Microbe-mediated salinity tolerance in plants
Lalit L. Kharbikar*, Shweta K. Nandanwar**, Arti S. Shanware***, Yogesh M. Yele*, P. N. Sivalingam*, Pankaj Kaushal* and Jagdish Kumar*
*ICAR – National Institute of Biotic Stress Management, Raipur, Chhattisgarh, 493 225, India.
**Harper Adams University, Newport, Shropshire, TF10 8NB, United Kingdom.
***Rajiv Gandhi Biotechnology Centre, RTM Nagpur University, Nagpur, 440 034, India.
Plant species that are tolerant to salinity are called halophytes and the microorganisms that can survive high salinity conditions are called extremophiles or halophiles. In any ecosystem, plants are always associated with microbes and the saline ecosystem is not devoid of this association. Plants that grow under salinity conditions are usually inhabited by microbes which are beneficial for the enhancement of their salinity tolerance mechanism. In this article, we briefed about the importance of salinity in agriculture, salinity signalling pathways and the hypothetical mechanism of microbe-mediated salinity tolerance in plants. Some examples of the microbe-plant interactions exhibiting salinity tolerance in plants as well as genes and/or mechanisms involved in these interactions are also described. The importance of stress-induced promoters in the successful establishment of microbe-mediated salinity tolerance in plants is discussed.
Importance of salinity and salinity signalling pathways
Salinity is a global problem, and the areas affected by salinity are increasing gradually because of scarce rainfall, poor irrigation systems, water pollution, salt deposition, and other environmental factors. Thirty to fifty percent of arable land loss has been expected due to salinity by the year 2050 resulting in huge depletion of agricultural productivity worldwide1. Therefore, breeding for improved salinity tolerance in crop plants remains a high priority in agricultural research. A number of genes are known to involve in the signalling, transcriptional control, osmoprotection and scavenging of free-radical and toxic-compounds during salt stress in plants. However, the molecular control mechanisms for activation and regulation of these genes are not fully exploited since the salinity stress tolerance is a very complex phenomenon. It is believed that some interlinked pathways trigger stress tolerance mechanisms leading to the up- or down-regulation of salt-responsive genes that produce multiple signalling proteins2. These stress signalling proteins play a protective role in plants under different abiotic stress conditions including salinity stress. For example, dehydrins (DHNs) or group 2 LEA (late embryogenesis abundant) proteins accumulate in vegetative tissues in response to desiccation stress in almost all plants3. The stress signalling proteins (for example, HS proteins, Csp, etc.) and of some of their regulators (for example, HrcA, CtsR) are functionally conserved across the kingdoms. However, some striking differences are observed between their structures; for example, the absence of a σB orthologue in a microorganism, Lactobacillus lactis4.
Mechanism of microbe-mediated salinity tolerance in plants
Since microorganisms interact with plants and contribute to the living ecosystem, they are believed to be an integral part of the defence mechanisms in plants against several stresses. Microorganisms can survive in diverse environments and therefore have enormous capabilities to mitigate stresses including salinity through their metabolism5. Under the salinity stress microorganisms triggers rapid fluxes of cell water along the osmotic gradient out of the cell and accumulates large amounts of organic osmolytes (Fig. 1). The organic osmolytes such as trehalose, proline, and glycine betaine, etc. offer an adaptive strategy to abiotic stresses, including high salinity. This strategy of mitigating abiotic stresses is evolutionarily highly conserved in both prokaryotic and eukaryotic microorganisms6,7. The first salt-tolerant gene isolated from a prokaryotic organism Escherichia coli was proB-74 that determines the over-accumulation of proline under salinity stress. This suggests that the synthesis of organic osmolytes is an important phenomenon for salt tolerance in prokaryotes. However, the first salt-tolerant gene isolated from a eukaryotic organism Saccharomyces cerevisiae was HAL1 which modulates the potassium transport and increases the intracellular level of this cation under salinity stress. This suggests that potassium homeostasis is an important phenomenon for salt tolerance in eukaryotes8.
Figure 1. The hypothetical depiction of microbe-mediated salinity tolerance in plants. The proB-74 like genes in microbes synthesizes organic osmolytes such as trehalose, proline, and glycine betaine, etc. which offer an adaptive strategy to abiotic stresses, including high salinity, through osmotic adjustment.
Examples of the microbe-plant interactions exhibiting salinity tolerance in plants
The genes and/or mechanisms for salt tolerance, existing independently in microorganisms or in association with their host plants, have been exploited to enhance salinity tolerance in plants. Apart from this, promotion of salinity tolerance has also been observed in natural microbe-plant interactions, evaluated experimentally. Some of these microbe-plant interactions exhibiting salinity tolerance in plants as well as genes and/or mechanisms involved in these interactions are described in the following table.
Table 1. Microbe-plant interactions exhibiting salinity tolerance in plants and the mechanisms involved in these interactions.
Stress-inducible promoters for the establishment of microbe-mediated salinity tolerance in plants
Most of the above microbe-plant interactions exhibiting salinity tolerance were studied by high-end transformation procedures that warrant the specific and temporal expression of genes. Microbes as an integral part of these interactions are modulating the plant transcriptional activators, in general. However, transcriptional activators should recognize the genes to facilitate their tissue-specific expression only under the stress conditions. This is possible only when the genes have a specific set of cis-acting sequences, called promoters, at their upstream which is recognized by a specific transcriptional activator.
With the increasing use of transformation strategies, the need of promoters for transgene expression in a variety of ways or in response to different stresses has greatly increased. A stress-inducible promoter selection has, therefore, become an important prerequisite for successful transfer and expression of salt-induced genes in plants. The broad spectrum stress-inducible promoters are available that differ in their ability to regulate the expression patterns of transgenes for improved salinity stress tolerance in crop plants. Recently, the use of stress-inducible promoters that have low background expression under normal growth condition in conjunction with the transgenes was accomplished13. The increased stress tolerance was achieved without the retarded growth of plants after using this promoter. As strong abiotic stress-inducible promoters are required for transgene expression responsible for different abiotic-stress tolerance at different growth stages, selection of a suitable promoter is critical. Promoters of various genes regulating abiotic stress tolerance have been identified previously from several plants and some of them are listed in the following table14,15,16.
Table 2. Promoters of various genes involving in abiotic stresses tolerance of plants
HSp 1 and HSp 2
Dehydration and cold stress
PvSR2 and cgmt1
Heavy metal stress
Methyl jasmonate stress
In conclusion, a number of genes are known to involve in the signalling, transcriptional control, and inhibition of salt stress in plants. However, the molecular control mechanisms of these genes are not fully exploited since the salinity stress tolerance is a very complex phenomenon. Microbes, either independently or in interaction with plants, synthesises some organic osmolytes and other substances which offer an adaptive strategy to salinity stress. While in interaction with plants, microbes modulate their transcriptional activator machinery and enhance the salinity stress by several-folds. However, to function this mechanism activated transcription factors should recognize the cis-acting elements, called promoters, of the stress-inducible or tolerant genes in plants. Therefore, promoters that guarantee the tissue-specific and temporal expression of stress-responsive genes are very important for the successful establishment of salinity stress in plants, with the advent of transgenic technologies.
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