Abiotic stress is the primary cause of crop loss worldwide, reducing average yields for most major crop plants by more than 50%. Among abiotic stress, drought, salinity, high temperature, and cold are major adverse environmental factors that limit the crop production and productivity by inhibiting the genetic potential of the plant. So, it leads to complete change of morphological, physiological, biochemical, and molecular behavior of the plants and modifies regular metabolism of life, thereby adversely affecting plant productivity. Major effects of the drought, salinity, extreme temperatures, and cold stress are often interconnected and form similar cellular damage. To adopt plants with various abiotic stresses, plants can initiate a number of molecular, cellular, and physiological changes in its system. Sensors are molecules that perceive the initial stress signal from the outside of the plant system and initiate a signaling cascade to transmit the signal and activate nuclear transcription factors to induce the expression of specific sets of genes. Understanding this molecular and physiological basis of plant responses produced because of abiotic stress will help in molecular and modern breeding applications toward developing improved stress-tolerant crops. This review presents an overview and implications of physiological and molecular aspects of main abiotic stress, i.e., drought, heat, salt, and cold. Potential strategies to improve abiotic tolerance in crops are discussed.
- abiotic stress
- signal transduction
- stress-inducible genes
- gene expression
- mitigation process
- genetic engineering and genome editing
Plants live in constantly changing environments that are often unfavorable or stressful for growth and development. These unfavorable environmental conditions for plant growth are drought or water stress, high temperature or heat stress, low temperature or cold stress, excessive salt or salinity stress, and heavy metals toxicity like aluminum, arsenate, and cadmium in the soil. These adverse abiotic stresses are major threat that limits agriculture production and productivity, thereby creating great food insecurity. In the near future, it is predicted that because of climate change, abiotic stresses may become more intense and frequent. Drought and salinity are becoming drastically increased in many regions and may cause serious salinization of more than 50% of all arable lands by the year 2050. Consequently, because of rising temperatures and frequent flooding events for several decades, fertile agricultural land and crop yields may decrease rapidly, especially in the mid-latitudes [1, 2]. In addition to these factors, anthropogenic activities may lead to an increased abundance of soil, water, and air pollutants, factors that plants must cope with. Moderate estimates propose that more than 90% of the land in rural areas is affected by abiotic stress factors at some point during the growing season . On the other hand, the population explosion has resulted in a higher demand for food and other natural resources.
Thus, understanding stress responses is essential when attempting to develop stress-resistant cultivars that can withstand abiotic stressors and in order to feed the growing population. Plants, which undergo various abiotic stresses, sense the enormous stress signal in order to respond to the stress condition. The primary signal caused by drought is hyperosmotic stress, which is often referred to simply as osmotic stress, and salt stress has both osmotic and ion toxicity effects in cells. The secondary effects of drought and salt stresses are complex and include oxidative stress; damage to cellular components such as membrane lipids, proteins, and nucleic acids; and metabolic dysfunction. Thus, drought and salt have unique and overlapping signals. Salt and drought stress disrupts homeostasis in water potential (osmotic homeostasis) and ion distribution (ionic homeostasis). This disruption of homeostasis occurs at both the cellular and the whole plant levels. Drastic changes in ion and water homeostasis lead to molecular damage, growth arrest, and even death. While some cellular responses are induced from primary stress signals, others arise mainly from secondary signals. An important feature of drought and salt stress is that the hyperosmotic signal causes the accumulation of the phytohormone abscisic acid (ABA), which in turn elicits many adaptive responses in plants . Cold or chilling stress affects plant growth and development, by changing the cell structure. First, symptom of cold stress is changing the cell membrane structure in plants; this event initiates primary cold stress responses in plants . Second, chilling stress disturbs the stability of proteins or protein complexes and reduces the activities of enzymes such as ROS scavenging enzymes. These processes result in photo-inhibition and impaired photosynthesis, as well as considerable membrane damage [6, 7]. Third, chilling stress affects gene expression and protein synthesis, as it favors the formation of secondary structures in RNA .
To achieve stress tolerance, three interconnected aspects of plant activities are important. First, damage must be prevented or alleviated. Second, homeostatic conditions must be reestablished in the new, stressful environment. Third, growth must resume, even though at a reduced rate . Significant progress has been made in understanding the physiological, cellular, and molecular mechanisms of plant responses to environmental stress factors . The detection of a stressful condition results in variations in gene expression, causing changes in the composition of plant transcriptome, proteome, and metabolome. Responses to stress are not linear pathways, but are complicated integrated circuits involving multiple pathways and specific cellular compartments, tissues, and the interaction of additional cofactors and/or signaling molecules to coordinate a specified response to a given stimulus . With advancement of omic technologies, i.e., genomics, transcriptomics, proteomics, and metabolomics, now it is possible to analyze and identify the most complicated interlink between various stress response, signal transduction, gene expression, and metabolites production in plants with respective to the abiotic stress [12, 13].
2. Crop plants and abiotic stresses
Generally, many stress factors act at same time, such as the frequently combined, heat, water, and high-light stress . Abiotic stress changes the expression pattern of the various genes in crop plants. So, this modification affects the regular function of plant metabolism, and source-sink relationship in turn reduces the growth, production, and productivity.
Distribution of rainfall is uneven due to the change in climate, which acts as an important stress as drought. Drought is the main abiotic stressor around the world and drastically reduces grain yields. It devastatingly influences the capability to meet the food demands of an ever-increasing global population. Drought stress is associated with water deficit and cellular dehydration. Plant adaptation to drought is a trait involving morphological, physiological, and biochemical changes. Plants reduce their growth of shoots under drought conditions and reduce their metabolic demands. Reduction in yield by as much as 40% was observed for maize and 21% for wheat at approximately a 40% water reduction . In the case of cowpea, yield reduction can vary between 34 and 68% depending on the developmental timing of the drought stress .
2.2 Heat or higher temperature
Plants are more sensitive to the temperature conditions; in extreme cases, the unfavorable temperature condition leads to plant death. Normally plant growth and function would be better at optimum temperature level; both conditions below and higher temperature than optimum temperature severely affect the plant growth and production. The rate of most biochemical, enzymatic reactions rises two-fold for every 10°C increase between 20 and 30°C. Temperatures outside this range reduce the reaction rate because enzymes become either inactivated gradually or denatured.
Change of a few degrees considerably affects the plants’ growth and development, especially reproduction. Abiotic stresses, specifically high and low temperatures, have a harmful effect on the early stage of male gametophyte in several agricultural crops such as rice, wheat, maize, barley, sorghum, and chickpea . Male sterility and abnormalities in the spikelets’ production were induced by heat stress in rice and wheat . In both wheat and rice, heat and cold stresses caused tapetum degradation, microspore callose wall and exine formation, and changes in carbohydrate metabolism, eventually resulting in male sterility . By contrast, temperature stress has no negative effect on female gametophyte development .
Soil salinization is a major threat to agriculture in arid and semi-arid regions, where water scarcity and inadequate drainage of irrigated lands severely reduce crop yield. More than 6% of the world’s total land area and out of 230 M ha of irrigated land 45 M ha (19.5%) is already affected by salt . Salt accumulation inhibits plant growth and reduces the ability to uptake water and nutrients, leading to osmotic or water-deficit stress. Salt stress tolerance level varies from one species to another. For cereal crops, barley (
Cold stress has proved to be the main abiotic stress that decreases productivity of agricultural crops by affecting the quality of crops and their postharvest life. Cold stress, including chilling (0–15°C) and freezing (<0°C), is an abiotic stress that adversely affects the growth and agricultural productivity of plants [24, 25]. Freezing stress is highly detrimental to plants when compared with chilling stress. Usually, freezing damage will start with formation of ice nucleation in between the cell, then slowly grow and form ice crystals, and induce water leakage, leading to cell dehydration [26, 27]. However, many important crops are still incompetent to the process of cold acclimation. Rice (
3. Stress and crops
Stress refers to any substance or stimulus that restricts plant metabolism, growth, development, and crop productivity, including biotic and abiotic stresses . Once this threshold is surpassed, an organism is stressed and mechanisms are activated at molecular, biochemical, physiological, and morphological levels. The activation of the mechanisms can result in the establishment of a new physiological state and homeostasis is reestablished . Stress-related alterations in plant development, growth, and productivity reduce yield and cause unacceptable economic losses in agriculture. It has been assessed that abiotic stresses may reduce up to 70% of crop production of many economically important crops and perform at only 30% of their genetic potential with respect to yield .
4. Abiotic stress sensing and responding mechanism in plants
Sensors are biological molecules that recognize the adverse environmental modification and evoke the immediate response to the particular environment change by initiating the signal molecules in the system. Drought, salt, and cold stresses are inducing more amount of Ca2+ entry into the cell cytoplasm from internal stores or apoplastic source. Passages controlling Ca2+ entry are considered as one type of sensor for the stress signals [32, 33, 34]. Other than Ca2+, ROS and nitric oxide (NO) are other messenger molecules involved in inducing plant response to cold stress. Reactive oxygen species (ROS) like superoxide (O2˙−), hydroxyl radicals (OH−), and hydrogen peroxide (H2O2) are produced in plants in order to face various stresses . Receptor-like kinases (RLKs) have an extracellular domain in which ligand is binding or protein-protein interaction will occur, a transmembrane domain, and an intracellular kinase domain. When the ligand or signal binds extracellular domain, histidine residue present in the intracellular kinase domain is auto-phosphorylated and the phosphoryl moiety is received by aspartate receiver part of the sensor protein or a separate protein. Then, the activated sensor protein(s) may induce cellular responses specific to signal through the mitogen-activated protein kinase (MAPK) cascade or directly phosphorylate specific targets. Intracellular signaling mode, i.e., protein phosphorylation and dephosphorylation regulate a wide range of cellular processes such as enzyme activation, assembly of macromolecules, protein localization, and degradation . Upon sensing of abiotic stress by plants, signaling cascades are induced that activate ion channels, kinase cascades, assembly of reactive oxygen species (ROS), and accumulation of plant hormones leads to induce expression of specific subsets of genes that responsible to combat the abiotic stress (Figure 1) .
5. Similar and variable features of drought, salt, and cold stress
All the three stresses such as drought, salt, and cold stresses cause a primary loss of cell water, which leads to decrease in cell osmotic potential but the reason of cell water loss varies among stresses: (i) the decrease of the cell water content under drought stress is due to water shortage in soil or/and in the atmosphere. (ii) In salt stress, osmotic or water potential of surrounding root zone is decreased by Na+ and Cl− solutes, which in turn create more difficulty in uptake by roots and water translocation to metabolically active cells; (iii) osmotic stress is created in cold stress mainly because of inability to transport the water available from the soil to the living cell of leaf mesophyll. This condition is called as physiological drought. Anyhow, water loss in cell increases abscisic acid (ABA) biosynthesis, and it is well-known fact that it is involved in activation of various drought, salt, and cold stresses, responsive genes in plant system . In plant system losing of cell water and increasing of solute concentration (especially Na+) by these three stress cause lower osmatic potential and it creates harmful effects to the protein and enzymes. This effect can be avoided by producing more amounts of low molecular osmolytes (carbohydrates , betaine , and proline ) that can counteract cellular dehydration and turgor loss . Production of low molecular osmolytes in higher quantity is a common stress alleviating process for drought, cold, and salt stress. While main cause of drought stress is osmotic, Na+, ion toxicity, for salt stress, and physiological drought for cold stress, all stresses have an influence on most biochemical reactions such as photosynthesis, carbon metabolism reactions, and enzyme activities.
6. Gene expression and regulation under abiotic stress
Expression of a variety of genes in plants is induced by environmental stresses such as drought, high salinity, and low temperature. Upon expression, various proteins are produced in various parts of the plants, which not only protect the cell but also initiate humpty number of genes which are responsible for inducing various abiotic resistance mechanisms in plants. Different types of proteins, i.e., chaperones or late embryogenesis abundant (LEA) proteins are produced mainly involved to create tolerance, whereas stress-responsive genes are all involved in to generate stress response . The regulation of stress-responsive plant genes at three levels: transcriptional, posttranscriptional, and posttranslational.
6.1 Gene regulation at transcriptional level
Transcriptional regulation involves (i) chromatin and its alteration and remodeling; (ii) cis-regulatory elements such as enhancers and promoters, which are often binding sites, located upstream and downstream the coding region; and trans-regulatory elements, usually transcription factors. Different environmental stresses create altered methylation pattern of DNA and changing histones protein in order to suppress or increase the transcription of the gene.
Promoters are specific sequences involved in regulatory function, where they bind RNA polymerase and different transcription factors to start the transcription . Dehydration-responsive element-binding (DREB) or C-repeat binding factor (CBF), MYB, basic-leucine zipper (bZIP), and zinc-finger families are some of the trans-regulatory elements involved in the regulation of plant defense and stress-responsive genes upon binding in cis element of the respective gene promoters . Overexpression of the
6.2 Gene regulation at posttranscriptional level
Regulation that occurs in the stage of pre-mRNA till translation of mRNA is called posttranscriptional gene regulation. It occurs in four stages: (i) pre-messenger (mRNA) processing (capping, splicing, and polyadenylation), (ii) mRNA nucleocytoplasmic trafficking, (iii) mRNA turnover and stability, and (iv) mRNA translation . One more strategy, i.e., alternative splicing (AS) is regulating the gene under cold and heat stress. STABILIZED1 (STA1), a gene coding for a nuclear pre-mRNA, is one of the best examples for alternate splicing factor which is involved in cold stress resistance in
6.3 Posttranslational level regulation
Phosphorylation, sumoylation, and ubiquitination of proteins are posttranslational-level processes that play vital roles in the changing of plant response to various abiotic stresses. Mitogen-activated protein kinases (MAPKs) and SNF-1-relatedprotein kinases (SnRKs) are formed numerous signal transduction cascades, induced by dehydration and osmotic stress through the phosphorylation of specificresidues . XERICO controls the level of ABA by enhancing the transcription of the key ABA biosynthetic gene AtNCED3. SnRK2 proteins and XERICO gene, encoding a H2-type zinc-finger E3 ubiquitin ligase, are involved in ABA-dependent responses to water deficit, like stomata closure [67, 68, 69].
Posttranslational histone modifications, along with DNA methylation, are associated with gene expression levels in response to cold stress. Histone acetylation/deacetylation catalyzed by histone acetyltransferases (HATs) and histone deacetylases (HDAs) plays a role in cold responses in plants .
7. Important signal transduction pathway for drought cold and salt
Abiotic stresses such as cold, drought, and salt inducing signal transduction networks are divided into three types: (I) osmotic/oxidative stress signaling that uses MAPK modules to generate ROS scavenging enzymes, antioxidant compounds, and osmolytes; (II) Ca2+-dependent signaling helps to activate late embryogenesis abundant (LEA)-type genes (such as the DRE/CRT class of genes), and (III) Ca2+-dependent salt overlay sensitive (SOS) signaling that regulates ion homeostasis (Figure 2) [14, 76].
7.1 Oxidative or osmatic stress signaling
Formation of reactive oxygen species (ROS) such as superoxide, hydrogen peroxide, and hydroxyl radicals is common for all the stresses, particularly drought, heat, salt, cold, and oxidative stress. Reactive oxygen species which are produced by the environmental stresses cause major plant damage (oxidative stress) . High amount of ROS acts as a signal, and synthesizing ROS scavengers is one of the protective mechanisms in plants. Osmotic stress stimulates many protein kinases; among them, one is mitogen-activated kinases, which are involved in reestablishing the osmotic homeostasis. Plant cells which undergo osmatic stress should produce more osmolytes in order to mitigate the negative effect of the ROS and maintain the osmotic homeostasis. So, the osmotic stress activate the receptors/sensors proteins such as protein tyrosine kinases, G-protein-coupled receptors, and two-component histidine kinases; this will trigger MAPK pathway and signal cascade, which is responsible for production of more amount of osmolytes that are necessary for osmotic adjustment. The main purpose of osmolytes is to maintain cell turgor, thus the driving gradient for water uptake. Compatible solutes such as amino acids (e.g., proline), quaternary amines (e.g., glycine betaine and dimethyl sulfoniopropionate), and polyol/sugars (e.g., mannitol and trehalose) will act as free radical scavengers or chemical chaperones by directly stabilizing membranes and proteins .
The MAP kinase pathways are intracellular signal modules that mediate signal transduction from the cell surface to the nucleus. The core MAPK cascades consist of three kinases that are activated sequentially by an upstream kinase. The MAP kinase kinase kinase (MAPKKK), upon activation, phosphorylates a MAP kinase kinase (MAPKK) on serine and threonine residues. This dual-specificity MAPKK in turn phosphorylates a MAP kinase (MAPK) on conserved tyrosine and threonine residues. The stimulated MAPK either travels to the nucleus to stimulate the transcription factor directly, or activates additional signal components to regulate gene expression, cytoskeleton-associated proteins or enzyme activities, or targets certain signal proteins for degradation .
7.2 Ca2+-dependent signaling to activate late embryogenesis abundant (LEA) genes
Abiotic stress induces more Ca2+ entry into the cell cytoplasm; channels which control the Ca2+ entry act as a sensor for these abiotic stress signals. Ca2+ activates the calcium-dependent protein kinases (CDPKs), and CDPKs are serine/threonine protein kinases with a C-terminal calmodulin-like domain with four EF-hand motifs that can directly bind Ca2+. CDPKs are encoded by multigene families, and the expression levels of these genes are spatially and temporally controlled throughout development. CDPK pathway is involved in production of high amount of anti-desiccation protection protein (LEA proteins) by activation of LEA-type genes including the dehydration-responsive element (DRE)/C-repeat (CRT) class of stress-responsive genes. Activation of LEA-type genes actually represents damage repair pathways but this is completely different from the pathways regulating osmolyte production [79, 80]. At the time of seed maturation, naturally it undergoes desiccation; to avoid desiccation shock during seed germination, seeds accumulate more transcripts and relatively high concentration proteins; for this reason, these proteins were named as late embryogenesis abundant (LEA) proteins . Water deficit, high osmolarity, and low temperature stress induce the accumulation of an LEA protein in crop plants. Such proteins are used to prevent protein denaturation or renaturing unfolded proteins, realm protein structure and membrane integrity, and sequestering ions in stressed tissues. Many scientific reports suggest that LEA proteins and chaperones are involved in protecting macromolecules such as enzymes, lipids, and mRNAs from dehydration, and these proteins have been grouped into at least six families on the basis of sequence similarity [12, 82, 83]. LEA proteins are specialized in desiccation protection of membranes; and antioxidant enzymes and molecules are involved to achieve desiccation tolerance. Both osmolytes and LEA proteins work together in stabilization of membrane and protein structures by conferring preferential hydration at moderate desiccation and replacing water at extreme desiccation .
7.3 Ca2+-dependent salt overlay sensitive (SOS) signaling
Calcium-dependent SOS signaling regulates ion homeostasis relatively specific to the salt stress. Ion transporters are main target for this type of signaling that controls ion homeostasis under salt stress. Excess extracellular or intracellular Na+ acts as an input for the SOS pathway and mainly increases a cytoplasmic Ca2+ signal, and this signal changes expression and activity of transporters for ions such as Na+, K+, and H+. The input for osmotic stress signaling is like a change in turgor. Salt stress signal transduction comprises of ionic and osmotic homeostasis signaling pathways, detoxification (e.g., damage control and repair) response pathways, and pathways for growth regulation . This signaling pathway mediates salt induction of the SOS1 gene in
Second messengers can control intracellular Ca2+ levels, often initiating a protein phosphorylation cascade that finally targets proteins directly involved in cellular protection or transcription factors controlling specific sets of stress-regulated genes. The products of stress-regulated genes like the plant hormones ABA, ethylene, and salicylic acid (SA) are mainly involved in the induction of stress-tolerant mechanism in plants. Salt and water-deficit stress participates in the production and activation of regulatory molecules, and to some extent, cold stress causes an increased biosynthesis and accumulation of ABA by activating genes coding for ABA biosynthetic enzymes, which can be quickly catabolized after the stress. Most of the abiotic stress-responsive genes are upregulated by ABA .
8. Managing abiotic stress by genetic engineering or genetic manipulation or genome editing
All over the world, abiotic stress significantly affects the production and yield potential of the crops and creates a major challenge for crop improvement sectors such as plant breeders and biotechnologists. Genetic manipulation of crops can be done to generate desirable character by so many ways. Among them, transgenic technology or genetic engineering and genome editing are the best strategies to develop abiotic resistant crops. Abiotic stress resistance in crops is possible by transgenic approach through boosting endogenous defense mechanisms by overexpressing of genes, which normally involves the synthesis of compatible osmolytes, antioxidants, polyamines, maintenance of hormone homeostasis, and modification of transporters and/or regulatory proteins, including transcription factors and alternative splicing events. Sometimes overexpression of some genes and thereby synthesizing of specific protein and metabolites will affect the normal metabolism and reducing the yield. Transgenic crop with abiotic tolerance but diminished yield potential and reduced growth is undesirable. So, it is important to analyze the functions of stress-inducible genes not only to understand the molecular mechanisms of stress tolerance and responses of higher plants but also to improve the stress tolerance without reducing the yield potential of crops by gene manipulation. Hundreds of genes are thought to be involved in abiotic stress responses .
8.1 Transgenic crop technology for abiotic tolerance
Transgenic crop or genetic engineering technology has ample opportunity in development of crops with specific objectives by overexpression of responsible genes or suppression of undesirable genes. Present engineering approaches rely on the transfer of one or several genes that are either involved in signaling and regulatory pathways or that encode enzymes present in pathways leading to the synthesis of functional and structural protectants, such as osmolytes and antioxidants, or that encode stress-tolerance-conferring proteins . Phytohormones such as ABA are major targets for genetic manipulation to obtain abiotic stress-tolerant crops. Overexpression of ABA biosynthetic pathway-related TFs imparts an ABA-hypersensitive response and also improves the osmotic stress tolerance in transgenic plants [90, 91]. Under moderate drought stress, during the flowering period, the yields of transgenic canola overexpressing a farnesyltransferase protein were significantly higher comparatively to the control . The overexpression of TFs that control root architecture induced drought tolerance in rice and transgenic
Water stress increases the formation of ROS through membrane perturbation of electron transport chains. The loss of catalase and gain of the glutathioneS-transferase/peroxidase functions in plants associate defenses against oxidative damage,which are more important in plant salt tolerance . Loss of osmotic homeostasis is the important process in the abiotic stress, which affects the cell ion concentration; so, to achieve abiotic tolerance especially salt, plants should re-establish homeostasis (ionic and osmotic homeostasis) under stressful conditions. More amount of Na+ within the cell inhibits enzyme activity and is harmful to the proteins; so, either compartmentalization of Na+ in the vacuole or controlling of Na+ accumulation in the cytoplasm is more important . To revert ionic and osmotic homeostasis, many ion transporters act as terminal determinants. Protein AtNHX1 of
8.2 Genome editing technology
Despite the benefits of commercial genetically engineered plants  and successfully addressing abiotic stresses, still this technology is not accepted unanimously because of the negative perception of the public; so, it limits the usage of this technique to develop the abiotic resistant crop varieties. The major concern in transgenic technology might be in many cases; the source of the gene to generate transgenic crop is taken from non-related organism, i.e., microorganism and non-related plant and animal; so, this issue can be addressed in a better manner by genome editing technology. In this technique, genetic modifications are accomplished by creating minor genome changes that are comparable with changes generated through mutation breeding (conventional crop improvement method) by using chemical and physical mutagenic agents. Mutational breeding produce changes in the genome at random manner; so, the success rate or chance of obtaining desirable genotype is quite low. But in genome editing, modification is done at targeted site, by application of sequence-specific nucleases that create double-stranded breaks in the target genomic loci selected for editing; so, the success rate of obtaining desirable genotype is very high. The major genome editing tools are zinc finger (ZF) nucleases, transcription activator-like effector nucleases (TALENs), and clustered regularly interspaced short palindromic repeats (CRISPR) . Many strategies or options are there to improve agronomic traits by using genome editing tools. Introduction of a premature stop codon to terminate the functional protein production or modify to a gene promoter motif to control gene expression is one of the best examples of genome editing. Genome editing techniques such as TALEN and CRISPR-Cas9 are used to introduce targeted mutations in MILDEW-RESISTANCE LOCUS (MLO) proteins in hexaploid bread wheat . On the other hand, Piatek et al. used synthetic transcriptional repressor and activator to increase gene expression . C-repeat binding factors (CBFs) are responsible for cold acclimation in plants. Since
Plants are developed with inherent adaptive mechanisms to cope up with varied and composite abiotic stresses. Now it is possible with the help of science and technological advancement to understand function of gene, gene manipulation strategy, and plant traits development to overcome the abiotic stress. Signaling pathways have to be regarded as complex networks. Molecular analyses of the signaling factors provide a better understanding of the signal-transduction cascades during abiotic stress. A notable improvement in crop genome characterization and functional annotation of the gene will advance our knowledge in genetic manipulation (transgenic technology) and optimization of genome editing technology toward development of abiotic stress-tolerant crops. In due course, to accomplish the desired improved varieties, genome editing and transgenic approaches both should be combined with conventional and marker-assisted breeding activities. Further, identification of new adapted germplasm is also most important to guide breeding programs in target trait identification for changing scenario of climate. These combined efforts will make notable progress to face effect of climate change, especially stress such as drought, heat, and cold stress and will contribute to enhanced crop production, productivity, and thereby food security.
Fedoroff NV, Battisti DS, Beachy RN, Cooper PJ, Fischhoff DA, Hodges CN, et al. Radically rethinking agriculture for the 21st century. Science. 2010; 327:833-834
Kundzewicz Z, Ulbrich U, Brucher T, Graczyk D, Kruger A, Leckebusch GC. Summer floods in Central Europe - Climate change track? Natural Hazards. 2005; 36:165-189
Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K. Effects of abiotic stress on plants: A systems biology perspective. BMC Plant Biology. 2011; 11:163-176
Zhu L, Chen S, Alvarez S, Asirvatham VS, Schachtman DP, Wu Y. Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water soluble and lightly ionically bound proteins. Plant Physiology. 2006; 140:311-325
Orvar BL, Sangwan V, Omann F, Dhindsa RS. Early steps in cold sensing by plant cells: The role of actin cytoskeleton and membrane fluidity. The Plant Journal. 2000; 23:785-794
Siddiqui KS, Cavicchioli R. Cold-adapted enzymes. Annual Review of Biochemistry. 2006; 75:403-433
Ruelland E, Vaultier MN, Zachowski A, Hurry V. Cold signalling and cold acclimation in plants. Advances in Botanical Research. 2009; 49:35-150
Rajkowitsch L, Chen D, Stampfl S, Semrad K, Waldsich C, Mayer O, et al. RNA chaperones, RNA annealers and RNA helicases. RNA Biology. 2007; 4:118-130
Fahad S, Muhammad ZI, Abdul K, Ihsanullah D, Saud S, Saleh A, et al. Consequences of high temperature under changing climate optima for rice pollen characteristics - Concepts and perspectives. Archives of Agronomy and Soil Science. 2018; 64(11):1473-1488. DOI: 10.1080/03650340.2018.1443213
Hadiarto T, Tran LS. Progress studies of drought-responsive genes in rice. Plant Cell Reports. 2011; 30:297-310
Dombrowski JE. Salt stress activation of wound-related genes in tomato plants. Plant Physiology. 2003; 132:2098-2107
Yamaguchi-Shinozaki K, Kasuga M, Liu Q , Nakashima K, Sakuma Y, Abe H. Biological mechanisms of drought stress response. JIRCAS Working Report. 2002:1-8
Shinozaki K, Yamaguchi SK, Seki M. Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology. 2003; 6:410-417
Xiong L, Schumaker KS, Zhu JK. Cell signaling during cold, drought, and salt stress. The Plant Cell. 2002:165-183
Daryanto S, Wang L, Jacinthe PA. Global synthesis of drought effects on maize and wheat production. PLoS One. 2016; 11:e0156362. DOI: 10.1371/journal.pone.0156362
Farooq M, Gogoi N, Barthakur S, Baroowa B, Bharadwaj N, Alghamdi SS. Drought stress in grain legumes during reproduction and grain filling. Journal of Agronomy and Crop Science. 2017; 203:81-102. DOI: 10.1111/jac.12169
Boyer JS, Westgate ME. Grain yields with limited water. Journal of Experimental Botany. 2004; 55:2385-2394
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, et al. Crop production under drought and heat stress: Plant responses and management options. Frontiers in Plant Science. 2017; 8:1147. DOI: 10.3389/fpls.2017.01147
Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG. Effects of chilling on male gametophyte development in rice. Cell Biology International. 2006; 30:583-591
Fahad S, Chen Y, Saud S, Wang K, Xiong D, Chen C, et al. Ultraviolet radiation effect on photosynthetic pigments, biochemical attributes, antioxidant enzyme activity and hormonal contents of wheat. Journal of Food, Agriculture and Environment. 2013; 11(3&4):1635-1641
FAO. The State of Food and Agriculture - Climate Change, Agriculture and Food Security. Rome, Italy: Food and Agricultural Organization of the United Nations; 2016
Maas EV, Hoffman GJ. Crop salt tolerance - Current assessment. Journal of the Irrigation and Drainage Division. 1977; 103:115-134
Munns R, Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology. 2008; 59:651-681
Guo XY, Liu DF, Chong K. Cold signaling in plants: Insights into mechanisms and regulation. Journal of Integrative Plant Biology. 2018; 60:745-756
Liu H, Yu C, Li H, Ouyang B, Wang T, Zhang J, et al. Overexpression of ShDHN, a dehydrin gene from Solanum habrochaitesenhances tolerance to multiple abiotic stresses in tomato. Plant Science. 2015; 231:198-211
Pearce RS. Plant freezing and damage. Annals of Botany. 2001; 87:417-424
Dowgert MF, Steponkus PL. Behavior of the plasma membrane of isolated protoplasts during a freeze-thaw cycle. Plant Physiology. 1984; 75:1139-1151
Chinnusamy V, Zhu J, Zhu JK. Cold stress regulation of gene expression in plants. Trends in Plant Science. 2007; 12(10):444-451
Lichtenthaler HK. The stress concept in plants: An introduction. Annals of the New York Academy of Sciences. 1998; 851:187-198
Jogaiah S, Govind SR, Tran LSP. Systems biology-based approaches toward understanding drought tolerance in food crops. Critical Reviews in Biotechnology. 2013; 33:23-29
Boyer JS. Plant productivity and environment. Science. 1982; 218:443-448
Knight H, Trewavas AJ, Knight MR. Cold calcium signaling in Arabidopsisinvolves two cellular pools and a change in calcium signature after acclimation. Plant Cell. 1996; 8:489-503
Plieth C, Hansen UP, Knight H, Knight MR. Temperature sensing by plants: The primary characteristics of signal perception and calcium response. The Plant Journal. 1999; 18:491-497
Knight MR, Knight H. Low-temperature perception leading to gene expression and cold tolerance in higher plants. The New Phytologist. 2012; 195:737-751
Tyystjarvi E. Photoinhibition of photosystem II. International Review of Cell and Molecular Biology. 2013; 300:243-303
Xiong L, Zhu JK. Abiotic stress signal transduction in plants: Molecular and genetic perspectives. Physiologia Plantarum. 2001; 112:152-166
Sha Valli Khan PS, Nagamallaiah GV, Dhanunjay Rao M, Sergeant K, Hausman JF. Abiotic stress tolerance in plants insights from proteomics. In: Ahmad P, editor. Emerging Technologies and Management of Crop Stress Tolerance. Elsevier Academic press; Vol. 2. 2014. pp. 23-68
Boudsocq M, Laurière C. Osmotic signaling in plants: Multiple pathways mediated by emerging kinase families. Plant Physiology. 2005; 138(3):1185-1194
Marques da Silva J, Arrabaça MC. Contributions of soluble carbohydrates to the osmotic adjustment in the C4 grass Setaria sphacelata: A comparison between rapidly and slowly imposed water stress. Journal of Plant Physiology. 2004; 161(5):551-555
Aziz K, Daniel KYT, Muhammad ZA, Honghai L, Shahbaz AT, Mir A, et al. Nitrogen fertility and abiotic stresses management in cotton crop: A review. Environmental Science and Pollution Research. 2017b; 24:14551-14566. DOI: 10.1007/s11356-017-8920-x
Hesham FA, Fahad S. Melatonin application enhances biochar efficiency for drought tolerance in maize varieties: Modifications in physio-biochemical machinery. Agronomy Journal. 2020:1-22
Beck EH, Fettig S, Knake C, Hartig K, Bhattarai T. Specific and unspecific responses of plants to cold and drought stress. Journal of Biosciences. 2007; 32(3):501-510
Kazuko YS, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology. 2006; 57:781-803
Juven-Gershon T, Hsu JY, Theisen JW, Kadonaga JT. The RNA polymerase II core promoter—The gateway to transcription. Current Opinion on Cell Biology. 2008; 20(3):253-259
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q , et al. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(35):12987-12992
Chen L, Song Y, Li S, Zhang L, Zou C, Yu D. The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta. 2012; 1819(2):120-128
Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Reports. 2009; 28(1):21-30
Yamaguchi-Shinozaki K, Shinozaki K. A novel cis-acting element in an Arabidopsisgene is involved in responsiveness to drought, low-temperature, or high-salt stress. The Plant Cell. 1994; 6:251-264
Stockinger EJ, Gilmour SJ, Thomashow MF. Arabidopsis thaliana CBF1encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94:1035-1040
Liu Q , Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, et al. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell. 1998; 10:1391-1406
Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF. Low temperature regulation of the ArabidopsisCBF family of AP2 transcriptional activators as an early step in cold-induced CORgene expression. The Plant Journal. 1998; 16:433-442
Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J. The Arabidopsis CBFgene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiology. 1999; 119:463-470
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. Arabidopsis CBF1overexpression induces CORgenes and enhances freezing tolerance. Science. 1998; 280:104-106
Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends in Plant Science. 2018; 23:623-637
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. Overexpression of the Arabidopsis CBF3transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology. 2000; 124:1854-1865
Zhang X, Fowler SG, Cheng HM, Lou YG, Rhee SY, Stockinger EJ, et al. Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. The Plant Journal. 2004; 39:905-919
Savitch LV, Allard G, Seki M, Robert LS, Tinker NA, Huner NPA, et al. The effect of overexpression of two BrassicaCBF/DREB1-like transcription factors on photosynthetic capacity and freezing tolerance in Brassica napus. Plant & Cell Physiology. 2005; 46:1525-1539
Floris M, Mahgoub H, Lanet E, Robaglia C, Menand B. Post-transcriptional regulation of gene expression in plants during abiotic stress. International Journal of Molecular Sciences. 2009; 10(7):3168-3185
Lee BH, Kapoor A, Zhu J, Zhu JK. STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. The Plant Cell. 2006; 18(7):1736-1749
Guan Q , Wu J, Zhang Y, Jiang C, Liu R, Chai C, et al. A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. The Plant Cell. 2013; 25:342-356
James AB, Syed NH, Bordage S, Marshall J, Nimmo GA, Jenkins GI, et al. Alternative splicing mediates responses of the Arabidopsiscircadian clock to temperature changes. The Plant Cell. 2012; 24:961-981
Calixto CPG, Guo WB, James AB, Tzioutziou NA, Entizne JC, Panter PE, et al. Rapid and dynamic alternative splicing impacts the Arabidopsiscold response transcriptome. The Plant Cell. 2018; 30:1424-1444
Sunkar R, Zhu JK. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell. 2004; 16(8):2001-2019
Bari R, Datt PB, Stitt M, Scheible WR. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology. 2006; 141(3):988-999
Sunkar R, Kapoor A, Zhu JK. Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsisis mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell. 2006; 18(8):2051-2065
Zhu JK. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology. 2002; 53:247-273
Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. The Journal of Biological Chemistry. 2006; 281(8):5310-5318
Ko JH, Yang SH, Han KH. Upregulation of an ArabidopsisRING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. The Plant Journal. 2006; 47(3):343-355
Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L. Abiotic stress response in plants: When post-transcriptional and post-translational regulations control transcription. Plant Science. 2008; 174(4):420-431
Kim JM, Sasaki T, Ueda M, Sako K, Seki M. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Frontiers in Plant Science. 2015; 6:114
To TK, Nakaminami K, Kim JM, Morosawa T, Ishida J, Tanaka M, et al. ArabidopsisHDA6 is required for freezing tolerance. Biochemical and Biophysical Research Communications. 2011; 406:414-419
Hu Y, Zhang L, Zhao L, Li J, He SB, Zhou K, et al. Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1gene in maize. PLoS One. 2011; 6:e22132
Roy D, Paul A, Roy A, Ghosh R, Ganguly P, Chaudhuri S. Differential acetylation of histone H3 at the regulatory region of OsDREB1b promoter facilitates chromatin remodelling and transcription activation during cold stress. PLoS One. 2014; 9:e100343
He XJ, Hsu YF, Zhu SH, Liu HL, Pontes O, Zhu JH, et al. A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development. Genes & Development. 2009; 23:2717-2722
Chan ZL, Wang YP, Cao MJ, Gong YH, Mu ZX, Wang HQ , et al. RDM4 modulates cold stress resistance in Arabidopsispartially through the CBF-mediated pathway. The New Phytologist. 2016; 209:1527-1539
Rodríguez M, Canales E, Borras-Hidalgo O. Molecular aspects of abiotic stress in plants. Biotecnologia Aplicada. 2005; 22:1-10
Sunkar R, Bartels D, Kirch HH. Overexpression of a stress-inducible dehydrogenase gene from Arabidopsis thalianain transgenic plants improves stress tolerance. The Plant Journal. 2003:35
Wang W, Vinocur B, Altman A. Plant responses to drought, salinity and extreme temperatures: Towards genetic engineering for stress tolerance. Planta. 2003; 218:1-14
Serrano R, Gaxiola R, Rios G, Forment J, Vicente O, Ros R. Salt stress proteins identified by a functional approach in yeast. Monatshefte für Chemie. 2003; 134:1445-1464
Fahad S, Nie L, Chen Y, Wu C, Xiong D, Saud S, et al. Crop plant hormones and environmental stress. Sustainable Agriculture Reviews. 2015b; 15:371-400
Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. The Journal of Biological Chemistry. 2000; 275(8):5668-5674
Fahad S, Bano A. Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pakistan Journal of Botany. 2012; 44:1433-1438
Eimer M. Transgenic drought- and salt-tolerant plants. Genetic Engineering Newsletter Special Issue. 2004; 15:1-14
Serrano R, Montesinos C. Molecular bases of desiccation tolerance in plant cells and potential applications in food dehydration. Food Science and Technology International. 2003; 9(3):157-161
Fahad S, Adnan M, Hassan S, Saud S, Hussain S, Wu C, et al. Rice responses and tolerance to high temperature. In: Hasanuzzaman M, Fujita M, Nahar K, Biswas JK, editors. Advances in Rice Research for Abiotic Stress Tolerance. Cambridge, England: Woodhead Publ Ltd; 2019b. pp. 201-224
Shi H, Ishitani M, Kim C, Zhu JK. The Arabidopsis thalianasalt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97:6896-6901
Guo Y, Halfter U, Ishitani M, Zhu JK. Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. The Plant Cell. 2001; 13:1383-1400
Saud S, Li X, Chen Y, Zhang L, Fahad S, Hussain S, et al. Silicon application increases drought tolerance of Kentucky bluegrassby improving plant water relations and morph physiological functions. Scientific World Journal. 2014:1-10. DOI: 10.1155/2014/368694
Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K. Molecular responses to drought, salinity and frost: Common and different paths for plant protection. Current Opinion in Biotechnology. 2003; 14:194-199
Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, et al. Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: Consequences for changing environment. Environmental Science and Pollution Research. 2014a; 22(7):4907-4921. DOI: 10.1007/s11356-014-3754-2
Gao JJ, Zhang Z, Peng RH, Xiong AS, Xu J, Zhu B. Forced expression of Mdmyb10, a myb transcription factor gene from apple, enhances tolerance to osmotic stress in transgenic Arabidopsis. Molecular Biology Reports. 2011; 38:205-211. DOI: 10.1007/s11033-010-0096-0
Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C. Molecular tailoring of farnesylation for plant drought tolerance and yield protection. The Plant Journal. 2005; 43:413-424. DOI: 10.1111/j.1365-313X.2005. 02463
Redillas MC, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD. The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnology Journal. 2012; 10:792-805. DOI: 10.1111/j.1467-7652.2012.00697
He GH, Xu YJ, Wang XY, Liu MJ, Li SP, Chen M. Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis. BMC Plant Biology. 2016; 16:116. DOI: 10.1186/s12870-016-0806-4
Legay S, Guerriero G, Andre C, Guignard C, Cocco E, Charton S. MdMyb93 is a regulator of suberin deposition in russeted apple fruit skins. The New Phytologist. 2016; 212:977-991. DOI: 10.1111/nph.14170
Fahad S, Hussain S, Matloob A, Khan FA, Khaliq A, Saud S, et al. Phytohormones and plant responses to salinity stress: A review. Plant Growth Regulation. 2014b; 75(2):391-404. DOI: 10.1007/s10725-014-0013-y
Singla-Pareek SL, Yadav SK, Pareek A, Reddy MK, Sopory SK. Enhancing salt tolerance in a crop plant by overexpression of glyoxalase II. Transgenic Research. 2008; 17:171-180. DOI: 10.1007/s11248-007-9082-2
Bhomkar P, Upadhyay CP, Saxena M, Muthusamy A, Prakash NS, Pooggin M. Salt stress alleviation in transgenic Vigna mungoL. Hepper (blackgram) by overexpression of the glyoxalase I gene using a novel cestrum yellow leaf curling virus (CmYLCV) promoter. Molecular Breeding. 2008; 22:169-181. DOI: 10.1007/s11032-008-9164-8
Lin F, Xu J, Shi J, Li H, Li B. Molecular cloning and characterization of a novel glyoxalase I gene TaGly I in wheat ( Triticum aestivumL.). Molecular Biology Reports. 2010; 37:729-735. DOI: 10.1007/s11033-009-9578-3
Tuomainen M, Ahonen V, Kärenlampi SO, Schat H, Paasela T, Svanys A. Characterization of the glyoxalase 1 gene TcGLX1 in the metal hyperaccumulator plant Thlaspi caerulescens. Planta. 2011; 233:1173-1184. DOI: 10.1007/s00425-011-1370-7
Wu C, Ma C, Pan Y, Gong S, Zhao C, Chen S. Sugar beet M14 glyoxalase I gene can enhance plant tolerance to abiotic stresses. Journal of Plant Research. 2013; 126:415-425. DOI: 10.1007/s10265-012-0532-4
Alvarez-Gerding X, Cortes-Bullemore R, Medina C, Romero-Romero JL, Inostroza-Blancheteau C, Aquea F. Improved salinity tolerance in Carrizo citrange rootstock through overexpression of glyoxalase system genes. BioMed Research International. 2015:1-7. DOI: 10.1155/2015/827951
Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M. Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. International Journal of Molecular Sciences. 2017; 18:200. DOI: 10.3390/ijms18010200
Adnan M, Zahir S, Fahad S, Arif M, Mukhtar A, Imtiaz AK, et al. Phosphate-solubilizing bacteria nullify the antagonistic effect of soil calcification on bioavailability of phosphorus in alkaline soils. Scientific Reports. 2018; 8:4339. DOI: 10.1038/s41598-018-22653-7
Datta SK. Recent developments in transgenics for abiotic stress tolerance in rice. JIRCAS Working Report. 2002:43-53
Sakamoto A, Alia HH, Murata N. Metabolic engineering of rice leading to biosynthesis of glycine betaine and tolerance to salt and cold. Plant Molecular Biology. 1998; 38:1011-1019
Fahad S, Hussain S, Saud S, Hassan S, Ihsan Z, Shah AN, et al. Exogenously applied plant growth regulators enhance the morphophysiological growth and yield of rice under high temperature. Frontiers in Plant Science. 2016c; 7:1250. DOI: 10.3389/fpls.2016. 01250
Penna S et al. Building stress tolerance through over-producing trehalose in transgenic plants. Trends in Plant Science. 2003; 8:355-357
Jang IC, Se-Jun O, Ju-Seok S, WonBin C, Song SI. Expression of a bifunctional fusion of the Escherichia coligenes for trehalose-6-phosphate synthase and trehalose-6-phosphate. Phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiology. 2003; 131:516-524
Wang WX, Barak T, Vinocur B, Shoseyov O, Altman A. Abiotic resistance and chaperones: Possible physiological role of SP1, a stable and stabilizing protein from Populus. In: Vasil IK, editor. Plant Biotechnology 2000. Dordrecht: Kluwer; 2003. pp. 439-443
Davison PA, Hunter CN, Horton P. Overexpression of b-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature. 2002; 418:203-206
Oberschall A, Deak M, Torok K, Sass L, Vass I, Kovacs I. A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. The Plant Journal. 2000; 24:437-446
Bartels D. Targeting detoxification pathways: An efficient approach to obtain plants with multiple stress tolerance. Trends in Plant Science. 2001; 6:284-286
Zhang HX, Blumwald E. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotechnology. 2001; 19
National Academies of Sciences, Engineering, and Medicine. Genetically Engineered Crops: Experiences and Prospects. Washington, DC: National Academies Press; 2017. DOI: 10.17226/23395
Voytas DF. Plant genome engineering with sequence specific nucleases. Annual Review of Plant Biology. 2013; 64:327-350. DOI: 10.1146/annurev-arplant-042811-105552
Wang Y, Cheng X, Shan Q , Zhang Y, Liu J, Gao C. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Biotechnology. 2014; 32:947-951. DOI: 10.1038/nbt.2969
Piatek A, Ali Z, Baazim H, Li L, Abulfaraj A, Al-Shareef S. RNA-guided transcriptional regulation in planta via synthetic dCas9-based transcription factors. Plant Biotechnology Journal. 2015; 13:578-589. DOI: 10.1111/pbi.12284
Jia YX, Ding YL, Shi YT, Zhang XY, Gong ZZ, Yang SH. The cbfstriple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. The New Phytologist. 2016; 212:345-353
Zhao CZ, Zhang ZJ, Xie SJ, Si T, Li YY, Zhu JK. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiology. 2016; 171:2744-2759