The Armadillo Repeat Gene ZAK IXIK Promotes Arabidopsis Early Embryo and Endosperm Development through a Distinctive Gametophytic Maternal Effect

Abstract

The proper balance of parental genomic contributions to the fertilized embryo and endosperm is essential for their normal growth and development. The characterization of many gametophytic maternal effect (GME) mutants affecting seed development indicates that there are certain classes of genes with a predominant maternal contribution. We present a detailed analysis of the GME mutant zak ixik (zix), which displays delayed and arrested growth at the earliest stages of embryo and endosperm development. ZIX encodes an Armadillo repeat (Arm) protein highly conserved across eukaryotes. Expression studies revealed that ZIX manifests a GME through preferential maternal expression in the early embryo and endosperm. This parent-of-origin-dependent expression is regulated by neither the histone and DNA methylation nor the DNA demethylation pathways known to regulate some other GME mutants. The ZIX protein is localized in the cytoplasm and nucleus of cells in reproductive tissues and actively dividing root zones. The maternal ZIX allele is required for the maternal expression of MINISEED3. Collectively, our results reveal a reproductive function of plant Arm proteins in promoting early seed growth, which is achieved through a distinct GME of ZIX that involves mechanisms for maternal allele-specific expression that are independent of the well-established pathways.

Arabidopsis LORELEI, a Maternally Expressed Imprinted Gene, Promotes Early Seed Development

“…LRE also is distinct from other MEGs in other respects, as its expression is imprinted in both zygote and proliferating endosperm. Additionally, monoallelic expression of LRE expression after fertilization in the developing seed is earlier than reported for other MEGs (Jahnke and Scholten, 2009;Ngo et al, 2012;Nodine and Bartel, 2012;Raissig et al, 2013). Because the patrigenic allele of LRE remains silent in various stages of seed development after 24 HAP Gehring et al, 2011;Hsieh et al, 2011;Nodine and Bartel, 2012;Raissig et al, 2013), our observations also cannot be explained by delayed paternal genome activation (Autran et al, 2011;Del Toro-De León et al, 2014;García-Aguilar and Gillmor, 2015).…”

“…Alternatively, the delay of early embryogenesis could be due to an indirect effect of loss of LRE in the endosperm. Nevertheless, our study adds LRE to a growing list of MEGs whose loss negatively impacts seed development, including ZIX, FH5, and NUWA in Arabidopsis (Ingouff et al, 2005;Fitz Gerald et al, 2009;Ngo et al, 2012;He et al, 2017) and MEG1 in maize (Gutiérrez-Marcos et al, 2004;Costa et al, 2012). Additionally, mutations in MEGs like FWA and AGL36 do not result in endosperm phenotypes (Kinoshita et al, 2004;Shirzadi et al, 2011).…”

“…Imprinting appears more common in endosperm but also occurs in embryos (Jahnke and Scholten, 2009;Luo et al, 2011;Ngo et al, 2012;Nodine and Bartel, 2012;Raissig et al, 2013;Pignatta et al, 2014). However, the interpretation of transcriptomic studies can be confounded by contamination from the maternal seed coat (Schon and Nodine, 2017).…”

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

“…An additional member of the IKU pathway is SHORT HYPOCOTYL UNDER BLUE LIGHT 1 (SHB1) that is recruited by WRKY10 on the promoters of IKU2 and WRKY10 (26,27). ZAK IXIK, a gametophytic maternal effect gene that controls the expression of WRKY10, might be involved in the IKU pathway as well (28).…”

Plant Wnt:Deciphering a Novel Signalling Pathway in Plants

“…However, ARPs which have also been identified in plants, are involved in intracellular signalling like their animal homologs 57 . Several studies have shown that ARPs play multiple roles in plant system including embryogenesis, endosperm development 58 , stress signalling and protein degradation 59,60 . ARM proteins have been associated with light signalling, hormonal response and maintenance of self-incompatibility in plants 57 .…”