Chromosomes Carrying Meiotic Avoidance Loci in Three Apomictic Eudicot Hieracium Subgenus Pilosella Species Share Structural Features with Two Monocot Apomicts    

Abstract

The LOSS OF APOMEIOSIS (LOA) locus is one of two dominant loci known to control apomixis in the eudicot Hieracium praealtum. LOA stimulates the differentiation of somatic aposporous initial cells after the initiation of meiosis in ovules. Aposporous initial cells undergo nuclear proliferation close to sexual megaspores, forming unreduced aposporous embryo sacs, and the sexual program ceases. LOA-linked genetic markers were used to isolate 1.2 Mb of LOA-associated DNAs from H. praealtum. Physical mapping defined the genomic region essential for LOA function between two markers, flanking 400 kb of identified sequence and central unknown sequences. Cytogenetic and sequence analyses revealed that the LOA locus is located on a single chromosome near the tip of the long arm and surrounded by extensive, abundant complex repeat and transposon sequences. Chromosomal features and LOA-linked markers are conserved in aposporous Hieracium caespitosum and Hieracium piloselloides but absent in sexual Hieracium pilosella. Their absence in apomictic Hieracium aurantiacum suggests that meiotic avoidance may have evolved independently in aposporous subgenus Pilosella species. The structure of the hemizygous chromosomal region containing the LOA locus in the three Hieracium subgenus Pilosella species resembles that of the hemizygous apospory-specific genomic regions in monocot Pennisetum squamulatum and Cenchrus ciliaris. Analyses of partial DNA sequences at these loci show no obvious conservation, indicating that they are unlikely to share a common ancestral origin. This suggests convergent evolution of repeat-rich hemizygous chromosomal regions containing apospory loci in these monocot and eudicot species, which may be required for the function and maintenance of the trait.Asexual seed formation, or apomixis, occurs in both monocot and eudicot plants and has evolved in more than 40 plant genera. Approximately 75% of apomicts exist in three families, the Poaceae, Asteraceae, and Rosaceae. Apomixis bypasses meiosis during female gametophyte formation. This contrasts with sexual female gametophyte development, which requires the meiosis of a megaspore mother cell (MMC) in the ovule (megasporogenesis) followed by nuclear proliferation of typically one of the meiotic

Evolution of apomixis loci in Pilosella and Hieracium (Asteraceae) inferred from the conservation of apomixis-linked markers in natural and experimental populations

“…The elongated LOA-carrying chromosome and linked markers were not detected in two apomictic P. aurantiaca (formerly H. aurantiacum) isolates (A35; A36, both containing Pilosella I cpDNA haplotype) investigated or a sexual P. officinarum (formerly H. pilosella) isolate (P36). This initial survey therefore revealed a tentative association between apospory-linked LOA marker presence and the Pilosella II cpDNA haplotype (Fehrer et al, , 2007aOkada et al, 2011).…”

“…A suite of characterized accessions, mutants and genetic and molecular tools have been developed to identify causal genes (Bicknell and Koltunow, 2004;Koltunow et al, 2013). Unlike Hieracium, inter-cytotype and inter-specific crosses are common in nature for Pilosella, and experimental crosses confirm that reproductive barriers are almost completely absent (for example, Fehrer et al, 2005Fehrer et al, , 2007bOkada et al, 2011).…”

“…Both loci are transmitted via pollen, and markers linked to both loci have been developed. Markers linked to LOA are non-genic although unique to the LOA region, and both genic and non-genic markers linked to LOP have been developed (Catanach et al, 2006;Koltunow et al, 2011;Okada et al, 2011). The LOA locus is subtelomeric on the long arm of a hemizygous chromosome and is associated with extensive repeats that extend along the long chromosome arm, although these extensive repeats are not essential for LOA function in R35 (Kotani et al, 2014).…”

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

“…Moreover, the mating system in plants has been shown to influence TE accumulation and distribution (Morgan 2001;Lockton and Gaut 2010), and there is evidence that genome size variability is influenced by TEs (Bennetzen et al 2005;Ray and Batzer 2011). In apomicts, TE accumulation has been implicated in the evolution of genomic regions that harbor apomixis factors (Akiyama et al 2004;Okada et al 2011) and is hypothesized to be a factor that contributes to eventual lineage extinction (Dolgin and Charlesworth 2006).…”

The Genetic Control of Apomixis: Asexual Seed Formation

“…In apomictic Pennisetum squamulatum, the apospory-specific genomic region (ASGR) is located at a heterochromatic and nonsynaptic telomeric region of a single chromosome (Akiyama et al 2004). Chromosomes carrying the ASGR in Pennisetum and the LOA locus in Hieracium are associated with extensive repetitive sequence and transposon-rich regions (Akiyama et al 2004;Okada et al 2011). Similarly, the hemizygous apomictic controlling locus (ACL) of Paspalum, which shows strong suppression of recombination, has undergone large-scale rearrangements due to transposable elements, when compared to a syntenic region in rice (Calderini et al 2006).…”