The Role of Catabolic Programs in Plant Adaptation to the Toxic Effects of Acute Chloride Salinity

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The accumulation of inorganic salts in the soil solution has a pronounced toxic effect on most higher plants that lack specific protection mechanisms. An excess of sodium cations and chloride anions leads to disruptions in normal cell function, reduced growth, and decreased yields of cultivated plants. Salt tolerance mechanisms represent a complex system of adaptive processes aimed at neutralizing the toxic effects caused by increased salt in the surrounding environment. The multicomponent and multigene control of the plant response to salt stress at the cellular, organ, and organism levels makes the selection of salt-tolerant genotypes a challenging task. This review examines the molecular and cellular mechanisms activated in plants when the concentration of sodium and chlorine ions sharply increases in the rhizosphere substrate. The pathways of ion uptake, ion channels, and transporters that maintain ionic homeostasis in root and leaf mesophyll cells are analyzed. Salt perception mechanisms and the main signaling system that transmits salinity signals from the root system to the plant shoots are briefly defined. Special attention is paid to cytological adaptation mechanisms, including cellular sensors and signaling cascades that trigger the physiological response to acute salinization, as well as autophagy — the process of regulated degradation of damaged cellular structures and macromolecules, which plays an important role in the adaptation of plants to salt stress. The information on the main types of nuclear and DNA structure disruptions that develop under salinity stress and lead to programmed cell death is also included. Thus, the review covers the primary mechanisms of glycophyte adaptation to salt stress and highlights the potential of studying catabolic programs for developing strategies to enhance the tolerance of agricultural crops.

About the authors

A. V Murtuzova

Komarov Botanical Institute RAS

Email: amurtuzova@binran.ru
ORCID iD: 0000-0002-2047-2617
PhD in Biology, Researcher St. Petersburg, Russian Federation

A. D Strizhenok

Komarov Botanical Institute RAS

Email: strileha03@mail.ru
Bachelor of Science in Biology St. Petersburg, Russian Federation

V. V Kuznetsov

Komarov Botanical Institute RAS

Email: vkuznetsov@binran.ru
Senior Engineer St. Petersburg, Russian Federation

E. V Tyutereva

Komarov Botanical Institute RAS

Email: ETutereva@binran.ru
ORCID iD: 0000-0002-6727-6656
PhD in Biology, Leading Researcher St. Petersburg, Russian Federation

References

  1. Munns R., Tester M. Mechanisms of salinity tolerance // Annu. Rev. Plant Biol. 2008. V. 59. P. 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
  2. Guo R., Zhao L., Zhang K., et al. Comparative genomics and transcriptomics of the extreme halophyte Puccinellia tenuiflora provides insights into salinity tolerance differentiation between Halophytes and glycophytes // Front. Plant Sci. 2021. V. 12. P. 649001.
  3. Osman K.T. Saline and sodic soils. In: Management of Soil Problems. Springer, Cham. 2018. P. 255–298.
  4. Van Zelm E., Zhang Y., Testerink C. Salt tolerance mechanisms of plants // Annu. Rev. Plant Biol. 2020. V. 71. P. 403–433. https://doi: 10.1146/annurev-arplant-050718-100005
  5. Zhao S., Zhang Q., Liu M., et al. Regulation of plant responses to salt stress // Int. J. Mol. Sci. 2021. V. 22. P. 4609.
  6. Negrão S., Schmöckel S.M., Tester M. Evaluating physiological responses of plants to salinity stress // Ann. Bot. 2017. V. 119. P. 1–11.
  7. Zhou H., Shi H., Yang Y., et al. Insights into plant salt stress signaling and tolerance // J. gen. genom. 2024. V. 51. P. 16–34. https://doi.org/10.1016/j.jgg.2023.08.007
  8. Safdar H., Amin A., Shafiq Y., et al. A review: Impact of salinity on plant growth // Nat. Sci. 2019. V. 17. P. 34–40.
  9. Hao S., Wang Y., Yan Y., et al. A review on plant responses to salt stress and their mechanisms of salt resistance // Horticulturae. 2021. V. 7. P. 132.
  10. Silva-Herrera H., Wege S., Franzisky B.L., et al. Chloride transport and homeostasis in plants // Quant Plant Biol. 2025. V. 6. P. 1–10. https://dx.doi.org/10.1017/qpb.2025.10008
  11. Keisham M., Mukherjee S., Bhatla S. Mechanisms of sodium transport in plants-progresses and challenges // Int. J. Mol. Sci. 2018. V. 19. P. 647. https://doi.org/10.3390/ijms19030647
  12. Ketehouli T., Idrice Carther K.F., Noman M., et al. Adaptation of plants to salt stress: characterization of Na+ and K+ transporters and role of CBL gene family in regulating salt stress response // Agronomy. 2019. V. 9. P. 687. https://doi.org/10.3390/agronomy9110687
  13. Joshi S., Nath J., Singh A.K., Pareek A., Joshi R. Ion transporters and their regulatory signal transduction mechanisms for salinity tolerance in plants // Physiol. Plant. 2022. V. 174. P. e13702.
  14. Lindberg S., Premkumar A. Ion changes and signaling under salt stress in wheat and other important crops // Plants. 2024. V. 13. P. 46. https://doi.org/10.3390/plants13010046
  15. Kronzucker H.J., Britto D.T. Sodium transport in plants: a critical review // New Phytol. 2011. V. 189. P. 54–81.
  16. Lorenzen I., Aberle T., Plieth C. Salt stress-induced chloride flux: a study using transgenic Arabidopsis expressing a fluorescent anion probe // Plant J. 2004. V. 38. P. 539–544.
  17. Teakle N.L., Tyerman S.D. Mechanisms of Cl- transport contributing to salt tolerance // Plant Cell Env. 2010. V. 33. P. 566–589.
  18. Nedelyaeva O.I., Shuvalov A.V., Balnokin Y.V. Chloride channels and transporters of the CLC family in plants // Russ. J. Plant Physiol. 2020. V. 67. P. 767–784. https://doi.org/10.1134/S1021443720050106
  19. Kovermann P., Meyer S., Hörtensteiner S., et al. The Arabidopsis vacuolar malate channel is a member of the ALMT family // Plant J. 2007. V. 52. P. 1169–1180.
  20. Meyer S., Scholz-Starke J., De Angeli A., et al. Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation // Plant J. 2011. V. 67. P. 247–257.
  21. Galvan-Ampudia C.S., Julkowska M.M., Darwish E., et al. Halotropism is a response of plant roots to avoid a saline environment // Curr. Biol. 2013. V. 23. P. 2044–2050.
  22. Mazumder A., Gaur V.S., Kole P.C., Mondal T.K. Root halotropism in plants: tolerance or escape? // Rhizosphere. 2024. V. 33. P. 101002. https://doi.org/10.1016/j.rhisph.2024.101002
  23. Jiang Z., Zhou X., Tao M., et al. Plant cell-surface gIPC sphingolipids sense salt to trigger Ca2+ influx // Nat. 2019. V. 572. P. 341–346.
  24. Steinhorst L., Kudla J. How plants perceive salt // Nat. 2019. V. 572. P. 318–320. https://doi.org/10.1038/d41586-019-02289-x
  25. Feng W., Kita D., Peaucelle A., et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling // Curr. Biol. 2018. V. 28. P. 666–675.
  26. Demidchik V., Tester M. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots // Plant Physiol. 2002. V. 128. P. 379–387.
  27. Demidchik V., Maathuis F.J.M. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development // New Phytol. 2007. V. 175. P. 387–405.
  28. Kiegle E., Moore C.A., Haseloff J., Tester M.A., Knight M.R. Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root // Plant J. 2000. V. 23. P. 267–278.
  29. Choi W.G., Toyota M., Kim S.H., Hilleary R., Gilroy S. Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants // PNAS. 2014. V. 111. P. 6497–6502.
  30. Demidchik V., Shabala S. Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’// Funct. Plant Biol. 2017. V. 45. P. 9–27.
  31. Ji H., Pardo J.M., Batelli G., et al. The Salt overly sensitive (SOS) pathway: established and emerging roles // Mol. Plant. 2013. V. 6. P. 275–286.
  32. Quan R., Lin H., Mendoza I., et al. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress // Plant Cell. 2007. V. 19. P. 1415–1431.
  33. Yang Y., Guo Y. unraveling salt stress signaling in plants // J. Integr. Plant Biol. 2018. V. 60. P. 796–804.
  34. Halfter U., Ishitani M., Zhu J.K. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3 // Proc. Natl. Acad. Sci. u. S. A. 2000. V. 97. P. 3735–3740.
  35. Lin J., Wang Y., Wang G. Salt stress-induced programmed cell death in tobacco protoplasts is mediated by reactive oxygen species and mitochondrial permeability transition pore status // J. Plant Physiol. 2006. V. 163. P. 731–739. https://doi.org/10.1016/j.jplph.2005.06.016
  36. Quintero F.J., Martinez-Atienza J., Villalta I., et al. Activation of the plasma membrane Na+/H+ antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain // PNAS. 2011. V. 108. P. 2611–2616. https://doi.org/10.1073/pnas.1018921108
  37. Donaldson L., Ludidi N., Knight M.R., Gehring C., Denby K. Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cgMP levels // FEBS Lett. 2004. V. 569. P. 317–320.
  38. Miller G.A.D., Suzuki N., Ciftci-Yilmaz S., Mittler R.O.N. Reactive oxygen species homeostasis and signalling during drought and salinity stresses // Plant Cell Envir. 2010. V. 33. P. 453–467.
  39. Testerink C., Munnik T. Phosphatidic acid: a multifunctional stress signaling lipid in plants // Trends Plant Sci. 2005. V. 10. P. 368–375.
  40. Testerink C., Munnik T. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants // J. Exp. Bot. 2011. V. 62. P. 2349–2361.
  41. Qin W., Pappan K., Wang X. Molecular heterogeneity of phospholipase D (PLD): cloning of PLDγ and regulation of plant PLDγ, -β, and -α by polyphosphoinositides and calcium // J. Biol. Chem. 1997. V. 272. P. 28267–28273.
  42. McLoughlin F., Testerink C. Phosphatidic acid, a versatile water-stress signal in roots // Front. Plant Sci. 2013. V. 4. P. 525.
  43. Julkowska M.M., McLoughlin F., Galvan-Ampudia C.S., et al. Identification and functional characterization of the Arabidopsis Snf1-related protein kinase SnRK2.4 phosphatidic acid-binding domain // Plant Cell Envir. 2015. V. 38. P. 614–624.
  44. Kulik A., Wawer I., Krzywińska E., Bucholc M., Dobrowolska G. SnRK2 protein kinases — key regulators of plant response to abiotic stresses // OMICS. 2011. V. 15. P. 859–872.
  45. Soma F., Mogami J., Yoshida T., et al. ABA-unresponsive SnRK2 protein kinases regulate mRNA decay under osmotic stress in plants // Nat. Plants. 2017. V. 3. P. 16204.
  46. Kawa D., Meyer A.J., Dekker H.L., et al. SnRK2 Protein Kinases and mRNA decapping machinery control root development and response to salt // Plant Physiol. 2020. V. 182. P. 361–377.
  47. Sun J., Dai S., Wang R., et al. Calcium mediates root K+/Na+ homeostasis in poplar species differing in salt tolerance // Tree Physiol. 2009. V. 29. P. 1175–1186.
  48. Gaxiola R.A., Palmgren M.G., Schumacher K. Plant proton pumps // FEBS Lett. 2007. V. 581. P. 2204. https://doi.org/10.1016/j.febslet.2007.03.050
  49. Bassil E., Blumwald E. The ins and outs of intracellular ion homeostasis: NHX-type cation/H+ transporters // Curr. Opin. Plant Biol. 2014. V. 22. P. 1–6.
  50. Isayenkov S.V., Maathuis F.J.M. Plant salinity stress: many unanswered questions remain // Front. Plant Sci. 2019. V. 10. P. 80. https://doi.org/10.3389/fpls.2019.00080
  51. Mishra G., Mohapatra S.K., Rout G.R. Plant membrane transporters function under abiotic stresses: a review // Planta. 2024. V. 260. P. 125. https://doi.org/10.1007/s00425-024-04548-2
  52. Roy S.J., Negrão S., Tester M. Salt resistant crop plants // Curr. Opin. Biotech. 2014. V. 26. P. 115–124.
  53. Wu H., Shabala L., Liu X., et al. Linking salinity stress tolerance with tissue-specific Na+ sequestration in wheat roots // Front. Plant Sci. 2015. V. 6. P. 71.
  54. Wang Y., Wu W.H. Potassium transport and signaling in higher plants // Annu. Rev. Plant Biol. 2013. V. 64. P. 451–476. https://doi.org/10.1146/annurev-arplant-050312-120153
  55. Leigh R.A., Wyn Jones R.G. A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell // New Phytol. 1984. V. 97. P. 1.
  56. Armengaud P., Sulpice R., Miller A.J., et al. Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots // Plant Physiol. 2009. V. 150. P. 772–785. https://doi.org/10.1104/pp.108.133629
  57. Almeida D.M., Oliveira M.M., Saibo N.J.M. Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants // genet. Mol. Biol. 2017. V. 40. P. 326–345.
  58. Jiang X., Leidi E.O., Pardo J.M. How do vacuolar NHX exchangers function in plant salt tolerance? // Plant Signal. Behav. 2010. V. 5. P. 792–795.
  59. Nieves-Cordones M., Alemán F., Martínez V., Rubio F. The Arabidopsis thaliana HAK5 K+ transporter is required for plant growth and K+ acquisition from low K+ solutions under saline conditions // Mol. Plant. 2010. V. 3. P. 326–333.
  60. Shabala S., Cuin T.A. Potassium transport and plant salt tolerance // Physiol. Plant. 2008. V. 133. P. 651–669.
  61. Deolu-Ajayi A.O., Meyer A.J., Haring M.A., Julkowska M.M., Testerink C. Root halotropism in plants: tolerance or escape? // Rhizosphere. 2024. V. 33. P. 101002. https://doi.org/10.1016/j.rhisph.2024.101002
  62. Cellier F., Conéjéro G., Ricaud L., et al. Characterization of AtCHX17, a member of the cation/H+ exchangers, CHX family, from Arabidopsis thaliana suggests a role in K+ homeostasis // Plant J. 2004. V. 39. P. 834–846.
  63. Hall D., Evans A.R., Newbury H.J., Pritchard J. Functional analysis of CHX21: a putative sodium transporter in Arabidopsis // J. Exp. Bot. 2006. V. 57. P. 1201–1210.
  64. Feng W., Lindner H., Robbins N.E., Dinneny J.R. growing out of stress: the role of cell- and organ-scale growth control in plant water-stress responses // Plant Cell. 2016. V. 28. P. 1769–1782.
  65. Cosgrove D.J. Diffuse growth of plant cell walls // Plant Physiol. 2018. V. 176. P. 16–27.
  66. Zwiewka M., Nodzyński T., Robert S., Vanneste S., Friml J. Osmotic stress modulates the balance between exocytosis and clathrin-mediated endocytosis in Arabidopsis thaliana // Mol. Plant. 2015. V. 8. P. 1175–1187.
  67. Flowers T.J., Munns R., Colmer T.D. Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes // Ann. Bot. 2015. V. 115. P. 419–431.
  68. Shabala S., White R.G., Djordjevic M.A., Ruan Y.-L., Mathesius U. Root-to-shoot signalling: integration of diverse molecules, pathways and functions // Funct. Plant Biol. 2016. V. 43. P. 87–104.
  69. Demidchik V., Shabala S., Isayenkov S., Cuin T.A., Pottosin I. Calcium transport across plant membranes: mechanisms and functions // New Phytol. 2018. V. 220. P. 49–69. https://doi.org/10.1111/nph.15266
  70. Yang X., Bassham D.C. New insight into the mechanism and function of autophagy in plant cells // Int. Rev. Cell Mol. Biol. 2015. V. 320. P. 1–40.
  71. Pu Y., Luo X., Bassham D.C. TOR-dependent and-independent pathways regulate autophagy in Arabidopsis thaliana // Front Plant Sci. 2017. V. 8. P. 1204.
  72. Wang X., Chen Z., Sui N. Sensitivity and responses of chloroplasts to salt stress in plants // Front. Plant Sci. 2024. V. 15. P. 1374086. https://doi.org/10.3389/fpls.2024.1374086
  73. Liu Y., Bassham D.C. Autophagy: pathways for self-eating in plant cells // Annu. Rev. Plant Biol. 2012. V. 63. P. 215.
  74. Zhou X.M., Zhao P., Wang W., et al. A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues // DNA res. 2015. V. 22. P. 245–257. https://doi.org/10.1093/dnares/
  75. Zhai Y., Guo M., Wang H., et al. Autophagy, a conserved mechanism for protein degradation, responds to heat, and other abiotic stresses in Capsicum annuum L. // Front. Plant Sci. 2016. V. 7. P. 131. https://doi.org/10.3389/fpls.2016.00131
  76. Avin-Wittenberg T. Autophagy and its role in plant abiotic stress management // Plant Cell Envir. 2019. V. 42. P. 1045–1053. https://doi.org/10.1111/pce.13404.
  77. Floyd B.E., Pu Y., Soto-Burgos J., Bassham D.C. To live or die: autophagy in plants // Plant Prog. Cell Death. V. 2015. P. 269–300.
  78. Petersen M., Avin-Wittenberg T., Bassham D.C., et al. Autophagy in plants // Autophagy Reports. 2024. V. 3. P. 2395731.
  79. Huh G.-H., Damsz B., Matsumoto T.K., et al. Salt causes ion disequilibrium-induced programmed cell death in yeast and plants // Plant J. 2002. V. 29. P. 649–659. https://doi.org/10.1046/j.0960-7412.2001.01247.x
  80. Luo L., Zhang P., Zhu R., et al. Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis // Front Plant Sci. 2017. V. 8. P. 1459. https://doi.org/10.3389/fpls.2017.01459
  81. Marshall R.S., Vierstra R.D. Autophagy: the master of bulk and selective recycling // Annu. Rev. Plant Biol. 2018. V. 69. P. 173–208.
  82. Xiang L., Etxeberria E., Van den Ende W. Vacuolar protein sorting mechanisms in plants // FEBS J. 2013. V. 280. P. 979–993.
  83. Liu Y., Xiong Y., Bassham D.C. Autophagy is required for tolerance of drought and salt stress in plants // Autophagy. 2009. V. 5. P. 954–963.
  84. Zhou J., Wang J., Cheng Y., et al. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses // PLoS genet. 2013. V. 9. P. e1003196. https://doi.org/10.1371/journal.pgen.1003196
  85. Michaeli S., Honig A., Levanony H., Peled-Zehavi H., Galili G. Arabidopsis ATg8-INTERACTINg PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole // Plant Cell. 2014. V. 26. P. 4084–4101. https://doi.org/10.1105/tpc.114.129999
  86. Pu Y., Soto-Burgos J., Bassham D.C. Regulation of autophagy through SnRK1 and TOR signaling pathways // Plant Signal. Behav. 2017. V. 12. P. e1395128.
  87. Xu Y., Chen S.Y., Ross K.N., Balk S.P. Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins // Cancer Res. 2006. V. 66. P. 7783–7792. https://doi.org/10.1158/0008-5472.CAN-05-4472
  88. Ragel P., Ródenas R., García-Martín E., et al. The CBL-interacting protein kinase CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots // Plant Physiol. 2015. V. 169. P. 2863–2873. https://doi.org/10.1104/pp.15.01401
  89. Li K.L., Xue H., Tang R.J., Luan S. TORC pathway intersects with a calcium sensor kinase network to regulate potassium sensing in Arabidopsis // Proc. Natl. Acad. Sci. u. S. A. 2023. V. 120. P. e2316011120. https://doi.org/10.1073/pnas.2316011120
  90. Tang T.M.S., Luk L.Y.P. Asparaginyl endopeptidases: enzymology, applications and limitations // Org. Biomol. Chem. 2021. V. 19. P. 5048–5062.
  91. Qi H., Xia F.N., Xie L.J., et al. TRAF family proteins regulate autophagy dynamics by modulating AuTOPHAgY PROTEIN6 stability in Arabidopsis // Plant Cell. 2018. V. 29. P. 890–911. https://doi.org/10.1105/tpc.17.00056
  92. Baena-González E., Lunn J.E. SnRK1 and trehalose 6-phosphate-two ancient pathways converge to regulate plant metabolism and growth // COPB. 2020. V. 55. P. 52–59.
  93. Van Leene J., Eeckhout D., Gadeyne A., et al. Mapping of the plant SnRK1 kinase signalling network reveals a key regulatory role for the class II T6P synthase-like proteins. // Nat. Plants. 2022. V. 8. P. 1245–1261. https://doi.org/10.1038/s41477-022-01269-w
  94. Blanford J., Zhai Z., Baer M.D., et al. Molecular mechanism of trehalose 6-phosphate inhibition of the plant metabolic sensor kinase SnRK1 // Sci. Adv. 2022. V. 10. P. eadn0895. https://doi.org/10.1126/sciadv.adn0895
  95. Yang C., Li X., Yang L., et al. A positive feedback regulation of SnRK1 signaling by autophagy in plants // Mol. Plant. 2023. V. 16. P. 1192–1211. https://doi.org/10.1016/j.molp.2023.07.001
  96. Soto-Burgos J., Bassham D.C. SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana // PLoS ONE. 2017. V. 12. P. e0182591.
  97. Chen L., Su Z.Z., Huang L., et al. genetic analyses of the Arabidopsis ATg1 kinase complex reveal both kinase-dependent and independent autophagic routes during fixed-carbon starvation // Plant Cell. 2019. V. 31. P. 2973–2995. https://doi.org/10.3389/fpls.2017.01201
  98. Huang X., Zheng C., Liu F., et al. genetic analyses of the Arabidopsis ATg1 kinase complex reveal both kinase-dependent and independent autophagic routes during fixed-carbon starvation // Plant Cell. 2019. V. 31. P. 2973–2995.
  99. Hasan M.M., Liu X.D., Waseem M., et al. ABA activated SnRK2 kinases: an emerging role in plant growth and physiology // Plant Signal. Behav. 2022. V. 17. P. 2071024.
  100. Xiong Y., Contento A.L., Nguyen P.Q., Bassham D.C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis // Plant Physiol. 2007. V. 143. P. 291–299. https://doi.org/10.1104/pp.106.092106
  101. Scherz-Shouval R., Shvets E., Fas E., et al. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4 // EMBO J. 2007. V. 26. P. 1749–1760. https://doi.org/10.1038/sj.emboj.7601623
  102. Hayward A.P., Tsao J., Dinesh-Kumar S.P. Autophagy and plant innate immunity: Defense through degradation // Semin. Cell Dev. Biol. 2009. V. 20. P. 1041–1047. https://doi.org/10.1016/j.semcdb.2009.04.012
  103. Rosenberger C.L., Chen J. To grow or not to grow: TOR and SnRK2 coordinate growth and stress response in Arabidopsis // Mol. Cell. 2018. V. 69. P. 3–4. https://doi.org/10.1016/j.molcel.2017.12.013
  104. Signorelli S., Tarkowski Ł.P., Van den Ende W., Bassham D.C. Linking autophagy to abiotic and biotic stress responses // Trends Plant Sci. 2019. V. 24. P. 413–430. https://doi.org/10.1016/j.tplants.2019.02.001
  105. Mallén-Ponce M.J., Pérez-Pérez M.E. Redox-mediated activation of ATg3 promotes ATg8 lipidation and autophagy progression in Chlamydomonas reinhardtii // Plant Physiol. 2023. V. 194. P. 359–375. https://doi.org/10.1093/plphys/kiad520
  106. Goussi R., Manaa A., Derbali W., et al. Comparative analysis of salt stress, duration and intensity, on the chloroplast ultrastructure and photosynthetic apparatus in Thellungiella salsuginea // J. Photochem. Photobiol. B: Biol. 2018. V. 183. P. 275–287. https://doi.org/10.1016/j.jphotobiol.2018.04.047
  107. Nakamura S., Hidema J., Sakamoto W., Ishida H., Izumi M. Selective elimination of membrane-damaged chloroplasts via microautophagy // Plant Physiol. 2018. V. 177. P. 1007–1026. https://doi.org/10.1104/pp.18.00444
  108. Wan C., Ling Q. Functions of autophagy in chloroplast protein degradation and homeostasis // Front. Plant Sci. 2022. V. 13. P. 993215. https://doi.org 10.3389/fpls.2022.993215
  109. Wijerathna-Yapa A., Signorelli S., Fenske R., et al. Autophagy mutants show delayed chloroplast development during de-etiolation in carbon limiting conditions // Plant J. 2021. V. 108. P. 459–477. https://doi.org/10.1111/tpj.15452
  110. Wan C., Zhang H., Cheng H., et al. Selective autophagy regulates chloroplast protein import and promotes plant stress tolerance // EMBO J. 2023. V. 42. P. e112534. https://doi.org/10.15252/embj.2022112534
  111. Shabala S., Cuin T.A., Prismall L., Nemchinov L.G. Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress // Planta. 2007. V. 227. P. 189–197. https://doi.org/10.1007/s00425-007-0606-z
  112. Fedoreyeva L.I., Lazareva E.M., Shelepova O.V., Baranova E.N., Kononenko N.V. Salt-induced autophagy and programmed cell death in wheat // Agronomy. 2022. V. 12. P. 1909.
  113. Yue J.Y., Wang Y.J., Jiao J.L., Wang H.Z. Silencing of ATg2 and ATg7 promotes programmed cell death in wheat via inhibition of autophagy under salt stress // Ecotoxicol. Environ. Saf. 2021. V. 225. P. 112761. https://doi.org/10.1016/j.ecoenv.2021.112761
  114. Tabur S., Demir K. Protective roles of exogenous polyamines on chromosomal aberrations in Hordeum vulgare exposed to salinity // Biologia. 2010. V. 65. P. 947–953. https://doi.org/10.2478/s11756-010-0118-3
  115. Yazdani M., Mahdieh M. Salinity induced apoptosis in root meristematic cells of rice // IJBBB. 2012. V. 2.
  116. Egorova V.P., Lo Y.S., Dai H. Programmed cell death induced by heat shock in mung bean seedlings // Bot. Stud. 2011. V. 52. P. 73–78.
  117. Fan T., Xing T. Heat shock induces programmed cell death in wheat leaves // Biol. Plant. 2004. V. 48. P. 389–394.
  118. Cvjetko P., Balen B., Peharec Štefanić P., et al. Dynamics of heat-shock induced DNA damage and repair in senescent tobacco plants // Biol. Plant. 2014. V. 58. P. 71–79.
  119. Katsuhara M., Kawasaki T. Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots // Plant Cell Physiol. 1996. V. 37. P. 169–173.
  120. Katsuhara M. Apoptosis-like cell death in barley roots under salt stress // Plant Cell Physiol. 1997. V. 38. P. 1091–1093. https://doi.org/10.1093/oxfordjournals.pcp.a02927
  121. Sihi O., Sharma O.K., Pathak H., et al. Effect of organic farming on productivity and quality of basmati rice // Oryza. 2012. V. 49. P. 24–29.
  122. Oney-Birol S. Exogenous L-carnitine promotes plant growth and cell division by mitigating genotoxic damage of salt stress // Sci. Rep. 2019. V. 9. P. 17229.
  123. Jabeen Z., Hussain N., Wu D., et al. Difference in physiological and biochemical responses to salt stress between Tibetan wild and cultivated barleys // Acta Physiol. Plant. 2015. V. 37. P. 180. https://doi.org/10.1007/s11738-015-1920-x

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Russian Academy of Sciences

Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).