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

Cellular functions of molecular oxygen are diverse. The most prominent role is as a substrate for oxidative phosphorylation and ATP production in the mitochondria. Low oxygen (hypoxia) can thus be detrimental for most plant tissues if levels drop below the threshold needed to sustain respiratory demands (Sasidharan et al. 2021). For instance, oxygen deficiency can quickly shift from aerobic production of 36 ATP to 2 ATP produced during glycolysis and fermentation (van Dongen and Licausi 2015). Despite these negative effects, hypoxia is common in nonphotosynthetic tissues with high metabolic demands and high cell density, such as meristems and seeds (Borisjuk and Rolletschek 2009; Weits et al. 2019). However, in these organs, oxygen limitation is not detrimental, but instead is central to their development (Kelliher and Walbot 2012, 2014). For example, maize (Zea mays) kernels normally grow with a low-oxygen, high-sugar environment inside their endosperm (Rolletschek et al. 2005). Early work by Rolletschek et al. (2005) has shown that steep oxygen gradients occur inside the maize endosperm, while levels are 10-fold higher in the embryo. The work indicates that oxygen gradients influence the fate of resource partitioning, local ATP concentration, and metabolite distribution. Moreover, transcriptional modifications are also evident in hypoxic niches (Koch et al. 2000; Gayral et al. 2017). All of these components favor starch accumulation in the hypoxic endosperm and lipid accumulation in the more oxygenated embryo. Questions remain about the mechanisms and other features driving the formation of oxygen gradients inside maize kernels, their effect on gene expression, signaling, and metabolism, and the temporal dynamics during seed 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. All the genotypes tested showed a steep reduction in oxygen levels starting at the apical portion of the kernel [immediately below the surface (100 to 400 μm)] and extending throughout the endosperm. Levels increased sharply at the basal transfer layer (lower endosperm) which remains oxygenated (Fig. 1A). The profile of oxygen levels paralleled that of starch and water distribution during seed filling. Starch accumulation in the upper-mid endosperm displaced water towards more oxygenated regions in the transfer layer and embryo (Fig. 1B). These oxygen and starch/water gradients suggested a potential role for the chalazal pericarp at the basal end of the kernel in the maintenance of oxygenated locales. Using X-ray μ-CT, the authors found a porous layer in the basal endosperm that extends towards the embryo (Fig. 1C). This identified void network has high diffusivity and can provide more than 40% of the oxygen that enters the endosperm and that is available to sustain embryonic respiratory demands. The lack of porous layers in the endosperm and outer pericarp was consistent with a higher resistance to gas diffusion and lower oxygen levels. These results, together with the observation that empty kernel sections in sugars will eventually be exported transporter 4c (sweet4C) mutants remained oxygenated, indicated the presence of a diffusion barrier at the endosperm level rather than at the nonphotosynthetic pericarp as has been previously suggested (Rolletschek et al. 2005; Borisjuk and Rolletschek 2009). The enhanced diffusion N ew s an d V ie w s