Skip to main content

Advertisement

Log in

Golgi-localized cyclophilin 21 proteins negatively regulate ABA signalling via the peptidyl prolyl isomerase activity during early seedling development

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Plant possesses particular Golgi-resident cyclophilin 21 proteins (CYP21s) and the catalytic isomerase activities have a negative effect on ABA signalling gene expression during early seedling development.

Abstract

Cyclophilins (CYPs) are essential for diverse cellular process, as these catalyse a rate-limiting step in protein folding. Although Golgi proteomics in Arabidopsis thaliana suggests the existence of several CYPs in the Golgi apparatus, only one putative Golgi-resident CYP protein has been reported in rice (Oryza sativa L.; OsCYP21-4). Here, we identified the Golgi-resident CYP21 family genes and analysed their molecular characteristics in Arabidopsis and rice. The CYP family genes (CYP21-1, CYP21-2, CYP21-3, and CYP21-4) are plant-specific, and their appearance and copy numbers differ among plant species. CYP21-1 and CYP21-4 are common to all angiosperms, whereas CYP21-2 and CYP21-3 evolved in the Malvidae subclass. Furthermore, all CYP21 proteins localize to cis-Golgi, trans-Golgi or both cis- and trans-Golgi membranes in plant cells. Additionally, based on the structure, enzymatic function, and topological orientation in Golgi membranes, CYP21 proteins are divided into two groups. Genetic analysis revealed that Group I proteins (CYP21-1 and CYP21-2) exhibit peptidyl prolyl cis–trans isomerase (PPIase) activity and regulate seed germination and seedling growth and development by affecting the expression levels of abscisic acid signalling genes. Thus, we identified the Golgi-resident CYPs and demonstrated that their PPIase activities are required for early seedling growth and development in higher plants.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahn JC, Kim DW, You YN, Seok MS, Park JM, Hwang H, Kim BG, Luan S, Park HS, Cho HS (2010) Classification of rice (Oryza sativa L. Japonica nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biol 10:253

    PubMed  PubMed Central  Google Scholar 

  • Barbosa Dos Santos I, Park SW (2019) Versatility of cyclophilins in plant growth and survival: a case study in Arabidopsis. Biomolecules 9:20

    PubMed Central  Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breiman A, Fawcett TW, Ghirardi ML, Mattoo AK (1992) Plant organelles contain distinct peptidylprolyl cis, trans-isomerases. J Biol Chem 267:21293–21296

    CAS  PubMed  Google Scholar 

  • Carles C, Bies-Etheve N, Aspart L, Leon-Kloosterziel KM, Koornneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373–383

    CAS  PubMed  Google Scholar 

  • Che P, Bussell JD, Zhou W, Estavillo GM, Pogson BJ, Smith SM (2010) Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis. Sci Signal 3:ra69

    PubMed  Google Scholar 

  • Chen X, Andrews PC, Wang Y (2012) Quantitative analysis of liver Golgi proteome in the cell cycle. Methods Mol Biol 909:125–140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daskalova SM, Pah AR, Baluch DP, Lopez LC (2009) The Arabidopsis thaliana putative sialyltransferase resides in the Golgi apparatus but lacks the ability to transfer sialic acid. Plant Biol (Stuttg) 11:284–299

    CAS  Google Scholar 

  • Dave A, Vaistij FE, Gilday AD, Penfield SD, Graham IA (2016) Regulation of Arabidopsis thaliana seed dormancy and germination by 12-oxo-phytodienoic acid. J Exp Bot 67:2277–2284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dekkers BJ, Willems L, Bassel GW, van Bolderen-Veldkamp RP, Ligterink W, Hilhorst HW, Bentsink L (2012) Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol 53:28–37

    CAS  PubMed  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    CAS  PubMed  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) Abscisic acid inhibition of radicle emergence but not seedling growth is suppressed by sugars. Plant Physiol 122:1179–1186

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finkkelstein R (2013) The Arabidopsis book

  • Fischer G, Bang H, Mech C (1984) Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides. Biomed Biochim Acta 43:1101–1111

    CAS  PubMed  Google Scholar 

  • Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell Environ 35:1769–1786

    CAS  Google Scholar 

  • Hawes A, Osterrieder A, Sparkes I (2008) The Golgi apparatus. Springer, Vienna

    Google Scholar 

  • He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heijne G (1986) The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5:3021–3027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    CAS  PubMed  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    CAS  PubMed  Google Scholar 

  • Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ingelsson B, Shapiguzov A, Kieselbach T, Vener AV (2009) Peptidyl-prolyl isomerase activity in chloroplast thylakoid lumen is a dispensable function of immunophilins in Arabidopsis thaliana. Plant Cell Physiol 50:1801–1814

    CAS  PubMed  Google Scholar 

  • Ito Y, Uemura T, Nakano A (2014) Formation and maintenance of the Golgi apparatus in plant cells. Int Rev Cell Mol Biol 310:221–287

    CAS  PubMed  Google Scholar 

  • Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Lee SC, Kim BG (2012) A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. J Exp Bot 63:1013–1024

    CAS  PubMed  Google Scholar 

  • Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36

    CAS  PubMed  Google Scholar 

  • Korves TM, Bergelson J (2003) A developmental response to pathogen infection in Arabidopsis. Plant Physiol 133:339–347

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SS, Park HJ, Jung WY, Lee A, Yoon DH, You YN, Kim HS, Kim BG, Ahn JC, Cho HS (2015) OsCYP21-4, a novel Golgi-resident cyclophilin, increases oxidative stress tolerance in rice. Front Plant Sci 6:797

    PubMed  PubMed Central  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    CAS  PubMed  Google Scholar 

  • Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98:4782–4787

    CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    CAS  PubMed  Google Scholar 

  • Magwa RA, Zhao H, Xing Y (2016) Genome-wide association mapping revealed a diverse genetic basis of seed dormancy across subpopulations in rice (Oryza sativa L.). BMC Genet 17:28

    PubMed  PubMed Central  Google Scholar 

  • Mayr C, Richter K, Lilie H, Buchner J (2000) Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 275:34140–34146

    CAS  PubMed  Google Scholar 

  • McCourt P, Creelman R (2008) The ABA receptors—we report you decide. Curr Opin Plant Biol 11:474–478

    CAS  PubMed  Google Scholar 

  • Min MK, Jang M, Lee M, Lee J, Song K, Lee Y, Choi KY, Robinson DG, Hwang I (2013) Recruitment of Arf1-GDP to Golgi by Glo3p-type ArfGAPs is crucial for golgi maintenance and plant growth. Plant Physiol 161:676–691

    CAS  PubMed  Google Scholar 

  • Mowbrey K, Dacks JB (2009) Evolution and diversity of the Golgi body. FEBS Lett 583:3738–3745

    CAS  PubMed  Google Scholar 

  • Nakamura S, Toyama T (2001) Isolation of a VP1 homologue from wheat and analysis of its expression in embryos of dormant and non-dormant cultivars. J Exp Bot 52:875–876

    CAS  PubMed  Google Scholar 

  • Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M, Kawaura K, Ogihara Y, Miura H (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell 23:3215–3229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano RT, Yamada K, Bednarek P, Nishimura M, Hara-Nishimura I (2014) ER bodies in plants of the Brassicales order: biogenesis and association with innate immunity. Front Plant Sci 5:73

    PubMed  PubMed Central  Google Scholar 

  • Nebenfuhr A, Staehelin LA (2001) Mobile factories: Golgi dynamics in plant cells. Trends Plant Sci 6:160–167

    CAS  PubMed  Google Scholar 

  • Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    CAS  PubMed  Google Scholar 

  • Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TP, Munro S, Lilley KS, Dupree P (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 160:1037–1051

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nikolovski N, Shliaha PV, Gatto L, Dupree P, Lilley KS (2014) Label-free protein quantification for plant Golgi protein localization and abundance. Plant Physiol 166:1033–1043

    PubMed  PubMed Central  Google Scholar 

  • Ohnishi T, Sugahara S, Yamada T, Kikuchi K, Yoshiba Y, Hirano HY, Tsutsumi N (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet Syst 80:135–139

    CAS  PubMed  Google Scholar 

  • Okekeogbu IO, Pattathil S, Gonzalez Fernandez-Nino SM, Aryal UK, Penning BW, Lao J, Heazlewood JL, Hahn MG, McCann MC, Carpita NC (2019) Glycome and proteome components of Golgi membranes are common between two angiosperms with distinct cell-wall structures. Plant Cell 31:1094–1112

    CAS  PubMed  Google Scholar 

  • Opat AS, van Vliet C, Gleeson PA (2001) Trafficking and localisation of resident Golgi glycosylation enzymes. Biochimie 83:763–773

    CAS  PubMed  Google Scholar 

  • Park HJ, Lee A, Lee SS, An DJ, Moon KB, Ahn JC, Kim HS, Cho HS (2017) Overexpression of Golgi protein CYP21-4 s improves crop productivity in potato and rice by increasing the abundance of mannosidic glycoproteins. Front Plant Sci 8:1250

    PubMed  PubMed Central  Google Scholar 

  • Parsons HT, Christiansen K, Knierim B, Carroll A, Ito J, Batth TS, Smith-Moritz AM, Morrison S, McInerney P, Hadi MZ, Auer M, Mukhopadhyay A, Petzold CJ, Scheller HV, Loque D, Heazlewood JL (2012a) Isolation and proteomic characterization of the Arabidopsis Golgi defines functional and novel components involved in plant cell wall biosynthesis. Plant Physiol 159:12–26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parsons HT, Drakakaki G, Heazlewood JL (2012b) Proteomic dissection of the Arabidopsis Golgi and trans-Golgi network. Front Plant Sci 3:298

    PubMed  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    CAS  PubMed  Google Scholar 

  • Rapoport TA, Goder V, Heinrich SU, Matlack KE (2004) Membrane-protein integration and the role of the translocation channel. Trends Cell Biol 14:568–575

    CAS  PubMed  Google Scholar 

  • Rock C (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396

    CAS  Google Scholar 

  • Rodriguez-Gacio Mdel C, Matilla-Vazquez MA, Matilla AJ (2009) Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal Behav 4:1035–1049

    PubMed  Google Scholar 

  • Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45

    CAS  PubMed  Google Scholar 

  • Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-Insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884

    PubMed  PubMed Central  Google Scholar 

  • Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002

    CAS  PubMed  Google Scholar 

  • Sprenger J, Lynn Fink J, Karunaratne S, Hanson K, Hamilton NA, Teasdale RD (2008) LOCATE: a mammalian protein subcellular localization database. Nucleic Acids Res 36:D230–D233

    CAS  PubMed  Google Scholar 

  • Tu L, Banfield DK (2010) Localization of Golgi-resident glycosyltransferases. Cell Mol Life Sci 67:29–41

    CAS  PubMed  Google Scholar 

  • Wang P, Heitman J (2005) The cyclophilins. Genome Biol 6:226

    PubMed  PubMed Central  Google Scholar 

  • Wei JH, Seemann J (2010) Unraveling the Golgi ribbon. Traffic 11:1391–1400

    PubMed  PubMed Central  Google Scholar 

  • Weiergraber OH, Eckhoff A, Granzin J (2006) Crystal structure of a plant immunophilin domain involved in regulation of MDR-type ABC transporters. FEBS Lett 580:251–255

    PubMed  Google Scholar 

  • Weitbrecht K, Muller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309

    CAS  PubMed  Google Scholar 

  • Wilson RL, Kim H, Bakshi A, Binder BM (2014) The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol 165:1353–1366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada K, Hara-Nishimura I, Nishimura M (2011) Unique defense strategy by the endoplasmic reticulum body in plants. Plant Cell Physiol 52:2039–2049

    CAS  PubMed  Google Scholar 

  • Yan A, Wu M, Yan L, Hu R, Ali I, Gan Y (2014) AtEXP2 is involved in seed germination and abiotic stress response in Arabidopsis. PLoS ONE 9:e85208

    PubMed  PubMed Central  Google Scholar 

  • Yang X, Yang YN, Xue LJ, Zou MJ, Liu JY, Chen F, Xue HW (2011) Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol 156:1397–1409

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon DH, Lee SS, Park HJ, Lyu JI, Chong WS, Liu JR, Kim BG, Ahn JC, Cho HS (2016) Overexpression of OsCYP19-4 increases tolerance to cold stress and enhances grain yield in rice (Oryza sativa). J Exp Bot 67:69–82

    CAS  PubMed  Google Scholar 

  • Yu Y, Wang J, Shi H, Gu J, Dong J, Deng XW, Huang R (2016) Salt stress and ethylene antagonistically regulate nucleocytoplasmic partitioning of COP1 to control seed germination. Plant Physiol 170:2340–2350

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XC, Wang WD, Wang JS, Pan JC (2013) PPIase independent chaperone-like function of recombinant human Cyclophilin A during arginine kinase refolding. FEBS Lett 587:666–672

    CAS  PubMed  Google Scholar 

  • Zong W, Tang N, Yang J, Peng L, Ma S, Xu Y, Li G, Xiong L (2016) Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes. Plant Physiol 171:2810–2825

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Dr. An Gynheung (Kyung Hee University, Korea) for kindly providing us with the T-DNA insertion mutant of OsCYP21-1. This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (Grant No. 2019R1A2C2002295) and Korea Research Institute of Bioscience and Biotechnology Research Initiative Programs (Grant Nos. KGM5371911 and KGM9481913) to H.S.C.

Author information

Authors and Affiliations

Authors

Contributions

HSC designed the research. HJ performed the most of experiments. SHJ performed a part of qRT-PCR analysis. HJP and AL helped in cell biology experiments. H-SK and H-JL contributed to the biological interpretation. HJ and HSC analysed all data and wrote the paper.

Corresponding author

Correspondence to Hye Sun Cho.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1274 kb)

Supplementary material 2 (DOCX 38 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jung, H., Jo, S.H., Park, H.J. et al. Golgi-localized cyclophilin 21 proteins negatively regulate ABA signalling via the peptidyl prolyl isomerase activity during early seedling development. Plant Mol Biol 102, 19–38 (2020). https://doi.org/10.1007/s11103-019-00928-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00928-5

Keywords

Navigation