Maize plants can enter a standby mode to cope with chilling stress

Laëtitia Riva-Roveda, Brigitte Escale, Catherine Giauffret, Claire Périlleux

European Flint maize inbred lines are used as a source of adaptation to cold in most breeding programs in Northern Europe. A deep understanding of their adaptation strategy could thus provide valuable clues for further improvement, which is required in the current context of climate change. We therefore compared six inbreds and two derived Flint x Dent hybrids for their response to one-week at low temperature (10 °C day/7 or 4 °C night) during steady-state vegetative growth. Leaf growth was arrested during chilling treatment but recovered fast upon return to warm temperature, so that no negative effect on shoot biomass was measured. Gene expression analyses of the emerging leaf in the hybrids suggest that plants maintained a 'ready-to-grow' state during chilling since cell cycle genes were not differentially expressed in the division zone and genes coding for expansins were on the opposite up-regulated in the elongation zone. In photosynthetic tissues, a strong reduction in PSII efficiency was measured. Chilling repressed chlorophyll biosynthesis; we detected accumulation of the precursor geranylgeranyl chlorophyll a and down-regulation of GERANYLGERANYL REDUCTASE (GGR) in mature leaf tissues. Excess light energy was mostly dissipated through fluorescence and constitutive thermal dissipation processes, rather than by light-regulated thermal dissipation. Consistently, only weak clues of xanthophyll cycle activation were found. CO2 assimilation was reduced by chilling, as well as the expression levels of genes encoding phosphoenolpyruvate carboxylase (PEPC), pyruvate orthophosphate dikinase (PPDK), and the small subunit of Rubisco. Accumulation of sugars was correlated with a strong decrease of the specific leaf area (SLA). Altogether, our study reveals good tolerance of the photosynthetic machinery of Northern European maize to chilling and suggests that growth arrest might be their strategy for fast recovery after a mild stress.