Skip to main content

Advertisement

Log in

SALT-INDUCED CHLOROPLAST PROTEIN (SCP) is Involved in Plant Tolerance to Salt Stress in Arabidopsis

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Soil salinization threats the agricultural production and food security worldwide. Salt stress induced plant senescence and chloroplast degradation. However, it remains largely unknown how the chloroplast-localized proteins affect plant response to salt stress. Here, we characterized a novel gene (At5g39520) in Arabidopsis, which is induced by salt stress and encodes a chloroplast-localized protein. Thus, this gene was named SALT-INDUCED CHLOROPLAST PROTEIN (SCP). A T-DNA insertion mutant of SCP gene (scp-1) showed the enhanced tolerance to salt stress, as indicated by the increased survival rates, fresh weights and chlorophyll contents compared with wild type plants under salt treatment. Salt-induced leaf senescence was also delayed in scp-1 mutant. The scp-1 complementation line and SCP overexpression lines displayed the hypersensitivity to salt stress. The qRT-PCR analysis indicated that the transcripts of CHLOROPLAST VESICULATION (CV), which mediates stress-induced chloroplast degradation, were altered in scp-1 mutant and SCP overexpression lines. Taken together, our results suggest that SCP gene plays a negative role in response to salt stress and has potential application for genetic modification of improving plant tolerance to salt stress.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bassham DC (2009) Function and regulation of macroautophagy in plants. Biochim Biophys Acta 1793:1397–1403

    Article  CAS  Google Scholar 

  • Carrion CA, Costa ML, Martinez DE, Mohr C, Humbeck K, Guiamet JJ (2013) In vivo inhibition of cysteine proteases provides evidence for the involvement of ‘senescence-associated vacuoles’ in chloroplast protein degradation during dark-induced senescence of tobacco leaves. J Exp Bot 64:4967–4980

    Article  CAS  Google Scholar 

  • Hanin M, Ebel C, Ngom M, Laplaze L, Masmoudi K (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Frontiers in Plant Science 7:1787

    Article  Google Scholar 

  • Honig A, Avin-Wittenberg T, Ufaz S, Galili G (2012) A new type of compartment, defined by plant-specific Atg8-interacting proteins, is induced upon exposure of Arabidopsis plants to carbon starvation. Plant Cell 24:288–303

    Article  CAS  Google Scholar 

  • Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77

    Article  CAS  Google Scholar 

  • Hortensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162

    Article  CAS  Google Scholar 

  • Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Molecular Biology 43:103–111

    Article  CAS  Google Scholar 

  • Ishida H, Wada S (2009) Autophagy of whole and partial chloroplasts in individually darkened leaves: a unique system in plants? Autophagy 5:736–737

    Article  CAS  Google Scholar 

  • Ishida H, Yoshimoto K (2008) Chloroplasts are partially mobilized to the vacuole by autophagy. Autophagy 4:961–962

    Article  CAS  Google Scholar 

  • Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T (2008) Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–155

    Article  CAS  Google Scholar 

  • Izumi M, Ishida H (2011) The changes of leaf carbohydrate contents as a regulator of autophagic degradation of chloroplasts via Rubisco-containing bodies during leaf senescence. Plant Signal Behav 6:685–687

    Article  CAS  Google Scholar 

  • Izumi M, Wada S, Makino A, Ishida H (2010) The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154:1196–1209

    Article  CAS  Google Scholar 

  • Kamranfar I, Xue GP, Tohge T, Sedaghatmehr M, Fernie AR, Balazadeh S, Mueller-Roeber B (2018) Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence. New Phytologist 218:1543–1557

    Article  CAS  Google Scholar 

  • Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology 63:215–237

    Article  CAS  Google Scholar 

  • Madhava Rao KV, Raghavendra AS, Janardhan Reddy K (2006) Physiology and Molecular Biology of Salinity Stress Tolerance in Plants. Current Science 86:407–421

    Google Scholar 

  • Martinez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol (Stuttg) 10 Suppl 10:15–22

    Article  CAS  Google Scholar 

  • Michaeli S, Honig A, Levanony H, Peled-Zehavi H, Galili G (2014) Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26:4084–4101

    Article  CAS  Google Scholar 

  • Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annual Review of Plant Biology 61:443–462

    Article  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual review of plant biology 59:651–681

    Article  CAS  Google Scholar 

  • Ohsumi Y (2001) Molecular dissection of autophagy two ubiquitinlike systems. Nature Reviews Molecular Cell Biology 2:211–216

    Article  CAS  Google Scholar 

  • Otegui MS (2018) Vacuolar degradation of chloroplast components: autophagy and beyond. J Exp Bot 69:741–750

    Article  CAS  Google Scholar 

  • Otegui MS, Noh YS, Martinez DE, Vila Petroff MG, Staehelin LA, Amasino RM, Guiamet JJ (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J 41:831–844

    Article  CAS  Google Scholar 

  • Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnology Journal 9:747–758

    Article  CAS  Google Scholar 

  • Perez-Patricio M, Camas-Anzueto JL, Sanchez-Alegria A, Aguilar-Gonzalez A, Gutierrez-Miceli F, Escobar-Gomez E, Voisin Y, Rios-Rojas C, Grajales-Coutino R (2018) Optical method for estimating the chlorophyll contents in plant leaves. Sensors (Basel) 18:650

    Article  Google Scholar 

  • Reumann S, Voitsekhovskaja O, Lillo C (2010) From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247:233–256

    Article  Google Scholar 

  • Rivero RM, Gimeno J, Van Deynze A, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing PSARK::IPT prevents the degradation of photosynthetic protein complexes during drought. Plant & Cell Physiology 51:1929–1941

    Article  CAS  Google Scholar 

  • Sade N, Umnajkitikorn K, Rubio Wilhelmi MDM, Wright M, Wang S, Blumwald E (2018) Delaying chloroplast turnover increases water-deficit stress tolerance through the enhancement of nitrogen assimilation in rice. J Exp Bot 69:867–878

    Article  CAS  Google Scholar 

  • Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andres CB, Kessler F, Hortensteiner S, Paek NC (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24:507–518

    Article  CAS  Google Scholar 

  • Spitzer C, Li F, Buono R, Roschzttardtz H, Chung T, Zhang M, Osteryoung KW, Vierstra RD, Otegui MS (2015) The endosomal protein charged multivesicular body protein1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 27:391–402

    Article  CAS  Google Scholar 

  • Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiology 149:885–893

    Article  CAS  Google Scholar 

  • Wang S, Blumwald E (2014) Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell 26:4875–4888

    Article  CAS  Google Scholar 

  • Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, Huang L, Du Y, Hong Y, Tang D, Liu Y (2013) Autophagy contributes to leaf starch degradation. Plant Cell 25:1383–1399

    Article  CAS  Google Scholar 

  • Xie Q, Michaeli S, Peled-Zehavi H, Galili G (2015) Chloroplast degradation: one organelle, multiple degradation pathways. Trends Plant Sci 20:264–265

    Article  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53:247–273

    Article  CAS  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  Google Scholar 

  • Zhuang X, Jiang L (2019) Chloroplast degradation: multiple routes into the vacuole. Frontiers in Plant Science 10:359

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by National Natural Science Foundation of China (Grant No. 31871354), the Hundred Talents Program (Chinese Academy of Sciences), Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences (Y4ZK111B01), and Key Program for International S&T Cooperation from Science & Technology Department of Sichuan Province (2017HH0025).

Author information

Authors and Affiliations

Authors

Contributions

YZ and SW designed the experiments; YZ, YL, YL, MW, YT, PL, ZL, HL, and WH conducted the experiments; YZ and SW analyzed the data; YZ and S W wrote the manuscript. All the authors agreed on the contents of the paper and post no conflicting interest.

Corresponding author

Correspondence to Songhu Wang.

Additional information

Supporting Information

Fig S1. Gene Co-expression Network showed that SCP is co-expressed with CV

Supporting Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhuang, Y., Liu, Y., Li, Y. et al. SALT-INDUCED CHLOROPLAST PROTEIN (SCP) is Involved in Plant Tolerance to Salt Stress in Arabidopsis. J. Plant Biol. 62, 429–435 (2019). https://doi.org/10.1007/s12374-019-0356-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-019-0356-z

Keywords

Navigation