Introduction

In the near future, climate change will likely intensify extreme weather events, increase average temperatures and increase the frequency of heat waves and dry summers, thus becoming the main threat to food security worldwide (Abbass et al. , 2022; Seneviratne et al. , 2023). It will also have a profound impact on the distribution of arable land, with potential gains in Russia and northern China (Zhang and Cai, 2011) and probable losses in Africa, South America and Europe. At the global scale, aridity could degrade 40% of arable land (Prăvălie et al. , 2021). To address the threat of climate change in the context of a growing population, agriculture must adapt to ensure human food security, feed and non-food services (Anderson et al. , 2020).
Early sowing (ES) is a traditional agricultural practice used in arid regions to reduce the impact of drought. It increases yields effectively because it places the key developmental stages of crops under the most favorable growing conditions. For instance, ES increases the duration of the vegetative stage and the yield of soybean (Glycine max ) (Taaime et al. , 2022). For sunflower (Helianthus annuus ) and wheat (Triticum aestivum ), ES promotes flowering earlier in the year, when rainfall is more frequent, which increases the yield (Hunt et al. , 2019; Abdelsatar, 2020; Giannini et al. , 2022).
One side effect of ES is that plantlets are exposed more to chilling stress (i.e. temperatures of 1-15°C), which can decrease productivity (Li et al. , 2017). For sunflower, suboptimal temperatures during initial stages of development decrease yield by ca. 34.7 kg/ha/d (Debaeke et al. , 2017). Thus, ES seems a promising solution to mitigate impacts of drought in Mediterranean climates, but it may be more difficult to implement in temperate climates (Mangin et al. , 2017).
Phenotypic responses to cold stress such as a decrease in plant height, stem diameter, canopy area and root weight were observed for soybean and maize (Zea mays ) (Hussain et al. , 2020; Borowska and Prusiński, 2021; Hassan et al. , 2021; Walne and Reddy, 2022). Morphological changes such as plant development are caused by underlying physiological processes. Low temperatures first make plant cell membranes more rigid. The decreased fluidity has a mechanical effect on calcium channels, resulting in calcium influx into the cytosol. Changes in the calcium balance then act as a signal transduction that modulates downstream pathways (Sangwan et al. , 2001). Membrane fluidity is an important parameter that governs other crucial processes, such as vesical trafficking and membrane permeability. Fluidity is maintained by increasing the unsaturation of lipids through the activity of desaturases (Murata and Los, 1997; Thakur and Nayyar, 2013; Manasaet al. , 2021)
Plant development is a direct function of photosynthetic efficiency. Low temperatures decrease the activity of enzymes in plants, which decreases photosynthesis (i.e., “photoinhibition”). For instance, low temperatures decrease the carboxylase capacity of RuBisCO and thus photosynthetic efficiency, which decreases biomass production (Galméset al. , 2013).
The production of reactive oxygen species (ROS) is another negative effect of cold stress. At low concentrations, ROS such as nitric oxide and hydrogen peroxide can act as a signaling molecule that modulates genes involved in defense-signaling pathways. At high concentrations, ROS cause cellular damage if they are not associated with an effective ROS scavenging mechanism (Ritonga and Chen, 2020).
These physiological processes are under genetic control, which are triggered by low temperatures. The ICE-CBF-COR is a signaling cascade activated by low temperatures that modulates the expression of multiple genes in order to resist low temperatures. For instance, CBF can bind to the promotor of COR genes, which code for cryoprotective proteins and enhance cold tolerance (Ritonga and Chen, 2020). Proteins such as late embryogenesis abundant (LEA) proteins, anti-freezing proteins and cold shock proteins are synthetized under cold stress and protect plants from injury (Ding et al. , 2019). These processes have been described well for model plants such as thale cress (Arabidopsis thaliana) , but no information is available for sunflower. These observations were performed 3-48 h after exposure under controlled conditions, but under field conditions, chilling stress occurs, persist longer than 48 h, and influence all initial developmental stages and late traits such as oil yield (Mangin et al. , 2017). For instance, Allinne et al.(2009) observed a decreased photochemical efficiency, chlorophyll content and leaf area and increased electrolyte leakage with ES compared to normal sowing for sunflower immediately before flowering (i.e., 800 degree days).
Although cold can be a major abiotic stressor for summer crops in the context of new cropping practices, the impacts of early chilling stress throughout the life cycle is not well documented for sunflower. Here, we assessed impacts of cold stress and ES using modern phenotyping platforms to compare controlled and semi-controlled conditions to field experiments in order to distinguish environmental factors and determine their impacts throughout the life cycle. On molecular and physiological levels, we described impacts of low temperatures on root, hypocotyl and leaf transcriptomes, as well as on fatty acid composition. We aimed to describe sunflower plasticity in response to night chilling stress and provide a framework for future studies of sunflower tolerance to cold.