Calcium-dependent protein kinase 2 plays a positive role in the salt stress response in potato

Grossi, Cecilia Eugenia María; Santin, Franco; Quintana, Silverio Andrés; Fantino, Elisa; Ulloa, Rita María

doi:10.1007/s00299-021-02676-7

Calcium-dependent protein kinase 2 plays a positive role in the salt stress response in potato

Original Article
Published: 02 March 2021

Volume 41, pages 535–548, (2022)
Cite this article

Plant Cell Reports Aims and scope Submit manuscript

Cecilia Eugenia María Grossi¹,
Franco Santin¹^nAff3,
Silverio Andrés Quintana¹^nAff4,
Elisa Fantino¹^nAff5 &
…
Rita María Ulloa ORCID: orcid.org/0000-0002-9355-4621^1,2

1327 Accesses
14 Citations
1 Altmetric
Explore all metrics

Abstract

Key message

StCDPK2 is an early player in the salt stress response in potato plants; its overexpression promoted ROS scavenging, chlorophyll stability, and the induction of stress-responsive genes conferring tolerance to salinity.

Abstract

The salinity of soils affects plant development and is responsible for great losses in crop yields. Calcium-dependent protein kinases (CDPKs) are sensor–transducers that decode Ca²⁺ signatures triggered by abiotic stimuli and translate them into physiological responses. Histochemical analyses of potato plants harboring StCDPK2 promoter fused to the reporter gene β-glucuronidase (Pro_StCDPK2:GUS) revealed that GUS activity was high in the leaf blade and veins, it was restricted to root tips and lateral root primordia, and was observed upon stolon swelling. Comparison with Pro_StCDPK1:GUS and Pro_StCDPK3:GUS plants revealed their differential activities in the plant tissues. Pro_StCDPK2:GUS plants exposed to high salt presented enhanced GUS activity in roots which correlated with the numerous stress-responsive sites predicted in its promoter sequence. Moreover, StCDPK2 expression increased in in vitro potato plants after 2 h of high salt exposure and in greenhouse plants exposed to a dynamic stress condition. As inferred from biometric data and chlorophyll content, plants that overexpress StCDPK2 were more tolerant than wild-type plants when exposed to high salt. Overexpressing plants have a more efficient antioxidant system; they showed reduced accumulation of peroxide and higher catalase activity under salt conditions, and enhanced expression of WRKY6 and ERF5 transcription factors under control conditions. Our results indicate that StCDPK2 is an early player in the salt stress response and support a positive correlation between StCDPK2 overexpression and tolerance towards salt stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

StCaM2, a calcium binding protein, alleviates negative effects of salinity and drought stress in tobacco

Article 24 February 2021

Overexpression of a tonoplast Na+/H+ antiporter from the halophytic shrub Nitraria sibirica improved salt tolerance and root development in transgenic poplar

Article 31 October 2020

Downregulation of stress-associated protein 1 (PagSAP1) increases salt stress tolerance in poplar (Populus alba × P. glandulosa)

Article 23 February 2018

Data availability

All data generated or analyzed during this study are included in this article (and its supplementary information files). The sequences that support the findings of this study are openly available in GenBank with the MK391002.1, NM_001288442.1, MK439960.1, and MN642059.1 accession numbers.

Abbreviations

A :: Net assimilation rate at saturating irradiance
ABA:: Abscisic acid
ABF:: ABA-binding factor
ABRE B:: ABA-responsive element B
bHLH:: Basic helix–loop–helix
bZIP:: Basic leucine zipper
CAT:: Catalase
CDPK:: Calcium-dependent protein kinase
CDS:: Coding sequence
Chl a :: Chlorophyll a
Chl b :: Chlorophyll b
Ci:: Intercellular CO₂ concentration
E :: Transpiration rate
Ec:: Electric conductivity
FPKM:: Fragments per kilobase exon model per million mapped reads
FW:: Fresh weight
gs:: Stomatal conductance
GUS:: β-Glucuronidase
MADF:: Myb/SANT-like domain in Adf-1
OE:: Overexpressing
ROS:: Reactive oxygen species
RT-qPCR:: RT-quantitative polymerase chain reaction
TF:: Transcription factor
Vmax:: Maximal velocity
WT:: Wild-type

References

Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Article CAS PubMed Google Scholar
Arnon DI (1949) Copper enzymes in isolated chloroplasts. polyphenoloxidase in beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Article CAS PubMed PubMed Central Google Scholar
Asano T, Hakata M, Nakamura H et al (2011) Functional characterisation of OsCPK21, a calcium-dependent protein kinase that confers salt tolerance in rice. Plant Mol Biol 75:179–191. https://doi.org/10.1007/s11103-010-9717-1
Article CAS PubMed Google Scholar
Asano T, Hayashi N, Kobayashi M et al (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36. https://doi.org/10.1111/j.1365-313X.2011.04766.x
Article CAS PubMed Google Scholar
Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes (Basel) 10:1–23. https://doi.org/10.3390/genes10100771
Article CAS Google Scholar
Bernstein N, Kafkafi U (2002) Root growth under salinity stress. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half, 3rd edn. Marcel Dekker, New York, pp 787–805
Chapter Google Scholar
Borkiewicz L, Polkowska-Kowalczyk L, Cieśla J et al (2020) Expression of maize calcium-dependent protein kinase (ZmCPK11) improves salt tolerance in transgenic Arabidopsis plants by regulating sodium and potassium homeostasis and stabilizing photosystem II. Physiol Plant 168:38–57. https://doi.org/10.1111/ppl.12938
Article CAS PubMed Google Scholar
Caldiz DO, Gaspari FJ, Haverkort AJ, Struik PC (2001) Agro-ecological zoning and potential yield of single or double cropping of potato in Argentina. Agric For Meteorol. https://doi.org/10.1016/S0168-1923(01)00231-3
Article Google Scholar
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Article CAS PubMed Google Scholar
Choi H, Park H-J, Park JH et al (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761. https://doi.org/10.1104/pp.105.069757
Article CAS PubMed PubMed Central Google Scholar
Chow C-N, Zheng H-Q, Wu N-Y et al (2016) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44:D1154–D1160. https://doi.org/10.1093/nar/gkv1035
Article CAS PubMed Google Scholar
Ding Y, Cao J, Ni L et al (2013) ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signalling in maize. J Exp Bot 64:871–884. https://doi.org/10.1093/jxb/ers366
Article CAS PubMed Google Scholar
Elkhatib HA, Elkhatib EA, Allah AMK, El-Sharkawy AM (2004) Yield response of salt-stressed potato to potassium fertilization: a preliminary mathematical model. J Plant Nutr 27:111–122. https://doi.org/10.1081/PLN-120027550
Article CAS Google Scholar
Fantino E, Segretin ME, Santin F et al (2017) Analysis of the potato calcium-dependent protein kinase family and characterization of StCDPK7, a member induced upon infection with Phytophthora infestans. Plant Cell Rep 36:1137–1157. https://doi.org/10.1007/s00299-017-2144-x
Article CAS PubMed Google Scholar
Ghosh A, Pareek A, Singla-Pareek SL (2015) Leaf disc stress tolerance assay for tobacco. Bio-protocol 5:e1440. https://doi.org/10.21769/BioProtoc.1440
Article Google Scholar
Giammaria V, Grandellis C, Bachmann S et al (2011) StCDPK2 expression and activity reveal a highly responsive potato calcium-dependent protein kinase involved in light signalling. Planta 233:593–609. https://doi.org/10.1007/s00425-010-1319-2
Article CAS PubMed Google Scholar
Grandellis C, Giammaria V, Bialer M et al (2012) The novel Solanum tuberosum calcium dependent protein kinase, StCDPK3, is expressed in actively growing organs. Planta 236:1831–1848. https://doi.org/10.1007/s00425-012-1732-9
Article CAS PubMed Google Scholar
Grossi CEM, Fantino E, Serral F et al (2020) Methylobacterium sp. 2A is a plant growth-promoting rhizobacteria that has the potential to improve potato crop yield under adverse conditions. Front Plant Sci 11:1–15. https://doi.org/10.3389/fpls.2020.00071
Article Google Scholar
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom. https://doi.org/10.1155/2014/701596
Article Google Scholar
Han EH, Petrella DP, Blakeslee JJ (2017) “Bending” models of halotropism: Incorporating protein phosphatase 2A, ABCB transporters, and auxin metabolism. J Exp Bot 68:3071–3089. https://doi.org/10.1093/jxb/erx127
Article CAS PubMed Google Scholar
Hasanuzzaman M, Hossain MA, da Silva JAT et al (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Venkateswarlu B, Shanker A, Shanker C, Maheswari M (eds) Crop stress and its management: perspectives and strategies. Springer, Dordrecht
Google Scholar
Hichri I, Muhovski Y, Žižková E et al (2017) The Solanum lycopersicum WRKY3 transcription factor SLWRKY3 is involved in salt stress tolerance in tomato. Front Plant Sci 8:1–18. https://doi.org/10.3389/fpls.2017.01343
Article Google Scholar
Hirsch CD, Hamilton JP, Childs KL et al (2014) Spud DB: a resource for mining sequences, genotypes, and phenotypes to accelerate potato breeding. Plant Genome 7:plantgenome2013.12.0042. https://doi.org/10.3835/plantgenome2013.12.0042
Article CAS Google Scholar
Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57(12):1332–1334. https://doi.org/10.1139/b79-163
Article CAS Google Scholar
Imbellone PA, Giménez JE, Panigatti JL (2010) Suelos de la Región Pampeana: Procesos de formación. Ed. INTA, Buenos Aires
Google Scholar
Isayenkov SV, Maathuis FJM (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci 10:80. https://doi.org/10.3389/fpls.2019.00080
Article PubMed PubMed Central Google Scholar
Jaarsma R, de Vries RSM, de Boer AH (2013) Effect of salt stress on growth, Na⁺ accumulation and proline metabolism in potato (Solanum tuberosum) cultivars. PLoS ONE. https://doi.org/10.1371/journal.pone.0060183
Article PubMed PubMed Central Google Scholar
Jakoby M, Weisshaar B, Dröge-Laser W et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111. https://doi.org/10.1016/S1360-1385(01)02223-3
Article CAS PubMed Google Scholar
Jiang K, Moe-Lange J, Hennet L, Feldman LJ (2016) Salt stress affects the redox status of arabidopsis root meristems. Front Plant Sci 7:1–10. https://doi.org/10.3389/fpls.2016.00081
Article Google Scholar
Junglee S, Urban L, Sallanon H, Lopez-Lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am J Anal Chem 05:730–736. https://doi.org/10.4236/ajac.2014.511081
Article CAS Google Scholar
Khan SA, Li MZ, Wang SM, Yin HJ (2018) Revisiting the role of plant transcription factors in the battle against abiotic stress. Int J Mol Sci. https://doi.org/10.3390/ijms19061634
Article PubMed PubMed Central Google Scholar
Khenifi ML, Boudjeniba M, Kameli A (2011) Effects of salt stress on micropropagation of potato (Solanum tuberosum L.). Afr J Biotechnol 10:7840–7845. https://doi.org/10.5897/AJB10.982
Article Google Scholar
Kudla J, Becker D, Grill E et al (2018) Advances and current challenges in calcium signaling. New Phytol 218:414–431. https://doi.org/10.1111/nph.14966
Article PubMed Google Scholar
Kumpf RP, Nowack MK (2015) The root cap: a short story of life and death. J Exp Bot 66:5651–5662. https://doi.org/10.1093/jxb/erv295
Article CAS PubMed Google Scholar
Li X, Guo C, Ahmad S et al (2019) Systematic analysis of MYB family genes in potato and their multiple roles in development and stress responses. Biomolecules 9:1–21. https://doi.org/10.3390/biom9080317
Article CAS Google Scholar
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Article CAS PubMed Google Scholar
Lynch T, Erickson BJ, Finkelstein RR (2012) Direct interactions of ABA-insensitive(ABI)-clade protein phosphatase(PP)2Cs with calcium-dependent protein kinases and ABA response element-binding bZIPs may contribute to turning off ABA response. Plant Mol Biol 80:647–658. https://doi.org/10.1007/s11103-012-9973-3
Article CAS PubMed Google Scholar
Manishankar P, Wang N, Köster P et al (2018) Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69:4215–4226. https://doi.org/10.1093/jxb/ery201
Article CAS Google Scholar
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, San Diego
Google Scholar
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Article CAS Google Scholar
Moore CA, Bowen HC, Scrase-Field S et al (2002) The deposition of suberin lamellae determines the magnitude of cytosolic Ca²⁺ elevations in root endodermal cells subjected to cooling. Plant J 30:457–465. https://doi.org/10.1046/j.1365-313X.2002.01306.x
Article CAS PubMed Google Scholar
Muñiz García MN, Giammaria V, Grandellis C et al (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235:761–778. https://doi.org/10.1007/s00425-011-1540-7
Article CAS PubMed Google Scholar
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Article CAS Google Scholar
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Article CAS Google Scholar
Pan Y, Seymour GB, Lu C et al (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31:349–360. https://doi.org/10.1007/s00299-011-1170-3
Article CAS PubMed Google Scholar
Raíces M, Ulloa RM, MacIntosh GC et al (2003) StCDPK1 is expressed in potato stolon tips and is induced by high sucrose concentration. J Exp Bot 54:2589–2591. https://doi.org/10.1093/jxb/erg282
Article PubMed Google Scholar
Saijo Y, Hata S, Kyozuka J et al (2000) Over-expression of a single Ca²⁺-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327. https://doi.org/10.1046/j.1365-313X.2000.00787.x
Article CAS PubMed Google Scholar
Santin F, Bhogale S, Fantino E et al (2017) Solanum tuberosum StCDPK1 is regulated by miR390 at the posttranscriptional level and phosphorylates the auxin efflux carrier StPIN4 in vitro, a potential downstream target in potato development. Physiol Plant 159:244–261. https://doi.org/10.1111/ppl.12517
Article CAS PubMed Google Scholar
Shavrukov Y (2013) Salt stress or salt shock: which genes are we studying? J Exp Bot 64(1):119–127. https://doi.org/10.1093/jxb/ers316
Article CAS PubMed Google Scholar
Smirnoff N (1996) BOTANICAL BRIEFING: the function and metabolism of ascorbic acid in plants. Ann Bot 78(6):661–669. https://doi.org/10.1006/anbo.1996.0175
Article CAS Google Scholar
Tracy FE, Gilliham M, Dodd AN et al (2008) NaCl-induced changes in cytosolic free Ca²⁺ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant Cell Environ 31:1063–1073. https://doi.org/10.1111/j.1365-3040.2008.01817.x
Article CAS PubMed Google Scholar
Vivek PJ, Resmi MS, Sreekumar S et al (2017) Calcium-dependent protein kinase in ginger binds with importin-α through its junction domain for nuclear localization, and further interacts with NAC transcription factor. Front Plant Sci 7:1–13. https://doi.org/10.3389/fpls.2016.01909
Article Google Scholar
Wang CT, Song W (2013) Calcium-dependent protein kinase gene ZmCPK12 from maize confers tolerance to drought and salt stresses in transgenic plants. Acta Physiol Plant 35:1659–1666. https://doi.org/10.1007/s11738-012-1208-3
Article CAS Google Scholar
Wang J, Cheng G, Wang C et al (2017) The bHLH transcription factor CgbHLH001 is a potential interaction partner of CDPK in halophyte Chenopodium glaucum. Sci Rep 7:1–16. https://doi.org/10.1038/s41598-017-06706-x
Article CAS PubMed PubMed Central Google Scholar
Wang B, Zhang Y, Bi Z et al (2019) Impaired function of the calcium-dependent protein kinase, OsCPK12, leads to early senescence in rice (Oryza sativa L.). Front Plant Sci 10:1–12. https://doi.org/10.3389/fpls.2019.00052
Article Google Scholar
Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calcium-independent kinase member of the Zea maysCDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38:544–558. https://doi.org/10.1111/pce.12414
Article CAS PubMed Google Scholar
Wen F, Ye F, Xiao Z et al (2020) Genome-wide survey and expression analysis of calcium-dependent protein kinase (CDPK) in grass Brachypodium distachyon. BMC Genom 21:1–17. https://doi.org/10.1186/s12864-020-6475-6
Article CAS Google Scholar
Xiong TC, Ronzier E, Sanchez F et al (2014) Imaging long distance propagating calcium signals in intact plant leaves with the BRET-based GFP-aequorin reporter. Front Plant Sci 5:1–13. https://doi.org/10.3389/fpls.2014.00043
Article Google Scholar
Xu P, Liu Z, Fan X et al (2013) De novo transcriptome sequencing and comparative analysis of differentially expressed genes in Gossypium aridum under salt stress. Gene 525:26–34. https://doi.org/10.1016/j.gene.2013.04.066
Article CAS PubMed Google Scholar
Yip Delormel T, Boudsocq M (2019) Properties and functions of calcium-dependent protein kinases and their relatives in Arabidopsis thaliana. New Phytol 224:585–604. https://doi.org/10.1111/nph.16088
Article CAS PubMed Google Scholar
Zhang Z, Ren C, Zou L et al (2018) Characterization of the GATA gene family in Vitis vinifera: genome-wide analysis, expression profiles, and involvement in light and phytohormone response. Genome 61:713–723. https://doi.org/10.1139/gen-2018-0042
Article CAS PubMed Google Scholar
Zhu SY, Yu XC, Wang XJ et al (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036. https://doi.org/10.1105/tpc.107.050666
Article CAS PubMed PubMed Central Google Scholar
Zou JJ, Li XD, Ratnasekera D et al (2015) Arabidopsis calcium-dependent protein kinase8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27:1445–1460. https://doi.org/10.1105/tpc.15.00144
Article CAS PubMed PubMed Central Google Scholar

Download references

Funding

This work was funded by CONICET (PIP 0455), Universidad de Buenos Aires (UBACYT), and Agencia Nacional de Promoción Científica y Tecnológica (PICT-2014 3018). RMU is a member of Carrera de Investigador Científico from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, Argentina) and is Associate Professor at Universidad de Buenos Aires (UBA). CEMG received a doctoral fellowship and FS and EF postdoctoral fellowships from CONICET. SAQA received a Fellowship Don Carlos Antonio López, Paraguay.

Author information

Franco Santin
Present address: Instituto de Botánica Darwinion (IBODA), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Silverio Andrés Quintana
Present address: Departamento de Biotecnología, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Asunción, San Lorenzo, Paraguay
Elisa Fantino
Present address: Laboratoire de Recherche Sur le Métabolisme Spécialisé Végétal, Département de Chimie, Biochimie et Physique, Université du Québec à Trois-Rivières, Québec, Canada

Authors and Affiliations

Laboratorio de Transducción de Señales en Plantas, Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (INGEBI), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Ciudad Autónoma de Buenos Aires (C.A.B.A., Buenos Aires, Argentina
Cecilia Eugenia María Grossi, Franco Santin, Silverio Andrés Quintana, Elisa Fantino & Rita María Ulloa
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Rita María Ulloa

Authors

Cecilia Eugenia María Grossi
View author publications
You can also search for this author in PubMed Google Scholar
Franco Santin
View author publications
You can also search for this author in PubMed Google Scholar
Silverio Andrés Quintana
View author publications
You can also search for this author in PubMed Google Scholar
Elisa Fantino
View author publications
You can also search for this author in PubMed Google Scholar
Rita María Ulloa
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

RMU conceived and designed the research. CEMG, FS, SAQA, and EF performed the experiments. FS and RMU performed computational analyses. RMU and CEMG analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Rita María Ulloa.

Ethics declarations

Conflicts of interest

The authors have no conflict of interest to declare.

Ethics approval

This work complies with ethical standards.

Consent for publication

All authors have read and approved the final manuscript.

Additional information

Communicated by Sheng Ying.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 81 KB)

Supplementary file2 (DOC 94 KB)

Supplementary file3 (DOC 93 KB)

Supplementary file4 (DOC 1606 KB)

Supplementary file5 (DOC 354 KB)

Supplementary file6 (XLSX 15 KB)

Supplementary file7 (XLSX 14 KB)

Supplementary file8 (XLSX 16 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grossi, C.E.M., Santin, F., Quintana, S.A. et al. Calcium-dependent protein kinase 2 plays a positive role in the salt stress response in potato. Plant Cell Rep 41, 535–548 (2022). https://doi.org/10.1007/s00299-021-02676-7

Download citation

Received: 20 November 2020
Accepted: 17 February 2021
Published: 02 March 2021
Issue Date: March 2022
DOI: https://doi.org/10.1007/s00299-021-02676-7

Keywords

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Calcium-dependent protein kinase 2 plays a positive role in the salt stress response in potato