ER Mutations Affect the Localization of Plant-Specific Insert (PSI) B in Arabidopsis †
Abstract
:1. Introduction
2. Material and Methods
2.1. Biological Material—Selection, Germination, and Growth Conditions
2.2. Vacuum Infiltration for Transient Transformation of Arabidopsis thaliana Seedlings
2.3. Drug Treatment Assays
2.4. CLSM Analysis
2.5. Extraction of Extracellular Proteins
2.6. Western Blot Analysis
3. Results
3.1. Expression and Localization of PSI B in ER-Defective Plants
3.2. Secretion Assays
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Morita, M.T.; Shimada, T. The Plant Endomembrane System—A Complex Network Supporting Plant Development and Physiology. Plant Cell Physiol. 2014, 55, 667–671. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cevher-Keskin, B. Endomembrane Trafficking in Plants. Electrodialysis 2020, 1–22. [Google Scholar] [CrossRef] [Green Version]
- Staehelin, L.A. The plant ER: A dynamic organelle composed of a large number of discrete functional domains. Plant J. 1997, 11, 1151–1165. [Google Scholar] [CrossRef] [PubMed]
- Stefan, C.J.; Manford, A.G.; Emr, S.D. ER-PM connections: Sites of information transfer and inter-organelle communication. Curr. Opin. Cell Biol. 2013, 25, 434–442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stefano, G.; Renna, L.; Lai, Y.; Slabaugh, E.; Mannino, N.; Buono, R.A.; Otegui, M.S.; Brandizzi, F. ER network homeostasis is critical for plant endosome streaming and endocytosis. Cell Discov. 2015, 1, 15033. [Google Scholar] [CrossRef] [Green Version]
- Nakano, R.T.; Matsushima, R.; Ueda, H.; Tamura, K.; Shimada, T.; Li, L.; Hayashi, Y.; Kondo, M.; Nishimura, M.; Hara-Nishimura, I. GNOM-LIKE1/ERMO1 and SEC24a/ERMO2 Are Required for Maintenance of Endoplasmic Reticulum Morphology in Arabidopsis thaliana. Plant Cell 2009, 21, 3672–3685. [Google Scholar] [CrossRef] [Green Version]
- Quader, H.; Schnepf, E. Endoplasmic reticulum and cytoplasmic streaming: Fluorescence microscopical observations in adaxial epidermis cells of onion bulb scales. Protoplasma 1986, 131, 250–252. [Google Scholar] [CrossRef]
- Matsushima, R.; Hayashi, Y.; Yamada, K.; Shimada, T.; Nishimura, M.; Hara-Nishimura, I. The ER Body, a Novel Endoplasmic Reticulum-Derived Structure in Arabidopsis. Plant Cell Physiol. 2003, 44, 661–666. [Google Scholar] [CrossRef] [Green Version]
- Hara-Nishimura, I.; Matsushima, R.; Shimada, T.; Nishimura, M. Diversity and Formation of Endoplasmic Reticulum-Derived Compartments in Plants. Are These Compartments Specific to Plant Cells? Plant Physiol. 2004, 136, 3435–3439. [Google Scholar] [CrossRef] [Green Version]
- Sampaio, M.; Neves, J.; Cardoso, T.; Pissarra, J.; Pereira, S.; Pereira, C. Coping with Abiotic Stress in Plants—An Endomembrane Trafficking Perspective. Plants 2022, 11, 338. [Google Scholar] [CrossRef]
- Marcos Lousa, C.; Gershlick, D.C.; Denecke, J. Mechanisms and Concepts Paving the Way towards a Complete Transport Cycle of Plant Vacuolar Sorting Receptors. Plant Cell 2012, 24, 1714–1732. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rojo, E.; Denecke, J. What is moving in the secretory pathway of plants? Plant Physiol. 2008, 147, 1493–1503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olbrich, A.; Hillmer, S.; Hinz, G.; Oliviusson, P.; Robinson, D.G. Newly formed vacuoles in root meristems of barley and pea seedlings have characteristics of both protein storage and lytic vacuoles. Plant Physiol. 2007, 145, 1383–1394. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paris, N.; Stanley, C.M.; Jones, R.L.; Rogers, J.C. Plant Cells Contain Two Functionally Distinct Vacuolar Compartments. Cell 1996, 85, 563–572. [Google Scholar] [CrossRef] [Green Version]
- Ramalho-Santos, M.; Verissimo, P.; Cortes, L.; Samyn, B.; Van Beeumen, J.; Pires, E.; Faro, C. Identification and proteolytic processing of procardosin A. Eur. J. Biochem. 1998, 255, 133–138. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira, M.; Pissarra, J.; Veríssimo, P.; Castanheira, P.; Costa, Y.; Pires, E.; Faro, C. Molecular cloning and characterization of cDNA encoding cardosin B, an aspartic proteinase accumulating extracellularly in the transmitting tissue of Cynara cardunculus L. Plant Mol. Biol. 2001, 45, 529–539. [Google Scholar] [CrossRef] [Green Version]
- Ramalho-Santos, M.; Pissarra, J.; Veríssimo, P.; Pereira, S.; Salema, R.; Pires, E.; Faro, C.J. Cardosin A, an abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 1997, 203, 204–212. [Google Scholar] [CrossRef]
- Pissarra, J.; Pereira, C.; Soares, D.; Figueiredo, R.; Duarte, P.; Teixeira, J.; Pereira, S.; da Costa, D.S.; Figueiredo, R.; Duarte, P.; et al. From Flower to Seed Germination in Cynara cardunculus: A Role for Aspartic Proteinases. Int. J. Plant Dev. Biol. 2007, 1, 274–281. [Google Scholar]
- Pereira, C.S.; da Costa, D.S.; Pereira, S.; de Moura Nogueira, F.; Albuquerque, P.M.; Teixeira, J.; Faro, C.; Pissarra, J. Cardosins in postembryonic development of cardoon: Towards an elucidation of the biological function of plant aspartic proteinases. Protoplasma 2008, 232, 203–213. [Google Scholar] [CrossRef] [Green Version]
- Oliveira, A.; Pereira, C.; da Costa, D.S.; Teixeira, J.; Fidalgo, F.; Pereira, S.; Pissarra, J. Characterization of aspartic proteinases in C. cardunculus L. callus tissue for its prospective transformation. Plant Sci. 2010, 178, 140–146. [Google Scholar] [CrossRef]
- Duarte, P.; Pissarra, J.; Moore, I. Processing and trafficking of a single isoform of the aspartic proteinase cardosin A on the vacuolar pathway. Planta 2008, 227, 1255–1268. [Google Scholar] [CrossRef] [PubMed]
- Pereira, C.; Pereira, S.; Satiat-Jeunemaitre, B.; Pissarra, J. Cardosin A contains two vacuolar sorting signals using different vacuolar routes in tobacco epidermal cells. Plant J. 2013, 76, 87–100. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- da Costa, D.S.; Pereira, S.; Moore, I.; Pissarra, J. Dissecting cardosin B trafficking pathways in heterologous systems. Planta 2010, 232, 1517–1530. [Google Scholar] [CrossRef] [PubMed]
- Simões, I.; Faro, C. Structure and function of plant aspartic proteinases. Eur. J. Biochem. 2004, 271, 2067–2075. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soares, A.; Ribeiro Carlton, S.M.; Simões, I. Atypical and nucellin-like aspartic proteases: Emerging players in plant developmental processes and stress responses. J. Exp. Bot. 2019, 70, 2059–2076. [Google Scholar] [CrossRef]
- Egas, C.; Lavoura, N.; Resende, R.; Brito, R.M.M.; Pires, E.; de Lima, M.C.P.; Faro, C. The Saposin-like Domain of the Plant Aspartic Proteinase Precursor Is a Potent Inducer of Vesicle Leakage. J. Biol. Chem. 2002, 275, 38190–38196. [Google Scholar] [CrossRef] [Green Version]
- Terauchi, K.; Asakura, T.; Ueda, H.; Tamura, T.; Tamura, K.; Matsumoto, I.; Misaka, T.; Hara-Nishimura, I.; Abe, K. Plant-specific insertions in the soybean aspartic proteinases, soyAP1 and soyAP2, perform different functions of vacuolar targeting. J. Plant Physiol. 2006, 163, 856–862. [Google Scholar] [CrossRef]
- De Moura, D.C.; Bryksa, B.C.; Yada, R.Y. In silico insights into protein-protein interactions and folding dynamics of the saposin-like domain of Solanum tuberosum aspartic protease. PLoS ONE 2014, 9, 18–22. [Google Scholar] [CrossRef]
- Frey, M.E.; D’Ippolito, S.; Pepe, A.; Daleo, G.R.; Guevara, M.G. Transgenic expression of plant-specific insert of potato aspartic proteases (StAP-PSI) confers enhanced resistance to Botrytis cinerea in Arabidopsis thaliana. Phytochemistry 2018, 149, 1–11. [Google Scholar] [CrossRef]
- Muñoz, F.; Palomares-Jerez, M.F.; Daleo, G.; Villalaín, J.; Guevara, M.G. Possible mechanism of structural transformations induced by StAsp-PSI in lipid membranes. Biochim. Biophys. Acta—Biomembr. 2014, 1838, 339–347. [Google Scholar] [CrossRef] [Green Version]
- De Caroli, M.; Lenucci, M.S.; Di Sansebastiano, G.-P.; Dalessandro, G.; De Lorenzo, G.; Piro, G. Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant J. 2011, 65, 295–308. [Google Scholar] [CrossRef] [PubMed]
- De Marchis, F.; Bellucci, M.; Pompa, A. Unconventional pathways of secretory plant proteins from the endoplasmic reticulum to the vacuole bypassing the Golgi complex. Plant Signal. Behav. 2013, 8, e25129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stigliano, E.; Faraco, M.; Neuhaus, J.-M.M.; Montefusco, A.; Dalessandro, G.; Piro, G.; Di Sansebastiano, G.-P. Pietro Two glycosylated vacuolar GFPs are new markers for ER-to-vacuole sorting. Plant Physiol. Biochem. 2013, 73, 337–343. [Google Scholar] [CrossRef] [PubMed]
- Di Sansebastiano, G.P.; Barozzi, F.; Piro, G.; Denecke, J.; Lousa, C.D.M. Trafficking routes to the plant vacuole: Connecting alternative and classical pathways. J. Exp. Bot. 2018, 69, 79–90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vieira, V.; Peixoto, B.; Costa, M.; Pereira, S.; Pissarra, J.; Pereira, C. N-linked glycosylation modulates Golgi-independent vacuolar sorting mediated by the plant specific insert. Plants 2019, 8, 312. [Google Scholar] [CrossRef] [Green Version]
- Matsushima, R.; Fukao, Y.; Nishimura, M.; Hara-Nishimura, I. NAI1 gene encodes a basic-helix-loop-helix-type putative transcription factor that regulates the formation of an endoplasmic reticulum-derived structure, the ER body. Plant Cell 2004, 16, 1536–1549. [Google Scholar] [CrossRef] [Green Version]
- Bernat-Silvestre, C.; De Sousa Vieira, V.; Sánchez-Simarro, J.; Aniento, F.; Marcote, M.J. Transient Transformation of A. thaliana Seedlings by Vacuum Infiltration. Methods Mol. Biol. 2021, 2200, 147–155. [Google Scholar] [CrossRef]
- Nebenführ, A.; Ritzenthaler, C.; Robinson, D.G. Brefeldin A: Deciphering an enigmatic inhibitor of secretion. Plant Physiol. 2002, 130, 1102–1108. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Cardoso, T.; Pereira, S.; Pissarra, J.; Pereira, C. ER Mutations Affect the Localization of Plant-Specific Insert (PSI) B in Arabidopsis. Biol. Life Sci. Forum 2022, 11, 8. https://doi.org/10.3390/IECPS2021-11930
Cardoso T, Pereira S, Pissarra J, Pereira C. ER Mutations Affect the Localization of Plant-Specific Insert (PSI) B in Arabidopsis. Biology and Life Sciences Forum. 2022; 11(1):8. https://doi.org/10.3390/IECPS2021-11930
Chicago/Turabian StyleCardoso, Tatiana, Susana Pereira, José Pissarra, and Cláudia Pereira. 2022. "ER Mutations Affect the Localization of Plant-Specific Insert (PSI) B in Arabidopsis" Biology and Life Sciences Forum 11, no. 1: 8. https://doi.org/10.3390/IECPS2021-11930
APA StyleCardoso, T., Pereira, S., Pissarra, J., & Pereira, C. (2022). ER Mutations Affect the Localization of Plant-Specific Insert (PSI) B in Arabidopsis. Biology and Life Sciences Forum, 11(1), 8. https://doi.org/10.3390/IECPS2021-11930