Carotenoids modulate kernel texture in maize by influencing amyloplast envelope integrity

Haihai Wang,Xing Huang,Xiaoli Xiang,Brian A Larkins,Yongrui Wu,Jiechen Wang,Changsheng Li,Xiaoyan Gao,Yongcai Huang,Qiao Xiao,Wenqin Wang,Qiong Wang,Yidong Zhu

doi:10.1038/s41467-020-19196-9

Abstract

The mechanism that creates vitreous endosperm in the mature maize kernel is poorly understood. We identified Vitreous endosperm 1 (Ven1) as a major QTL influencing this process. Ven1 encodes β-carotene hydroxylase 3, an enzyme that modulates carotenoid composition in the amyloplast envelope. The A619 inbred contains a nonfunctional Ven1 allele, leading to a decrease in polar and an increase in non-polar carotenoids in the amyloplast. Coincidently, the stability of amyloplast membranes is increased during kernel desiccation. The lipid composition in endosperm cells in A619 is altered, giving rise to a persistent amyloplast envelope. These changes impede the gathering of protein bodies and prevent them from interacting with starch grains, creating air spaces that cause an opaque kernel phenotype. Genetic modifiers were identified that alter the effect of Ven1A619, while maintaining a high β-carotene level. These studies provide insight for breeding vitreous kernel varieties and high vitamin A content in maize.

Highlights

The mechanism that creates vitreous endosperm in the mature maize kernel is poorly understood
When the endosperm cells were examined by Scanning electron microscopy (SEM), we found that starch grains (SGs) in NILW64A were tightly surrounded by protein bodies (PBs), appearing to be embedded in a proteinaceous cytoskeletal matrix
In SEM, the SGs in NILW64A were observed to be tightly seamed together, with PBs developing distinctive features of vitreous endosperm formation, whereas the SGs in NILA619 were loosely packed with air space between them, a typical characteristic of opaque endosperm (Supplementary Fig. 8j, l). These results demonstrated that compaction of PBs and SGs is affected during desiccation of NILA619 endosperm

Summary

Introduction

The mechanism that creates vitreous endosperm in the mature maize kernel is poorly understood. The lipid composition in endosperm cells in A619 is altered, giving rise to a persistent amyloplast envelope These changes impede the gathering of protein bodies and prevent them from interacting with starch grains, creating air spaces that cause an opaque kernel phenotype. A large number of mutations affecting zein proteins and starch synthesis have been identified and provided insight into the mechanisms that create vitreous endosperm[8,9], little is known about quantitative trait loci and their metabolic products that explain the genetic variation in kernel texture found in natural populations. High levels of β-carotene appear to prevent the breakdown of amyloplast membranes and affect the quantity and composition of lipids in desiccating endosperm cells This disrupts interactions between SGs and PBs, leading to air spaces and, opacity of the mature endosperm

Methods

Results

Conclusion