Responses to Hypoxia and Endoplasmic Reticulum Stress Discriminate the Development of Vitreous and Floury Endosperms of Conventional Maize (Zea mays) Inbred Lines

Mathieu Gayral,Stéphanie Pateyron,Khalil Elmorjani,Sylvie Brunet,Sandrine M Balzergue,Caroline Delluc,Didier Marion,Laurent Linossier,Marie-Hélène Morel,Michèle Dalgalarrondo,Bénédicte Bakan

doi:10.3389/fpls.2017.00557

Abstract

Major nutritional and agronomical issues relating to maize (Zea mays) grains depend on the vitreousness/hardness of its endosperm. To identify the corresponding molecular and cellular mechanisms, most studies have been conducted on opaque/floury mutants, and recently on Quality Protein Maize, a reversion of an opaque2 mutation by modifier genes. These mutant lines are far from conventional maize crops. Therefore, a dent and a flint inbred line were chosen for analysis of the transcriptome, amino acid, and sugar metabolites of developing central and peripheral endosperm that is, the forthcoming floury and vitreous regions of mature seeds, respectively. The results suggested that the formation of endosperm vitreousness is clearly associated with significant differences in the responses of the endosperm to hypoxia and endoplasmic reticulum stress. This occurs through a coordinated regulation of energy metabolism and storage protein (i.e., zein) biosynthesis during the grain-filling period. Indeed, genes involved in the glycolysis and tricarboxylic acid cycle are up-regulated in the periphery, while genes involved in alanine, sorbitol, and fermentative metabolisms are up-regulated in the endosperm center. This spatial metabolic regulation allows the production of ATP needed for the significant zein synthesis that occurs at the endosperm periphery; this finding agrees with the zein-decreasing gradient previously observed from the sub-aleurone layer to the endosperm center. The massive synthesis of proteins transiting through endoplasmic reticulum elicits the unfolded protein responses, as indicated by the splicing of bZip60 transcription factor. This splicing is relatively higher at the center of the endosperm than at its periphery. The biological responses associated with this developmental stress, which control the starch/protein balance, leading ultimately to the formation of the vitreous and floury regions of mature endosperm, are discussed.

Highlights

Endosperm texture is an important quality trait of maize (Zea mays L.), determined by the proportions of vitreous and floury endosperm
Maize grain development starts with the double fertilization of the female gamete and the central cells, which leads to the development of the embryo and the endosperm respectively
We will refer to these regions as maize endosperm center (MEC) and maize endosperm periphery (MEP)

Summary

Introduction

Endosperm texture is an important quality trait of maize (Zea mays L.), determined by the proportions of vitreous and floury endosperm. The identification of the physicochemical mechanisms leading to vitreousness is fundamental in terms of both nutritional and agronomical issues This was mainly achieved by studying different opaque/floury mutants, especially opaque (o2), and Quality Protein Maize (QPM), where vitreous endosperm is restored by introgressing “o2 modifier” genes (mo2) within an o2 background (Gibbon and Larkins, 2005). These studies highlighted the close relationships between zeins, starch, and maize vitreousness. O2 encodes a defective transcription factor (TF) that, in its wildtype form, regulates the expression of several genes during endosperm development Such mutations result in a decrease in zein content and smaller protein bodies (Schmidt et al, 1987, 1990). The recovery of a vitreous endosperm in QPM is related to an increase in amylose content and shorter amylopectin branching (Gibbon et al, 2003; SalazarSalas et al, 2014) as well as an increase in 27 kDa γ-zein content and well-shaped protein bodies (Wu et al, 2010)

Methods

Results

Conclusion