Molecular Mechanisms of Cell Wall Integrity in Plants Under Salt Stress

doi:10.13560/j.cnki.biotech.bull.1985.2023-0622

Abstract

Abstract:

Cell wall not only supports and protects plant cells, but also serves as the first barrier for plants to resist environmental stresses. As one of the major abiotic stresses that restrict agricultural production, salt stress can cause the alteration of cell wall composition and structure, and these changes can be perceived by cell wall integrity sensors, such as CrRLK1Ls, LRXs, and WAKs, to activate intracellular salt stress responses. In the cell interior, salt stress-induced influx of Ca²⁺and activation of phytohormone signaling promote the expressions of genes that are associated with cell wall biosynthesis and modification, which in turn facilitate the maintenance of cell wall integrity and improve the adaptation of plants to high salinity. In this review, the main components of primary cell wall polysaccharides and their cross-linking with each other are summarized. The impact of salt stress on cell wall polysaccharides, and the molecular mechanisms by which plants perceive and maintain cell wall integrity under salt stress, are also elucidated. Finally, the scientific questions that need to be further addressed in the research field of cell wall integrity under salt stress are discussed.

Key words: cell wall integrity, salt stress, cell wall sensor, CrRLK1Ls, LRXs

WANG Ming-tao, LIU Jian-wei, ZHAO Chun-zhao. Molecular Mechanisms of Cell Wall Integrity in Plants Under Salt Stress[J]. Biotechnology Bulletin, 2023, 39(11): 18-27.

Figures/Tables 1

References 74

[1]	Botella MA, Rosado A, Bressan RA, et al. Plant adaptive responses to salinity stress[M]// JenksMA, HasegawaPM.,Eds. Plant Abiotic Stress. Oxford, UK: Blackwell Publishing Ltd, 2005: 37-70.
[2]	Shrivastava P, Kumar R. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation[J]. Saudi J Biol Sci, 2015, 22(2): 123-131. doi: 10.1016/j.sjbs.2014.12.001 pmid: 25737642
[3]	Singh A. Soil salinization management for sustainable development: a review[J]. J Environ Manage, 2021, 277: 111383. doi: 10.1016/j.jenvman.2020.111383 URL
[4]	Colin L, Ruhnow F, Zhu JK, et al. The cell biology of primary cell walls during salt stress[J]. Plant Cell, 2023, 35(1): 201-217. doi: 10.1093/plcell/koac292 URL
[5]	Yu ZP, Duan XB, Luo L, et al. How plant hormones mediate salt stress responses[J]. Trends Plant Sci, 2020, 25(11): 1117-1130. doi: 10.1016/j.tplants.2020.06.008 pmid: 32675014
[6]	Zhang HM, Zhu JH, Gong ZZ, et al. Abiotic stress responses in plants[J]. Nat Rev Genet, 2022, 23(2): 104-119. doi: 10.1038/s41576-021-00413-0
[7]	Jiang ZH, Zhou XP, Tao M, et al. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca²⁺ influx[J]. Nature, 2019, 572(7769): 341-346. doi: 10.1038/s41586-019-1449-z
[8]	Anderson CT, Kieber JJ. Dynamic construction, perception, and remodeling of plant cell walls[J]. Annu Rev Plant Biol, 2020, 71: 39-69. doi: 10.1146/annurev-arplant-081519-035846 pmid: 32084323
[9]	Voxeur A, Höfte H. Cell wall integrity signaling in plants: to grow or not to grow that’s the question[J]. Glycobiology, 2016, 26(9): 950-960. pmid: 26945038
[10]	Liu JW, Zhang W, Long SJ, et al. Maintenance of cell wall integrity under high salinity[J]. Int J Mol Sci, 2021, 22(6): 3260. doi: 10.3390/ijms22063260 URL
[11]	Hamann T. The plant cell wall integrity maintenance mechanism—a case study of a cell wall plasma membrane signaling network[J]. Phytochemistry, 2015, 112: 100-109. doi: 10.1016/j.phytochem.2014.09.019 URL
[12]	Feng W, Kita D, Peaucelle A, et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca²⁺ signaling[J]. Curr Biol, 2018, 28(5): 666-675.e5. doi: S0960-9822(18)30025-3 pmid: 29456142
[13]	Bacete L, Hamann T. The role of mechanoperception in plant cell wall integrity maintenance[J]. Plants, 2020, 9(5): 574. doi: 10.3390/plants9050574 URL
[14]	Rui Y, Dinneny JR. A wall with integrity: surveillance and maintenance of the plant cell wall under stress[J]. New Phytol, 2020, 225(4): 1428-1439. doi: 10.1111/nph.16166 pmid: 31486535
[15]	Newman RH, Hill SJ, Harris PJ. Wide-angle X-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls[J]. Plant Physiol, 2013, 163(4): 1558-1567. doi: 10.1104/pp.113.228262 pmid: 24154621
[16]	Paredez AR, Somerville CR, Ehrhardt DW. Visualization of cellulose synthase demonstrates functional association with microtubules[J]. Science, 2006, 312(5779): 1491-1495. doi: 10.1126/science.1126551 pmid: 16627697
[17]	Gutierrez R, Lindeboom JJ, Paredez AR, et al. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments[J]. Nat Cell Biol, 2009, 11(7): 797-806. doi: 10.1038/ncb1886 pmid: 19525940
[18]	McFarlane HE, Döring A, Persson S. The cell biology of cellulose synthesis[J]. Annu Rev Plant Biol, 2014, 65: 69-94. doi: 10.1146/annurev-arplant-050213-040240 pmid: 24579997
[19]	Persson S, Paredez A, Carroll A, et al. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis[J]. Proc Natl Acad Sci USA, 2007, 104(39): 15566-15571. doi: 10.1073/pnas.0706592104 URL
[20]	McFarlane HE, Watanabe Y, Yang WL, et al. Golgi- and trans-Golgi network-mediated vesicle trafficking is required for wax secretion from epidermal cells[J]. Plant Physiol, 2014, 164(3): 1250-1260. doi: 10.1104/pp.113.234583 pmid: 24468625
[21]	Endler A, Kesten C, Schneider R, et al. A mechanism for sustained cellulose synthesis during salt stress[J]. Cell, 2015, 162(6): 1353-1364. doi: 10.1016/j.cell.2015.08.028 pmid: 26343580
[22]	Scheller HV, Ulvskov P. Hemicelluloses[J]. Annu Rev Plant Biol, 2010, 61: 263-289. doi: 10.1146/annurev-arplant-042809-112315 pmid: 20192742
[23]	Pauly M, Gille S, Liu LF, et al. Hemicellulose biosynthesis[J]. Planta, 2013, 238(4): 627-642. doi: 10.1007/s00425-013-1921-1 pmid: 23801299
[24]	Park YB, Cosgrove DJ. Xyloglucan and its interactions with other components of the growing cell wall[J]. Plant Cell Physiol, 2015, 56(2): 180-194. doi: 10.1093/pcp/pcu204 pmid: 25613914
[25]	Zabotina OA, van de Ven WTG, Freshour G, et al. Arabidopsis XXT5 gene encodes a putative alpha-1, 6-xylosyltransferase that is involved in xyloglucan biosynthesis[J]. Plant J, 2008, 56(1): 101-115. doi: 10.1111/tpj.2008.56.issue-1 URL
[26]	Zabotina OA, Avci U, Cavalier D, et al. Mutations in multiple XXT genes of Arabidopsis reveal the complexity of xyloglucan biosynthesis[J]. Plant Physiol, 2012, 159(4): 1367-1384. doi: 10.1104/pp.112.198119 pmid: 22696020
[27]	Brown DM, Goubet F, Wong VW, et al. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis[J]. Plant J, 2007, 52(6): 1154-1168. doi: 10.1111/j.1365-313X.2007.03307.x pmid: 17944810
[28]	Lee CH, Zhong RQ, Ye ZH. Arabidopsis family GT43 members are xylan xylosyltransferases required for the elongation of the xylan backbone[J]. Plant Cell Physiol, 2012, 53(1): 135-143. doi: 10.1093/pcp/pcr158 URL
[29]	Verhertbruggen Y, Yin L, Oikawa A, et al. Mannan synthase activity in the CSLD family[J]. Plant Signal Behav, 2011, 6(10): 1620-1623. doi: 10.4161/psb.6.10.17989 pmid: 21904114
[30]	Caffall KH, Mohnen D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides[J]. Carbohydr Res, 2009, 344(14): 1879-1900. doi: 10.1016/j.carres.2009.05.021 URL
[31]	Mohnen D. Pectin structure and biosynthesis[J]. Curr Opin Plant Biol, 2008, 11(3): 266-277. doi: 10.1016/j.pbi.2008.03.006 pmid: 18486536
[32]	Atmodjo MA, Hao ZY, Mohnen D. Evolving views of pectin biosynthesis[J]. Annu Rev Plant Biol, 2013, 64: 747-779. doi: 10.1146/annurev-arplant-042811-105534 pmid: 23451775
[33]	Harholt J, Suttangkakul A, Vibe Scheller H. Biosynthesis of pectin[J]. Plant Physiol, 2010, 153(2): 384-395. doi: 10.1104/pp.110.156588 pmid: 20427466
[34]	Wolf S, Mouille G, Pelloux J. Homogalacturonan methyl-esterification and plant development[J]. Mol Plant, 2009, 2(5): 851-860. doi: 10.1093/mp/ssp066 pmid: 19825662
[35]	Delmas F, Séveno M, Northey JGB, et al. The synthesis of the rhamnogalacturonan II component 3-deoxy-D-manno-2-octulosonic acid(Kdo)is required for pollen tube growth and elongation[J]. J Exp Bot, 2008, 59(10): 2639-2647. doi: 10.1093/jxb/ern118 URL
[36]	Byrt CS, Munns R, Burton RA, et al. Root cell wall solutions for crop plants in saline soils[J]. Plant Sci, 2018, 269: 47-55. doi: S0168-9452(17)30918-4 pmid: 29606216
[37]	Cosgrove DJ. Growth of the plant cell wall[J]. Nat Rev Mol Cell Biol, 2005, 6(11): 850-861.
[38]	Wang T, Park YB, Caporini MA, et al. Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls[J]. Proc Natl Acad Sci USA, 2013, 110(41): 16444-16449. doi: 10.1073/pnas.1316290110 pmid: 24065828
[39]	Phyo P, Wang T, Xiao CW, et al. Effects of pectin molecular weight changes on the structure, dynamics, and polysaccharide interactions of primary cell walls of Arabidopsis thaliana: insights from solid-state NMR[J]. Biomacromolecules, 2017, 18(9): 2937-2950. doi: 10.1021/acs.biomac.7b00888 URL
[40]	Miart F, Desprez T, Biot E, et al. Spatio-temporal analysis of cellulose synthesis during cell plate formation in Arabidopsis[J]. Plant J, 2014, 77(1): 71-84. doi: 10.1111/tpj.2013.77.issue-1 URL
[41]	Zhang SS, Sun L, Dong XR, et al. Cellulose synthesis genes CESA6 and CSI₁ are important for salt stress tolerance in Arabidopsis[J]. J Integr Plant Biol, 2016, 58(7): 623-626. doi: 10.1111/jipb.v58.7 URL
[42]	Tang YJ, Wang MH, Cao LY, et al. OsUGE3-mediated cell wall polysaccharides accumulation improves biomass production, mechanical strength, and salt tolerance[J]. Plant Cell Environ, 2022, 45(8): 2492-2507. doi: 10.1111/pce.v45.8 URL
[43]	Li ST, Zhang L, Wang Y, et al. Knockdown of a cellulose synthase gene BoiCesA affects the leaf anatomy, cellulose content and salt tolerance in broccoli[J]. Sci Rep, 2017, 7: 41397. doi: 10.1038/srep41397 pmid: 28169290
[44]	Nagashima Y, Ma ZY, Liu XT, et al. Multiple quality control mechanisms in the ER and TGN determine subcellular dynamics and salt-stress tolerance function of KORRIGAN1[J]. Plant Cell, 2020, 32(2): 470-485. doi: 10.1105/tpc.19.00714 URL
[45]	Dabravolski SA, Isayenkov SV. The regulation of plant cell wall organisation under salt stress[J]. Front Plant Sci, 2023, 14: 1118313. doi: 10.3389/fpls.2023.1118313 URL
[46]	Yan JW, Huang Y, He H, et al. Xyloglucan endotransglucosylase-hydrolase30 negatively affects salt tolerance in Arabidopsis[J]. J Exp Bot, 2019, 70(19): 5495-5506. doi: 10.1093/jxb/erz311 URL
[47]	Xu PP, Fang S, Chen HY, et al. The brassinosteroid-responsive xyloglucan endotransglucosylase/hydrolase 19(XTH19)and XTH23 genes are involved in lateral root development under salt stress in Arabidopsis[J]. Plant J, 2020, 104(1): 59-75. doi: 10.1111/tpj.v104.1 URL
[48]	Shomer I, Novacky AJ, Pike SM, et al. Electrical potentials of plant cell walls in response to the ionic environment[J]. Plant Physiol, 2003, 133(1): 411-422. pmid: 12970506
[49]	Gigli-Bisceglia N, van Zelm E, Huo WY, et al. Arabidopsis root responses to salinity depend on pectin modification and cell wall sensing[J]. Development, 2022, 149(12): dev200363. doi: 10.1242/dev.200363 URL
[50]	Yan JW, He H, Fang L, et al. Pectin methylesterase31 positively regulates salt stress tolerance in Arabidopsis[J]. Biochem Biophys Res Commun, 2018, 496(2): 497-501. doi: 10.1016/j.bbrc.2018.01.025 URL
[51]	Chen J, Chen XH, Zhang QF, et al. A cold-induced pectin methyl-esterase inhibitor gene contributes negatively to freezing tolerance but positively to salt tolerance in Arabidopsis[J]. J Plant Physiol, 2018, 222: 67-78. doi: 10.1016/j.jplph.2018.01.003 URL
[52]	Mahajan M, Yadav SK. Overexpression of a tea flavanone 3-hydroxylase gene confers tolerance to salt stress and Alternaria solani in transgenic tobacco[J]. Plant Mol Biol, 2014, 85(6): 551-573. doi: 10.1007/s11103-014-0203-z pmid: 24880475
[53]	Yan JW, Liu Y, Yang L, et al. Cell wall β-1, 4-galactan regulated by the BPC1/BPC2-GALS1 module aggravates salt sensitivity in Arabidopsis thaliana[J]. Mol Plant, 2021, 14(3): 411-425. doi: 10.1016/j.molp.2020.11.023 URL
[54]	Yan JW, Liu Y, Yan JW, et al. The salt-activated CBF1/CBF2/CBF3-GALS1 module fine-tunes galactan-induced salt hypersensitivity in Arabidopsis[J]. J Integr Plant Biol, 2023.
[55]	Zhu JH, Lee BH, Dellinger M, et al. A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis[J]. Plant J, 2010, 63(1): 128-140.
[56]	Zhao H, Li ZX, Wang YY, et al. Cellulose synthase-like protein OsCSLD4 plays an important role in the response of rice to salt stress by mediating abscisic acid biosynthesis to regulate osmotic stress tolerance[J]. Plant Biotechnol J, 2022, 20(3): 468-484. doi: 10.1111/pbi.v20.3 URL
[57]	Liu HH, Ma Y, Chen N, et al. Overexpression of stress-inducible OsBURP16, the β subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice[J]. Plant Cell Environ, 2014, 37(5): 1144-1158. doi: 10.1111/pce.2014.37.issue-5 URL
[58]	Jin J, Duan JL, Shan C, et al. Ethylene insensitive3-like2(OsEIL2)confers stress sensitivity by regulating OsBURP16, the β subunit of polygalacturonase(PG1β-like)subfamily gene in rice[J]. Plant Sci, 2020, 292: 110353. doi: 10.1016/j.plantsci.2019.110353 URL
[59]	Franck CM, Westermann J, Boisson-Dernier A. Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond[J]. Annu Rev Plant Biol, 2018, 69: 301-328. doi: 10.1146/annurev-arplant-042817-040557 pmid: 29539271
[60]	Lin WW, Tang WX, Pan X, et al. Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling[J]. Curr Biol, 2022, 32(3): 497-507.e4. doi: 10.1016/j.cub.2021.11.030 URL
[61]	Tang WX, Lin WW, Zhou X, et al. Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis[J]. Curr Biol, 2022, 32(3): 508-517.e3. doi: 10.1016/j.cub.2021.11.031 URL
[62]	Herger A, Dünser K, Kleine-Vehn J, et al. Leucine-rich repeat extensin proteins and their role in cell wall sensing[J]. Curr Biol, 2019, 29(17): R851-R858. doi: 10.1016/j.cub.2019.07.039
[63]	Zhao CZ, Zayed O, Yu ZP, et al. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis[J]. Proc Natl Acad Sci USA, 2018, 115(51): 13123-13128. doi: 10.1073/pnas.1816991115 URL
[64]	Dünser K, Gupta S, Herger A, et al. Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana[J]. EMBO J, 2019, 38(7): e100353. doi: 10.15252/embj.2018100353 URL
[65]	Sede AR, Borassi C, Wengier DL, et al. Arabidopsis pollen extensins LRX are required for cell wall integrity during pollen tube growth[J]. FEBS Lett, 2018, 592(2): 233-243. doi: 10.1002/1873-3468.12947 pmid: 29265366
[66]	Galindo-Trigo S, Blanco-Touriñán N, DeFalco TA, et al. CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception[J]. EMBO Rep, 2020, 21(2): e48466. doi: 10.15252/embr.201948466 URL
[67]	Lin W, Wang YH, Liu XY, et al. OsWAK112, A wall-associated kinase, negatively regulates salt stress responses by inhibiting ethylene production[J]. Front Plant Sci, 2021, 12: 751965. doi: 10.3389/fpls.2021.751965 URL
[68]	Kaur R, Singh K, Singh J. A root-specific wall-associated kinase gene, HvWAK1, regulates root growth and is highly divergent in barley and other cereals[J]. Funct Integr Genomics, 2013, 13(2): 167-177. doi: 10.1007/s10142-013-0310-y URL
[69]	Van der Does D, Boutrot F, Engelsdorf T, et al. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses[J]. PLoS Genet, 2017, 13(6): e1006832. doi: 10.1371/journal.pgen.1006832 URL
[70]	Yu LJ, Nie JN, Cao CY, et al. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana[J]. New Phytol, 2010, 188(3): 762-773. doi: 10.1111/nph.2010.188.issue-3 URL
[71]	Zhou S, Chen QH, Li XY, et al. MAP65-1 is required for the depolymerization and reorganization of cortical microtubules in the response to salt stress in Arabidopsis[J]. Plant Sci, 2017, 264: 112-121. doi: S0168-9452(17)30399-0 pmid: 28969791
[72]	Wang C, Li JJ, Yuan M. Salt tolerance requires cortical microtubule reorganization in Arabidopsis[J]. Plant Cell Physiol, 2007, 48(11): 1534-1547. pmid: 17906320
[73]	Kesten C, Wallmann A, Schneider R, et al. The companion of cellulose synthase 1 confers salt tolerance through a Tau-like mechanism in plants[J]. Nat Commun, 2019, 10(1): 857. doi: 10.1038/s41467-019-08780-3 pmid: 30787279
[74]	Lindwall G, Cole RD. Phosphorylation affects the ability of tau protein to promote microtubule assembly[J]. J Biol Chem, 1984, 259(8): 5301-5305. pmid: 6425287