Abiotic stresses have a detrimental impact on plant growth and productivity and are a major threat to sustainable crop production in rapidly changing environments. Proline, an important amino acid, plays an important role in maintaining the metabolism and growth of plants under abiotic stress conditions. Many insights indicate a positive relationship between proline accumulation and tolerance of plants to various abiotic stresses. Because of its metal chelator properties, it acts as a molecular chaperone, an antioxidative defence molecule that scavenges reactive oxygen species (ROS), as well as having signalling behaviour to activate specific gene functions that are crucial for plant recovery from stresses. It also acts as an osmoprotectant, a potential source to acquire nitrogen as well as carbon, and plays a significant role in the flowering and development of plants. Overproduction of proline in plant cells contributes to maintaining cellular homeostasis, water uptake, osmotic adjustment and redox balance to restore the cell structures and mitigate oxidative damage. Many reports reveal that transgenic plants, particularly those overexpressing genes tailored for proline accumulation, exhibit better adaptation to abiotic stresses. Therefore, this review aims to provide a comprehensive update on proline biosynthesis and accumulation in plants and its putative regulatory roles in mediating plant defence against abiotic stresses. Additionally, the current and future directions in research concerning manipulation of proline to induce gene functions that appear promising in genetics and genomics approaches to improve plant adaptive responses under changing climate conditions are also highlighted.
INTRODUCTION
Abiotic stresses on plants have become more frequent and severe due to rapid global climate change (Surabhi, 2018; Ali et al. 2019). Commonly, plants are confronted by different abiotic stresses which interrupt cellular membrane and developmental processes throughout their life cycle (Jeandroz & Lamotte, 2017; Aamer et al. 2018; Cheng et al. 2018; Ghaffari et al. 2019; Hasanuzzaman et al. 2019; Kerchev et al. 2020; Mohammadi et al. 2020). Abiotic stresses, for instance, drought, salinity and heavy metals, are responsible for the production of excess quantities of reactive oxygen species (ROS), peroxidation of lipids, activation of antioxidant systems and accretion of osmolytes (Kazemi-Shahandashti & Maali-Amiri, 2018; Yang & Guo, 2018; Khan et al. 2019; Sharma et al. 2019; Ghosh et al. 2021).
Plant cells normally allow the influx, gathering and synthesis of proline and accumulate it to maintain homeostasis and keep the cell turgid for growth and development in abiotic stress environments (Parida & Das, 2005; Sharma & Dietz, 2006; Burg & Ferraris, 2008). Proline acts as a chelator and can chelate heavy metals in plants (in vitro condition) and form a nontoxic metal–proline complex (Sharma et al. 1998). It also acts as a molecular chaperone, preserving protein integrity and speeding up the activity of many enzymes (Rajendrakumar et al. 1997). The oxidation of one proline molecule produces 30 ATP equivalents, and this amino acid is required for sustaining high energy-requiring processes (Atkinson, 1977). In response to harsh environmental conditions, increased synthesis of proline has widely been observed (Ashraf & Harris, 2004; Hoque et al. 2007; Urano et al. 2009; Lugan et al. 2010).
Proline lessens the damaging effects of a number of abiotic stresses and protects cells; increased proline accumulation is also regarded as a reflection of abiotic stress tolerance. Normally, plants recognize stress through their root systems and transmit signals to formulate or unify protective components in many parts to alter their physiological and morphological settings (Siopongco et al. 2015). One of the most important responses of plants to osmotic and oxidative stress is the biosynthesis and accumulation of proline.
The accretion of proline is the outcome of different stress signalling pathways (phytohormones, calcium signalling and mitogen-activated protein (MAP) kinase pathways). Proline is essential for the existence of plants under an abiotic stress environment. The biosynthesis of proline has already been studied in detail (Trovato et al. 2008; Verslues & Sharma, 2010; Feng et al. 2016). Furthermore, multiple studies have indicated that plants with modified metabolism (genetically engineered plants) to induce proline biosynthesis have improved performance and tolerance to abiotic stresses. Thus, controlling cellular osmotic balance, ion homeostasis and activation of enzymatic, as well as non-enzymatic antioxidant systems, are the most important conserved mechanisms that confer stress tolerance in plants (Zhu, 2001; Munns, 2002; Vinocur & Altman, 2005).
In this review, efforts have been made to provide a comprehensive update related to proline biosynthesis and metabolism in plant responses to abiotic stress conditions. In addition, the regulatory roles of proline in physiological and phytohormonal associations to induce flowering and developmental processes that confer abiotic stresses are addressed. The current and future trends in research aiming to improve plant performance, especially under abiotic stress scenarios using cutting-edge genomics and biotechnological tools, are also reviewed.
OVERVIEW OF PROLINE BIOSYNTHESIS AND METABOLISM IN CROP PLANTS
Proline is one of the most studied osmoprotectants in plants (Rejeb et al. 2014; Kaur & Asthir, 2015; Zandalinas et al. 2018). Biosynthesis of proline usually occurs either through the glutamate pathway or the ornithine pathway (Trovato et al. 2008; Verslues & Sharma, 2010). Proline can be accumulated de novo, through decreased degradation, or both (Dos Reis et al. 2012). Figure 1 depicts the process of proline biosynthesis and its diverse involvement in mediating abiotic stress tolerance in plants. Proline synthesis occurs in the cytoplasm and/or chloroplasts of plants: glutamate, with the help of the P5CS enzyme, is then reduced to L-glutamate γ-semialdehyde (GSA) and then further changed into pyrroline-5-carboxylate (P5C). Thus, pyrroline-5-carboxylate reductase (P5CR) plays a major role in reducing P5C to proline. In mitochondria, however, the action of proline dehydrogenase or proline oxidase enzymes results in the formation of pyrroline-5-carboxylate from proline and pyrroline-5-carboxylate dehydrogenase (P5CDH), which finally replenishes glutamate from P5C. In a different approach, proline can also be produced from ornithine, which is initially transmitted via the ornithine-delta-aminotransferase (OAT) enzyme, delivering GSA and P5C, which are then converted to proline (Verbruggen & Hermans, 2008; Liang et al. 2013; Rai & Penna, 2013; Iqbal et al. 2014).
An overview showing the multifaceted role of proline in plant adaptive physiological processes mediating abiotic stress tolerance. Upon ‘seeing’ the abiotic stress signal, the related signalling pathway is initiated and results in the induction of stress-responsive transcription factors which, consequently, upregulate stress-responsive genes related to biosynthesis and accumulation of proline to protect and increase plant tolerance to encountered abiotic stresses.
The glutamine pathway for proline synthesis functions under osmotic stress conditions, whereas the ornithine pathway works under limited nitrogen situations as well as seedling development in plants (Roosens et al. 1998; Armengaud et al. 2004). There are two genes involves in the encoding: P5CS and P5CR in most plants (Furlan et al. 2020).
In general, the conversion product of P5C is responsible for generation of a huge amount of ROS during the biosynthesis of proline (Hellmann et al. 2000; Szekely et al. 2008). Therefore, if the stress is relieved, plants should degrade ROS promptly. Inside mitochondria, two genes encode PDH during catabolism of proline, whereas just one gene, P5CDH, has been reported in Arabidopsis and in Nicotiana tabacum plants (Kiyosue et al. 1996; Verbruggen et al. 1996; Ribarits et al. 2007). The alternation between proline and glutamate is often known as the ‘proline cycle’ (Verslues & Sharma, 2010).
In general, the only way for plants to degrade an excess amount of proline seems to be the catabolic pathway that includes PDH and P5CDH. Deuschle et al. (2001) and Nanjo et al. (2003) demonstrated that Arabidopsis PDH mutants (missing a useful PDH) and P5CDH mutants (without a functioning P5CDH) were oversensitive to exogenously supplied proline and were unable to remove excess proline. P5CDH overproduction increases the rate of P5C degradation, thereby affecting the death of cells (Hellmann et al. 2000; Deuschle et al. 2001). Proline can be synthesized in various subcellular compartments, depending on environmental conditions (Szabados & Savoure, 2010). Research has shown that proline biosynthesis in Arabidopsis is regulated by P5CS2 (Szekely et al. 2008; Szabados & Savoure, 2010), which is found in meristematic tissue division (Madan, 1995; Deuschle et al. 2001; Tripathi & Gaur, 2004). The stress-induced P5CS1 gene in Arabidopsis regulates proline synthesis in chloroplasts (Savoure et al. 1995; Strizhov et al. 2003; Szekely et al. 2008; Szabados & Savoure, 2010). In abiotic stress environments, an upgraded rate of proline biosynthesis has been identified, which can maintain a low NADPH:NADP+ ratio, adding support to the electron stream between excitation hubs of the photosynthetic process, maintain the redox equilibrium and reduce photoinhibition and damage to the photosynthetic apparatus in chloroplasts (Hare & Cress, 1997).
HOW PROLINE RESPONDS IN VARYING ENVIRONMENTS AND A BIOENGINEERING APPROACH: DEVELOPMENT OF PROLINE-INDUCED STRESS-TOLERANT CROPS
Salinity
Salt stress is one of the key constraints restricting agricultural production, affecting at least 20% of arable land worldwide (Zhu & Gong, 2014; Rizwan et al. 2015). Salinity is responsible for inducing osmotic and ionic (high Na+/K+ ratio) stresses, which cause water deficit, phytotoxicity and nutrient imbalance in plants (Sheldon et al. 2017; Safdar et al. 2019; van Zelm et al. 2020). Salt increases oxygenase activity by impeding the carboxylase action of RuBPcase under saline conditions. At high proline concentrations, the oxygenase activity is potentially reduced. Hence, proline plays a key role in shielding photosynthetic activity during abiotic stress (Bohnert et al. 1992; Rajendrakumar et al. 1994; Sivakumar et al. 2000; Hamilton & Heckathorn, 2001). Reducing expansion of the leaf surface is the most common response to salt stress (Munns, 2002), and exogenously applied proline can improve salt tolerance in crop plants (Heuer, 2016). For instance, foliar application of proline enhanced plant growth and yield traits in salts tressed Zea mays (Alam et al. 2016). The combined application of nitrogen and sulphur also improved salt stress impact on photosynthetic activity of plants with upgraded production of proline (Rais & Masood, 2013). In halophyte species of different families, osmotic modification mediated by accumulating of proline has widely been reported (Deuschle et al. 2001; Lokhande et al. 2010; Cvikrova et al. 2013; Slama et al. 2015). Application of exogenous proline reduced the Na+/ K+ ratio in salt-affected rice plants (Nounjan et al. 2012).
Application of proline suppresses the uptake of Na-induced trisodium-8-hydroxy-1,3,6-pyrenetrisulfonic acid (an apoplastic tracer) and accretion of Na+ (Sobahan et al. 2009). In saline zones with an increased degree of proline accumulation, the salt-tolerant Bangladesh Rice Research Institute (BRRI) rice variety, dhan54, showed increased salt tolerance (Hasanuzzaman et al. 2014). Crop plants exposed to salt stress had been found to increase activity of ROS scavenging enzymes, such as peroxidase, superoxide dismutase and catalase, leading to improved levels of proline generation (Hoque et al. 2008; Islam et al. 2009). Several studies have found that proline is associated with increasing salinity tolerance of groundnut (Arachis hypogaea L.) (Hayat et al. 2012), tomato (Solanum lycopersicum L) (Kahlaoui et al. 2018), pea (Pisum sativum) (Shahid et al. 2014).
Drought
Research has demonstrated that drought induces proline accumulation in numerous plants and that exogenous proline application contributes significantly to ensure drought tolerance in crop plants (Yamada et al. 2005; Vendruscolo et al. 2007; El-Beltagi et al. 2020). Mohammadkhani & Heidari (2008) showed that proline content in Zea mays L. leaves was 1.56–3.13 times higher than in control leaves under dehydration. In another experiment, a 56-day exposure to water deficit resulted in a 2.4-fold increase in shoot proline levels of drought-stressed oak compared to control shoots (Oufir et al. 2009).
Ali et al. (2013) reported that exogenous proline application significantly increased sugar, oil, moisture, protein, fibre and ash content in seeds under drought conditions. In addition, the content of oleic and linoleic acid and concentrations of antioxidants, viz. flavonoids carotenoids, phenolics and tocopherols, increased significantly. Proline significantly improved maize tolerance to drought (60% field capacity, 15 days) in a study using exogenous proline (30 and 60 mM as foliar spray) by enhancing growth and development, photosynthesis rate, sub-stomatal CO2, stomatal conductance and photosynthetic pigment levels in drought stress scenarios (Ali et al. 2007). Moreover, previous studies indicated that proline caused drought tolerance in lentil (Lens culinaris) (Molla et al. 2014; Bekka et al. 2018).
Flooding/waterlogging
Flooding is abiotic stress that drastically affects the normal growth, physiological functions and yield of plants (Jackson & Ram, 2003; Normile, 2008; Jackson et al. 2009; Bailey-Serres et al. 2010). Waterlogging causes hypoxic conditions around the root system of plants, affecting water and nutrient uptake, carbohydrate mobilization, ROS metabolism, production of superoxide radicals, hydrogen peroxide and hydroxyl radical, as well as the peroxidation of membrane lipids, resulting in mechanical damage to the water-stressed parts (Ram et al. 1999; Jackson & Colmer, 2005; Wu et al. 2013; Pucciariello et al. 2014; Yang et al. 2015; Arbona et al. 2017). Reduced oxygen, sunlight and carbon dioxide in flooded conditions impede photosynthesis and aerobic respiration, resulting in a scarcity of carbohydrates, thus limiting growth and development of crop plants (Voesenek & Bailey-Serres, 2013). To cope with this flood stress, plants use different morphological, physiological and anatomical changes to protect themselves (Colmer & Voesenek, 2009; Striker & Colmer, 2017). The most common but important morphological adaptation to flooding is the growth of an adventitious root system that aids in uptake of water and nutrients under such submerged states (Zhang et al. 2017). The generation of aerenchyma in plant tissues is an anatomical response, which allows the passage of oxygen from shoots to root tissues (Colmer, 2003).
When exposed to flooding, there was an increase in proline content in rice plants through adjusting osmotic potential in the cytoplasm (Chanu & Sarangthem, 2015). In response to waterlogging, there was also an increase of GR (glutathione reductase) activity in citrus seedlings (Arbona et al. 2008). According to Barickman et al. (2019), there was a 58.9% increase in proline concentration in leaf tissue of waterlogged cucumber plants in comparison with non-waterlogged conditions.
Heavy metals
On exposure to heavy metals, increased accumulation of proline has been reported in various plant species (Chen et al. 2001; Zengin & Munzuroglu, 2005; Radic et al. 2010; Sofy et al. 2020). In plants, prior to entering the xylem and being moved to the shoot, heavy metals in the soil can enter through the roots by either symplastic or apoplastic pathways (Lux et al. 2011). Delivery through the phloem can also play a decisive role in metal transport (Mendoza-Cozatl et al. 2011). Several experiments revealed that metal toxicity leads to leaf chlorosis, growth reduction, changes in secondary structure of proteins, necrosis and modifications to the redox status of the cell, ultimately leading to plant death (Nies, 1999; Sandalio et al. 2001; Nazar et al. 2012; Asgher et al. 2013; Kapoor & Bhardwaj, 2014).
Proline eliminates ROS and increases the function of various antioxidant enzymes (Islam et al. 2009; Hayat et al. 2013). In cells of Nicotiana tabacum, exogenous proline can restore membrane integrity (Islam et al. 2009). Proline pretreated rice plants displayed tolerance to mercury through removing ROS. Similarly, cadmium (Cd) tolerance in Triticum aestivum increased proline content (Khan et al. 2015).
Proline expression is amplified under all test concentrations of Cd and can chelate Cd in a non-hazardous complex of Cd–proline (Sharma et al. 1998; Aly, 2012). Exposure to heavy metal stress leads to accumulation of proline and accelerates the development of phytochelatins that chelate metals and thus reduce metal toxicity (De Knecht et al. 1994). Toxicity of Hg2+ in rice (Oryza sativa) is also reduced by proline pretreatment, which helps to eliminate ROS, particularly H2O2 (Doke, 1997). However, in fighting metal toxicity, although application of proline typically prevents the damaging effects at optimal doses, at higher doses it can impede growth (Ehsanpour & Fatahian, 2003; Nanjo et al. 2003; Ashraf et al. 2008). An early study found that proline mitigates selenium toxicity (Aggarwal et al. 2011) in common bean (Phaseolus vulgaris L).
Extreme temperature
Heat stress is becoming a major agricultural problem as global temperatures rise, affecting crop yield and causing morpho-anatomical, physiological, biochemical and genetic changes in plants (Wahid et al. 2007). Heat affects plants at different development stages, and high temperature reduces seed germination, photosynthesis and respiration, as well as membrane permeability (Xu et al. 2013). Both high and low temperatures have a significant impact on plant growth and development. Any deviation from optimum temperature results in membrane disturbances, fluctuations in protein content, enzyme activity and amino acids, leading to electrolyte leakage from cells (Hayat et al. 2012). Low-temperature treatment of tropical and subtropical plants, e.g. soybean and mung bean, resulted in severe physiological and biochemical modifications, particularly associated with ROS (Mittler, 2002). Seed treated with low temperature had lower germination as well as inhibited growth, thus reducing the yield (Larcher, 1981). In A. thaliana, exogenously applied proline enhanced seed germination (Hare et al. 2003). Moreover, exogenous application of proline improved tolerance to chilling stress at 5 °C for 2–6 days (Hayat et al. 2012).
Exogenous proline is a reactive oxygen scavenger, reduces lipid peroxidation and can also act as a source of carbon and nitrogen that improves seedling growth in Vigna radiata exposed to chilling stress (Posmyk & Janas, 2007). Treatment of chickpea with proline alleviated the production of H2O2 and malondialdehyde (MDA) at 40/35 °C and 45/40 °C (Kaushal et al. 2011). Exogenous application of proline enhanced the resilience of barley leaves to high temperatures (45 °C) by stabilizing complex II of the electron transport system (Oukarroum et al. 2012).
Plant–microbial signalling to alleviate abiotic stress toxicity
The important role of microorganisms in alleviating abiotic stresses in plants has become an area of great concern in the recent decades (Nadeem et al. 2014). Microbial diversity is the most important and complex living system on Earth. Due to rapid changes in climate conditions, it has now become imperative to define and interpret plant–microbe relationships in terms of protection against abiotic stresses (Meena et al. 2017). Microbes, with their intrinsic metabolic and genetic capacities, can contribute to alleviating abiotic stresses in plants (Gopalakrishnan et al. 2014). The plant microbiome delivers fundamental support to plants in acquiring nutrients, resisting diseases and tolerating abiotic stresses (Turner et al. 2013). The microbiome interactions with plants provoke various local and systemic responses that improve plant metabolic capacity to fight abiotic stress (Nguyen et al. 2016).
Inoculation with arbuscular mycorrhizal fungi (AMF) led to more proline accretion in leaves and increased P5CS activity under waterlogged conditions, and the AMF Funneliformis mosseae made a positive contribution to waterlogging tolerance of peach plants by promoting proline and chlorophyll biosynthesis (Tuo et al. 2015). Kumari et al. (2015) inoculated soybean with Pseudomonas sp. AK-1 and Bacillus sp. SJ-5 that induced systemic tolerance (IST) in response to salinity stress through proline accumulation. Increased proline accumulation was also reported upon inoculation of wheat with the bacterial endophytes Azospirillum sp. and B. aquimaris SU8 that alleviated salinity stress (Zarea et al. 2012; Bal et al. 2013). Maximum accumulation of proline (298 μg g−1 fresh weight) was seen under 1.5 M NaCl stress by addition of Staphylococcus haemolyticus (ST-9), although further accumulation of proline decreased with increasing salt concentration (Ramos-Cormenzana, 2020). Tomato plants inoculated with Pseudomonas frederiksbergensis exhibited tolerance to chilling stress through increases in proline content and antioxidant enzymes (Subramanian et al. 2016). Plants treated with Bacillus strains increased proline content when exposed to a water stress, possibly due to the upregulation of P5CS, which is related to biosynthesis of proline, and inhibition of expression of the gene ProDH, which is mainly involved in metabolism of proline (Yoshiba et al. 1997).
PROLINE-RELATED METABOLIC FLUX
Carbohydrate regulation
The production and accumulation of soluble sugars directly contributes to radical scavenging, osmotic adjustment, carbon storage and stabilization of protein structures (Huisinga, 1964; Dubey & Singh, 1999). Sugars are important for osmotic adjustment in several plant species and function as osmoprotectants, substrates for growth and regulators of gene expression during abiotic stress (Koch, 1996; Ghosh et al. 2021). Increased total soluble sugar (TSS) content of plants under salinity stress is one of the vital defence strategies to cope with salinity stress. An increased amount of proline and TSS in wheat inoculated with PGPR (Plant Growth Regulating Rhizobacteria) significantly improved osmotolerance (Upadhyay et al. 2011). Some rice cultivars and Medicago species showed increases in TSS under saline conditions (López et al. 2008). Additionally, the enhanced root colonizing capacity of Pseudomonas sp. and ability to produce exopolysaccharides (EPS) leads to enhanced salt tolerance (Etesami, 2019). An increase in trehalose has also been found in drought-stressed Vigna sinensis (Vurukonda et al. 2016).
Exopolysaccharide secretion by PGPR forms an organo-mineral sheath around the microbial cells, which enables specific bacteria to survive under abiotic stress conditions and confers drought tolerance to plants through osmotic and intracellular adjustment (Sandhya et al. 2009). Under stress conditions, bacteria persist in the form of biofilm communities, providing an extracellular matrix for an infinite range of macromolecules. It has been suggested that the major components of biofilms in the model bacterium Bacillus subtilis are polysaccharides and Tas A protein, and mutation of these components have severe effects on biofilm production (Timmusk, 2003).
Arabidopsis plants produce a large amount of raffinose and galactinol, which are involved in tolerance to drought, high salinity and cold stresses, and these also act as signals to mediate abiotic stress responses (Valluru and Van den Ende, 2011).
Polyamines
Polyamines are found in living cells and participate in various cellular mechanisms (Ghosh et al. 2021). Levels of polyamines and proline are linked as their biosynthetic and catabolic pathways share some common intermediates (Aziz et al. 1998). During metabolic processing, oxidative deamination of putrescine yields pyrroline, which can be used as a substrate for proline synthesis (Bagni & Tassoni, 2001). In contrast, accumulated proline can be catabolized to glutamate, which provides a substrate in polyamine synthesis (Nanjo et al. 2003). Transgenic plants containing higher levels of proline and polyamines have been shown to have better abiotic stress tolerance (Simon-Sarkadi et al. 2006b). In plants, putrescine, spermidine and spermine are the most abundant polyamines and have a significant role in mitigating different abiotic stresses (de Oliveira et al. 2017). The cationic behaviour of polyamines allows them to work together with all negatively charged cellular components, such as DNA, RNA, phospholipids and proteins (Liu, 2006; Pang et al. 2007; Kusano et al. 2008). Polyamines are also well known for their ability to block ion channels (the mode in which they achieve osmotic adjustment through inorganic ions) and scavenging ROS in plants. Putrescine, spermidine and spermine improve drought tolerance (Sadeghipour, 2019) by increasing net photosynthesis, soluble protein content, relative water content and salinity tolerance in Vigna radiata (Nahar et al. 2016). An increase in levels of putrescine has been observed in response to chilling stress in wheat (Nadeau et al. 1987). Exogenous application of spermidine and putrescine increase postharvest shelf-life of Capsicum annuum (Patel et al. 2019).
Aromatic compounds (e.g. 2-acetyl-1-pyrroline)
The compound 2-acetyl-1-pyrroline (2AP) is the main compound in aromatic rice varieties. The Δ1-pyrroline-5-carboxylate synthetase (P5CS) gene is reported to control proline synthesis in plants and is the precursor of 2AP (Kaikavoosi et al. 2015). 2AP is the main flavour compound of fragrant rice varieties. with a pop-corn-like aroma (Buttery et al. 1982; Buttery, 1983). Increases in the level of 2AP were found through feeding rice seedlings and calli with amino acids, such as proline, ornithine and glutamic acid (Yoshihashi et al. 2002a). Proline is a prominent amino acid that leads to maximum increases in 2AP levels. Increasing 2AP and GABA content was observed in rice grains during shade treatment at grain filling stage in Yuxiangyouzhan and Nongxiang 18 rice varieties of south China (Mo et al. 2015).
Rice plants accumulate significantly larger amounts of precursors like proline when exposed to abiotic stress, particularly drought and salinity stress at vegetative and reproductive stages, and these effectively enhance 2AP content in rice grains (Yoshihashi et al. 2002b; Poonlaphdecha et al. 2012). Recently, molecular mechanisms like RNAi have been employed to silence the betaine aldehyde dehydrogenase 2 (BADH2) gene and induce 2AP in japonica rice (Niu et al. 2008). The upregulation of P5CS in aromatic rice might be associated with increases in Δ1-pyrroline-5-carboxylic acid (P5C), thus resulting in the accumulation of a considerable amount of 2AP (Huang et al. 2008). Current studies suggest two pathways for 2AP biosynthesis in rice – via proline (Bradbury et al. 2008) and glutamic acid (Huang et al. 2008) – but both involve 1-pyrroline. This was also found to be an important intermediate in the formation of 2AP through the Maillard reaction (Hofmann & Schieberle, 1998).
MECHANISMS OF ACTION THROUGH PHYTOHORMONES
In many plant species, in reaction to osmotic stress caused by abscisic acid (ABA), proline accumulation increases (Hare et al. 1999). The use of exogenous ABA increases O-acetyl-L- serine concentrations and, consequently, may lead indirectly to proline accretion. ABA treatment of Solanum tuberosum increased the PCS1 transcript and phytochelatin synthase activity in roots (Stroinski et al. 2013). Therefore, ABA has been suggested to be responsible for the initiation of proline accumulation in stressed plants (Mäkelä et al. 2003).
The increased activity of superoxide dismutase (SOD), ABA and proline prevent oxidative damage in seedlings of Phaseolus vulgaris (Bahmani et al. 2012). ABA enhances nitrate reductase enzyme activity in Phaseolus aconitifolius cotyledons (Sankhla & Huber, 1975). In the Medicago truncatula LATD mutant, a correlation between ABA and signalling behaviour of nitrogen has been identified (Yendrek et al. 2010). In addition, the role of calcium (Ca) on proline accumulation and ABA lead to increases in calcium in the cytosol of guard cells (MacRobbie, 1992; Grabov & Blatt, 1998). Table 1 shows the response to phytohormones and the effects on proline accumulation.
Table 1.
Phytohormone-mediated changes in proline accumulation in plants.
External application of salicylic acid (SA) significantly decreased development of the superoxide anion and peroxidation of lipids in response to cadmium stress (Hayat et al. 2014; Zhang et al. 2015). SA also increased the assimilation of nitrogen and sulphur during salt stress (Nazar et al. 2011). Basalah et al. (2013) found that by enhancing proline accumulation together with SA and nitric oxide (NO) helps in relieving the negative effects of metal stress. In general, NO is responsible for upregulation of the enzymes required for proline synthesis (P5CS) leading to increases in production of proline (Zhang et al. 2008). In cucumber seedlings, NO can reduce damage caused by salinity by regulating proline metabolism through increasing activity of P5CS and decreasing activity of PDH (Fan et al. 2012).
ROLE OF PROLINE IN FLOWERING AND DEVELOPMENTAL PROCESSES↑
Several studies have reported that proline is associated with flowering and other developmental processes (Samach et al. 2000; Trovato et al. 2001; Mattioli et al. 2008; Szekely et al. 2008; Lehmann et al. 2010). By acting as a metabolite, proline can become a potential signalling molecule and has a prominent role in the flowering of plants (Mattioli et al. 2009). The genes required for production of proline metabolizing enzymes have been detected during seed development in several plant species, viz. Oryza sativa, Solanum lycopersicum, Medicago truncatula and Arabidopsis (Verbruggen et al. 1993; Fujita et al. 1998; Armengaud et al. 2004; Hur et al. 2004). The functions of proline in the propagative parts of plants have been described (Schwacke et al. 1999; Mattioli et al. 2012). Different tomato organs that amass proline have been analysed, and levels were found to be 60-fold higher in flowers than in other organs (Schwacke et al. 1999). In A. thaliana, proline is essential for development of pollen and for fertilization (Mattioli et al. 2012). Apical meristems with a low proline content signal that conditions are met for flowering, whereas higher proline levels indicate a stress signal for the plant (Mattioli et al. 2008, 2009). Constitutive overexpression of P5CS1 has been reported to cause early flowering under favourable condition in transgenic plants (Mattioli et al. 2008) and under salt stress situations (Kishor et al. 1995).
Use of proline by plant cells during development encompassing rapid cell growth could signal a potential energy supply (Mattioli et al. 2009). Proline protects developing cells from damage by osmotic stress during pollen development and embryogenesis (Trovato et al. 2008; Mattioli et al. 2009).
Several genetic engineering studies have confirmed that biosynthetic and metabolic genes accumulate proline, and this has opened avenues for systematic research into the role of proline in stress responses (Huang et al. 2000; Groppa & Benavides, 2008; Giri, 2011; Suprasanna et al. 2014). Progress in molecular and cellular biology has allowed essential proline biosynthetic genes to be cloned and transferred to crop plants (Wang et al. 2003). Transgenic plants show enhanced seedling growth and contain more ribulose1, 5-bisphosphate carboxylase and phosphoenolpyruvate compared to the wild type (Yan et al. 2011). For example, overproduction of proline-producing genes improved drought stress tolerance in tobacco (Kishor et al. 1995). Table 2 provides an overview of transgenic plants designed to increase proline-synthesizing or metabolic genes that improve tolerance to abiotic stresses.
Table 2.
Overexpression of proline biosynthetic genes in transgenic plants increases stress tolerance.
Using 1-pyrroline-5-carboxylate synthetase genes (OsP5CS gene from O. sativa or AtP5CS gene from A. thaliana), transgenic lines of Petunia hybrida have been developed with higher proline content that display drought stress tolerance (Yamada et al. 2005). Enhanced tolerance to drought stress has been shown in transgenic (VaP5CS from Vigna aconitifolia) wheat plants (Vendruscolo et al. 2007). Under different stress conditions, viz. salt, PEG, ABA and heat stress, P5CR has been overexpressed in Arabidopsis. Overexpression of proline P5CR increased proline accumulation in soybean (Glycine max cv. Ibis) leading to enhanced tolerance to drought (Simon-Sarkadi et al. 2006a). Guan et al. (2020) revealed that overexpressing PvP5CS1 and PvP5CS2 improved salt tolerance in switchgrass. Therefore, addition of proline biosynthesis genes will provide an efficient method to improve crop tolerance to numerous abiotic stress conditions.
CONCLUSION AND FUTURE PERSPECTIVES
This review has highlighted numerous positive influences of proline on plants and the capacity of proline to induce abiotic stress tolerance. By scavenging ROS, maintaining cell turgor, protecting cell structures and maintaining ion homeostasis, proline can enhance plant growth and physiological responses (Fig. 1). This integrated network might influences flowering and development processes that could lead to plant adaptation to abiotic stresses. Proline modulation of abiotic stress has revealed a new path for genetic manipulation of crop species to ensure long-term agricultural sustainability. In the last decade, this has also revealed a strategy targeted at improvement of plant performance through engineering proline biosynthetic multiple-gene functions in a holistic approach. In today’s breeding projects, cutting-edge as well as common genetic engineering tools have been successfully applied. Multigene stacking tools, such as the Golden Gate modular cloning system, have been established to modify several genes at the same time. Multiple-gene transformation is possible using a variety of approaches that allow large DNA fragments to be introduced. Plastid transformation is another promising and reliable method. As a cutting-edge breeding tool, CRISPR/Cas9 has delivered a revolution in gene engineering. The CRISPR/Cas9 system could be readily employed to effectively introduce mutations both in regulatory elements and coding sequences. These tremendous technological advances will enable us to modify genes that induce proline to enhance crop productivity under adverse environmental conditions. Finally, a complete understanding of plant adaptive/regulatory mechanisms related to growth performance in response to multiple abiotic stresses factors is crucial to develop modern varieties which could have better adaptability to changing field conditions.
Acknowledgements
The authors thank the Ministry of Science and Technology, People’s Republic of Bangladesh, for financial support regarding this study.
Conflict of interest
The authors declare no conflict of interest.
References
Aamer M., Muhammad U., Li Z., Abid A., Su Q., Liu Y., Adnan R., Muhammad A., Tahir A., Huang G. (2018) Foliar application of glycinebetaine (GB) alleviates the cadmium (Cd) toxicity in spinach through reducing Cd uptake and improving the activity of anti-oxidant system. Applied Ecology and Environmental Research, 16, 7575–7583.
Aggarwal M., Sharma S., Kaur N., Pathania D., Bhandhari K., Kaushal N., Kaur R., Singh K., Srivastava A., Nayyar H. (2011) Exogenous proline application reduces phytotoxic effects of selenium by minimising oxidative stress and improves growth in bean (Phaseolus vulgaris L.) seedlings. Biological Trace Element Research, 140, 354–367. https://doi.org/10.1007/s12011-010-8699-9
Alam R., Das D., Islam M., Murata Y., Hoque M. (2016) Exogenous proline enhances nutrient uptake and confers tolerance to salt stress in maize (Zea mays L.). Progressive Agriculture, 27, 409–417.
Ali Q., Anwar F., Ashraf M., Saari N., Perveen R. (2013) Ameliorating effects of exogenously applied proline on seed composition, seed oil quality and oil antioxidant activity of maize (Zea mays L.) under drought stress. International Journal of Molecular Sciences, 14, 818–835. https://doi.org/10.3390/ijms14010818
Ali Q., Ashraf M., Athar H.-U.-R. (2007) Exogenously applied proline at different growth stages enhances growth of two maize cultivars grown under water deficit conditions. Pakistan Journal of Botany, 39, 1133–1144.
Ali S., Eum H.-I., Cho J., Dan L.I., Khan F., Dairaku K., Shrestha M.L., Hwang S., Nasim W., Khan I.A., Fahad S. (2019) Assessment of climate extremes in future projections downscaled by multiple statistical downscaling methods over Pakistan. Atmospheric Research, 222, 114–133.
Aly A.A. (2012) Application of DNA (RAPD) and ultrastructure to detect the effect of cadmium stress in Egyptian clover and Sudan grass plantlets. Journal of Stress Physiology & Biochemistry, 8, 241–257.
Anuradha S., Rao S.S.R. (2008) The effect of brassinosteroids on radish (Raphanus sativus L.) seedlings growing under cadmium stress. Plant, Soil and Environment, 53, 465–472. https://doi.org/10.17221/2307-pse
Arbona V., Manzi M., Zandalinas S.I., Vives-Peris V., Pérez-Clemente R.M., Gómez-Cadenas A. (2017) Physiological, metabolic, and molecular responses of plants to abiotic stress. In: M. Sarwat, A. Ahmad, M.Z. Abdin, M.M. Ibrahim (Eds), Stress Signaling in Plants: Genomics and Proteomics Perspective, Vol 2. Springer, Berlin, Germany, pp 1–35.
Asgher M., Khan M.I.R., Iqbal N., Masood A., Khan N.A. (2013) Cadmium tolerance in mustard cultivars: dependence on proline accumulation and nitrogen assimilation. Journal of Functional and Environmental Botany, 3, 30–42.
Ashraf M., Athar H.R., Harris P.J.C., Kwon T.R. (2008) Some Prospective strategies for improving crop salt tolerance. Advances in Agronomy, 97, 45–110. https://doi.org/10.1016/s0065-2113(07)00002-8
Aziz A., Martin-Tanguy J., Larher F. (1998) Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiologia Plantarum, 104, 195–202. https://doi.org/10.1034/j.1399-3054.1998.1040207.x
Bagni N., Tassoni A. (2001) Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. Amino Acids, 20, 301–317. https://doi.org/10.1007/s007260170046
Bahmani R., Bihamta M., Habibi D., Forozesh P., Ahmadvand S. (2012) The effect of cadmium stress on growth, SOD activity, proline and ABA content in bean seedlings (Phaseolus vulgaris L.)., pp 26–27. In: First International and the 4th National Congress on Recycling of Organic Waste in Agriculture.
Bailey-Serres J., Fukao T., Ronald P., Ismail A., Heuer S., Mackill D. (2010) Submergence Tolerant Rice: SUB1’s Journey from Landrace to Modern Cultivar. Rice, 3, 138–147. https://doi.org/10.1007/s12284-010-9048-5
Bal H.B., Das S., Dangar T.K., Adhya T.K. (2013) ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. Journal of Basic Microbiology, 53, 972–984. https://doi.org/10.1002/jobm.201200445
Basalah M.O., Ali H.M., Al-Whaibi M.H., Siddiqui M.H., Sakran A.M., Al Sahli A.A. (2013) Nitric oxide and salicylic acid mitigate cadmium stress in wheat seedlings. Journal of Pure and Applied Microbiology, 7, 139–148.
Bekka S., Abrous-Belbachir O., Djebbar R. (2018) Effects of exogenous proline on the physiological characteristics of Triticum aestivum L. and Lens culinaris Medik. under drought stress. Acta Agriculturae Slovenica, 111, 477–491.
Bradbury L.M.T., Gillies S.A., Brushett D.J., Waters D.L.E., Henry R.J. (2008) Inactivation of an aminoaldehyde dehydrogenase is responsible for fragrance in rice. Plant Molecular Biology, 68, 439–449. https://doi.org/10.1007/s11103-008-9381-x
Burg M.B., Ferraris J.D. (2008) Intracellular organic osmolytes: function and regulation. Journal of Biological Chemistry, 283, 7309–7313. https://doi.org/10.1074/jbc.R700042200
Chanu W.S., Sarangthem K. (2015) Changes in proline accumulation, amino acid, sugar and chlorophyll content in leaf and culm of Phourel-amubi, a rice cultivar of Manipur in response to flash flood. Indian Journal of Plant Physiology, 20, 10–13.
Colmer T. (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment, 26, 17–36.
Cvikrova M., Gemperlova L., Martincova O., Vankova R. (2013) Effect of drought and combined drought and heat stress on polyamine metabolism in proline-over-producing tobacco plants. Plant Physiology and Biochemistry, 73, 7–15. https://doi.org/10.1016/j.plaphy.2013.08.005
De Knecht J.A., Van Dillen M., Koevoets P., Schat H., Verkleij J., Ernst W. (1994) Phytochelatins in Cadmium-Sensitive and Cadmium-Tolerant Silene vulgaris (Chain Length Distribution and Sulfide Incorporation). Plant Physiology, 104, 255–261. https://doi.org/10.1104/pp.104.1.255
Deuschle K., Funck D., Hellmann H., Daschner K., Binder S., Frommer W.B. (2001) A nuclear gene encoding mitochondrial Delta-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. The Plant Journal, 27, 345–356. https://doi.org/10.1046/j.1365-313x.2001.01101.x
Doke N. (1997) The oxidative burst: roles in signal transduction and plant stress. Oxidative stress and the molecular biology of antioxidant defenses. Plant Physiology, 27, 159–172.
Dubey R.S., Singh A.K. (1999) Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biologia Plantarum, 42, 233–239. https://doi.org/10.1023/a:1002160618700
El-Beltagi H.S., Mohamed H.I., Sofy M.R. (2020) Role of ascorbic acid, glutathione and proline applied as singly or in sequence combination in improving chickpea plant through physiological change and antioxidant defense under different levels of irrigation intervals. Molecules, 25, 1702. https://doi.org/10.3390/molecules25071702
Etesami H. (2019) Plant Growth Promotion and Suppression of Fungal Pathogens in Rice (Oryza sativa L.) by Plant Growth-Promoting Bacteria. In: K.G. Ramawat (Ed), Sustainable Development and Biodiversity. Springer International, New York, USA, pp 351–383. https://doi.org/10.1007/978-3-030-30926-8_13
Fan H.-F., Du C.-X., Guo S.-R. (2012) Effect of nitric oxide on proline metabolism in cucumber seedlings under salinity stress. Journal of the American Society for Horticultural Science, 137, 127–133. https://doi.org/10.21273/jashs.137.3.127
Feng X.J., Li J.R., Qi S.L., Lin Q.F., Jin J.B., Hua X.J. (2016) Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proceedings of the National Academy of Sciences, USA, 113, E8335–E8343. https://doi.org/10.1073/pnas.1610670114
Fujita T., Maggio A., Garcia-Rios M., Bressan R.A., Csonka L.N. (1998) Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Delta1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiology, 118, 661–674. https://doi.org/10.1104/pp.118.2.661
Furlan A.L., Bianucci E., Giordano W., Castro S., Becker D.F. (2020) Proline metabolic dynamics and implications in drought tolerance of peanut plants. Plant Physiology and Biochemistry, 151, 566–578. https://doi.org/10.1016/j.plaphy.2020.04.010
Ghaffari H., Tadayon M.R., Nadeem M., Cheema M., Razmjoo J. (2019) Proline-mediated changes in antioxidant enzymatic activities and the physiology of sugar beet under drought stress. Acta Physiologiae Plantarum, 41, 23.
Ghosh U.K., Islam M.N., Siddiqui M.N., Khan M.A.R. (2021) Understanding the roles of osmolytes for acclimatizing plants to changing environment: a review of potential mechanism. Plant Signaling & Behavior, 16, 1913306. https://doi.org/10.1080/15592324.2021.1913306
Grabov A., Blatt M.R. (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proceedings of the National Academy of Sciences, USA, 95, 4778–4783. https://doi.org/10.1073/pnas.95.8.4778
Guan C., Cui X., Liu H.Y., Li X., Li M.Q., Zhang Y.W. (2020) Proline biosynthesis enzyme genes confer salt tolerance to switchgrass (Panicum virgatum L.) in cooperation with polyamines metabolism. Frontiers Plant Science, 11, 46. https://doi.org/10.3389/fpls.2020.00046
Hamilton E.W. 3rd, Heckathorn S.A. (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiology, 126, 1266–1274. https://doi.org/10.1104/pp.126.3.1266
Hare P.D., Cress W.A., van Staden J. (1999) Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. Journal of Experimental Botany, 50, 413–434. https://doi.org/10.1093/jxb/50.333.413
Hare P.D., Cress W.A., van Staden J. (2003) A regulatory role for proline metabolism in stimulating Arabidopsis thaliana seed germination. Plant Growth Regulation, 39, 41–50. https://doi.org/10.1023/A:1021835902351
Hasanuzzaman M., Alam M.M., Rahman A., Hasanuzzaman M., Nahar K., Fujita M. (2014) Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Research International, 2014, 757219. https://doi.org/10.1155/2014/757219
Hasanuzzaman M., Fujita M., Oku H., Islam M. (2019) Effect of seed priming on abiotic stress tolerance in plants. In: V. Choudhary, S. Chander, C. Chethan, B. Kumar (Eds), Plant Tolerance to Environmental Stress: Role of Phytoprotectants, pp 29–46. Taylor & Francis, London, UK.
Hayat S., Hayat Q., Alyemeni M.N., Wani A.S., Pichtel J., Ahmad A. (2012) Role of proline under changing environments: a review. Plant Signaling & Behavior, 7, 1456–1466. https://doi.org/10.4161/psb.21949
Hayat S., Hayat Q., Alyemeni M.N., Ahmad A. (2013) Proline enhances antioxidative enzyme activity, photosynthesis and yield of Cicer arietinum L. exposed to cadmium stress. Acta Botanica Croatica, 72, 323–335. https://doi.org/10.2478/v10184-012-0019-3
Hayat S., Hayat Q., Alyemeni M.N., Ahmad A. (2014) Salicylic acid enhances the efficiency of nitrogen fixation and assimilation in Cicer arietinum plants grown under cadmium stress. Journal of Plant Interactions, 9, 35–42.
Heuer B. (2016) Role of proline in plant response to drought and salinity. In: M. Pessarakli (Ed), Handbook of plant and crop stress. CRC Press, Boca Raton, FL, USA, pp 213–238.
Hofmann T., Schieberle P. (1998) 2-Oxopropanal, hydroxy-2-propanone, and 1-pyrrolineimportant intermediates in the generation of the roast-smelling food flavor compounds 2-acetyl-1-pyrroline and 2-acetyltetrahydropyridine. Journal of Agricultural and Food Chemistry, 46, 2270–2277. https://doi.org/10.1021/jf970990g
Hoque M.A., Banu M.N., Okuma E., Amako K., Nakamura Y., Shimoishi Y., Murata Y. (2007) Exogenous proline and glycinebetaine increase NaCl-induced ascorbate-glutathione cycle enzyme activities, and proline improves salt tolerance more than glycinebetaine in tobacco Bright Yellow-2 suspension-cultured cells. Journal of Plant Physiology, 164, 1457–1468. https://doi.org/10.1016/j.jplph.2006.10.004
Huang T.-C., Teng C.-S., Chang J.-L., Chuang H.-S., Ho C.-T., Wu M.-L. (2008) Biosynthetic Mechanism of 2-Acetyl-1-pyrroline and its Relationship with Δ1-Pyrroline-5-carboxylic Acid and Methylglyoxal in Aromatic Rice (Oryza sativa L.) Callus. Journal of Agricultural and Food Chemistry, 56, 7399–7404. https://doi.org/10.1021/jf8011739
Huisinga B. (1964) Influence of light on growth, geotropism and guttation of avena seedlings grown in total darkness. Acta Botanica Neerlandica, 13, 445–487. https://doi.org/10.1111/j.1438-8677.1964.tb00169.x
Hur J., Jung K.-H., Lee C.-H., An G. (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Science, 167, 417–426. https://doi.org/10.1016/j.plantsci.2004.04.009
Iqbal N., Umar S., Khan N.A., Khan M.I.R. (2014) A new perspective of phytohormones in salinity tolerance: Regulation of proline metabolism. Environmental and Experimental Botany, 100, 34–42. https://doi.org/10.1016/j.envexpbot.2013.12.006
Islam M.M., Hoque M.A., Okuma E., Banu M.N., Shimoishi Y., Nakamura Y., Murata Y. (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. Journal of Plant Physiology, 166, 1587–1597. https://doi.org/10.1016/j.jplph.2009.04.002
Jackson M.B., Colmer T.D. (2005) Response and adaptation by plants to flooding stress. Annals of Botany, 96, 501–505. https://doi.org/10.1093/aob/mci205
Jackson M.B., Ishizawa K., Ito O. (2009) Evolution and mechanisms of plant tolerance to flooding stress. Annals of Botany, 103, 137–142. https://doi.org/10.1093/aob/mcn242
Jackson M.B., Ram P.C. (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany, 91(2), 227–241. https://doi.org/10.1093/aob/mcf242
Jeandroz S., Lamotte O. (2017) Editorial: plant responses to biotic and abiotic stresses: lessons from cell signaling. Frontiers in Plant Science, 8, 1772. https://doi.org/10.3389/fpls.2017.01772
Kahlaoui B., Hachicha M., Misle E., Fidalgo F., Teixeira J. (2018) Physiological and biochemical responses to the exogenous application of proline of tomato plants irrigated with saline water. Journal of the Saudi Society of Agricultural Sciences, 17, 17–23.
Kapoor D., Bhardwaj R. (2014) Physiological mechanisms of Brassica juncea L. plants exposed to cadmium metal stress. Indian. Journal of Applied Research, 4.
Kaushal N., Gupta K., Bhandhari K., Kumar S., Thakur P., Nayyar H. (2011) Proline induces heat tolerance in chickpea (Cicer arietinum L.) plants by protecting vital enzymes of carbon and antioxidative metabolism. Physiology and Molecular Biology of Plants, 17, 203–213. https://doi.org/10.1007/s12298-011-0078-2
Kazemi-Shahandashti S.S., Maali-Amiri R. (2018) Global insights of protein responses to cold stress in plants: Signaling, defence, and degradation. Journal of Plant Physiology, 226, 123–135. https://doi.org/10.1016/j.jplph.2018.03.022
Kerchev P., van der Meer T., Sujeeth N., Verlee A., Stevens C.V., Van Breusegem F., Gechev T. (2020) Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnology Advances, 40, 107503.
Khan M.I., Nazir F., Asgher M., Per T.S., Khan N.A. (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. Journal of Plant Physiology, 173, 9–18. https://doi.org/10.1016/j.jplph.2014.09.011
Kishor P., Hong Z., Miao G.H., Hu C., Verma D. (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology, 108, 1387–1394. https://doi.org/10.1104/pp.108.4.1387
Kiyosue T., Yoshiba Y., Yamaguchi-Shinozaki K., Shinozaki K. (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. The Plant Cell, 8, 1323–1335. https://doi.org/10.1105/tpc.8.8.1323
Kumari S., Vaishnav A., Jain S., Varma A., Choudhary D.K. (2015) Bacterial-Mediated Induction of Systemic Tolerance to Salinity with Expression of Stress Alleviating Enzymes in Soybean (Glycine max L. Merrill). Journal of Plant Growth Regulation, 34, 558–573. https://doi.org/10.1007/s00344-015-9490-0
Larcher W. (1981) effects of low temperature stress and frost injury on plant productivity. In: C.B. Johnson (Eds), Physiological Processes Limiting Plant Productivity, Elsevier., Amsterdam, the Netherlands, pp 253–269. https://doi.org/10.1016/b978-0-408-10649-8.50018-6.
Lehmann S., Funck D., Szabados L., Rentsch D. (2010) Proline metabolism and transport in plant development. Amino Acids, 39, 949–962. https://doi.org/10.1007/s00726-010-0525-3.
Liu J.H. (2006) Polyamine biosynthesis of apple callus under salt stress: importance of the arginine decarboxylase pathway in stress response. Journal of Experimental Botany, 57, 2589–2599. https://doi.org/10.1093/jxb/erl018.
Lokhande V.H., Nikam T.D., Patade V.Y., Ahire M.L., Suprasanna P. (2010) Effects of optimal and supra-optimal salinity stress on antioxidative defence, osmolytes and in vitro growth responses in Sesuvium portulacastrum L. Plant Cell, Tissue and Organ Culture, 104, 41–49. https://doi.org/10.1007/s11240-010-9802-9.
López M., Tejera N.A., Iribarne C., Lluch C., Herrera-Cervera J.A. (2008) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiologia Plantarum, 134, 575–582.
Lugan R., Niogret M.F., Leport L., Guegan J.P., Larher F.R., Savoure A., Kopka J., Bouchereau A. (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. The Plant Journal, 64, 215–229. https://doi.org/10.1111/j.1365-313X.2010.04323.x.
Lux A., Martinka M., Vaculik M., White P.J. (2011) Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany, 62, 21–37. https://doi.org/10.1093/jxb/erq281.
MacRobbie E.A.C. (1992) Calcium and ABA-induced stomatal closure. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 338, 5–18.
Madan S. (1995) Proline and Proline Metabolising Enzymes in in-vitro Selected NaCl-tolerant Brassica juncea L. under Salt Stress. Annals of Botany, 76, 51–57. https://doi.org/10.1006/anbo.1995.1077
Mäkelä P., Munns R., Colmer T.D., Peltonen-Sainio P. (2003) Growth of tomato and an ABA-deficient mutant (sitiens) under saline conditions. Physiologia Plantarum, 117, 58–63. https://doi.org/10.1034/j.1399-3054.2003.1170107.x
Mattioli R., Biancucci M., Lonoce C., Costantino P., Trovato M. (2012) Proline is required for male gametophyte development in Arabidopsis. BMC Plant Biology, 12, 236. https://doi.org/10.1186/1471-2229-12-236
Mattioli R., Falasca G., Sabatini S., Altamura M.M., Costantino P., Trovato M. (2009) The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiologia Plantarum, 137, 72–85. https://doi.org/10.1111/j.1399-3054.2009.01261.x
Mattioli R., Marchese D., D'Angeli S., Altamura M.M., Costantino P., Trovato M. (2008) Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Molecular Biology, 66, 277–288. https://doi.org/10.1007/s11103-007-9269-1.
Mo Z., Li W., Pan S., Fitzgerald T.L., Xiao F., Tang Y., Wang Y., Duan M., Tian H., Tang X. (2015) Shading during the grain filling period increases 2-acetyl-1-pyrroline content in fragrant rice. Rice, 8, https://doi.org/10.1186/s12284-015-0040-y.
Mohammadi H., Hazrati S., Ghorbanpour M. (2020) Tolerance mechanisms of medicinal plants to abiotic stresses. In: D.K. Tripathi, V.P. Singh, S. Sharma, S. Prasad, N.K. Dubey, N. Ramawat (Eds), Plant Life Under Changing Environment. Elsevier, Amsterdam, the Netherlands, pp 663–679.
Mohammadkhani N., Heidari R. (2008) Drought-induced accumulation of soluble sugars and proline in two maize varieties. World Applied Sciences Journal, 3, 448–453.
Molinari H.B.C., Marur C.J., Daros E., de Campos M.K.F., de Carvalho J.F.R.P., Filho J.C.B., Pereira L.F.P., Vieira L.G.E. (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum, 130, 218–229. https://doi.org/10.1111/j.1399-3054.2007.00909.x.
Molla M.R., Ali M.R., Hasanuzzaman M., Al-Mamun M.H., Ahmed A., Nazim-Ud-Dowla M., Rohman M.M. (2014) Exogenous proline and betaine-induced upregulation of glutathione transferase and glyoxalase I in lentil (Lens culinaris) under drought stress. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 42, 73–80.
Nadeau P., Delaney S., Chouinard L. (1987) Effects of Cold Hardening on the Regulation of Polyamine Levels in Wheat (Triticum aestivum L.) and Alfalfa (Medicago sativa L.). Plant Physiology, 84, 73–77. https://doi.org/10.1104/pp.84.1.73.
Nadeem S.M., Ahmad M., Zahir Z.A., Javaid A., Ashraf M. (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology Advances, 32, 429–448. https://doi.org/10.1016/j.biotechadv.2013.12.005.
Nahar K., Hasanuzzaman M., Rahman A., Alam M.M., Mahmud J.-A., Suzuki T., Fujita M. (2016) Polyamines Confer Salt Tolerance in Mung Bean (Vigna radiata L.) by Reducing Sodium Uptake, Improving Nutrient Homeostasis, Antioxidant Defense, and Methylglyoxal Detoxification Systems. Frontiers in Plant Science, 7. https://doi.org/10.3389/fpls.2016.01104
Nanjo T., Fujita M., Seki M., Kato T., Tabata S., Shinozaki K. (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant and Cell Physiology, 44, 541–548. https://doi.org/10.1093/pcp/pcg066
Nazar R., Iqbal N., Syeed S., Khan N.A. (2011) Salicylic acid alleviates decreases in photosynthesis under salt stress by enhancing nitrogen and sulfur assimilation and antioxidant metabolism differentially in two mungbean cultivars. Journal of Plant Physiology, 168, 807–815. https://doi.org/10.1016/j.jplph.2010.11.001
Nazar R., Iqbal N., Masood A., Khan M.I.R., Syeed S., Khan N.A. (2012) Cadmium Toxicity in Plants and Role of Mineral Nutrients in its Alleviation. American Journal of Plant Sciences, 03, 1476–1489. https://doi.org/10.4236/ajps.2012.310178
Nguyen D., Rieu I., Mariani C., van Dam N.M. (2016) How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Molecular Biology, 91, 727–740. https://doi.org/10.1007/s11103-016-0481-8.
Niu X., Tang W., Huang W., Ren G., Wang Q., Luo D., Xiao Y., Yang S., Wang F., Lu B.-R., Gao F., Lu T., Liu Y. (2008) RNAi-directed downregulation of OsBADH2 results in aroma (2-acetyl-1-pyrroline) production in rice (Oryza sativa L.). BMC Plant Biology, 8, 100. https://doi.org/10.1186/1471-2229-8-100
Nounjan N., Nghia P.T., Theerakulpisut P. (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. Journal of Plant Physiology, 169, 596–604. https://doi.org/10.1016/j.jplph.2012.01.004
de Oliveira L.F., Elbl P., Navarro B.V., Macedo A.F., Dos Santos A.L., Floh E.I., Cooke J. (2017) Elucidation of the polyamine biosynthesis pathway during Brazilian pine (Araucaria angustifolia) seed development. Tree Physiology, 37, 116–130.
Oufir M., Schulz N., Sha Vallikhan P.S., Wilhelm E., Burg K., Hausman J.F., Hoffmann L., Guignard C. (2009) Simultaneous measurement of proline and related compounds in oak leaves by high-performance ligand-exchange chromatography and electrospray ionization mass spectrometry for environmental stress studies. Journal of Chromatography A, 1216, 1094–1099. https://doi.org/10.1016/j.chroma.2008.12.030
Oukarroum A., El Madidi S., Strasser R.J. (2012) Exogenous glycine betaine and proline play a protective role in heat-stressed barley leaves (Hordeum vulgare L.): a chlorophyll a fluorescence study. Plant Biosystems, 146, 1037–1043. https://doi.org/10.1080/11263504.2012.697493
Pang X.-M., Zhang Z.-Y., Wen X.-P., Ban Y., Moriguchi T. (2007) Polyamines, all-purpose players in response to environment stresses in plants. Plant Stress, 1, 173–188.
Parida A.K., Das A.B. (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicology and Environmental Safety, 60, 324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Patel N., Gantait S., Panigrahi J. (2019) Extension of postharvest shelf-life in green bell pepper (Capsicum annuum L.) using exogenous application of polyamines (spermidine and putrescine). Food Chemistry, 275, 681–687. https://doi.org/10.1016/j.foodchem.2018.09.154
Poonlaphdecha J., Maraval I., Roques S., Audebert A., Boulanger R., Bry X., Gunata Z. (2012) Effect of Timing and Duration of Salt Treatment during Growth of a Fragrant Rice Variety on Yield and 2-Acetyl-1-pyrroline, Proline, and GABA Levels. Journal of Agricultural and Food Chemistry, 60, 3824–3830. https://doi.org/10.1021/jf205130y
Posmyk M.M., Janas K.M. (2007) Effects of seed hydropriming in presence of exogenous proline on chilling injury limitation in Vigna radiata L. seedlings. Acta Physiologia Plantarum, 29, 509–517. https://doi.org/10.1007/s11738-007-0061-2
Radic S., Babic M., Skobic D., Roje V., Pevalek-Kozlina B. (2010) Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna minor L. Ecotoxicology and Environmental Safety, 73, 336–342. https://doi.org/10.1016/j.ecoenv.2009.10.014
Rady M.M. (2011) Effect of 24-epibrassinolide on growth, yield, antioxidant system and cadmium content of bean (Phaseolus vulgaris L.) plants under salinity and cadmium stress. Scientia Horticulturae, 129, 232–237. https://doi.org/10.1016/j.scienta.2011.03.035
Rais L., Masood A. (2013) Sulfur and Nitrogen Co-ordinately Improve Photosynthetic Efficiency, Growth and Proline Accumulation in Two Cultivars of Mustard Under Salt Stress. Journal of Plant Biochemistry & Physiology, 1, https://doi.org/10.4172/2329-9029.1000101
Rajendrakumar C.S., Suryanarayana T., Reddy A.R. (1997) DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process. FEBS Letters, 410, 201–205. https://doi.org/10.1016/s0014-5793(97)00588-7
Dos Reis S.P., Lima A.M., de Souza C.R. (2012) Recent molecular advances on downstream plant responses to abiotic stress. International Journal of Molecular Sciences, 13, 8628–8647. https://doi.org/10.3390/ijms13078628
Rejeb K.B., Abdelly C., Savouré A. (2014) How reactive oxygen species and proline face stress together. Plant Physiology and Biochemistry, 80, 278–284.
Ribarits A., Abdullaev A., Tashpulatov A., Richter A., Heberle-Bors E., Touraev A. (2007) Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development. Planta, 225, 1313–1324. https://doi.org/10.1007/s00425-006-0429-3
Rizwan M., Ali S., Ibrahim M., Farid M., Adrees M., Bharwana S.A., Zia-Ur-Rehman M., Qayyum M.F., Abbas F. (2015) Mechanisms of silicon-mediated alleviation of drought and salt stress in plants: a review. Environmental Science and Pollution Research International, 22, 15416–15431. https://doi.org/10.1007/s11356-015-5305-x
Roosens N.H., Thu T.T., Iskandar H.M., Jacobs M. (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiology, 117, 263–271. https://doi.org/10.1104/pp.117.1.263
Safdar H., Amin A., Shafiq Y., Ali A., Yasin R., Shoukat A., Hussan M.U., Sarwar M.I. (2019) A review: Impact of salinity on plant growth. Nature and Science, 17, 34–40.
Samach A., Onouchi H., Gold S.E., Ditta G.S., Schwarz-Sommer Z., Yanofsky M.F., Coupland G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288, 1613–1616. https://doi.org/10.1126/science.288.5471.1613
Sandalio L.M., Dalurzo H.C., Gomez M., Romero-Puertas M.C., del Rio L.A. (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. Journal of Experimental Botany, 52, 2115–2126. https://doi.org/10.1093/jexbot/52.364.2115
Sandhya V., Sk. z. A., Grover M., Reddy G., Venkateswarlu B. (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biology and Fertility of Soils, 46, 17–26. https://doi.org/10.1007/s00374-009-0401-z
Sankhla N., Huber W. (1975) Effect of Salt and Abscisic Acid on in vivo Activity of Nitrate Reductase in Seedlings of Phaseolus aconitifolius. Zeitschrift Für Pflanzenphysiologie, 76, 467–470. https://doi.org/10.1016/s0044-328x(75)80010-9
Savoure A., Jaoua S., Hua X.J., Ardiles W., Van Montagu M., Verbruggen N. (1995) Isolation, characterization, and chromosomal location of a gene encoding the delta 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Letters, 372, 13–19. https://doi.org/10.1016/0014-5793(95)00935-3
Schwacke R., Grallath S., Breitkreuz K.E., Stransky E., Stransky H., Frommer W.B., Rentsch D. (1999) LeProT1, a transporter for proline, glycine betaine, and gamma-amino butyric acid in tomato pollen. The Plant Cell, 11, 377–392. https://doi.org/10.1105/tpc.11.3.377
Shahid M.A., Balal R.M., Pervez M.A., Abbas T., Aqeel M.A., Javaid M.M., Garcia-Sanchez F. (2014) Exogenous proline and proline-enriched Lolium perenne leaf extract protects against phytotoxic effects of nickel and salinity in Pisum sativum by altering polyamine metabolism in leaves. Turkish Journal of Botany, 38, 914–926.
Sharma P., Sharma P., Arora P., Verma V., Khanna K., Saini P., Bhardwaj R. (2019) Role and regulation of ROS and antioxidants as signaling molecules in response to abiotic stresses. In: M. I. Khan, P. S. Reddy, A. Ferrante, N. Khan (eds), Plant signaling molecules. Elsevier, Amsterdam, the Netherlands, pp 141–156.
Sharma S.S., Dietz K.J. (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany, 57, 711–726. https://doi.org/10.1093/jxb/erj073
Sharma S.S., Schat H., Vooijs R. (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry, 49, 1531–1535. https://doi.org/10.1016/s0031-9422(98)00282-9
Simon-Sarkadi L., Kocsy G., Várhegyi Á., Galiba G., Ronde, J.A.d. (2006b) Effect of drought stress at supraoptimal temperature on polyamine concentrations in transgenic soybean with increased proline levels. Zeitschrift für Naturforschung C, 61, 833–839. https://doi.org/10.1515/znc-2006-11-1211
Slama I., Abdelly C., Bouchereau A., Flowers T., Savoure A. (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany, 115, 433–447. https://doi.org/10.1093/aob/mcu239
Sobahan M.A., Arias C.R., Okuma E., Shimoishi Y., Nakamura Y., Hirai Y., Mori I.C., Murata Y. (2009) Exogenous proline and glycinebetaine suppress apoplastic flow to reduce Na(+) uptake in rice seedlings. Bioscience, Biotechnology, and Biochemistry, 73, 2037–2042. https://doi.org/10.1271/bbb.90244
Strizhov N., Ábrahám E., Ökrész L., Blickling S., Zilberstein A., Schell J., Koncz C., Szabados L. (2003) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. The Plant Journal, 12, 557–569. https://doi.org/10.1111/j.0960-7412.1997.00557.x
Stroinski A., Gizewska K., Zielezinska M. (2013) Abscisic acid is required in transduction of cadmium signal to potato roots. Biologia Plantarum, 57, 121–127. https://doi.org/10.1007/s10535-012-0135-x
Subramanian P., Kim K., Krishnamoorthy R., Mageswari A., Selvakumar G., Sa T. (2016) Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) under low temperatures. PLoS One, 11, e0161592. https://doi.org/10.1371/journal.pone.0161592
Surabhi G.-K. (2018) Update in root proteomics with special reference to abiotic stresses: achievements and challenges. Journal of Proteins and Proteomics, 9, 31–35.
Szekely G., Abraham E., Cseplo A., Rigo G., Zsigmond L., Csiszar J., Ayaydin F., Strizhov N., Jasik J., Schmelzer E., Koncz C., Szabados L. (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. The Plant Journal, 53, 11–28. https://doi.org/10.1111/j.1365-313X.2007.03318.x
Tripathi B.N., Gaur J.P. (2004) Relationship between copper- and zinc-induced oxidative stress and proline accumulation in Scenedesmus sp. Planta, 219, 397–404. https://doi.org/10.1007/s00425-004-1237-2
Trovato M., Maras B., Linhares F., Costantino P. (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proceedings of the National Academy of Sciences, 98(23), 13449–13453. https://doi.org/10.1073/pnas.231320398
Trovato M., Mattioli R., Costantino P. (2008) Multiple roles of proline in plant stress tolerance and development. Rendiconti Lincei. Scienze Fisiche E Naturali, 19, 325–346. https://doi.org/10.1007/s12210-008-0022-8
Tuo X.-Q., Li S., Wu Q.-S., Zou Y.-N. (2015) Alleviation of waterlogged stress in peach seedlings inoculated with Funneliformis mosseae: Changes in chlorophyll and proline metabolism. Scientia Horticulturae, 197, 130–134.
Urano K., Maruyama K., Ogata Y., Morishita Y., Takeda M., Sakurai N., Suzuki H., Saito K., Shibata D., Kobayashi M., Yamaguchi-Shinozaki K., Shinozaki K. (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. The Plant Journal, 57, 1065–1078. https://doi.org/10.1111/j.1365-313X.2008.03748.x
Vendruscolo E.C., Schuster I., Pileggi M., Scapim C.A., Molinari H.B., Marur C.J., Vieira L.G. (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. Journal of Plant Physiology, 164, 1367–1376. https://doi.org/10.1016/j.jplph.2007.05.001
Verbruggen N., Hua X.J., May M., van Montagu M. (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proceedings of the National Academy of Sciences USA, 93, 8787–8791. https://doi.org/10.1073/pnas.93.16.8787
Verbruggen N., Villarroel R., Van Montagu M. (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiology, 103, 771–781. https://doi.org/10.1104/pp.103.3.771
Verslues P.E., Sharma S. (2010) Proline metabolism and its implications for plant-environment interaction. The Arabidopsis Book, 8, e0140. https://doi.org/10.1199/tab.0140
Vinocur B., Altman A. (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current Opinion in Biotechnology, 16, 123–132. https://doi.org/10.1016/j.copbio.2005.02.001
Voesenek L.A., Bailey-Serres J. (2013) Flooding tolerance: O2 sensing and survival strategies. Current Opinion in Biotechnology, 16, 647–653. https://doi.org/10.1016/j.pbi.2013.06.008
Wahid A., Gelani S., Ashraf M., Foolad M.R. (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany, 61, 199–223. https://doi.org/10.1016/j.envexpbot.2007.05.011
Wang Q., Liang X., Dong Y., Xu L., Zhang X., Kong J., Liu S. (2013) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress. Journal of Plant Growth Regulation, 32, 721–731. https://doi.org/10.1007/s00344-013-9339-3
Wang W., Vinocur B., Altman A. (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 218, 1–14. https://doi.org/10.1007/s00425-003-1105-5
Wu Q.-S., Zou Y.-N., Huang Y.-M. (2013) The arbuscular mycorrhizal fungus Diversispora spurca ameliorates effects of waterlogging on growth, root system architecture and antioxidant enzyme activities of citrus seedlings. Fungal Ecology, 6, 37–43.
Xu Z., Shimizu H., Ito S., Yagasaki Y., Zou C., Zhou G., Zheng Y. (2013) Effects of elevated CO2, warming and precipitation change on plant growth, photosynthesis and peroxidation in dominant species from North China grassland. Planta, 239, 421–435. https://doi.org/10.1007/s00425-013-1987-9
Yamada M., Morishita H., Urano K., Shiozaki N., Yamaguchi-Shinozaki K., Shinozaki K., Yoshiba Y. (2005) Effects of free proline accumulation in petunias under drought stress. Journal of Experimental Botany, 56, 1975–1981. https://doi.org/10.1093/jxb/eri195
Yan Z., Guo S., Shu S., Sun J., Tezuka T. (2011) Effects of proline on photosynthesis, root reactive oxygen species (ROS) metabolism in two melon cultivars (Cucumis melo L.) under NaCl stress. African Journal of Biotechnology, 10, 18381–18390.
Yang F., Han C., Li Z., Guo Y., Chan Z. (2015) Dissecting tissue- and species-specific responses of two Plantago species to waterlogging stress at physiological level. Environmental and Experimental Botany, 109, 177–185.
Yang Y., Guo Y. (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytologist, 217, 523–539. https://doi.org/10.1111/nph.14920
Yendrek C.R., Lee Y.C., Morris V., Liang Y., Pislariu C.I., Burkart G., Meckfessel M.H., Salehin M., Kessler H., Wessler H., Lloyd M., Lutton H., Teillet A., Sherrier D.J., Journet E.P., Harris J.M., Dickstein R. (2010) A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. The Plant Journal, 62, 100–112. https://doi.org/10.1111/j.1365-313X.2010.04134.x
Yoshiba Y., Kiyosue T., Nakashima K., Yamaguchi-Shinozaki K., Shinozaki K. (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant and Cell Physiology, 38, 1095–1102. https://doi.org/10.1093/oxfordjournals.pcp.a029093
Yoshihashi T., Huong N.T.T., Inatomi H. (2002a) Precursors of 2-acetyl-1-pyrroline, a potent flavor compound of an aromatic rice variety. Journal of Agricultural and Food Chemistry, 50, 2001–2004. https://doi.org/10.1021/jf011268s
Yoshihashi T., Kabaki N., Nguyen T., Inatomi H. (2002b) Formation of flavor compound in aromatic rice and its fluctuations with drought stress. Japan International Research Center for Agricultural Sciences.
Zandalinas S.I., Mittler R., Balfagon D., Arbona V., Gomez-Cadenas A. (2018) Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162, 2–12. https://doi.org/10.1111/ppl.12540
Zarea M.J., Hajinia S., Karimi N., Mohammadi Goltapeh E., Rejali F., Varma A. (2012) Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biology and Biochemistry, 45, 139–146. https://doi.org/10.1016/j.soilbio.2011.11.006
Zengin F.K., Munzuroglu O. (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biologica Cracoviensia Series Botanica, 47, 157–164.
Zhang L.P., Mehta S.K., Liu Z.P., Yang Z.M. (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant and Cell Physiology, 49, 411–419. https://doi.org/10.1093/pcp/pcn017
Zhang Q., Huber H., Beljaars S.J.M., Birnbaum D., de Best S., de Kroon H., Visser E.J.W. (2017) Benefits of flooding-induced aquatic adventitious roots depend on the duration of submergence: linking plant performance to root functioning. Annals of Botany, 120, 171–180. https://doi.org/10.1093/aob/mcx049
Zhang Y., Xu S., Yang S., Chen Y. (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma, 252, 911–924. https://doi.org/10.1007/s00709-014-0732-y
Please check your email for instructions on resetting your password.
If you do not receive an email within 10 minutes, your email address may not be registered,
and you may need to create a new Wiley Online Library account.
Request Username
Can't sign in? Forgot your username?
Enter your email address below and we will send you your username
If the address matches an existing account you will receive an email with instructions to retrieve your username
The full text of this article hosted at iucr.org is unavailable due to technical difficulties.
