Genome-Wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-Origin–Dependent Regulation of AGAMOUS-LIKE36

Reza Shirzadi,Ellen D Andersen,Csaba Koncz,Arp Schnittger,Maren Heese,Barbara M Gloeckle,Alexander Ungru,Reidunn B Aalen,Katrine N Bjerkan,Per Winge,Paul E Grini

doi:10.1371/journal.pgen.1001303

Abstract

Seed development in angiosperms is dependent on the interplay among different transcriptional programs operating in the embryo, the endosperm, and the maternally-derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed. Here we have exploited cdka;1 fertilization as a novel tool for the identification of seed regulators and factors involved in parent-of-origin–specific regulation during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds and identified approximately 600 genes that are downregulated in the absence of a paternal genome. Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented. Here, AGL36 was chosen for an in-depth study and shown to be imprinted. We demonstrate that AGL36 parent-of-origin–dependent expression is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.

Highlights

Seed development is a tightly regulated process that is controlled, both before and after fertilization and requires tight coordination of parental gene expression [1]
A prevailing hypothesis predicts that a parental tug-of-war on the allocation of available recourses to the developing progeny has led to the evolution of imprinting systems where genes expressed from the mother dampen growth whereas genes expressed from the father are growth enhancers
The number of imprinted genes identified in plants is low compared to mammals, and this precludes the elucidation of the epigenetic mechanisms responsible for this specialized expression system

Summary

Introduction

Seed development is a tightly regulated process that is controlled, both before and after fertilization and requires tight coordination of parental gene expression [1]. A paradigm for the importance of balanced parental contribution is the observation that certain genes in the developing offspring of flowering plants are exclusively or preferentially expressed from only one of the two parental genomes, a phenomenon called genomic imprinting that has been observed in mammals [2,3]. An increase in the paternal genome results in larger seeds, while the opposite is observed if the maternal gene dosage is higher than normal [5]. This is in agreement with the parental conflict theory, which implies that fathers direct maximal amount of maternal resources to their own offspring and thereby promote growth. Maternal factors are thought to dampen growth [6]

Methods

Findings

Discussion

Conclusion