When a plant undergoes cold stress, several morphological alterations occur (Equiza et al., 2001); subsequently, root-shoot growth is restricted and productivity is reduced. In winter cereals, low-temperature stress at the vegetative phase cause leaves chlorosis and wilting and ultimately leads to necrosis and inhibited growth (Janowiak et al., 2002). Cold stress severely affects germination and seedling establishment causes delayed germination, poor emergence, reduced plant density, and uneven stand establishment in wheat (Jame and Cutforth, 2004). Winter wheat initially suffers low-temperature stress when tillering begins and whenphotosynthate assimilation and nutrient absorption sites are under development (Rinalducci et al., 2011). Cromey et al. (1998) exposed wheat plants to freezing stress (from 0 to −13°C) in a controlled chamber for 2 h, frost devastation begins at −3°C and complete burning of flag leaf and ears occurred at −7°C; consequently, a substantial reduction in grain yield was observed. Similarly, cold exposure at jointing leads to reduced leaf size, leaf area, and lower shoot biomass (Valluru et al., 2012) and limits the final output (Li et al., 2014). Additionally, applying freezing stress (−8 and −9°C) at the stem elongation stage limits the internode extension, denatures the spikelets, reduces assimilate transport, restricts the dry matter accumulation, and causes a significant reduction in grain yield (Whaley et al., 2004).

Low temperature also affects the root growth of wheat as root growth is an ecologically controlled parameter (Buriro et al., 2011; Kul et al., 2020). Root length is more sensitive to sub-optimal temperature than dry weight. It causes a significant reduction in root branching and root surface area; consequently, normal water and nutrient uptake were disrupted (Hussain et al., 2018). Restricted root surface area inhibits the ability of the plant to explore the water and nutrients resources (Richner et al., 1996).

In summary, cold stress at the initial seedling stage results in delayed emergence and poor stand establishment. Prolonged exposure to cold stress results in stunted growth, diminished root-shoot surface area, leaf chlorosis, and disturbed water and nutrient relations. Such indicators lead to a significant reduction in wheat yield and quality. Additionally, few studies have investigated roots activity with reference to low-temperature stress, which needs to be explored.

The reproductive growth phase is more sensitive to cold stress than the vegetative phase in wheat (Thakur et al., 2010). The reproductive growth stage begins with flowering, which continues with floral differentiation (into male and female parts), sporogenesis, pollen grain and embryo development, pollination, fertilization, and, finally, grain development. Plant exposure to cold contact at the reproductive growth phase causes many structural and functional deformities, leading to a reduction in growth and development. Chilling at flowering causes flower shedding, pollen tube deformation (Chakrabarti et al., 2011), pollen sterility, and ovule distortion (Ji et al., 2017), and before anthesis, it lowers down the number of grains and disrupts the grain development (Dolferus et al., 2011; Barton et al., 2014). Such conditions lead to incomplete fruit setting, which reduces the final wheat production (Hussain et al., 2018). Though counterresponse varies at every growth phase, collectively, all responses are not enough to resist net yield loss.

Imposing chilling and freezing stress at the jointing stage has severely damaged the morphological attributes (such as burned leaf blade, chlorosis, decreased shoot biomass, and denatured spikelets) compared with control (Figure 1). Assimilates accumulation during grain filling is extremely sensitive to suboptimal temperature conditions negatively influencing the grain quality and quantity (Yang and Zhang, 2006). Cold exposure at booting and flowering stages resulted in a considerable reduction in the number of grains per spike; consequently, final grain output diminished to 78% (Subedi et al., 1998). During the reproductive stage, a 1°C decrease in temperature below the threshold level may result in a 10–90% wheat crop damage (Marcellos and Single, 1984; Ji et al., 2017). A field experiment revealed that frost damage of a 5 day span (with a temperature range of 0–4°C) at the stem elongation stage might cause a nearly 15% reduction in the number of spikes and ultimately result in 14% reduction in yield loss (Li et al., 2015). If these frost spells continue, yield losses will be higher (Wu et al., 2014). In conclusion, the wheat crop is more sensitive to cold stress at the reproductive stage, especially the frost spells are disastrous, causing flower shedding, pollen infertility, denatured spikes, and incomplete/poor fruit setting, resulting in significant yield losses (Figure 2).

Primarily, cellular membranes are the first site of the plant, which is directly affected by cold stress repercussions, leading to other ultra-structural physiological and biochemical changes (Figure 3). Cold stress induces many ultrastructural alterations in cold-sensitive plant species (Pomeroy and Andrews, 1978; Kratsch and Wise, 2000), which causes the imbalance of membrane fluid content and permeability that leads to disturbance to all membrane linked physiological and biochemical processes (Bohn et al., 2007; Los et al., 2013). Most often, these adverse effects are accompanied by structural alterations in the membrane (Bohn et al., 2007), which were subsequently followed by cellular leakage of electrolytes and amino acids, diversion of electron flow toward alternate pathways (Seo et al., 2010), alterations in protoplasmic streaming, and re-distribution of intracellular calcium ions. These severe symptoms are directly correlated with injury to membrane structures of cells and changed lipid composition. Cold-induced alterations in crop plants lead to decreased ATP synthase activity, followed by inhibition of Rubisco regeneration and photophosphorylation (Yordanova and Popova, 2007). Cold-induced photo-inhibition subsequently leads to a reduction in photosynthetic activity (Groom et al., 1990; Oquist et al., 1993). If cold stress remained for a shorter duration, plants could recover their normal state, but such a situation is irreversible under prolonged duration.

In grains like wheat, photosynthesis, and bio-mass accumulations are the major sources for grain production and vital physiological processes in the crop growth phases; these processes are highly vulnerable to low-temperature stress (Rinalducci et al., 2011; Khan et al., 2017). It has been reported that cold stress causes reductions in final yield, which is associated with a decline in spike number, spike length (Karimi et al., 2011), biomass, leaf area, size, and carbohydrate metabolic reactions. Such morphological and physiological alterations are correlated with reduced photosynthetic efficiency (Theocharis et al., 2012; Valluru et al., 2012). Research findings revealed that imposing low-temperature stress (day:night, 5°C:5°C) at the seedling stage resulted in a 45% decrease in the photosynthetic rate of primary leaves as compared with control (day:night, 20°C:16°C) (Leonardos et al., 2003). Similarly, in another investigation, when wheat seedlings are subjected to low temperature (4°C) in a closed chamber for 7 days, an 18% decrease in photosynthetic activity has been recorded after 5 h. Over-excitation of photosystem II has been observed under cold stress, which triggers energy dissipation through non-radiative reactions (Cvetkovic et al., 2017). The maximum efficiency of Photosystem II decreased by 18% after 1 day exposure to cold (Venzhik et al., 2011). Further, photosynthetic activity in cold-sensitive cultivars is more sensitive to cold stress than cold-tolerant cultivars (Yamori et al., 2009). During the jointing stage, cold exposure inhibits gaseous exchange, thus reducing the quantum efficiency of photosystem II, resulting in decreased photosynthesis that leads to a 5–14% reduction in yield (Li et al., 2015). Flag leaf burning due to freezing stops the photosynthetic activity that resulted in up to 100% yield losses (Rajcan and Swanton, 2001).

Cold-induced photosynthetic inhibition is due to various reasons, i.e., reduced chlorophyll synthesis, poor chloroplast development, diminished efficiency of photosynthetic apparatus, restricted carbohydrates transportation, limited stomatal conductivity, suppressed Rubisco activity during carbon assimilation, disrupted electron transport chain, and decreased energy stock (Bota et al., 2004; Hussain et al., 2018). The chilling conditions instigate drought stress, which reduces molecular oxygen and produces ROS that cause severe damage to photosynthetic apparatus (Basu et al., 2016). During the vegetative stage, cold stress reduced the leaf area, which is considered more critical since it reduces photosynthetic activity, resulting in a source–sink imbalance (Paul and Foyer, 2001; Liu L. et al., 2019; Liu Y. et al., 2019).

Cold stress disrupts the photosynthetic activity at every growth stage, resulting in a reduction in photo-assimilation and assimilate transportation. These conditions lead to significant yield losses.

The cold stress directly or indirectly induces a series of changes in biological and biochemical functions of the wheat plant, such as decreased respiration rate, reduced enzymatic activity, oxidative stress, and deterioration of seed reserves (Li et al., 2013; Esim et al., 2014). Cold-sensitive plant species, in general, show imbalanced homeostasis of respiration in leaves compared with tolerant species (Yamori et al., 2009). A low respiration rate at the initial seedling stage limits the ATP synthesis; subsequently, the germination process is hindered (Cheplick and Priestley, 1986). The prolonged cold stress period causes severe damage to the mitochondrial structure, slows down the flow of kinetic energy, and disrupts enzymatic activity, ultimately diminishing the respiration rate (Pomeroy and Andrews, 1975; Ikkonen et al., 2020). There are not enough literature studies found in this aspect; particularly for wheat, it is still an under-explored area.

Some studies in soybean reported increased respiration rate under prolonged cold stress; the reason for such increase is irreversible metabolism (dysfunction) and accumulation of oxidized metabolites (Yadegari et al., 2008). Furthermore, it is evident from investigations that chilling triggers the alternative respiratory systems in wheat and maize. Such alternative systems of respiration play a pivotal role in mitigating chilling stress and reducing mitochondrial structural damage (Ribas-Carbo et al., 2000; Feng et al., 2008).

Respiration and photosynthesis are vital processes that define the fate of any plant life. And both physiological processes are prone to cold stress. Structural injury to mitochondria interrupts the energy flow; subsequently, the respiration process is restricted. Such conditions compelled the plant cell to exploit the energy molecules (ATP); energy imbalance disturbed the various biochemical reactions inside the plant cell. Rare studies depict that chilling prompted respiration activity through adopting alternative respiratory pathways and prevented the plant from structural damages.

Low-temperature stress affects cellular turgidity and instigates drought stress (Yadav, 2010). This drought situation reduces the root hydraulic conductivity, limits the root growth, and dents the leaf turgidity in wheat (Siddique et al., 2000), which causes unavoidable wilting of leaves. Subsequently, water relations, nutrient uptake, carbohydrate metabolism, and translocation of assimilates are severely disrupted (Li et al., 1994). Apart from this, temperature fluctuation trends alter the soil physiochemical properties that disturb the beneficial microbial activity in the soil and influence plant-nutrient relationships (Jezierska-Tys et al., 2012; Massenssini et al., 2015). Further, low temperature slows down root growth and development by reducing root length and biomass. Such a reduction in root volume minimizes the root opportunities to explore new water and nutrient resources; consequently, mineral uptake is severely reduced (Al-Hamdani et al., 1990), resulting in decreased aboveground biomass. Despite the disruption of primary nutrients (NPK), water-deficient conditions also triggered the micronutrient (i.e., Mn, Zn, Fe, Mo, etc.) deficiencies in the plant (Gavito et al., 2001), which otherwise are readily available under well-watered conditions.

In conclusion, there is a direct relationship between nutrient acquisition concerning soil temperature and available soil moisture. It is well-evidenced that chilling and drought directly influence the macro and micronutrient availability, uptake, inflow transport, enzymatic activity, and other metabolic activities in plants. Only few previous studies have been reported on nutrient relations for chilling and drought stress factors; hence, there is a dire need for further investigation.

Generally, stress accelerates the biosynthesis of ABA, followed by the closure of stomata and gene expressions (Lee and Luan, 2012). ABA is a primary intracellular receptor that stimulates the activity of secondary messengers, i.e., ROS and Ca²⁺ (Xue-Xuan et al., 2010). The instant signal perception of abiotic stress is transduced via the increased ROS and hydrogen peroxide (H₂O₂) (Saxena et al., 2016). ROS oxidative surge responded by the release of Ca²⁺ (Rao et al., 2006) that triggers the NADPH oxidase course of action and subsequently proceeds to the accumulation of antioxidant compounds (i.e., H₂O₂) (Agarwal et al., 2005). Therefore, Ca2+ is recognized as an essential component in signal transduction. Primarily, three types of Ca²⁺ proteins include CaM (calmodulin), Ca²⁺ dependent kinases, and calcineurin binding proteins. CaM was found to regulate the CBF regulon by binding with the regulatory element of gene promoter and help in cold tolerance (Doherty et al., 2009). Enhanced Ca²⁺ concentration initiates the calcium-regulated protein kinase (CDPKs), which helps in mitigating cold stress. Among 20 CDPKs, 7 responded to various abiotic stresses (Li et al., 2008). ABA-dependent pathway is also dependent on MYB/MYC (myeloblastosis) transcription factors (TFs) (Abe et al., 2003). Among 60 MYB genes of wheat, 15 were characterized as ABA regulated genes (Zhang et al., 2012), such as TaMYB33, which plays a part in the production of antioxidants, favoring ROS scavenging, assisting in proline accumulation, and modifying osmotic imbalance (Qin et al., 2012).

Cereal crops (wheat, barley, and rye) from the Poaceae family contain a large number of DRE or CBF genes, as only wheat contains 25 various kinds of CBF genes (Badawi et al., 2007). COR gene expressions are mainly regulated by CBF TFs (CBF1, CBF2, and CBF3) (Thomashow, 2001). In wheat, the role of CBF has been well-recognized toward many signal perception pathways and enhanced cold tolerance capacity (Morran et al., 2011). Vágújfalvi et al. (2003) found a positive comparative relationship between COR expression and wheat cold acclimation. The COR proteins are labeled as hydrophilic proteins that are considered affiliated with LEA or DHNs (Close, 1997). For instance, in Arabidopsis thaliana, overexpression of LEA and wheat cold specific (WCS19) augments the freeze tolerance capacity (Dong et al., 2002). DHNs or LEA protein groups are highly tolerant to osmotic stress, as cold stress also causes an osmotic imbalance in winter cereals. Hence, their accumulation is equally essential in cold acclimation (Borovskii et al., 2005). The WCS120 is an impressive cold responsive gene of wheat; it also belongs to the LEA protein family (Fowler, 2001). Along with WCS120, other COR genes responsible for cold tolerance include WCS180, WCS200, WCS66, and WCS40 (Sarhan et al., 1997); however, proteins that belong to WCS120 showed higher transduction in winter cereals and were characterized as best in cold tolerance (Vítámvás and Prášil, 2008).