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

Abstract

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.

Engineering 6-phosphogluconate dehydrogenase to improve heat tolerance in maize seed development

“…4B). Under controlled conditions, the W22 inbred shows reduced grain-fill under elevated nighttime temperatures (6). In these two plantings, the grain-fill period from first pollination until harvest showed no difference in the length of time at temperatures above 33°C (Fig.…”

“…Plastidic 6PGDH activity is reduced by heat treatment. Long-term growth at elevated temperatures during grain-fill reduced the level of 6-phosphogluconate in endosperm (6) suggesting that flux through the PPP could be a heat sensitive step in endosperm metabolism. Heat stability of 6PGDH was tested by treating W22 endosperm extracts at 42ºC and assaying isozyme activity by native PAGE (Fig.…”

“…Accelerated development during grain-fill reduces the time available for seed storage molecule accumulation (6). Heat also reduces gene expression of carbohydrate metabolic enzymes, potentially reducing the flux of fixed carbon into carbohydrate and protein storage (6,31,32). It is important to understand these mechanisms and how they interrelate in order to breed cereals that maintain yield in high temperature environments.…”

“…The first committed step of starch biosynthesis is catalyzed by ADP-glucose pyrophosphorylase (AGPase) and is a thermolabile enzyme (6). Increasing heat stability of AGPase in maize endosperm also results in mitigation of heat-induced yield losses (33,34).…”

“…Metabolite profiling of maize pgd3 mutant endosperm showed a moderate increase in histidine and less than two fold changes in pentose levels suggesting that these metabolite pools are much less impacted than would be predicted by Arabidopsis mutants (14). Intriguingly, metabolite profiling of heat-stressed maize endosperm shows that the substrate for 6PGDH, 6-phosphogluconate, is reduced while ribose products are increased suggesting a perturbation of oxPPP during heat stress that is inconsistent with specific loss of 6PGDH activity (6). However, this study also tested 20 carbon metabolism enzyme activities, and six were differentially affected by high nighttime heat supporting more complex heat stress impacts on carbon metabolism than simply reducing 6PGDH activity.…”