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.
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
Barbosa Dos Santos I, Park SW (2019) Versatility of cyclophilins in plant growth and survival: a case study in Arabidopsis. Biomolecules 9:20
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Breiman A, Fawcett TW, Ghirardi ML, Mattoo AK (1992) Plant organelles contain distinct peptidylprolyl cis, trans-isomerases. J Biol Chem 267:21293–21296
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
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
Chen X, Andrews PC, Wang Y (2012) Quantitative analysis of liver Golgi proteome in the cell cycle. Methods Mol Biol 909:125–140
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
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
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
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Finkelstein RR, Lynch TJ (2000) Abscisic acid inhibition of radicle emergence but not seedling growth is suppressed by sugars. Plant Physiol 122:1179–1186
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
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell Environ 35:1769–1786
Hawes A, Osterrieder A, Sparkes I (2008) The Golgi apparatus. Springer, Vienna
He Z, Li L, Luan S (2004) Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol 134:1248–1267
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
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
Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54
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
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
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
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
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36
Korves TM, Bergelson J (2003) A developmental response to pathogen infection in Arabidopsis. Plant Physiol 133:339–347
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
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222
Liu JX, Howell SH (2010) Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930–2942
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
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
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
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
McCourt P, Creelman R (2008) The ABA receptors—we report you decide. Curr Opin Plant Biol 11:474–478
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
Mowbrey K, Dacks JB (2009) Evolution and diversity of the Golgi body. FEBS Lett 583:3738–3745
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
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
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
Nebenfuhr A, Staehelin LA (2001) Mobile factories: Golgi dynamics in plant cells. Trends Plant Sci 6:160–167
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
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
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
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
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
Opat AS, van Vliet C, Gleeson PA (2001) Trafficking and localisation of resident Golgi glycosylation enzymes. Biochimie 83:763–773
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
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
Parsons HT, Drakakaki G, Heazlewood JL (2012b) Proteomic dissection of the Arabidopsis Golgi and trans-Golgi network. Front Plant Sci 3:298
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401
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
Rock C (2000) Pathways to abscisic acid-regulated gene expression. New Phytol 148:357–396
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
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
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
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
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
Tu L, Banfield DK (2010) Localization of Golgi-resident glycosyltransferases. Cell Mol Life Sci 67:29–41
Wang P, Heitman J (2005) The cyclophilins. Genome Biol 6:226
Wei JH, Seemann J (2010) Unraveling the Golgi ribbon. Traffic 11:1391–1400
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
Weitbrecht K, Muller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309
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
Yamada K, Hara-Nishimura I, Nishimura M (2011) Unique defense strategy by the endoplasmic reticulum body in plants. Plant Cell Physiol 52:2039–2049
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
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
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
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
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
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
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
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
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.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-019-00928-5