Causes and consequences of endogenous hypoxia on growth and metabolism of developing maize kernels

Abstract

Maize (Zea mays) kernels are the largest cereal grains, and their endosperm is severely oxygen deficient during grain fill. The causes, dynamics, and mechanisms of acclimation to hypoxia are minimally understood. Here, we demonstrate that hypoxia develops in the small, growing endosperm, but not the nucellus, and becomes the standard state, regardless of diverse structural and genetic perturbations in modern maize (B73, popcorn, sweet corn), mutants (sweet4c, glossy6, waxy), and non-domesticated wild relatives (teosintes and Tripsacum species). We also uncovered an interconnected void space at the chalazal pericarp, providing superior oxygen supply to the placental tissues and basal endosperm transfer layer. Modelling indicated a very high diffusion resistance inside the endosperm, which, together with internal oxygen consumption, could generate steep oxygen gradients at the endosperm surface. Manipulation of oxygen supply induced reciprocal shifts in gene expression implicated in controlling mitochondrial functions (23.6 kDa Heat-Shock Protein, Voltage Dependent Anion Channel 2) and multiple signalling pathways (core hypoxia genes, cyclic nucleotide metabolism, ethylene synthesis). Metabolite profiling revealed oxygen-dependent shifts in mitochondrial pathways, ascorbate metabolism, starch synthesis, and auxin degradation. Long-term elevated oxygen supply enhanced the rate of kernel development. Altogether, evidence here supports a mechanistic framework for the establishment of and acclimation to hypoxia in the maize endosperm.

Spatio-temporal dynamics of the metabolome of climacteric fruit during ripening and post-harvest storage

“…The existence of gas gradients in pome fruit and other plant organs has been shown by us and other groups experimentally (Banks, 1983;Bologa et al, 2003;Lammertyn et al, 2003a;Berry and Society, 2008;Borisjuk and Rolletschek, 2009;Ho et al, 2010b;Pedersen et al, 2020) and in silico (Ho et al, 2011(Ho et al, , 2016Verboven et al, 2013;Nugraha et al, 2022;Verreydt et al, 2022;Langer et al, 2023). If the supply of O 2 by diffusion is too small, the oxidative phosphorylation stalls because of lack of substrate, and the TCA cycle is reconfigured and the metabolic flux through the latter is decreased dramatically (Bailey-Serres and Voesenek, 2008).…”

Is hypoxia good or bad? Role of oxygen levels in maize kernel development

“…All of these questions have been addressed by Langer et al (2023) . In this issue of Plant Physiology , the authors found that development of localized hypoxic environments inside maize kernels is not a result of domestication but a conserved feature observed in modern maize and wild relatives.…”

“…The work of Langer et al (2023) is exciting as it uncovered structural features of maize kernels and solves long standing questions about formation of endogenous oxygen gradients in this organ. The research also raises questions regarding the formation of porous layers on the chalazal region and the possibility of manipulating internal oxygen availability through the void network and the lipidous layers on the outer endosperm.…”

“…More work will be needed to test these possibilities and the contributions of the lipid and cutin/waxin layers on gas diffusion. Modeling and sophisticated visualization techniques used by Langer et al (2023) also provide a framework to study other aspects of kernel development, such as water relations and source/sink dynamics.…”