Warm nights disrupt transcriptome rhythms in field-grown rice panicles

Abstract

Significance The effects of warmer nighttime temperatures (WNT) on crops are one poorly understood dimension of climate change. WNT result from the asymmetrical increase in nighttime versus daytime temperatures. In rice, WNT reduce grain yield and quality. WNT reduce the amplitude of daily temperature cycles plants use to set their circadian clock. Therefore, we examined how WNT affect the timing of molecular activities. In field-grown plants, WNT alter the daily pattern of the transcriptome. Genes with strong rhythmic expression and those under circadian control are affected most by WNT. Many candidate regulators of the disrupted genes are circadian clock associated, emphasizing the altered timing under WNT. The pathways and mechanisms identified can assist efforts to identify lines tolerant to WNT. In rice, a small increase in nighttime temperature reduces grain yield and quality. How warm nighttime temperatures (WNT) produce these detrimental effects is not well understood, especially in field conditions where the typical day-to-night temperature fluctuation exceeds the mild increase in nighttime temperature. We observed genome-wide disruption of gene expression timing during the reproductive phase in field-grown rice panicles acclimated to 2 to 3 °C WNT. Transcripts previously identified as rhythmically expressed with a 24-h period and circadian-regulated transcripts were more sensitive to WNT than were nonrhythmic transcripts. The system-wide perturbations in transcript levels suggest that WNT disrupt the tight temporal coordination between internal molecular events and the environment, resulting in reduced productivity. We identified transcriptional regulators whose predicted targets are enriched for sensitivity to WNT. The affected transcripts and candidate regulators identified through our network analysis explain molecular mechanisms driving sensitivity to WNT and identify candidates that can be targeted to enhance tolerance to WNT.