Evolution of the apomixis transmitting chromosome in Pennisetum

Abstract

BackgroundApomixis is an intriguing trait in plants that results in maternal clones through seed reproduction. Apomixis is an elusive, but potentially revolutionary, trait for plant breeding and hybrid seed production. Recent studies arguing that apomicts are not evolutionary dead ends have generated further interest in the evolution of asexual flowering plants.ResultsIn the present study, we investigate karyotypic variation in a single chromosome responsible for transmitting apomixis, the Apospory-Specific Genomic Region carrier chromosome, in relation to species phylogeny in the genera Pennisetum and Cenchrus. A 1 kb region from the 3' end of the ndhF gene and a 900 bp region from trnL-F were sequenced from 12 apomictic and eight sexual species in the genus Pennisetum and allied genus Cenchrus. An 800 bp region from the Apospory-Specific Genomic Region also was sequenced from the 12 apomicts. Molecular cytological analysis was conducted in sixteen Pennisetum and two Cenchrus species. Our results indicate that the Apospory-Specific Genomic Region is shared by all apomictic species while it is absent from all sexual species or cytotypes. Contrary to our previous observations in Pennisetum squamulatum and Cenchrus ciliaris, retrotransposon sequences of the Opie-2-like family were not closely associated with the Apospory-Specific Genomic Region in all apomictic species, suggesting that they may have been accumulated after the Apospory-Specific Genomic Region originated.ConclusionsGiven that phylogenetic analysis merged Cenchrus and newly investigated Pennisetum species into a single clade containing a terminal cluster of Cenchrus apomicts, the presumed monophyletic origin of Cenchrus is supported. The Apospory-Specific Genomic Region likely preceded speciation in Cenchrus and its lateral transfer through hybridization and subsequent chromosome repatterning may have contributed to further speciation in the two genera.

Reproductive Systems

“…In addition, its chromosomal location appears to vary over evolutionary time. Although Akiyama et al (2011) argue that the apospory-specific region originated only once in Cenchrus and was transferred to other species via hybridization, their data are also consistent with independent recruitment of related genomic regions. A similar structure has been found in Paspalum simplex (Grimanelli 2012) and in Tripsacum dactyloides.…”

Copy Number Variation in Transcriptionally Active Regions of Sexual and Apomictic Boechera Demonstrates Independently Derived Apomictic Lineages

“…In extending the idea of deleterious mutation accumulation in asexual genomes (i.e., Muller's ratchet;Muller 1964;Neiman et al 2010), such structural variation represents a type of macromutation that should inevitably contribute toward extinction of asexual lineages (Muller 1964;Lynch and Gabriel 1990;Charlesworth et al 1993). Increased mutational load in asexual taxa has, for the most part, been inferred through the analysis of phenotypic or life history traits (Lynch 1985), but on a higher level of organization it is clear that asexual taxa exhibit relatively high levels of chromosomal instability (e.g., heteromorphy, aneuploidy, hemizygosity; Mayer and Aguilera 1990; Kantama et al 2007;Akiyama et al 2011). Considering that these traits are ubiquitous among asexual taxa (Mayer and Aguilera 1990;Roche et al 2001;Kantama et al 2007), it is unclear whether they represent important factors associated with the expression of asexuality (Kantama et al 2007;Akiyama et al 2011), or whether they are the byproducts of disturbed meiosis and have no evolutionary significance.…”

Development and Characterization of a Hexaploid <i>Pennisetum orientale</i> (2<i>n</i>=6<i>x</i>=54) Cytotype Recovered through B_III Hybridization

“…Although 6x cytotypes in P. orientale have been reported earlier in limited cases as geographical collections (Jauhar 1981, Koul et al 1999, Akiyama et al 2011, their mode of origin was never proved. Two possible pathways have been suggested for the origin of 6x cytotypes: either through random genome duplication of 3x cytotypes (Koul et al 1999) or by fertilization of an unreduced egg cell with a reduced male gamete (Akiyama et al 2011). Recovery of the 6x plant from a 4x maternal plant in the present study provides the first direct experimental evidence for the later possibility.…”

“…Most of the hybrids were sterile owing to major genomic differences between the two species. However, the hybrids generated appreciable information on genome relatedness between the two species (Dujardin and Hanna 1983, Hanna and Dujardin 1982, Zadoo and Singh 1986, Patil and Singh 1964, Kaushal et al 2010 as well as molecular studies on evolution of genomes and mode of reproduction (Akiyama et al 2011, Sahu et al 2012.…”