Seed development and inheritance studies in apomictic maize-Tripsacum hybrids reveal barriers for the transfer of apomixis into sexual crops

Abstract

Apomixis in plants covers a variety of cloning systems through seeds of great potential for plant breeding. Among long-standing approaches for crop improvement is the attempt to exploit wild relatives as natural, vast reservoirs for novel genetic variation. With regard to apomixis, maize possesses an apomictic wild relative, Tripsacum, which we used to produce advanced maize-Tripsacum hybrid generations. However, introgression of apomixis in maize has failed so far. In order to understand the how's and why's, we undertook characterization of seed development and inheritance studies in these materials. We show that apomictic seeds suffer from epigenetic loads. Both seed tissues, the endosperm and the embryo, displayed developmental defects resulting from imbalanced parental genomic contributions and aberrant methylation patterns, respectively. Progeny characterization of several maize-Tripsacum hybrid generations allowed significant progress toward the unraveling of the genetics of apomixis. First, chromosome deletion mapping showed that expression of apomixis requires one single Tripsacum chromosome. However, inheritance studies revealed that female gametes inheriting this segment were unequivalent carriers depending on their origin: unreduced gametes transmit a functional segment, whereas progeny derived from reduced ones reproduced sexually. Finally, chromosomal or genomic dosage variation barely affected the apomictic phenotype suggesting no dependency for ploidy in these materials. We conclude that epigenetic information imposes constraints for apomictic seed development and seems pivotal for transgenerational propagation of apomixis. The nature of the triggering mechanisms remains unknown as-yet, but it certainly explains the modest success relative to the development of apomictic maize thus far.

Inactivation of a DNA Methylation Pathway in Maize Reproductive Organs Results in Apomixis-Like Phenotypes

“…Our data suggest that the downregulation of a reproductive RdDM-like pathway can result in alterations in both sporogenesis (which gives rise to unreduced gametes) and gametogenesis (which gives rise to extra ESs). This is in line with the fact that apomeiosis and parthenogenesis in Tripsacum are genetically linked (Leblanc et al, 2009). On the other hand, neither dmt102 nor dmt103 inactivation resulted in the production of fully apomictic maize progeny.…”

“…Additionally, DRM2 is the main de novo methyltransferase in all sequence contexts, and we cannot exclude the possibility that de novo methylation activity might also be affected in apomictic progeny. Indeed, previous data showed that apomictic reproduction faithfully reproduces the genome through generations but often fails to properly replicate DNA methylation patterns (Leblanc et al, 2009).…”

“…38C reproduces via diplosporous apomixis: an unreduced ES is derived from a MMC and premature divisions of the unreduced egg cell result in a precocious, parthenogenetic pro-embryo, formed before fertilization. This apomictic model plant has been described in previous publications (Leblanc et al, 1996(Leblanc et al, , 2009Grimanelli et al, 2003;Grimanelli et al, 2005). This is an imperfect model for expression studies because of its very complex genetic background.…”

“…The 38C apomictic maize-Tripsacum hybrid has been previously described in detail (Leblanc et al, 1996(Leblanc et al, , 2009Grimanelli et al, 2003). Transgenic version of 38C expressing pES1-GFP were produced as described by Leblanc et al (1996) using a pZmES1-GFP maize (Zea mays) line provided by Thomas Dresselhaus (University of Regensburg, Germany).…”

Identification of Candidate Genes Related to Polyploidy and/or Apomixis in <i>Eragrostis curvula</i>

“…It has been shown that the apomixis-governing locus is a heterochromatic region enriched in retrotransposons and repetitive DNA [23][24][25][26]. A parent-of-origin effect of meiosis on expression of apomixis was reported [27]: in segregating populations, the apomixis locus was not inherited in a functional state (i.e., it could not induce apomixis) when transmitted through a reduced female gamete, but it remained functional when transmitted via male meiosis. More evidence for a possible epigenetic basis of apomixis came recently from the analysis of Arabidopsis thaliana plants with a defective ARGONAUTE9 (AGO9) gene [28].…”