PLANTS SENSORY-RESPONSE MECHANISMS FOR SALINITY AND HEAT STRESS.
Plants, being sessile in nature, have evolved efficient sensory mechanisms to cope with the dynamic environment. Their survival depends on a network of robust and densely interconnected systems for rapid signal perception, transduction, reaction and adaptation to biotic and abiotic stimuli. Among the abiotic stresses, heat and salt stress are the major threats to modern agriculture especially in the scenario of climate change. At cellular level, signal perception and response is critical for the establishment of stress tolerance. This review gives an insight of sensory and response mechanisms induced by salt and heat stress. Saline conditions activate membrane bound sensors including ion transporters followed by activation of second messengers and signaling cascades (like TFs, MAPKs, SnRK2s and SOS pathways) for the activation of response mechanisms.
Heat stress affects membrane properties and initiate sensory events followed by activation of response mechanisms (like TFs, HSFs, chaperones and osmo-protectants). Such observations emphasize the importance of signal messengers as well as transcription factors for cellular performance of plants under confrontational circumstances. Better understanding of these stress-sensory mechanisms can facilitate the breeding programs for the development of climate-resilient plants which may perform better in a challenging environment and can contribute to the global food security.
Keywords: Salinity, Heat, sensory mechanisms, stress response, climate change.
Plant survival depends on a network of robust and densely interconnected systems for rapid signal perception, reaction and adaptation to suboptimal environmental conditions. Under stress conditions, plants are unable to show complete genetic potential, which negatively affects plant growth, development and agronomic yield. But to feed the fast growing population, there is a need for almost 70% sustainable increase in major food crop production (FAOSTAT, 2009). This increase could be achieved by overcoming the yield losses due to environmental stresses without increasing input demand. Abiotic stresses are responsible for more than 50% of the primary crop yield loss (Albacete et al., 2014) and deterioration of agricultural lands. Among major abiotic stresses, salinity and heat stress play a predominant role in limiting crop yield.
Soil salinity is a serious problem for plants. It affects plants by disturbing the water extraction capacity of roots and continuous uptake of salts that becomes toxic for plant. Primarily, the salt stress affects seed germination, plant growth, photosynthesis, water relation, nutrient balance, plant yield and may lead to even death of the plant (Munns and Tester, 2008; Yadav et al., 2011; Arefian et al., 2014; Parihar et al., 2015). Plants have developed various physiological, biochemical and molecular mechanisms to survive on saline soils (Gupta and Huang, 2014).
Heat stress is another major abiotic constraint for crop productivity. According to predictions, at the end of 21st century temperature of the growing season in the tropics and subtropics will surpass the highest seasonal temperature observed during 1900-2006 (Battisti and Naylor, 2009). Global warming has profound and diverse effects on plants. During 1980-2008 high temperature has decreased world maize and wheat production by 3.8 and 5.5%, respectively (Lobell and Field, 2007; Lobell et al., 2011). Worldwide yields of the six most important crops (wheat, rice, maize, soybeans, barley, and sorghum) have declined by 0.6~8.9% for every 1degC rise in temperature (Lobell and Field, 2007). Climate change models have forecasted that there will be more frequent and intense heat waves in the future, causing a gradual increase in ambient temperature and it will be a major threat for agricultural production (Suzuki et al., 2014).
High temperature interrupts plant growth, development and physiological processes, thus contributing significantly to yield reduction. Major consequences of heat stress include production of reactive oxygen species (ROS) and disturbance in the photosynthetic activities of plants (Davies et al., 2006; Hasanuzzaman et al., 2013).
Therefore, it is critical to understand how plants feel the heat and adapt protective measures for survival.
In the open environment, plants are simultaneously exposed to multiple stresses. Generally, plants have to respond to combinations of two or more stresses. Recent findings suggest that plants exhibit unique responses under such conditions (Zhang et al., 2015; Sham et al., 2015; Saucedo-GarcA* aet al., 2015; Nigam et al., 2015; Krasensky and Jonak, 2012). Sometimes, plant responses to a combination of stresses become even more complex. It is because, the responses to the collective stresses are mostly controlled by diverse, and occasionally contrasting, signaling pathways that may have negative effects on each other. Therefore, it is really important to decipher the mechanisms that execute the integration of stress perception, signal transduction and plant responses.
Current review is focused on mechanisms of plants for sensing and response to two major environmental constraints: salt and heat stress.
Sensing the stress stimulus: In general, signal transduction pathway includes signal perception, activation of second messengers, modulation of intracellular Ca+2 levels and triggering a protein phosphorylation cascade. Depending upon the nature of stimulus, either one or both classes of following proteins are activated: proteins directly involved in cellular protection or transcription factors that modulate stress-regulated genes.
In the stress signaling cascade certain second messengers also act as sensor for the detection of stress signal. Among different classes of Ca2+ sensors calmodulin (CaM), calcineurin B-like proteins (CBLs) and CBL-interacting protein kinases (CIPKs), are the best characterized (Reddy et al., 2011; Yu et al., 2014). These transducers of Ca2+ signaling are also involved in stress signal sensing. This is because the sensing and the signaling events of calcium and other ions like Na+, are very closely interconnected and are very difficult to be dissociated as the sensing event immediately transmits signal (DeFalco et al., 2010; Conde et al., 2011).
Other second messengers include cyclic nucleotides cAMP/cGMP (Walker and Berkowitz, 2013), Polyphosphoinositides (Munnik and Vermeer, 2010), nitric oxide (NO) (Agurla et al., 2014), sugars (Rolland et al., 2002), abscisic acid (ABA) (Raghavendra et al., 2010) and jasmonates (JA) (Wasternack and Hause, 2013).
Sensing salt stress stimuli: Plants can sense and exhibit an effective response against hyperosmotic and ionic components of salt stress (Munns and Tester, 2008). The Arabidopsis Histidine Kinase receptor protein (HK1) is an important candidate for osmo-sensors because it can balance the loss of the yeast osmo-sensor Sln1 and overexpression/loss-of function plants exhibit drought and osmotic stress-associated phenotypes (Urao et al., 1999; Tran et al., 2007; Wohlbach et al., 2008; Kumar et al., 2013; Kushwaha et al., 2013). Some of the physiological activities induced by osmotic stress were altered in hk1 mutants, but others remained unaffected. Therefore, other proteins must still perceive the osmotic stress in the hk1 mutant (Kumar et al., 2013). It is assumed that hyperosmolality and other environmental stimuli increase cytosolic free calcium concentration ([Ca2+]) and osmosensing Ca2+ channels in animals and bacteria function as osmosensors (Kung, 2005; Arnadottir and Chalfie, 2010).
In Arabidopsis thaliana, hyperosmolality gated calcium-permeable channel (OSCA1) is important for osmosensing (Yuan et al., 2014). Similarly, a plasma membrane localized receptor-like protein (NtC7) functions in osmotic adjustment and its transcripts are upregulated rapidly after salt, osmotic and wounding stress (Tamura et al., 2003).
Membrane embedded Mechanosensitive channels (MS) are important for plant osmosensing machinery (Peyronnet et al., 2014). These channels serve as sensors and effectors of physical responses. The most extensively characterized MS channels belong to the MscL (MS channel Large conductance) or MscS (Small conductance) families (Hamill and Martinac, 2001; Martinac et al., 2008). Upon membrane stretching in response to environmental stimuli, MS channels are immediately activated along with cellular ion fluxes and ROS variations (Monshausen and Gilroy, 2009; Coutand, 2010). Therefore, it is speculated that MS channels, are involved either directly or indirectly in modulating ion luxes, especially Ca 2+ (Peyronnet et al., 2014). As the cytosolic Ca increase is a hallmark of osmotic stress, MS channels are thought to play role in osmosensing and subsequent responses (Figure 1).
Salinity and hyperosmotic exposure trigger several early signaling events including ROS formation (Miller et al., 2010; Jiang et al., 2013), the induction of PLD-mediated phosphatidic acid production (Bargmann et al., 2009; Darwish et al., 2009; Yu et al., 2010), accumulation of nitric oxide (Khan et al., 2012), formation of cAMP/cGMP (Donaldson et al., 2004), synthesis of abscisic acid (ABA) (Dinneny, 2014) and transient increases in cytosolic Ca 2+ concentrations (Laohavisit et al., 2012; Laohavisit et al., 2013). Arabidopsis annexins mediate both NaCl and ROS-induced Ca +2 responses in roots (Laohavisit et al., 2012; Laohavisit et al., 2013; Richards et al., 2014). Although the rapid Ca 2+ increase is an important response to osmotic stress but Ca 2+ -independent osmotic sensory mechanisms may also be present.
Genetic identification of osmotic and Na + sensors will be very helpful to know about these early sensory mechanisms.
Na+ imparts the ionic component of salt stress. Extracellular Na+ is thought to be detected by a membrane receptor while intracellular Na+ is expected to be detected either by membrane proteins or by one of the Na+-sensitive enzymes in the cytoplasm (Zhu, 2003; Maathuis et al., 2014; Maathuis, 2014). The molecular nature of Na+ sensors is still unclear, the plasma membrane Na+/H+ antiporter SOS1 (Salt Overly Sensitive1) is a possible candidate because its cytoplasmic end is assumed to be involved in Na+ sensing (Zhu, 2003).
Under normal conditions, plant cells sustain a high level of K+/Na+ in the cytosol and such control is mediated by a tight regulation of ion flux. It involves primary active transport and secondary transport mediated by H+-ATPases and co-transporters/channels, respectively (Hauser and Horie, 2010). A rise of Na+ in root zone promotes the entry of Na+ ions inside the plant body either through plasma-membrane non-selective cation channels (NSCCs), HKT transporters, or via anatomical 'leaks' in the root endodermis (Demidchik and Tester, 2002; Munns and Tester, 2008; Hamamoto et al., 2015).
Sensing high temperature stress stimulus: Plants can detect temperature changes as small as 1degC (Penfield, 2008) and activate response mechanisms (Saidi et al., 2011; Conde et al., 2011; Grover et al., 2013; Cerny et al., 2014; Gao et al., 2014; Liu et al., 2015). Despite a number of dedicated efforts, still it is difficult to nominate the primary heat sensor(s). Plasma membrane Cyclic Nucleotide Gated Calcium Channels (CNGCs) (Younousse Saidi et al., 2009; Finka et al., 2012), two unfolded protein sensors, ER-UPR and Cyt-UPR (Sugio et al., 2009; Deng et al., 2011) and a histone variant (H2A.Z) containing nucleosomes (Kumar and Wigge, 2010) are considered putative heat sensors. Heat stress activates CNGCs, ER-UPR, and Cyt-UPR, and triggers signaling through multiple kinases as well as transcriptional regulators of the HSR, such as HSFs, MBF1c, and Rboh. Protein translation capacity of chloroplasts generates the retrograde signals to activate HsfA2-dependent heat-responsive genes in the nucleus.
Thus, the chloroplasts are proposed as heat sensors as well (Liu et al., 2015).
Plasma membrane is also considered as an important sensor for heat stress (Figure 2). It perceives temperature changes and transduces them into the nucleus where the transcriptome is rehabilitated (Saidi et al., 2009; Conde et al., 2011). Membrane lipid composition plays a key role in regulating calcium dependent heat-signaling pathway (Saidi et al., 2010). Elevation in external temperature brings about the activation of Ca2+ channels in plasma membrane causing the Ca2+ influx inside the plant cells. Moreover, heat stress leads to the alteration in properties of plasma membrane (Hofmann, 2009), which signals the activation of heat responsive (HR) regulatory networks. Other metabolites such as nitric oxide (NO) and hydrogen peroxide (H2O2) are also produced in response to heat stress and probably activate similar molecular mechanisms for improving the heat stress tolerance of plant (Hua, 2009; Saidi et al., 2011).
Response to stress
Salt stress response: When [Na+]cyt surpasses a threshold, response mechanisms are initiated (Figure 1), which involve vacuolar sequestration and/or extrusion of Na+ to the apoplast and a reduction in Na+ conductance of membranes (Maathuis, 2014). Once an osmotic or ionic stress component is sensed by plants, a signaling cascade involving different second messengers is initiated followed by activation of downstream kinases, calcium-dependent protein kinases (CDPKs) and calcineurin B-like proteins (CBLs) with CBL-interacting protein kinases (CIPKs) (Weinl and Kudla, 2009; Boudsocq and Sheen, 2013). It may transduce the signal to downstream transcription factors including Calmodulin Binding Transcription Activators (CAMTAs) (Pandey et al., 2013), GT-element-binding-like proteins (GTLs) (Weng et al., 2012) and MYBs (Yoo et al., 2005; Xie et al., 2014).
Although a prompt variation of Ca2+ is a hallmark response to osmotic stress, there may also exist Ca2+-independent osmotic sensory mechanisms. Genetic identification of osmotic and Na+ sensors is likely to be instrumental in resolving these early sensory mechanisms (Figure 1).
During stress conditions, a family of sensor transmitters, Calcineurin B-like proteins (CBL) and their respective kinase effectors, CBL-interacting protein kinases (CIPK), together make a primary element in signaling cascade responsible for Ca2+ signaling and is named as CIPK/CBL pathway (Yu et al., 2014). The CIPK-CBL complex regulates downstream targets like ion channels and transporters (Manik et al., 2015) and play significant role against various abiotic stresses (Luan et al., 2009). Opening of Ca2+ channels due to abiotic stress signals (Figure 3) causes a rapid influx of Ca2+ ions, that starts a cascade of stress signaling (White, 2000; Sanders et al., 2002). The Ca2+ signal stimulates the binding of calcineurin B-like protein, CBL, with Ca2+ leading to the formation of CBL-CIPK-type kinases complex which is responsible for decoding the Ca2+ signals (Zhu et al., 2013).
The interaction occurs when a conserved serine residue within the C terminus of CBLs gets phosphorylated by the interacting CIPKs which interact with CBL via CIPK-NAF domain (Hashimoto et al., 2012). This interaction then leads to the phosphorylation of downstream target proteins which leads to the development of stress tolerance.
An important adoption of plants for salinity tolerance is the extrusion of Na+ ions from plant body, which is brought about by SOS signaling pathway (Zhu et al., 1998; Ji et al., 2013). Salt stress induces the increase in cytosolic Ca2+. A calcium sensor SOS3 binds with Ca2+ and activates a serine/threonine protein kinase SOS2 of the SnRK3 family of protein kinases (Zhu et al., 1998; Halfter et al., 2000; Liu et al., 2000; Hrabak et al., 2003; Zhu, 2003). The SOS3 and SOS2 complex activates plasma membrane-localized Na+/H+ antiporter SOS1. This complex is responsible for a significant extrusion of Na+ ions from the cytosol (Shi et al., 2000; Qiu et al., 2002; Quintero et al., 2002; Zhu, 2003; Quan et al., 2007; Quintero et al., 2011). This signaling cascade is not as simple as it was thought to be. The activation of SOS1 does not completely depend on SOS3-SOS2 complex (Shabala et al., 2005).
Thus, the regulation of salt stress and extrusion of Na+ ions by SOS pathway is far more complex process and is not the only pathway responsible for maintaining ion-homeostasis and extruding excess Na+ ions from plant body.
Plants also compartmentalize Na+ ions to prevent their excess build-up in the cell. During salt stress, compartmentalization of Na+ ions is crucial for plant growth. Na+ ions enter the cytoplasm and are then transported to the vacuole via Na+/H+ antiporter (Gupta and Huang, 2014). Accumulation of Na+ ions in vacuoles lead to increased osmotic adjustment and increased sequestration of Na+ ions in root and leaf vacuoles (Munns and Tester, 2008).
Reduced rate of photosynthesis resulting from salinity induced oxidative stress, leads to the increased formation of reactive oxygen species (ROS), which are rapidly detoxified by various cellular enzymes (Apel and Hirt, 2004; Foyer and Noctor, 2005; Bose et al., 2014). RSA1, a nuclear-localized calcium-binding protein, its interacting partner, RITF1, and a transcription factor bHLH are involved in the regulation of salt stress by hunting reactive oxygen species (ROS) and regulating SOS1 gene (Guan et al., 2013).
One of the major and most important responses of plants to environmental stresses is the biosynthesis of ABA which activates a number of genes involved in respective stress response (Dong et al., 2015) and on the other hand, such responses could follow ABA-dependent or ABA-independent pathways (Agarwal and Jha, 2010). Under stress conditions, ABA responsive genes get activated. The activation of these genes, results from the binding of ABA induced TFs to their respective binding sites/cis-regulatory elements in the promoter region of these genes. The ABA induced TFs include AREB, DREB2A, DREB 2B, MYB/MYC, bZIP and RD22BP1 (Zhu, 2002; Yoshida et al., 2014; E et al., 2014). In response to salt stress, the basic leucine zipper transcription factor called AREB binds to ABRE elements leading to the activation of RD29B stress responsive gene, which is involved in providing tolerance against salinity.
Two of these ABRE motifs have been reported in Arabidopsis, which are involved in the regulation of LEA-like (late embryogenesis abundant) protein encoding RD29B gene (Narusaka et al., 2003).
The TFs, DREB2A and DREB2B, are drought inducible and their expression is regulated by ABA dependent pathways. These genes are responsible for the activation of RD29A stress responsive gene, leading to the maintenance of osmotic equilibrium during drought stress. The MYB/MYC TFs get induced at the late stages of stress response. RD2BP1 and MYB/MYC TFs cause the activation of RD22 gene in response to stress (Tuteja and Sopory, 2008).
Heat stress response: Heat stress differently affects the stability of several membranes, proteins, cytoskeleton and RNA structures. Cytoskeleton de-polymerization, protein conformation, metabolic reactions and membrane fluidity are regarded as the temperature sensitive processes (Ruelland and Zachowski, 2010). Moreover, high temperature negatively affects the efficiency of enzymatic reactions, which disturbs the major physiological and metabolic processes (Hasanuzzaman et al., 2013).
Plants have developed several physiological and molecular pathways to cope with heat stress (Figure 2). Plant response to heat stress is regulated both by genetic and epigenetic mechanisms (Qu et al., 2013; Sanchez and Paszkowski, 2014; Liu et al., 2015). Heat stress-responsive genes and proteins in plants include protein kinases, transcription factors, heat shock proteins (HSPs) and catalases (Qu et al., 2013). Moreover, plants might regulate the heat stress response at the post-transcriptional level by inducing a global mRNA decay process (Merret et al., 2013).
Various secondary messengers; nitric oxide (NO), hydrogen peroxide (H2O2), Ca2+ ions and plasma membrane are basic elements of heat stress signaling pathways (Bolwell, 1999; Durner and Klessig, 1999; Smekalova et al., 2014; Pandey et al., 2015). The downstream components; mitogen-activated protein kinases, Hsp90 and calmodulins are involved in the activation of Heat-shock transcription factors (Hsf). Heat signal transduction induced through different pathways causes activation of Hsfs, the expression of Hsps and the onset of thermos-tolerance (Saidi et al., 2011).
The expression of Hsfs depends on the intensity of stress. Upon very high temperature overexpression of Hsf causes the activation of all the heat stress responsive genes. There are multiple copies of Hsfs in plants like 17 in tomato, 19 in rice (Baniwal et al., 2004) and 21 in Arabidopsis (Nover et al., 2001). These genes are grouped into three classes A, B and C, depending on the differences in the protein structural features like flexible linkers and oligomerization domains (Nover et al., 2001; Baniwal et al., 2004). Each Hsp subfamily has a different mechanism of action, some of them cause the degradation of misfolded proteins, some prevent the aggregation of Hsps by binding to different intermediates of folding (Hsp70 and Hsp60) and Hsp100 re-activates the already aggregated proteins. HsfA8 functions as redox sensing transcription factor within the stress-responsive transcriptional network (Giesguth et al., 2015).
These proteins are specific in expression and are expressed at certain developmental stages of plant like seed germination, embryogenesis, microsporogenesis and fruit maturation (Prasinos et al., 2005).
Previous studies on Arabidopsis concluded that Arabidopsis mitogen-activated protein kinase MPK6 become activated under heat stress (Sinha et al., 2011). MPK6 specifically activates HsfA2 (Evrard et al., 2013) followed by activation of MAPKs. MAPK-dependent responses to heat stress in alfalfa and tomato plants have previously been described (Link et al., 2002; Sangwan et al., 2002). ZmMAPK1 overexpressing A. thaliana plants respond better to drought and heat stress (Wu et al., 2015).
Heat stress response mechanisms have also shown correlation with epigenetic gene silencing in Arabidopsis. This has been confirmed by inducing mutations in gene silencing pathways. The mutated plants showed hypersensitivity to heat stress. The response to temperature stress at transcription level co-ordinates with RNA-dependent DNA methylation pathway for the induction of resistance (Popova et al., 2013).
A significant fraction of the HSPs seems to be co-regulated by cytokinin. It is argued that temperature and cytokinin signaling pathways are interconnected through Ca2+ ions fluxes. Furthermore, the response of proteome to cytokinin treatment at low and standard temperatures partially minimizes the effects of heat shocks on it. Therefore, cytokinin may directly contribute in heat signaling pathway. Finally, most of the heat shock and cytokinin responsive proteins are present together in the chloroplast. (Cerny et al., 2014)
Besides Hsps, there are certain other genes as well, found to be up regulated by heat stress. Arabidopsis cytosolic ascorbate peroxidase gene (APX1) is up regulated by heat stress. A functional heat shock element (HSE) is located in its 5'-promoter region (Storozhenko et al., 1998). Under stressful conditions plants accumulate H2O2 in their cytosol, which may lead to cell death. The accumulation of toxic H2O2 is prevented by the expression of APX1 which is a major hydrogen peroxide-scavenging enzyme in the cytosol (Mittler et al., 2004). In response to a combined heat and drought stress treatment, APX1-deficient mutant (apx1), accumulated more hydrogen peroxide in the cytosol and was considerably more sensitive to the stress combination than wild type. This shows that APX1 plays a key role in providing thermo-tolerance to plants (Koussevitzky et al., 2008).
In Arabidopis thaliana MBF1c (multi-protein binding factor 1c) plays a key role in the regulation of thermo-tolerance. MFB1c interacts with heat inducible TPS5 (trehalose phosphate synthase 5) to function during heat stress and the mutants deficient for TPS5 are sensitive to high temperature (Suzuki et al., 2008). Along with MFB1c, AtSAP5, a nuclear localized protein, affects cellular responses to abiotic stresses i.e. water deficiency, salinity, osmotic imbalance and heat stress (Kang et al., 2011).
Li et al. (2011) categorized the function of WRKY33, WRKY26, and WRKY25 as effective controllers of response against heat stress. This categorization was based on the analysis of both their loss-of-function and over-expression phenotypes, and potential upstream and downstream targets of these genes. It is suggested that these three regulators exhibit fractional redundancy in thermo-tolerance and help in coordination between Hsps-related signaling and MBF1c (ethylene)-activated pathways that facilitate responses to heat stress. Similarly, members of DREB family are also important for plant response to heat stress (Qu et al., 2013). There are also other genes involved in Hsp independent pathways. AtPARK13 is a heat stress-induced protease which is localized in mitochondria. It confers thermo-tolerance in Arabidopsis and degrades miss-folded proteins (Basak et al., 2014).
Cross-talk of salt and heat stress response in plants: Heat and salinity stress combination may affect agronomic traits of plants, either positively or negatively (Suzuki et al., 2014) and direct rearrangements in metabolic and regulatory networks (Krasensky and Jonak, 2012). Therefore, an understanding of such mechanisms could be fruitful in developing multiple stress tolerant plants. To fight with these types of abiotic stresses, plants modulate their physiological and biochemical pathways. Like, salt stress causes the activation of pathways which are aimed at detoxifying the ROS and maintaining the ion-homeostasis. In the same way heat stress induces the metabolic pathways which employ heat shock proteins for the development of thermo-tolerance.
Correlation among different regulatory networks is referred to as cross talk. Studies have revealed the existence of cross-talk among the heat and non-heat stress regulatory pathways, where Hsfs act as intersecting points in response to various types of stresses including thermal and non-thermal stresses like drought, salt, cold and heat stresses. Genome-wide transcriptional profiling led to the finding that unlike other stresses, osmotic, cold, and salt treatments induced a strong Hsps expression.The degree of crosstalk varies depending on the intensity of stress (Swindell et al., 2007). Among all the four abiotic stresses stated before, the highest induction of Hsp100 is caused by both heat and salt stresses. Hsf and Hsps gene families have shown to be widely induced by heat, drought and salt treatments, whereas, Hsp100, Hsp90 and Hsp70 families are more specific in response to stresses (Hu et al., 2009).
Moreover, plant response to a combination of heat and drought stress could be different from individual drought or heat stress. This is because of the two correlated multi-gene defense pathways as well as specific expression of 454 transcripts during combination of heat and drought stress (Rizhsky et al., 2004). AtHsfA6a works as a transcriptional activator of stress-responsive genes following the ABA-dependent signaling system. Moreover, plants over-expressing AtHsfA6a were highly sensitive to ABA and showed increased resistance against drought and salt stresses (Hwang et al., 2014). DREB2A is involved in the upregulation of heat and salinity stress responsive genes (Sakuma et al., 2006). In response to multiple stresses some proteins work together and activate genes coding for regulators as miRNAs and TFs (Nigam et al., 2015). These regulatory genes are responsible for downstream target genes regulation for providing stress resistance.
It is very important to understand the relationship between regulators and target genes in vivo.
Conclusions and perspectives: It has clearly been established that plants deploy special sensory-response mechanisms to cope with challenging environment. Starting from the onset of stress, plants respond through a chain of inter-connected and inter-dependent events. Over the years, a significant amount of information has been gathered for plant stress response mechanisms. Current understanding of the epigenetic regulatory mechanisms (like chromatin regulation mediated by histone modification and DNA methylation, and RNA-mediated regulation) involved in plant abiotic stress responses has gradually been improved in recent years (Kim et al., 2015; Mittal et al., 2016). Still there are many unanswered questions. The putative nature of stress sensors (Shabala et al., 2015a,b) adds complexity to our understandings. An intense investigation is suggested to explore novel genetic resources (including wild parents and extremophiles) for the identification of stress sensors.
As plasma membrane is the only barrier between cellular contents and the environment, membrane bound transport proteins might be given more attention.
Acknowledgements: The author wishes to acknowledge support in terms of research grant from the Higher Education Commission of Pakistan (Project#PD-IPFP/HRD/HEC/2013/1978) and International Foundation for Science (Project number# C/5684-1).
Conflict of interests: The research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Authors contributions: IR, HN, MHS and FA planned, designed and drafted the manuscript. MHS, AU and FA generated the figure. RMA, MAA, AU, FR, MAf, MAb, and FA read and approved the final manuscript.
Agarwal, P.K. and B. Jha (2010). Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol. Plant., 54: 201-212.
Agurla, S., G. Gayatri, and A.S. Raghavendra (2014). Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens. Nitric Oxide, 43: 89-96.
Albacete, A.A., C. Martinez-andujar and F. Perez-alfocea (2014). Hormonal and metabolic regulation of source - sink relations under salinity and drought: From plant survival to crop yield stability. Biotechnol. Adv., 32: 12-30.
Apel, K. and H. Hirt (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol., 55: 373-99.
Arefian, M., S. Vessal and A. Bagheri (2014). Biochemical changes in response to salinity in chickpea (Cicer arietinum L.) during early stages of seedling growth. J. Anim. Plant Sci. 24, 1849-1857
Arnadottir, J. and M. Chalfie (2010). Eukaryotic mechanosensitive channels. Annu. Rev. Biophys., 39, 111-137.
Baniwal, S.K., K. Bharti, K.Y. Chan, M. Fauth, A. Ganguli, S. Kotak, S.K. Mishra, L. Nover, M. Port, K.-D. Scharf, J. Tripp, C. Weber, D. Zielinski, and P. von Koskull-Doring (2004). Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J. Biosci., 29, 471-87.
Bargmann, B.O.R., A.M. Laxalt, B. Riet, B. Schooten, E. Merquiol, C. Testerink, M.A. Haring, D. Bartels and T. Munnik (2009). Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol., 50, 78-89.
Basak, I., R. Pal, K.S. Patil, A. Dunne, H.-P. Ho, S. Lee, D. Peiris, J. Maple-Grodem, M. Odell, E.J. Chang, J.P. Larsen, and S.G. Moller (2014). Arabidopsis AtPARK13, which confers thermotolerance, targets misfolded proteins. J. Biol. Chem., 289, 14458-14469.
Battisti, D.S. and R.L. Naylor (2009). Historical warnings of future food insecurity with unprecedented seasonal heat. Science, 323: 240-4.
Bolwell, G.P. (1999). Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol., 2: 287-294.
Bose, J., A. Rodrigo-Moreno and S. Shabala (2014). ROS homeostasis in halophytes in the context of salinity stress tolerance. J. Exp. Bot., 65: 1241-1257.
Boudsocq, M. and J. Sheen (2013). CDPKs in immune and stress signaling. Trends Plant Sci., 18: 30-40.
Cerny, M., P.L. Jedelsky, J. Novak, A. Schlosser and B. Brzobohaty (2014). Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant. Cell Environ., 37: 1641-55.
Conde, A., M.M. Chaves and H. Geros (2011). Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol., 52: 1583-602.
Coutand, C. (2010) Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci., 179: 168-182.
Darwish, E., C. Testerink, M. Khalil, O. El-Shihy and T. Munnik (2009). Phospholipid Signaling Responses in Salt-Stressed Rice Leaves. Plant Cell Physiol., 50, 986-997.
Davies, C., R. Shin, W. Liu, M.R. Thomas and D.P. Schachtman (2006). Transporters expressed during grape berry (Vitis vinifera L.) development are associated with an increase in berry size and berry potassium accumulation. J. Exp. Bot., 57: 3209-16.
DeFalco, T., K.W. Bender and W. Snedden (2010). Breaking the code: Ca2+ sensors in plant signalling. Biochem. J., 425: 27-40.
Demidchik, V. and M. Tester (2002). Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiol., 128, 379-387.
Deng, Y., S. Humbert, J.X. Liu, R. Srivastava, S.J. Rothstein and S.H. Howell (2011). Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc. Natl. Acad. Sci., 108: 7247-7252.
Dinneny, J.R. (2014). Traversing organizational scales in plant salt-stress responses. Curr. Opin. Plant Biol., 23C: 70-75.
Donaldson, L., N. Ludidi, M.R. Knight, C. Gehring and K. Denby (2004). Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Lett., 569: 317-320.
Dong, T., Y. Park and I. Hwang (2015). Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem., 58: 29-48.
Durner, J. and D.F. Klessig (1999). Nitric oxide as a signal in plants. Curr. Opin. Plant Biol., 2: 369-374.
E, Z.G., Y.P. Zhang, J.H. Zhou and L. Wang (2014). Mini Review Roles of the bZIP gene family in rice. Genet. Mol. Res., 13: 3025-36.
Evrard, A., M. Kumar, D. Lecourieux, J. Lucks, P. Koskull-Doring and H. Hirt (2013). Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. Peer J, 1: e59.
FAOSTAT, D. (2009) Food and Agriculture Organization of the United Nations Year book,.
Finka, A., A.F.H. Cuendet, F.J.M. Maathuis, Y. Saidi and P. Goloubinoff (2012). Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell, 2: 3333-3348.
Foyer, C.H. and G. Noctor (2005). Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17: 1866-1875.
Gao, K., Y. L. Liu, B. Li, R.G. Zhou, D.Y. Sun and S. Z. Zheng (2014). Arabidopsis thaliana phosphoinositide-specific phospholipase C isoform 3 (AtPLC3) and AtPLC9 have an additive effect on thermotolerance. Plant Cell Physiol., 55: 1873-83.
Giesguth, M., A. Sahm, S. Simon and K.-J. Dietz (2015). Redox-dependent translocation of the heat shock transcription factor AtHSFA8 from the cytosol to the nucleus in Arabidopsis thaliana. FEBS Lett., 589: 718-725.
Grover, A., D. Mittal, M. Negi and D. Lavania (2013). Generating high temperature tolerant transgenic plants: Achievements and challenges. Plant Sci., 205-206: 38-47.
Guan, Q., J. Wu, X. Yue, Y. Zhang and J. Zhu (2013). A nuclear calcium-sensing pathway is critical for gene regulation and salt stress tolerance in arabidopsis. PLoS Genet., 9: e1003755.
Gupta, B. and B. Huang (2014). Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. Int. J. Genomics, 2014: 1-18.
Halfter, U., M. Ishitani and J.K. Zhu (2000). The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. U. S. A., 97: 3735-40.
Hamamoto, S., T. Horie, F. Hauser, U. Deinlein, J.I. Schroeder and N. Uozumi (2015). HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr. Opin. Biotechnol., 32: 113-120.
Hamill, O.P. and B. Martinac (2001). Molecular basis of mechanotransduction in living cells. Physiol. Rev., 81: 685-740.
Hasanuzzaman, M., K. Nahar, M.M. Alam, R. Roychowdhury and M. Fujita (2013). Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci., 14: 9643-9684.
Hashimoto, K., C. Eckert, U. Anschutz, et al. (2012). Phosphorylation of Calcineurin B-like (CBL) Calcium Sensor Proteins by their CBL-interacting Protein Kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. J. Biol. Chem., 287, 7956-7968.
Hauser, F. and T. Horie (2010). A conserved primary salt tolerance mechanism mediated by HKT transporters: A mechanism for sodium exclusion and maintenance of high K+/Na+ ratio in leaves during salinity stress. Plant, Cell Environ., 33: 552-565.
Hofmann, N.R. (2009) The Plasma Membrane as First Responder to Heat Stress. Plant Cell Online, 21: 2544.
Hrabak, E.M., C.W.M. Chan, M. Gribskov, J.F. Harper, J.H. Choi, N. Halford, S. Luan, H.G. Nimmo, M.R. Sussman, M. Thomas, K. Walker-simmons, J. Zhu, and A.C. Harmon (2003). The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol., 132: 666-680.
Hu, W., G. Hu and B. Han (2009). Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci., 176: 583-590.
Hua, J. (2009). From freezing to scorching, transcriptional responses to temperature variations in plants. Curr. Opin. Plant Biol., 12: 568-573.
Hwang, S.M., D.W., Kim, M.S. Woo, H.S. Jeong, Y.S. Son, S. Akhter, G.J. Choi and J.D. Bahk (2014). Functional characterization of Arabidopsis HsfA6a as a heat-shock transcription factor under high salinity and dehydration conditions. Plant. Cell Environ., 37: 1202-1222.
Ji, H., J.M. Pardo, G. Batelli, M.J. Oosten, R.A. Bressan and X. Li (2013). The Salt Overly Sensitive (SOS) pathway: established and emerging roles. Mol. Plant, 6: 275-286.
Jiang, Z., S. Zhu, R. Ye, Y. Xue, A. Chen, L. An and Z.-M. Pei (2013). Relationship between NaCl-and H2O2-induced cytosolic Ca2+ increases in response to stress in Arabidopsis. PLoS One, 8: e76130.
Kang, M., M. Fokar, H. Abdelmageed and R.D. Allen (2011). Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Mol. Biol., 75: 451-466.
Kim, J.M., T. Sasaki, M. Ueda, K. Sako and M. Seki (2015). Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front. Plant Sci., 6: 114
Khan, M.N., M.H. Siddiqui, F. Mohammad and M. Naeem (2012). Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide - Biol. Chem., 27: 210-218.
Koussevitzky, S., N. Suzuki, S. Huntington, L. Armijo, W. Sha, D. Cortes, V. Shulaev and R. Mittler (2008). Ascorbate Peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem., 283: 34197-34203.
Krasensky, J. and C. Jonak (2012). Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J. Exp. Bot., 63: 1593-1608.
Kumar, M.N., W.-N. Jane and P.E. Verslues (2013). Role of the putative osmosensor Arabidopsis Histidine Kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol., 161: 942-953.
Kumar, S.V. and P.A. Wigge (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in arabidopsis. Cell, 140: 136-147.
Kung, C. (2005). A possible unifying principle for mechanosensation. Nature, 436: 647-654.
Kushwaha, H.R., S.L. Singla-Pareek and A. Pareek (2013). Putative osmosensor - OsHK3b - a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J. Biomol. Struct. Dyn., 32: 37-41.
Laohavisit, A., S.L. Richards, L. Shabala, C. Chen, R.D.D.R. Colaco, S.M. Swarbreck, E. Shaw, A. Dark, S. Shabala, Z. Shang, and J.M. Davies (2013) Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin1. Plant Physiol., 163: 253-62.
Laohavisit, A., Z. Shang, L. Rubio, T.A Cuin, A.A. Very, A. Wang, J.C. Mortimer, N. Macpherson, K.M. Coxon, N.H. Battey, C. Brownlee, O.K. Park, H. Sentenac, S. Shabala, A.R. Webb, J.M. Davies (2012). Arabidopsis annexin1 mediates the radical-activated plasma membrane Ca2+-and K+-permeable conductance in root cells. Plant Cell, 24: 1522-33.
Li, S., Q. Fu, L. Chen, W. Huang and D. Yu (2011). Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta, 233: 1237-1252.
Link, V., A.K. Sinha, P. Vashista, M.G. Hofmann, R.K. Proels, R. Ehness and T. Roitsch (2002). A heat-activated MAP kinase in tomato: A possible regulator of the heat stress response. FEBS Lett., 531, 179-183.
Liu, J., L. Feng, J. Li and Z. He (2015). Genetic and epigenetic control of plant heat responses. Front. Plant Sci., 06: 1-21.
Liu, J., M. Ishitani, U. Halfter, C.S. Kim and J.K. Zhu (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc. Natl. Acad. Sci. U. S. A., 97: 3730-3734.
Lobell, D.B. and C.B. Field (2007). Global scale climate- crop yield relationships and the impacts of recent warming. Environ. Res. Lett., 2: 014002.
Lobell, D.B., W. Schlenker and J. Costa-Roberts (2011). Climate trends and global crop production since 1980. Science, 333: 616-620.
Luan, S., W. Lan and S. Chul Lee (2009). Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network. Curr. Opin. Plant Biol., 12: 339-346.
Maathuis, F.J.M. (2014) Sodium in plants: perception, signalling, and regulation of sodium fluxes. J. Exp. Bot., 65: 849-858.
Maathuis, F.J.M., I. Ahmad and J. Patishtan (2014). Regulation of Na+ fluxes in plants. Front. Plant Sci., 5: 1-9.
Manik, S.M.N., S. Shi, J. Mao, L. Dong, Y. Su, Q. Wang and H. Liu (2015). The calcium sensor CBL-CIPK is involved in plant's response to abiotic stresses. Int. J. Genomics, 2015: 493191.
Martinac, B., Y. Saimi and C. Kung (2008). Ion Channels in Microbes. Physiol. Rev., 88: 1449-1490.
Merret, R., J. Descombin, Y.T. Juan, J.J. Favory, M.C. Carpentier, C. Chaparro, Y.Y. Charng, J.M. Deragon and C. Bousquet-Antonelli (2013). XRN4 and LARP1 are required for a heat-triggered mRNA decay pathway involved in plant acclimation and survival during thermal stress. Cell Rep., 5: 1279-1293.
Mittal1, D., N. Sharma, V. Sharma, S.K. Sopory and N. Sanan-Mishra (2016). Role of microRNAs in rice plant under salt stress. Ann Appl Biol. 168: 2-18
Miller, G., N. Suzuki, S. Ciftci-Yilmaz and R. Mittler (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell Environ., 33: 453-467.
Mittler, R., S. Vanderauwera, M. Gollery and F. Breusegem (2004). Reactive oxygen gene network of plants. Trends Plant Sci., 9: 490-498.
Monshausen, G.B. and S. Gilroy (2009). Feeling green: mechanosensing in plants. Trends Cell Biol., 19: 228-235.
Munnik, T. and J.E.M. Vermeer (2010). Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant. Cell Environ., 33: 655-69.
Munns, R. and M. Tester (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59: 651-81.
Narusaka, Y., K. Nakashima, Z.K. Shinwari, Y. Sakuma, T. Furihata, H. Abe, M. Narusaka, K. Shinozaki and K. Yamaguchi-Shinozaki (2003). Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J., 34: 137-48.
Nigam, D., S. Kumar, D.C. Mishra, A. Rai, S. Smita and A. Saha (2015). Synergistic regulatory networks mediated by microRNAs and transcription factors under drought, heat and salt stresses in Oryza Sativa spp. Gene, 555: 127-139.
Nover, L., K. Bharti, P. Doring, S.K. Mishra, A. Ganguli and K.D. Scharf (2001). Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones, 6: 177-189.
Pandey, N., A. Ranjan, P. Pant, R.K. Tripathi, F. Ateek, H.P. Pandey, U.V. Patre and S.V. Sawant (2013). CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics, 14: 216.
Pandey, P., V. Ramegowda and M. Senthil-Kumar (2015). Shared and unique responses of plants to multiple individual stresses and stress combinations: physiological and molecular mechanisms. Front. Plant Sci., 6: 723.
Parihar, P., S. Singh, R. Singh, V.P. Singh and S.M. Prasad (2015). Effect of salinity stress on plants and its tolerance strategies: a review. Environ. Sci. Pollut. Res., 22, 4056-4075.
Penfield, S. (2008). Temperature perception and signal transduction in plants. New Phytol., 179: 615-628.
Peyronnet, R., D. Tran, T. Girault and J.-M. Frachisse (2014). Mechanosensitive channels: feeling tension in a world under pressure. Front. Plant Sci., 5: 558.
Popova, O. V, H.Q. Dinh, W. Aufsatz and C. Jonak (2013). The RdDM pathway is required for basal heat tolerance in Arabidopsis. Mol. Plant, 6: 396-410.
Prasinos, C., K. Krampis, D. Samakovli and P. Hatzopoulos (2005). Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development. J. Exp. Bot., 56: 633-644.
Qiu, Q., Y. Guo, M.A. Dietrich, K.S. Schumaker and J. Zhu (2002). Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc. Natl. Acad. Sci. U. S. A., 99: 8436-8441.
Qu, A.-L., Y.-F. Ding, Q. Jiang and C. Zhu (2013). Molecular mechanisms of the plant heat stress response. Biochem. Biophys. Res. Commun., 432: 203-7.
Quan, R., H. Lin, I. Mendoza, Y. Zhang, W. Cao, Y. Yang, M. Shang, S. Chen, J.M. Pardo, and Y. Guo (2007). SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell, 19: 1415-1431.
Quintero, F.J., J. Martinez-Atienza, I. Villalta, X. Jiang, W.-Y. Kim, Z. Ali, H. Fujii, I. Mendoza, D.J. Yun, J.K. Zhu, and J.M. Pardo (2011). Activation of the plasma membrane Na+/H+ antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc. Natl. Acad. Sci., 108: 2611-2616.
Quintero, F.J., M. Ohta, H. Shi, J. Zhu and J.M. Pardo (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc. Natl. Acad. Sci. U. S. A., 99: 9061-9066.
Raghavendra, A.S., V.K. Gonugunta, A. Christmann and E. Grill (2010). ABA perception and signalling. Trends Plant Sci., 15: 395-401.
Reddy, A.S.N., G.S. Ali, H. Celesnik and I.S. Day (2011). Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expression. Plant Cell, 23: 2010-2032.
Richards, S.L., A. Laohavisit, J.C. Mortimer, L. Shabala, S.M. Swarbreck, S. Shabala and J.M. Davies (2014). Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots. Plant J., 77: 136-145.
Rizhsky, L., H. Liang, J. Shuman, V. Shulaev, S. Davletova, and R. Mittler (2004). When Defense Pathways Collide. The Response of Arabidopsis to a Combination of Drought and Heat Stress. Plant Physiol., 134: 1683-1696.
Rolland, F., B. Moore and J. Sheen (2002). Sugar sensing and signaling in plants. Plant Cell, 14:Suppl, S185-S205.
Ruelland, E. and A. Zachowski (2010). How plants sense temperature. Environ. Exp. Bot., 69, 225-232.
Saidi, Y., A. Finka and P. Goloubinoff (2011). Heat perception and signalling in plants: a tortuous path to thermotolerance. New Phytol., 190: 556-65.
Saidi, Y., A. Finka, M. Muriset, Z. Bromberg, Y.G.Weiss, F.J.M. Maathuisand, P. Goloubinoff (2009). The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell Online, 21: 2829-2843.
Saidi, Y., M. Peter, A. Finka, C. Cicekli, L. Vigh and P. Goloubinoff (2010). Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response. Plant Signal. Behav., 5: 1530-1533.
Sakuma, Y., K. Maruyama, F. Qin, Y. Osakabe, K. Shinozaki and K. Yamaguchi-Shinozaki (2006). Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. U. S. A., 103: 18822-18827.
Sanchez, D.H. and J. Paszkowski (2014). Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genet., 10: e1004806..
Sanders, D., J. Pelloux, C. Brownlee and J.f. Harper (2002). Calcium at the crossroads of signaling. Plant Cell, 14 Suppl, S401-S417.
Sangwan, V., B.L. Orvar, J. Beyerly, H. Hirt and S. D. Rajinder (2002). Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J., 31: 629-638.
Saucedo-Garcia, M. M. Gavilanes-Ruiz, and O. Arce-Cervantes (2015). Long-chain bases, phosphatidic acid, MAPKs, and reactive oxygen species as nodal signal transducers in stress responses in Arabidopsis. Front. Plant Sci., 6: 1-14.
Shabala, L., T. Cuin, I. Newman and S. Shabala (2005). Salinity-induced ion flux patterns from the excised roots of Arabidopsis sos mutants. Planta, 222: 1041-1050.
Shabala, S., J. Bose, A.T. Fuglsang and I. Pottosin (2015a). On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. J. Exp. Bot. 67: 1015-1031
Shabala, S., H. Wu and J. Bose (2015b). Review: Salt stress sensing and early signaling events in plant roots: current knowledge and hypothesis. Plant Sci. 241: 109-19
Sham, A., K. Moustafa, S. Al-Ameri, A. Al-Azzawi, R. Iratni and S. AbuQamar (2015). Identification of Arabidopsis candidate genes in response to biotic and abiotic stresses using comparative microarrays. PLoS One, 10: e0125666.
Shi, H., M. Ishitani, C. Kim and J.K. Zhu (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc. Natl. Acad. Sci. U. S. A., 97: 6896-6901.
Sinha, A.K., M. Jaggi, B. Raghuram and N. Tuteja (2011). Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal. Behav., 6: 196-203.
Smekalova, V., A. Doskocilova, G. Komis and J. Samaj (2014). Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants. Biotechnol. Adv., 32: 2-11.
Storozhenko, S., P. Pauw, M. Van Montagu, D. Inze and S. Kushnir (1998). The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol., 118: 1005-1014.
Sugio, A., R. Dreos, F. Aparicio and A.J. Maule (2009). The cytosolic protein response as a subcomponent of the wider heat shock response in Arabidopsis. Plant Cell Online, 21: 642-654.
Suzuki, N., S. Bajad, J. Shuman, V. Shulaev and R. Mittler (2008). The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana. J. Biol. Chem., 283, 9269-9275.
Suzuki, N., R.M. Rivero, V. Shulaev, E. Blumwald and R. Mittler (2014). Abiotic and biotic stress combinations. New Phytol., 203: 32-43.
Swindell, W.R., M. Huebner and A.P. Weber (2007). Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics, 8, 125.
Tamura, T., K. Hara, Y. Yamaguchi, N. Koizumi and H. Sano (2003). Osmotic stress tolerance of transgenic tobacco expressing a gene encoding a membrane-located receptor-like protein from tobacco plants. Plant Physiol., 131, 454-62.
Tran, L.P., T. Urao, F. Qin, K. Maruyama, T. Kakimoto, K. Shinozaki and K. Yamaguchi-Shinozaki (2007). Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A., 104, 20623-8.
Tuteja, N. and S.K. Sopory (2008). Chemical signaling under abiotic stress environment in plants. Plant Signal. Behav., 3, 525-536.
Urao, T., B. Yakubov, R. Satoh, K. Yamaguchi-Shinozaki, M. Seki, T. Hirayama and K. Shinozaki (1999). A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell, 11, 1743-54.
Wahid, A., S. Gelani, M. Ashraf and M.R. Foolad (2007). Heat tolerance in plants: An overview. Env. and Exp. Bot. 61, 199-223
Walker, R.K. and G.A. Berkowitz (2013). Detection of reactive oxygen species downstream of cyclic nucleotide signals in plants. Cyclic Nucleotide Signaling in Plants. pp. 245-252.
Wasternack, C. and B. Hause (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development.Ann. Bot., 111, 1021-1058.
Weinl, S. and J. Kudla (2009). The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol., 184: 517-28.
Weng, H., C.Y. Yoo, M.J. Gosney, P.M. Hasegawa and M.V. Mickelbart (2012). Poplar GTL1 is a Ca2+/calmodulin-binding transcription factor that functions in plant water use efficiency and drought tolerance. PLoS One, 7: e32925.
White, P.J. (2000) Calcium channels in higher plants. Biochim. Biophys. Acta - Biomembr., 1465: 171-189.
Wohlbach, D.J., B.F. Quirino and M.R. Sussman (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell, 20: 1101-1117.
Wu, L., X. Zu, H. Zhang, L. Wu, Z. Xi and Y. Chen (2015). Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana. Plant Mol. Biol., 88, 429-443.
Xie, R. J., L. Zheng, L. Deng, S.L. He, S. Yi, Q. Lv and Y.Q. Zheng (2014). The role of R2R3MYB transcription factors in plant stress tolerance. J. Anim. Plant Sci. 24, 1821-1833
Yadav, S., M. Irfan, A. Ahmad and S. Hayat (2011). Causes of salinity and plant manifestations to salt stress: A review. J. Environ. Biol., 32, 667-685.
Yoo, J.H., C.Y. Park, J.C. Kim, W. Do Heo, M.S. Cheong, H.C. Park, M.C. Kim, B.C. Moon, M.S. Choi, Y.H. Kang, J.H. Lee, H.S. Kim, S.M. Lee, H.W. Yoon, C.O. Lim, D.-J. Yun, S.Y. Lee, W.S. Chung, and M.J. Cho (2005). Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in arabidopsis. J. Biol. Chem., 280, 3697-706.
Yoshida, T., J. Mogami and K. Yamaguchi-Shinozaki (2014). ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr. Opin. Plant Biol., 21, 133-139.
Yu, L., J. Nie, C. Cao, Y. Jin, M. Yan, F. Wang, J. Liu, Y. Xiao, Y. Liang, and W. Zhang (2010). Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol., 188, 762-773.
Yu, Q., L. An and W. Li (2014). The CBL-CIPK network mediates different signaling pathways in plants. Plant Cell Rep., 33, 203-214.
Yuan, F., H. Yang, Y. Xue, D. Kong, R. Ye, C. Li, J. Zhang, L. Theprungsirikul, T. Shrift, B. Krichilsky, D.M. Johnson, G.B. Swift, Y. He, J.N. Siedow, and Z.M. Pei (2014). OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature, 514, 367-371.
Zhang, Y.P., Z.G.E, H. Jiang, L. Wang, J. Zhou and D.F. Zhu (2015). A comparative study of stress-related gene expression under single stress and intercross stress in rice. Genet. Mol. Res., 14: 3702-17.
Zhu, J. (2002). salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol., 1-25.
Zhu, J., J. Liu and L. Xiong (1998). Genetic analysis of salt tolerance in arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell, 10: 1181-1191.
Zhu, J.K. (2003). Regulation of ion homeostasis under salt stress. Curr. Opin. Plant Biol., 6, 441-445.
Zhu, X., Y. Feng, G. Liang, N. Liu and J. Zhu (2013). Aequorin-based luminescence imaging reveals stimulus-and tissue-specific Ca2+ dynamics in Arabidopsis plants. Mol. Plant, 6: 444-455.
|Printer friendly Cite/link Email Feedback|
|Publication:||Journal of Animal and Plant Sciences|
|Date:||Apr 30, 2017|
|Previous Article:||THE EFFECT OF EXPLANT SOURCES AND GROWTH REGULATORS ON CALLUS INDUCTION AND REGENERATION IN DIFFERENT TOMATO CULTIVARS.|
|Next Article:||ASSESMENT OF BIOCHEMICAL AND IONIC ATTRIBUTES AGAINST SALT STRESS IN EGGPLANT (Solanum melongena L.) GENOTYPES.|