Chasing the Apomictic Factors in the Ranunculus auricomus Complex: Exploring Gene Expression Patterns in Microdissected Sexual and Apomictic Ovules

Abstract

<jats:p>Apomixis, the asexual reproduction via seeds, is associated to polyploidy and hybridization. To identify possible signatures of apomixis, and possible candidate genes underlying the shift from sex to apomixis, microarray-based gene expression patterns of live microdissected ovules at four different developmental stages were compared between apomictic and sexual individuals of the Ranunculus auricomus complex. Following predictions from previous work on mechanisms underlying apomixis penetrance and expressivity in the genus, gene expression patterns were classified into three categories based on their relative expression in apomicts compared to their sexual parental ancestors. We found evidence of misregulation and differential gene expression between apomicts and sexuals, with the highest number of differences detected during meiosis progression and emergence of aposporous initial (AI) cells, a key developmental stage in the ovule of apomicts where a decision between divergent reproductive pathways takes place. While most of the differentially expressed genes (DEGs) could not be annotated, gene expression was classified into transgressive, parent of origin and ploidy effects. Genes related to gametogenesis and meiosis demonstrated patterns reflective of transgressive and genome dosage effects, which support the hypothesis of a dominant factor controlling apomixis in Ranunculus and modulated by secondary modifiers. Three genes with probable functions in sporogenesis and gametogenesis development are identified and characterized for future studies.</jats:p>

Environmental and Genetic Factors Affecting Apospory Expressivity in Diploid Paspalum rufum

“…A similar variation of apospory expressivity was previously reported in hybrids of Paspalum notatum [ 46 ] and Hieracium [ 29 ], leading the authors to suggest that unknown factors segregate in the genetic background modifying apospory expressivity. In line with these observations, recent comparative gene expression work between apomictic and sexual genotypes of Ranunculus auricomus reported that the pattern of gene expression was reflective of transgressive and genome dosage effects, supporting the hypothesis of a dominant factor controlling apomixis and modulated by secondary modifiers [ 90 ].…”

Can We Use Gene-Editing to Induce Apomixis in Sexual Plants?

“…According to this hypothesis, apomixis in hybrids (mainly allopolyploids) arises as a consequence of the evolutionary divergence of regulatory sequences controlling sporogenesis and gametogenesis in parental species, and in polyploids (mainly autopolyploids) arises as a consequence of dosage effects and stoichiometric disbalances of macromolecular complexes. This idea has nowadays been reinforced by gene expression and transcriptomic analyses on different plant species exposing significant changes in expression levels (up- and down-regulations) of many genes in apomictic compared to sexual ovules [ 51 , 52 , 53 , 54 , 55 , 56 ]. Such regulatory alterations might well support weaker controls on cell fate and key developmental steps allowing, e.g., nucellar cells to acquire a gametogenesis fate (in apospory), or the primary endosperm to develop under imbalanced paternal to maternal genome ratios.…”

Skipping sex: A nonrecombinant genomic assemblage of complementary reproductive modules

“…[ 24,78 ] All natural apomicts studied so far show major shifts in gene expression, the extent and patterning of which require further investigation. Such regulatory changes in gene expression – many related to germ cell specification, meiotic progression and gametogenesis [ 81 ] – are associated to temporal and spatial developmental asynchronies, and are subjected to environmental modulation (e.g., in Boechera spp., [ 27,28,33 ] ; in Brachiaria spp., [ 82 ] ; in Eragrostis spp., [ 83,84 ] ; in Hieracium spp., [ 29,85 ] ; in Hypericum spp., [ 86,87 ] ; in Panicum spp., [ 88 ] ; in Paspalum spp., [ 34,48,89–91 ] in Pennisetum spp., [ 31,92 ] ; in Poa spp., [ 93 ] ; in Tripsacum spp., [ 26 ] ; in Ranunculus spp., [ 3,32,94–97 ] ).…”