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Review
. 2019;14(11):1665455.
doi: 10.1080/15592324.2019.1665455. Epub 2019 Sep 28.

Calcium signaling and salt tolerance are diversely entwined in plants

Maryam Seifikalhor  1 , Sasan Aliniaeifard  2 , Aida Shomali  2 , Nikoo Azad  1 , Batool Hassani  3 , Oksana Lastochkina  4   5 , Tao Li  6
Affiliations
Review

Calcium signaling and salt tolerance are diversely entwined in plants

Maryam Seifikalhor et al. Plant Signal Behav. 2019.

Abstract

In plants dehydration imposed by salinity can invoke physical changes at the interface of the plasma membrane and cell wall. Changes in hydrostatic pressure activate ion channels and cause depolarization of the plasma membrane due to disturbance in ion transport. During the initial phases of salinity stress, the relatively high osmotic potential of the rhizosphere enforces the plant to use a diverse spectrum of strategies to optimize water and nutrient uptake. Signals of salt stress are recognized by specific root receptors that activate an osmosensing network. Plant response to hyperosmotic tension is closely linked to the calcium (Ca2+) channels and interacting proteins such as calmodulin. A rapid rise in cytosolic Ca2+ levels occurs within seconds of exposure to salt stress. Plants employ multiple sensors and signaling components to sense and respond to salinity stress, of which most are closely related to Ca2+ sensing and signaling. Several tolerance strategies such as osmoprotectant accumulation, antioxidant boosting, polyaminses and nitric oxide (NO) machineries are also coordinated by Ca2+ signaling. Substantial research has been done to discover the salt stress pathway and tolerance mechanism in plants, resulting in new insights into the perception of salt stress and the downstream signaling that happens in response. Nevertheless, the role of multifunctional components such as Ca2+ has not been sufficiently addressed in the context of salt stress. In this review, we elaborate that the salt tolerance signaling pathway converges with Ca2+ signaling in diverse pathways. We summarize knowledge related to different dimensions of salt stress signaling pathways in the cell by emphasizing the administrative role of Ca2+ signaling on salt perception, signaling, gene expression, ion homeostasis and adaptive responses.

Keywords: Calcium; osmoprotection; salinity; secondary messengers; signaling pathway.

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Figures

Figure 1.
Figure 1.
Diagrammatic representation of the Ca2+ role in salt stress responses in plants. Prominent role of Ca2+ under salt has been proposed in this scheme. Na+ influx to the cytosol is mediated by CNGC, HKT, GLR and AtNCl. Na+ efflux is derived by SOS. NHX and CAX are involved in Na+/H+ and Ca2+/H exchanges through vacuolar membrane, respectively. Ca2+ in the center implicates the Na+ current either by direct interaction with ion channels or indirectly through Ca2+ related modules (CBL-CIPK and CaM). FER activates Ca2+ channels via unknown pathway and bears a transient Ca2+ signaling. AtNCL: Na+/Ca2+ exchanger-like protein, CAX: Vacuolar H+/Ca2+ antiporter, CNGS: Cyclic nucleotide gated channels, FER: FERONIA, GLR: Glutamate-activated channels, HKT: Na+ transporter, NHX: Vacuolar located Na+/H+ antiporters, SOS: Salt overly sensitive, SS: Salt stress.
Figure 2.
Figure 2.
Schema model of SOS pathway regulated by Ca2+ under saline shock. Ca2+ signaling triggered by salt stress activate SOS3 causes interaction with SOS2. SOS3/SOS2 complex activates SOS1 by direct phosphorylation driven by SOS2 and result in Na+ efflux. Alternatively, SOS2 regulates vacuolar channels (CAX and NHX) and balance Na+ vacuolar sequestration. CAX: Vacuolar H+/Ca2+ antiporter, CBL: Calcineurin B-like protein, CIPK: CBL-interacting protein kinase, NHX: Vacuolar located Na+/H+ antiporters, SOS: Salt overly sensitive, SS: Salt stress. SRR: Sal responsive receptors.
Figure 3.
Figure 3.
Metabolic scheme for regulation of salt stress responses by polyamines (PAs), nitric oxide (NO) and proline mediated by cytosolic Ca2+ signaling. Under salt stress, elevated PAs content affect Ca2+ level in the cell by either direct activation of PMCA and contributes to Ca2+ excursion (this will result in a steady state level of Ca2+ for normal metabolism in the cell); or indirectly by stimulation of NO and ROS production that results in downstream Ca2+ signaling. Similarly by salt shock, enhanced proline content influences the Ca2+ read out by ROS engagement; while NO is multiply associated with Ca2+ signaling comprising: direct manipulation of the Ca2+ signaling, effect on Ca2+ channels and regulation of MAPKs. CR: Cysteine residue, cGMP: Cyclic GMP, cADPR: Cyclic ADP ribose (cADPR), CaM: Calmodulin, CDPK: Ca2+ dependent protein kinases, MAPK: mitogen-activated proteins kinase, NO: Nitric oxide, PAs: Polyamines, PMCA: plasma membrane-Ca2+-ATPase, Pro: Proline, ROS: Reactive oxygen species, SR: Salt responses, SRR: Salt responsive receptors.
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Grants and funding

Financial supports from Iran National Science Foundation (INSF) Grant number 97007583 to Dr. Maryam Seifikalhor and Grant number 96006991 to Dr. Sasan Aliniaeifard are gratefully acknowledged.

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