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.