Exploring the Developmental Progression of Endosperm Cavity Formation in Maize Grain and the Underlying Molecular Basis Using X-Ray Tomography and Genome Wide Association Study

Endosperm cavity (EC) in maize grain reduces yield and causes grain breakage during mechanical harvesting, hence representing a major problem in the maize industry. Despite this, little is known regarding the biological processes governing EC formation. Here, we attempted to address this issue by (i) determining the spatial and temporal progression of EC in a non-invasive manner and (ii) identifying candidate genes that may be linked to the formation of EC by using a genome wide association study (GWAS). Visualization and measurement using X-ray micro-computed tomography established that EC first appeared at the central starch endosperm at about 12 days after pollination (DAP) and became enlarged thereafter. GWAS-based screening of a panel of 299 inbred lines with a wide range of EC size identified nine candidate genes that showed significant association with EC formation. Most of the candidate genes exhibited a decrease at 12 DAP, coinciding with the timing of EC appearance. Among them, ZmMrp11 was annotated as a member encoding a multidrug resistance-associated protein that has been shown in other studies to sequestrate toxic metabolites from the cytosol to the vacuole, thereby detoxifying the cellular environment. This, together with the reduced expression of ZmMrp11 in maize grains from 12 DAP, prompted us to propose that the low expression of ZmMrp11 may block cellular detoxification in the maize endosperm cells, leading to cell death and ultimately the formation of EC.