•A strong genetic variation in salinity tolerance exist amongst quinoa accessions.•Both epidermal bladder cells (EBC) development and stomata patterning play an essential role conferring salinity ...tolerance trait in quinoa.•Bladders density was increased in most accessions under saline condition while the bladder’s diameter remained unchanged.•The correlation analysis indicated a significant positive association between EBC diameter and salinity tolerance index (STI) on one hand and EBC volume and STI on the other hand, in a salt-tolerant group.
The presence of epidermal bladder cells (EBCs) in halophytes allows considerable amount of Na+ being accumulated in these external structures, away from the metabolically active mesophile cells. Also, stomatal patterning may represent a primary mechanism by which plants can optimise its water-use efficiency under saline condition. This investigation was aimed to explore the varietal differences in a salinity tolerance of quinoa (Chenopodium quinoa) by evaluating a broad range of accessions and linking the overall salinity tolerance with changes in stomatal characteristics and EBC parameters. One hundred and fourteen accessions were grown under temperature-controlled glasshouse under non-saline and 400 mM NaCl conditions, and different physiological and anatomical characteristics were measured. Accessions were classified into three classes (sensitive, intermediate and tolerant) based on a relative dry weight defined as salinity tolerance index (STI). Results showed a large variability in STI indicating a strong genetic variation in salinity tolerance in quinoa. Bladders density was increased in a majority of accessions under saline condition while the bladder’s diameter remained unchanged; this resulted in a large variability in a bladder’s volume as a dependant variable. Stomata density remained unchanged between saline and non-saline conditions while the stomata length declined between 3% to 43% amongst accessions. Leaf Na+ concentration varied from 669 μmol/gDW to 3155 μmol/gDW under saline condition and, with an exception of a few accessions, leaf K+ concentration increased under saline conditions. Correlation analysis indicated a significant positive association between EBC diameter and STI on one hand and EBC volume and STI on the other hand, in a salt-tolerant group. These observations are consistent with the role of EBCs in sequestration of toxic Na+ in the external structures, away from the cytosol. A negative association was found between EBC density and diameter in salt-sensitive plants. A negative association between STI and stomata length was also found in a salt-tolerant group, suggesting that these plants were able to efficiently regulate stomatal patterning to balance water loss and CO2 assimilation under saline conditions. Both salt-sensitive and salt-tolerant groups had the same Na+ concentration in the shoot under saline conditions; however, a negative association between leaf Na+ concentration and STI in salt-sensitive plants indicated a more efficient Na+ sequestration process into the EBCs in salt-tolerant plants.
Salinity stress affects global food producing areas by limiting both crop growth and yield. Attempts to develop salinity-tolerant rice varieties have had limited success due to the complexity of the ...salinity tolerance trait, high variation in the stress response and a lack of available donors for candidate genes for cultivated rice. As a result, finding suitable donors of genes and traits for salinity tolerance has become a major bottleneck in breeding for salinity tolerant crops. Twenty-two wild
relatives have been recognized as important genetic resources for quantitatively inherited traits such as resistance and/or tolerance to abiotic and biotic stresses. In this review, we discuss the challenges and opportunities of such an approach by critically analyzing evolutionary, ecological, genetic, and physiological aspects of
species. We argue that the strategy of rice breeding for better Na
exclusion employed for the last few decades has reached a plateau and cannot deliver any further improvement in salinity tolerance in this species. This calls for a paradigm shift in rice breeding and more efforts toward targeting mechanisms of the tissue tolerance and a better utilization of the potential of wild rice where such traits are already present. We summarize the differences in salinity stress adaptation amongst cultivated and wild
relatives and identify several key traits that should be targeted in future breeding programs. This includes: (1) efficient sequestration of Na
in mesophyll cell vacuoles, with a strong emphasis on control of tonoplast leak channels; (2) more efficient control of xylem ion loading; (3) efficient cytosolic K
retention in both root and leaf mesophyll cells; and (4) incorporating Na
sequestration in trichrome. We conclude that while amongst all wild relatives,
is arguably a best source of germplasm at the moment, genes and traits from the wild relatives,
,
, and
, should be targeted in future genetic programs to develop salt tolerant cultivated rice.
Abstract
Although control of xylem ion loading is essential to confer salinity stress tolerance, specific details behind this process remain elusive. In this work, we compared the kinetics of xylem ...Na+ and K+ loading between two halophytes (Atriplex lentiformis and quinoa) and two glycophyte (pea and beans) species, to understand the mechanistic basis of the above process. Halophyte plants had high initial amounts of Na+ in the leaf, even when grown in the absence of the salt stress. This was matched by 7-fold higher xylem sap Na+ concentration compared with glycophyte plants. Upon salinity exposure, the xylem sap Na+ concentration increased rapidly but transiently in halophytes, while in glycophytes this increase was much delayed. Electrophysiological experiments using the microelectrode ion flux measuring technique showed that glycophyte plants tend to re-absorb Na+ back into the stele, thus reducing xylem Na+ load at the early stages of salinity exposure. The halophyte plants, however, were capable to release Na+ even in the presence of high Na+ concentrations in the xylem. The presence of hydrogen peroxide (H2O2) mimicking NaCl stress-induced reactive oxygen species (ROS) accumulation in the root caused a massive Na+ and Ca2+ uptake into the root stele, while triggering a substantial K+ efflux from the cytosol into apoplast in glycophyte but not halophytes species. The peak in H2O2 production was achieved faster in halophytes (30 min vs 4 h) and was attributed to the increased transcript levels of RbohE. Pharmacological data suggested that non-selective cation channels are unlikely to play a major role in ROS-mediated xylem Na+ loading.
While most water loss from leaf surfaces occurs via stomata, part of this loss also occurs through the leaf cuticle, even when the stomata are fully closed. This component, termed residual ...transpiration, dominates during the night and also becomes critical under stress conditions such as drought or salinity. Reducing residual transpiration might therefore be a potentially useful mechanism for improving plant performance when water availability is reduced (e.g. under saline or drought stress conditions). One way of reducing residual transpiration may be via increased accumulation of waxes on the surface of leaf. Residual transpiration and wax constituents may vary with leaf age and position as well as between genotypes. This study used barley genotypes contrasting in salinity stress tolerance to evaluate the contribution of residual transpiration to the overall salt tolerance, and also investigated what role cuticular waxes play in this process. Leaves of three different positions (old, intermediate and young) were used.
Our results show that residual transpiration was higher in old leaves than the young flag leaves, correlated negatively with the osmolality, and was positively associated with the osmotic and leaf water potentials. Salt tolerant varieties transpired more water than the sensitive variety under normal growth conditions. Cuticular waxes on barley leaves were dominated by primary alcohols (84.7-86.9%) and also included aldehydes (8.90-10.1%), n-alkanes (1.31-1.77%), benzoate esters (0.44-0.52%), phytol related compounds (0.22-0.53%), fatty acid methyl esters (0.14-0.33%), β-diketones (0.07-0.23%) and alkylresorcinols (1.65-3.58%). A significant negative correlation was found between residual transpiration and total wax content, and residual transpiration correlated significantly with the amount of primary alcohols.
Both leaf osmolality and the amount of total cuticular wax are involved in controlling cuticular water loss from barley leaves under well irrigated conditions. A significant and negative relationship between the amount of primary alcohols and a residual transpiration implies that some cuticular wax constituents act as a water barrier on plant leaf surface and thus contribute to salinity stress tolerance. It is suggested that residual transpiration could be a fundamental mechanism by which plants optimize water use efficiency under stress conditions.
Hydrogen peroxide is an important regulatory agent in plants. This study demonstrates that exogenous H₂O₂ application to Arabidopsis thaliana root epidermis results in dose-dependent transient ...increases in net Ca²⁺ influx. The magnitude and duration of the transients were greater in the elongation zone than in the mature epidermis. In both regions, treatment with the cation channel blocker Gd³⁺ prevented H₂O₂-induced net Ca²⁺ influx, consistent with application of exogenous H₂O₂ resulting in the activation of plasma membrane Gd³⁺-sensitive Ca²⁺-influx pathways. Application of 10 m smallcapital m H₂O₂ to the external plasma membrane face of elongation zone epidermal protoplasts resulted in the appearance of a hyperpolarization-activated Ca²⁺-permeable conductance. This conductance differed from that previously characterized as being responsive to extracellular hydroxyl radicals. In contrast, in mature epidermal protoplasts a plasma membrane hyperpolarization-activated Ca²⁺-permeable channel was activated only when H₂O₂ was present at the intracellular membrane face. Channel open probability increased with intracellular H₂O₂ and at hyperpolarized voltages. Unitary conductance decreased thus: Ba²⁺ > Ca²⁺ (14.5 pS) > Mg²⁺ > Zn²⁺ (20 m smallcapital m external cation, 1 m smallcapital m H₂O₂). Lanthanides and Zn²⁺ (but not TEA⁺) suppressed the open probability without affecting current amplitude. The results suggest spatial heterogeneity and differential sensitivity of Ca²⁺ channel activation by reactive oxygen species in the root that could underpin signalling.
Epidermal bladder cells (EBCs) have been postulated to assist halophytes in coping with saline environments. However, little direct supporting evidence is available. Here, Chenopodium quinoa plants ...were grown under saline conditions for 5 weeks. One day prior to salinity treatment, EBCs from all leaves and petioles were gently removed by using a soft cosmetic brush and physiological, ionic and metabolic changes in brushed and non‐brushed leaves were compared. Gentle removal of EBC neither initiated wound metabolism nor affected the physiology and biochemistry of control‐grown plants but did have a pronounced effect on salt‐grown plants, resulting in a salt‐sensitive phenotype. Of 91 detected metabolites, more than half were significantly affected by salinity. Removal of EBC dramatically modified these metabolic changes, with the biggest differences reported for gamma‐aminobutyric acid (GABA), proline, sucrose and inositol, affecting ion transport across cellular membranes (as shown in electrophysiological experiments). This work provides the first direct evidence for a role of EBC in salt tolerance in halophytes and attributes this to (1) a key role of EBC as a salt dump for external sequestration of sodium; (2) improved K+ retention in leaf mesophyll and (3) EBC as a storage space for several metabolites known to modulate plant ionic relations.
Epidermal bladder cells (EBCs) have been postulated to assist halophytes in coping with saline environments; however, no direct evidence was provided until now. In this work, we show that the gentle removal of EBC results in a salt‐sensitive phenotype and attribute this phenomenon to a key role of EBC as a salt dump and a storage space for several metabolites known to modulate plant ionic relations.
The Darwin plantDionaea muscipulais able to grow on mineral-poor soil, because it gains essential nutrients from captured animal prey. Given that no nutrients remain in the trap when it opens after ...the consumption of an animal meal, we here asked the question of howDionaeasequesters prey-derived potassium. We show that prey capture triggers expression of a K⁺ uptake system in the Venus flytrap. In search of K⁺ transporters endowed with adequate properties for this role, we screened aDionaeaexpressed sequence tag (EST) database and identified DmKT1 and DmHAK5 as candidates. On insect and touch hormone stimulation, the number of transcripts of these transporters increased in flytraps. After cRNA injection of K⁺-transporter genes intoXenopusoocytes, however, both putative K⁺ transporters remained silent. Assuming that calcium sensor kinases are regulatingArabidopsisK⁺ transporter 1 (AKT1), we coexpressed the putative K⁺ transporters with a large set of kinases and identified the CBL9-CIPK23 pair as the major activating complex for both transporters inDionaeaK⁺ uptake. DmKT1 was found to be a K⁺-selective channel of voltage-dependent high capacity and low affinity, whereas DmHAK5 was identified as the first, to our knowledge, proton-driven, high-affinity potassium transporter with weak selectivity. When the Venus flytrap is processing its prey, the gland cell membrane potential is maintained around −120 mV, and the apoplast is acidified to pH 3. These conditions in the green stomach formed by the closed flytrap allow DmKT1 and DmHAK5 to acquire prey-derived K⁺, reducing its concentration from millimolar levels down to trace levels
Osmotic stress that is induced by salinity and drought affects plant growth and development, resulting in significant losses to global crop production. Consequently, there is a strong need to develop ...stress-tolerant crops with a higher water use efficiency through breeding programs. Water use efficiency could be improved by decreasing stomatal transpiration without causing a reduction in CO
uptake under osmotic stress conditions. The genetic manipulation of stomatal density could be one of the most promising strategies for breeders to achieve this goal. On the other hand, a substantial amount of water loss occurs across the cuticle without any contribution to carbon gain when the stomata are closed and under osmotic stress. The minimization of cuticular (otherwise known as residual) transpiration also determines the fitness and survival capacity of the plant under the conditions of a water deficit. The deposition of cuticular wax on the leaf epidermis acts as a limiting barrier for residual transpiration. However, the causal relationship between the frequency of stomatal density and plant osmotic stress tolerance and the link between residual transpiration and cuticular wax is not always straightforward, with controversial reports available in the literature. In this review, we focus on these controversies and explore the potential physiological and molecular aspects of controlling stomatal and residual transpiration water loss for improving water use efficiency under osmotic stress conditions via a comparative analysis of the performance of domesticated crops and their wild relatives.
Arid/semi-arid and coastal agricultural areas of the world are especially vulnerable to climate change-driven soil salinity. Salinity tolerance in plants is a complex trait, with salinity negatively ...affecting crop yield. Plants adopt a range of mechanisms to combat salinity, with many transporter genes being implicated in Na+-partitioning processes. Within these, the high-affinity K+ (HKT) family of transporters play a critical role in K+ and Na+ homeostasis in plants. Among HKT transporters, Type I transporters are Na+-specific. While Arabidopsis has only one Na + -specific HKT (AtHKT1;1), cereal crops have a multiplicity of Type I and II HKT transporters. AtHKT1; 1 (Arabidopsis thaliana) and HKT1; 5 (cereal crops) ‘exclude’ Na+ from the xylem into xylem parenchyma in the root, reducing shoot Na+ and hence, confer sodium tolerance. However, more recent data from Arabidopsis and crop species show that AtHKT1;1/HKT1;5 alleles have a strong genetic association with ‘shoot sodium accumulation’ and concomitant salt tolerance. The review tries to resolve these two seemingly contradictory effects of AtHKT1;1/HKT1;5 operation (shoot exclusion vs shoot accumulation), both conferring salinity tolerance and suggests that contrasting phenotypes are attributable to either hyper-functional or weak AtHKT1;1/HKT1;5 alleles/haplotypes and are under strong selection by soil salinity levels. It also suggests that opposite balancing mechanisms involving xylem ion loading in these contrasting phenotypes exist that require transporters such as SOS1 and CCC. While HKT1; 5 is a crucial but not sole determinant of salinity tolerance, investigation of the adaptive benefit(s) conferred by naturally occurring intermediate HKT1;5 alleles will be important under a climate change scenario.
•High-affinity K+ (HKT) family of transporters play a critical role in K+ and Na+ homeostasis in plants.•HKT1/HKT1;5 operate in both shoot Na + exclusion and shoot Na + accumulation.•Contrasting phenotypes are attributable to either hyper-functional or weak HKT1/HKT1;5 alleles/haplotypes.
The global population is projected to experience a rapid increase in the future, which poses a challenge to global food sustainability. The "Green Revolution" beginning in the 1960s allowed grain ...yield to reach two billion tons in 2000 due to the introduction of semi-dwarfing genes in cereal crops. Semi-dwarfing genes reduce the gibberellin (GA) signal, leading to short plant stature, which improves the lodging resistance and harvest index under modern fertilization practices. Here, we reviewed the literature on the function of GA in plant growth and development, and the role of GA-related genes in controlling key agronomic traits that contribute to grain yield in cereal crops. We showed that: (1) GA is a significant phytohormone in regulating plant development and reproduction; (2) GA metabolism and GA signalling pathways are two key components in GA-regulated plant growth; (3) GA interacts with other phytohormones manipulating plant development and reproduction; and (4) targeting GA signalling pathways is an effective genetic solution to improve agronomic traits in cereal crops. We suggest that the modification of GA-related genes and the identification of novel alleles without a negative impact on yield and adaptation are significant in cereal crop breeding for plant architecture improvement. We observed that an increasing number of GA-related genes and their mutants have been functionally validated, but only a limited number of GA-related genes have been genetically modified through conventional breeding tools and are widely used in crop breeding successfully. New genome editing technologies, such as the CRISPR/Cas9 system, hold the promise of validating the effectiveness of GA-related genes in crop development and opening a new venue for efficient and accelerated crop breeding.
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