could facilitate loss of SI in allopolyploid crucifers. We focus on the allotetraploid species Capsella bursa-pastoris, which formed ~300 kya by hybridization and whole-genome duplication involving progenitors from the lineages of Capsella orientalis and Capsella grandiflora. We conduct targeted long-read sequencing to assemble and analyze eight full-length S-locus haplotypes, representing both homeologous subgenomes of C. bursa-pastoris. We further analyze small RNA (sRNA) sequencing data from flower buds to identify candidate dominance modifiers. We find that C. orientalis-derived S-haplotypes of C. bursa-pastoris harbor truncated versions of the male SI specificity gene SCR and express a conserved sRNA-based candidate dominance modifier with a target in the C. grandiflora-derived S-haplotype. These results suggest that pollen-level dominance may have facilitated loss of SI in C. bursa-pastoris. Finally, we demonstrate that spontaneous somatic tetraploidization after a wide cross between C. orientalis and C. grandiflora can result in production of self-compatible tetraploid offspring. We discuss the implications of this finding on the mode of formation of this widespread weed.

Pleistocene dynamics of the Eurasian steppe as a driving force of evolution: Phylogenetic history of the genus Capsella (Brassicaceae)

“…( 2015 ) also “clearly rule out a single polyploid origin from two haploid gametes”. Recently uncovered spontaneous somatic tetraploidization following hybridization between C. orientalis and C. grandiflora experimentally supports the origin of C. bursa‐pastoris (Bachmann et al., 2021 ) and offers further interpretation on the polyplodization process.…”

“…Capsella bursa‐pastoris and C. thracica emerged from hybridization between the western and eastern lineages. Meanwhile, Capsella has become a model system for genomic studies of plant mating systems (e.g., Bachmann et al., 2019 , 2021 ; Brandvain et al, 2013 ; Mattila et al., 2020 ; Woźniak et al., 2020 ) and polyploidization (Douglas et al., 2015 ; Han et al., 2015 ; Kryvokhyzha, Salcedo et al., 2019 ; Omelchenko et al., 2020 ). In contrast to the increasing knowledge about Capsella at the genomic level, a detailed phylogeographical aspect of its evolution, especially of the eastern lineage consisting of C. orientalis , is currently missing.…”

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

“…The population structure of C. bursa-pastoris suggests that its multiple origins span distinct geographical regions, such as Europe, the Middle East, and Asia (Cornille et al 2016;Kryvokhyzha et al 2016;Wesse et al 2021). However, in the subgenome inherited from C. orientalis, all but one C. bursa-pastoris accession from putatively distinct origins share the same frameshift deletion in SCR with C. orientalis (Bachmann et al 2019(Bachmann et al , 2021, consistent with the notion that C. orientalis was probably selfing long before it contributed to the allotetraploid C. bursa-pastoris (Douglas et al 2015). The only C. bursa-pastoris accession with a different S-allele in the C. orientalis subgenome was sampled in Central Asia (Cbp_DUB-RUS9, accession number SRR8904462 (Kryvokhyzha et al 2019)).…”

“…Various transitions from diploidy to polyploidy were reviewed by Comai ( 2005 ). While unreduced gametes are considered the primary cause of polyploidy (Thompson and Lumaret 1992 ; Bretagnolle and Thompson 1995 ; Kreiner et al 2017a ) and the evidence for somatic doubling is scarce (Newton and Pellew 1929 ; Nasrallah et al 2007 ; Bachmann et al 2021 ), the relative contribution of each route to polyploid formation is unknown.…”

Transition to self-compatibility associated with dominantS-allele in a diploid Siberian progenitor of allotetraploidArabidopsis kamchaticarevealed byArabidopsis lyratagenomes

“…This means that the transition to selfing in A. kamchatica was most likely immediate. Similar examples where a dominant loss-of-function mutation in one of the progenitors facilitated transition to selfing in allotetraploids exist in A. suecica (Novikova et al 2017), Capsella bursa-pastoris (Bachmann et al 2021) and Brassica napus (Okamoto et al 2007; Kitashiba and Nasrallah 2014). It should be noted that both progenitors of A. kamchatica also co-exist in Europe without forming other allotetraploids (Clauss and Koch 2006; Schmickl et al 2010), although it is possible to create such an interspecific cross (Sarret et al 2009).…”