Recent Advances on Salt Stress Sensitivity and Related Calcium Signals in Plants

doi:10.7525/j.issn.1673-5102.2022.04.021

Abstract

Abstract:

Salt stress had a critical impact on plant growth and development， including osmotic stress and ion toxicity， which seriously damaged agricultural production and food security. Under salt stress， plant related receptors were stimulated to send Ca²⁺ enter the cytoplasmic matrix through the Ca²⁺ channels opened on the cell membrane and intracellular calcium storage membrane， resulting in the increase of intracellular Ca²⁺ concentration and calcium signal. Ca²⁺， as an important second messenger， transmited signals within and between plant cells， downstream， and caused a series of physiological responses to salt stress at different growth and development stages. Calcium signals mainly included calmodulin（CaM）， calmodulin like protein（CML）， calcium dependent protein kinase（CDPK） and calcineurin B-like protein（CBL） and CBL interacting protein kinase（CIPK）， and sensed and transmited specific calcium signal information to the downstream， and activated plant physiological response to salt stress. This paper reviewed how plants perceived salt stress stimulation and the mechanism of calcium signal regulation， and looked forward to the problems should be solved in this research field.

Key words: salt stress, Ca²⁺ signal, Ca²⁺ sensor, CIPK

CLC Number:

Q945.4

Jiaorao CHEN, Xu XU, Zhangli HU, Shuang YANG. Recent Advances on Salt Stress Sensitivity and Related Calcium Signals in Plants[J]. Bulletin of Botanical Research, 2022, 42(4): 713-720.

Figures/Tables 2

References 39

1	MORTON M J L， AWLIA M， AL-TAMIMI N，et al.Salt stress under the scalpel-dissecting the genetics of salt tolerance［J］.The Plant Journal，2019，97（1）：148-163.
2	URI N.Cropland soil salinization and associated hydrology：trends，processes and examples［J］.Water，2018，10（8）：1030.
3	向晶，钟甫宁.人口结构变动对未来粮食需求的影响：2010—2050［J］.中国人口·资源与环境，2013，23（6）：117-121.
	XIANG J， ZHONG F N.Impact of demographic transition on food demand in China：2010-2050［J］.China Population，Resources and Environment，2013，23（6）：117-121．
4	NEGRÃO S， SCHMÖCKEL S M， TESTER M.Evaluating physiological responses of plants to salinity stress［J］.Annals of Botany，2017，119（1）：1-11.
5	EVAN ZELM， ZHANG Y X， TESTERINK C.Salt tolerance mechanisms of plants［J］.Annual Review of Plant Biology，2020，71（1）：403-433.
6	LIANG W J， MA X L， WAN P，et al.Plant salt-tolerance mechanism：a review［J］.Biochemical and Biophysical Research Communications，2018，495（1）：286-291.
7	JULKOWSKA M M， TESTERINK C.Tuning plant signaling and growth to survive salt［J］.Trends in Plant Science，2015，20（9）：586-594.
8	YANG Y Q， GUO Y.Elucidating the molecular mechanisms mediating plant salt-stress responses［J］.New Phytologist，2018，217（2）：523-539.
9	BOSE J， POTTOSIN I I， SHABALA S S，et al.Calcium efflux systems in stress signaling and adaptation in plants［J］.Frontiers in Plant Science，2011，2：85.
10	GONG C M， SHI C， DING X T，et al.Hydrogen sulfide induces Ca²⁺ signal in guard cells by regulating reactive oxygen species accumulation［J］.Plant Signaling & Behavior，2020，15（11）： 1805228.
11	ZHANG Q， SONG T， GUAN C，et al.OsANN4 modulates ROS production and mediates Ca²⁺ influx in response to ABA［J］.BMC Plant Biology，2021，21（1）：474.
12	李甜，原丽，张军，等.非损伤微测技术实时检测海马脑片跨膜钙离子流［J］.生理学报，2017，69（4）：467-476.
	LI T， YUAN L， ZHANG J，et al.Real-time measurement of Ca²⁺ flux in hippocampal slice with non-invasive microtest technique［J］.Acta Physiologica Sinica，2017，69（4）：467-476.
13	MANISHANKAR P， WANG N L， KÖSTER P，et al.Calcium signaling during salt stress and in the regulation of ion homeostasis［J］.Journal of Experimental Botany，2018，69（17）：4215-4226.
14	VINCENT T R， AVRAMOVA M， CANHAM J，et al.Interplay of plasma membrane and vacuolar ion channels，together with BAK1，elicits rapid cytosolic calcium elevations in Arabidopsis during aphid feeding［J］.The Plant Cell，2017，29（6）：1460-1479.
15	GONG Z Z， XIONG L M， SHI H Z，et al.Plant abiotic stress response and nutrient use efficiency［J］.Science China-Life Sciences，2020，63（5）：635-674.
16	FENG W， KITA D， PEAUCELLE A，et al.The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca²⁺ signaling［J］.Current Biology，2018，28（5）：666-675.
17	ZHAO C Z， JIANG W， ZAYED O，et al.The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones［J］.National Science Review，2021，8（1）：nwaa149.
18	JIANG Z， ZHOU X， TAO M，et al.Plant cell-surface GIPC sphingolipids sense salt to trigger Ca²⁺ influx［J］.Nature，2019，572（7769）：341-346.
19	YUAN F， YANG H， XUE Y，et al.OSCA1 mediates osmotic-stress-evoked Ca²⁺ increases vital for osmosensing in Arabidopsis ［J］.Nature，2014，514（7522）：367-371.
20	LIU X， WANG J W， SUN L F.Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2［J］.Nature Communications，2018，9：5060.
21	ZHAI Y J， WEN Z H， HAN Y，et al.Heterogeneous expression of plasma-membrane-localised OsOSCA1.4 complements osmotic sensing based on hyperosmolality and salt stress in Arabidopsis oscal mutant［J］.Cell Calcium，2020，91：102261.
22	THOR K， JIANG S S， MICHARD E，et al.The calcium - permeable channel OSCA1.3 regulates plant stomatal immunity［J］.Nature，2020，585（7826）：569-573.
23	ALDON D， MBENGUE M， MAZARS C，et al.Calcium signalling in plant biotic interactions［J］.International Journal of Molecular Sciences，2018，19（3）：665.
24	SHI S J， LI S G， ASIM M，et al.The Arabidopsis calcium-dependent protein kinases（CDPKs） and their roles in plant growth regulation and abiotic stress responses［J］.International Journal of Molecular Sciences，2018，19（7）：1900.
25	GAO X Q，COXJR. K L，HE P.Functions of calcium-dependent protein kinases in plant innate immunity［J］.Plants：Basel，Switzerland，2014，3（1）：160-176.
26	LIESE A， ROMEIS T.Biochemical regulation of in vivo function of plant calcium-dependent protein kinases（CDPK）［J］.Biochimica et Biophysica Acta（BBA）-Molecular Cell Research，2013，1833（7）：1582-1589.
27	HAMEL L P， SHEEN J， SÉGUIN A.Ancient signals：comparative genomics of green plant CDPKs［J］.Trends in Plant Science，2014，19（2）：79-89.
28	HUANG K， PENG L， LIU Y Y，et al. Arabidopsis calcium-dependent protein kinase AtCPK1 plays a positive role in salt/drought-stress response［J］.Biochemical and Biophysical Research Communications，2018，498（1）：92-98.
29	ZHANG H L， ZHANG Y N， DENG C，et al.The Arabidopsis Ca²⁺- dependent protein kinase CPK12 is involved in plant response to salt stress［J］.International Journal of Molecular Sciences，2018，19（12）：4062.
30	GAO W， XU F C， GUO D D，et al.Calcium-dependent protein kinases in cotton：insights into early plant responses to salt stress［J］.BMC Plant Biology，2018，18（1）：15.
31	ZHAO R， SUN H M， ZHAO N，et al.The Arabidopsis Ca²⁺- dependent protein kinase CPK27 is required for plant response to salt-stress［J］.Gene，2015，563（2）：203-214.
32	BECKMANN L， EDEL K H， BATISTIČ O，et al.A calcium sensor-protein kinase signaling module diversified in plants and is retained in all lineages of Bikonta species［J］.Scientific Reports，2016，6：31645.
33	ZHANG K， HAN Y T， ZHAO F L，et al.Genome-wide identification and expression analysis of the CDPK gene family in grape，Vitis spp.［J］.BMC Plant Bology，2015，15：164.
34	KLEE C B， VANAMAN T C.Calmodulin［J］.Advances in Protein Chemistry，1982，35：213-321.
35	ZENG H Q， ZHANG Y X， ZHANG X J，et al.Analysis of EF-hand proteins in soybean genome suggests their potential roles in environmental and nutritional stress signaling［J］.Frontiers in Plant Science，2017，8：877.
36	ZHOU S， JIA L X， CHU H Y，et al. Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-nitrosoglutathione reductase via direct binding［J］.PLoS Genetics，2016，12（9）：e1006255.
37	MA X， LI Q H， YU Y N，et al.The CBL-CIPK pathway in plant response to stress signals［J］.International Journal of Molecular Sciences，2020，21（16）：5668.
38	KLEIST T J， SPENCLEY A L， LUAN S.Comparative phylogenomics of the CBL-CIPK calcium - decoding network in the moss Physcomitrella，Arabidopsis，and other green lineages［J］.Frontiers in Plant Science，2014，5：187.
39	MA L， YE J M， YANG Y Q，et al.The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress［J］.Developmental Cell，2019，48（5）：697-709.

[1]	Lei XU, Xiao XU, Qinsong LIU. Effects of Exogenous Salicylic Acid on Antioxidant System and Gene Expression of Davidia involucrata Seedlings under Salt Stress [J]. Bulletin of Botanical Research, 2023, 43(4): 572-581.
[2]	Li LI, Xin WANG, Yuejing ZHANG, Lingyun JIA, Hailong PANG, Hanqing FENG. Effects of Abiotic Stresses on the Intracellular and Extracellular ATP Levels of Tobacco Suspension Cells [J]. Bulletin of Botanical Research, 2023, 43(2): 179-185.
[3]	Shixian LIAO, Yuting WANG, Liben DONG, Yongmei GU, Fenglin JIA, Tingbo JIANG, Boru ZHOU. Function Analysis of the Transcription Factor PsnbZIP1 of Populus simonii×P. nigra in Response to Salt Stress [J]. Bulletin of Botanical Research, 2023, 43(2): 288-299.
[4]	Senyao LIU, Fenglin JIA, Qing GUO, Gaofeng FAN, Boru ZHOU, Tingbo JIANG. Response Analysis of Transcription Factor PsnbHLH162 Gene in Populus simonii × P. nigra under Salt Stress and Low Temperature Stress [J]. Bulletin of Botanical Research, 2023, 43(2): 300-310.
[5]	Liran YUE, Yingjie LIU, Chenxu LIU, Yunwei ZHOU. Cloning and Functional Analysis of miR398a from Chrysanthemum× grandiflora in Response to Salt Stress [J]. Bulletin of Botanical Research, 2022, 42(6): 986-996.
[6]	Denggao LI, Rui LIN, Qinghui MU, Na ZHOU, Yanru ZHANG, Wei BAI. Cloning and Functional Analysis of StNPR4 gene in Solanum tuberosum [J]. Bulletin of Botanical Research, 2022, 42(5): 821-829.
[7]	He CHENG, Shuanghui TIAN, Yang ZHANG, Cong LIU, De’an XIA, Zhigang WEI. Genome-wide Identification and Expression Analysis of nsLTP Gene Family in Populus trichocarpa [J]. Bulletin of Botanical Research, 2022, 42(3): 412-423.
[8]	Shuang-Hui TIAN, He CHENG, Yang ZHANG, Cong LIU, De-An XIA, Zhi-Gang WEI. Genome-wide Identification and Expressional Analysis of Carotenoid Cleavage Dioxygenases(CCD) Gene Family in Populus trichocarpa under Drought and Salt Stress [J]. Bulletin of Botanical Research, 2021, 41(6): 993-1005.
[9]	Meng-Xuan REN, Yang ZHANG, Shuang WANG, Rui-Qi WANG, Cong LIU, Zhi-Gang WEI. Genome-wide Identification and Expression Analysis GATA Family of Populus trichocarpa [J]. Bulletin of Botanical Research, 2021, 41(1): 107-118.
[10]	CAO Ming-Wu, LUO Rui, AN Hui, PANG Qiu-Ying. Physiological Response of Suspension Cells of Helianthus tuberosus to NaCl Stress [J]. Bulletin of Botanical Research, 2019, 39(2): 222-228.
[11]	ZHAO Xiao-Ju, ZHANG Li-Xia, MAN Xiu-Ling. Effects of Exogenous NO on Seed Germination and Physiological Metabolism in Catharanthus roseus Seedling under NaCl Stress [J]. Bulletin of Botanical Research, 2018, 38(5): 669-674.
[12]	ZHANG Li-Li, ZHANG Fu-Chun. Transcriptomic Analysis of the Halostachys caspica in Response to Short-term Salt Stress [J]. Bulletin of Botanical Research, 2018, 38(1): 91-99.
[13]	WANG Pei-Long, LIU Zhong-Yuan, ZHANG Teng-Qian, TANG Fei-Fei, QU Guan-Zheng, GAO Cai-Qiu. Cloning and Expression Analysis of ThPP2C Gene from Tamarix hispida [J]. Bulletin of Botanical Research, 2017, 37(3): 395-401.
[14]	DU Chi, ZHANG Ji, ZHANG Fu-Chun. Expression Analysis of Rev1 and Rev3 of Halostachys caspica under Salt Stress [J]. Bulletin of Botanical Research, 2017, 37(2): 211-215.
[15]	SI Jing-Na；ZHOU Tao；XU Fang；BO Wen-Hao；WU Rong-Ling. Salt-responsive MicroRNAs in Populus euphratica* by Deep Sequencing [J]. Bulletin of Botanical Research, 2015, 35(6): 836-842.