Effects of long‐term exposure to elevated temperature on Zea mays endosperm development during grain fill

Summary Cereal yields decrease when grain fill proceeds under conditions of prolonged, moderately elevated temperatures. Endosperm‐endogenous processes alter both rate and duration of dry weight gain, but underlying mechanisms remain unclear. Heat effects could be mediated by either abnormal, premature cessation of storage compound deposition or accelerated implementation of normal development. This study used controlled environments to isolate temperature as the sole environmental variable during Zea mays kernel‐fill, from 12 days after pollination to maturity. Plants subjected to elevated day, elevated night temperatures (38°C day, 28°C night (38/28°C])) or elevated day, normal night (38/17°C), were compared with those from controls grown under normal day and night conditions (28/17°C). Progression of change over time in endosperm tissue was followed to dissect contributions at multiple levels, including transcriptome, metabolome, enzyme activities, product accumulation, and tissue ultrastructure. Integrated analyses indicated that the normal developmental program of endosperm is fully executed under prolonged high‐temperature conditions, but at a faster rate. Accelerated development was observed when both day and night temperatures were elevated, but not when daytime temperature alone was increased. Although transcripts for most components of glycolysis and respiration were either upregulated or minimally affected, elevated temperatures decreased abundance of mRNAs related to biosynthesis of starch and storage proteins. Further analysis of 20 central‐metabolic enzymes revealed six activities that were reduced under high‐temperature conditions, indicating candidate roles in the observed reduction of grain dry weight. Nonetheless, a striking overall resilience of grain filling in the face of elevated temperatures can be attributed to acceleration of normal endosperm development. Significance Statement Prolonged moderate temperature elevation during cereal grain fill reduces the period of storage compound accumulation, and hence yield, but the mechanisms responsible are unknown. This study revealed that the complete program of apparently normal development is executed, but at a faster rate, therefore enabling new approaches toward ameliorating yield loss in critical food crops as average global temperatures rise.