Balance between maternal and paternal alleles sets the timing of resource accumulation in the maize endosperm

Abstract

Key aspects of seed development in flowering plants are held to be under epigenetic control and to have evolved as a result of conflict between the interests of the male and female gametes (kinship theory). Attempts to identify the genes involved have focused on imprinted sequences, although imprinting is only one mechanism by which male or female parental alleles may be exclusively expressed immediately post-fertilization. We have studied the expression of a subset of endosperm gene classes immediately following interploidy crosses in maize and show that departure from the normal 2 : 1 ratio between female and male genomes exerts a dramatic effect on the timing of expression of some, but not all, genes investigated. Paternal genomic excess prolongs the expression of early genes and delays accumulation of reserves, while maternal genomic excess foreshortens the expression period of early genes and dramatically brings forward endosperm maturation. Our data point to a striking interdependence between the phases of endosperm development, and are consonant with previous work from maize showing progression from cell proliferation to endoreduplication is regulated by the balance between maternal and paternal genomes, and from Arabidopsis suggesting that this 'phasing' is regulated by maternally expressed imprinted genes. Our findings are discussed in context of the kinship theory.

Dynamic Expression of Imprinted Genes Associates with Maternally Controlled Nutrient Allocation during Maize Endosperm Development

“…Although the specific role of auxin and auxin-signaling pathways during early endosperm development is unknown, the results of our analysis of endosperm imprinted genes and their associated GO functions highlight a potential role for auxin-mediated control of nutrient uptake from maternal tissues through a complementary set of functions performed by distinct MEGs and PEGs. As such, this study supports the recent observations of the effects of parental genome excess on the timing of gene expression during the same developmental period in interploidy maize crosses (Li and Dickinson, 2010). Our data indicate potential interplay between the relatively rapid upregulation of MEGs involved in nutrient accumulation at 10 DAP and the concomitant downregulation of an earlier expressed set of PEGs with potential cell proliferation regulatory functions.…”

Flavonoids and the regulation of seed size in Arabidopsis

“…Thus extra copies of either the paternal or maternal genomes in the endosperm, as would occur in interploidy hybridizations, upset the normal developmental programme of the seed. More recently, work on the model species Arabidopsis thaliana and maize has confirmed the crucial importance of the ratio of maternal and paternal genomic contributions in the endosperm to seed development and highlighted that the direction of interploidy crosses have profoundly differing effects on endosperm development [26,27]. The EBN hypothesis assigns a particular 'genomic strength' to maternally or paternally derived genomes from different species that equates to an effective ploidy.…”

“…These parent-oforigin effects, centred on the endosperm, are largely the result of differential genomic imprinting of maternal and paternal gametes [25][26][27]29]. Thus a ratio of two maternal to one paternal genomes (2m:1p) is established, which, if changed, for example through interploidy hybridization, results in aberrant development of the endosperm.…”

Kin Conflict in Seed Development: An Interdependent but Fractious Collective

“…Maternal excess causes early silencing of genes associated with endosperm proliferation and early activation of genes associated with grain filling. Paternal excess has opposite effects (Li & Dickinson 2010). …”