The role of EGY2 protease in response to high light stress
Robert Luciński
A * , Jędrzej Dobrogojski B , Takao Ishikawa C and Małgorzata Adamiec A
A
B
C
Abstract
In this study, we investigated the importance of one of the intramembrane proteases, EGY2, for the proper functioning of PSII under short-term high light stress conditions. EGY2 is a chloroplast intramembrane protease of the S2P family, whose absence in Arabidopsis thaliana affects PSII protein composition. The egy2 mutants exhibited a slower degradation of PsbA and decreased content of PsbC and PsbD. During exposure to high light stress, these stoichiometric changes affect the functional state of PSII, leading to its higher sensitivity to photoinhibition of the PSII reaction centre and increased heat dissipation. Furthermore, we explored the relationship between EGY2 and the pTAC16 transcription factor, which is a potential EGY2 substrate. Under light stress, WT plants showed decreased levels of pTAC16, while it remained unchanged in the egy2 mutants. This finding suggests that EGY2 may release pTAC16 from thylakoid membranes through proteolytic cleavage. We also confirmed the physical interaction between EGY2 and pTAC16 using the yeast two-hybrid system, providing evidence of EGY2’s involvement in the regulation of PsbA and PsbC/PsbD operons by releasing pTAC16 from the thylakoid membrane.
Keywords: Arabidopsis thaliana, chloroplast, EGY2, intramembrane proteases, photosynthesis, photosystem II, regulated intramembrane proteolysis, transcription factor.
References
Adamiec M, Ciesielska M, Zalaś P, Luciński R (2017) Arabidopsis thaliana intramembrane proteases. Acta Physiologiae Plantarum 39, 146.
| Crossref | Google Scholar |
Adamiec M, Misztal L, Kosicka E, Paluch-Lubawa E, Luciński R (2018) Arabidopsis thaliana egy2 mutants display altered expression level of genes encoding crucial photosystem II proteins. Journal of Plant Physiology 231, 155-167.
| Crossref | Google Scholar | PubMed |
Adamiec M, Misztal L, Ciesielska M, Luciński R (2021) The changes of PSII supercompelex stoichiometry in egy1 mutants are related to chlorophyll b deficiency. Photosynthetica 59, 294-302.
| Crossref | Google Scholar |
Adamiec M, Dobrogojski J, Wojtyla Ł, Luciński R (2023) Stress-related expression of the chloroplast EGY3 pseudoprotease and its possible impact on chloroplasts’ proteome composition. Frontiers in Plan Science 13, 9665143.
| Crossref | Google Scholar |
Arsova B, Hoja U, Wimmelbacher M, Greiner E, Üstün S, Melzer M, et al. (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22(5), 1498-1515.
| Crossref | Google Scholar | PubMed |
Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P, Hennig L, et al. (2012) Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Molecular Systems Biology 8, 606.
| Crossref | Google Scholar | PubMed |
Chang SH, Lee S, Um TY, Kim JK, Choi YD, Jang G (2017) pTAC10, a key subunit of plastid-encoded RNA polymerase, promotes chloroplast development. Plant Physiology 174(1), 435-449.
| Crossref | Google Scholar | PubMed |
Chen G, Law K, Ho P, Zhang X, Li N (2012) EGY2, a chloroplast membrane metalloprotease, plays a role in hypocotyl elongation in Arabidopsis. Molecular Biology Reports 39, 2147-2155.
| Crossref | Google Scholar | PubMed |
Chi W, He B, Mao J, Jijang J, Zhang L (2015) Plastid sigma factors: their individual functions and regulation in transcription. Biochimica et Biophysica Acta – Bioenergetics 1847(9), 770-778.
| Crossref | Google Scholar |
Chotewutmontri P, Barkan A (2020) Light-induced psbA translation in plants is triggered by photosystem II damage via an assembly-linked autoregulatory circuit. Proceedings of the National Academy of Science of the United States of America 117, 21775–21784. doi:10.1073/pnas.2007833117. pubmed id:32817480
Feng L, Yan H, Wu Z, Yan N, Wang Z, Jeffrey PD, Shi Y (2007) Structure of a site-2 protease family intramembrane metalloprotease. Science 318, 1608-1612.
| Crossref | Google Scholar | PubMed |
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta – General Subject 990, 87-92.
| Crossref | Google Scholar |
Gu Y, Lee W, Shen J (2014) Site-2 protease responds to oxidative stress and regulates oxidative injury in mammalian cells. Science Reports 4, 6268.
| Crossref | Google Scholar | PubMed |
Hajdukiewicz PTJ, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO Journal 16, 4041-4048.
| Crossref | Google Scholar | PubMed |
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, et al. (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Advances in Bioinformatics 2008, 420747.
| Crossref | Google Scholar |
Ibrahim IM, McKenzie SD, Chung J, Aryal UK, Leon-Salas WD, Puthiyaveetil S (2022) Photosystem stoichiometry adjustment is a photoreceptor-mediated process in Arabidopsis. Scientific Reports 12, 10982.
| Crossref | Google Scholar | PubMed |
Ingelsson B, Vener AV (2012) Phosphoproteomics of Arabidopsis chloroplasts reveals involvement of the STN7 kinase in phosphorylation of nucleoid protein pTAC16. FEBS Letters 586, 1265-1271.
| Crossref | Google Scholar | PubMed |
Kameniarova M, Černý M, Novák J, Ondrisková V, Hrušková L, Berka M, Vankova R, Brzobohatý B (2022) Light quality modulates plant cold response and freezing tolerance. Frontiers in Plant Science 13, 887103.
| Crossref | Google Scholar | PubMed |
Kapri-Perdes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19, 1039-1047.
| Crossref | Google Scholar |
Kato Y, Sakamoto W (2018) FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. Frontiers in Plant Science 9, 855.
| Crossref | Google Scholar | PubMed |
Kristensen SS, Diep DB, Kjos M, Mathiesen G (2023) The role of site-2-proteases in bacteria: a review on physiology, virulence, and therapeutic potential. Microlife 4, uqad025.
| Crossref | Google Scholar |
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
| Crossref | Google Scholar | PubMed |
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research 40, D1202-D1210.
| Crossref | Google Scholar | PubMed |
Liu J, Last RL (2017) A chloroplast thylakoid lumen protein is required for proper photosynthetic acclimation of plants under fluctuating light environments. Proceedings of the National Academy of Science of the United States of America 114, E8110-E8117.
| Crossref | Google Scholar | PubMed |
Liu Y, Beyer A, Aebersold R (2016) On the dependency of cellular protein levels on mRNA abundance. Cell 165, 535-550.
| Crossref | Google Scholar | PubMed |
Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, et al. (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiology 158, 156-189.
| Crossref | Google Scholar |
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659-668.
| Crossref | Google Scholar | PubMed |
Motohashi R, Rödiger A, Agne B, Baerenfaller K, Baginsky S (2012) Common and specific protein accumulation patterns in different albino/pale-green mutants reveals regulon organization at the proteome level. Plant Physiology 160, 2189-2201.
| Crossref | Google Scholar | PubMed |
Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106, 1-16.
| Crossref | Google Scholar | PubMed |
Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, et al. (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14, 216.
| Crossref | Google Scholar | PubMed |
Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18, 176-197.
| Crossref | Google Scholar | PubMed |
Qi Y, Wang X, Lei P, et al. (2020) The chloroplast metalloproteases VAR2 and EGY1 act synergistically to regulate chloroplast development in Arabidopsis. Journal of Biological Chemistry 295, 1036-1046.
| Crossref | Google Scholar | PubMed |
Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807, 375-383.
| Crossref | Google Scholar | PubMed |
Schönberg A, Baginsky S (2012) Signal integration by chloroplast phosphorylation networks: an update. Frontiers in Plant Science 3, 256.
| Crossref | Google Scholar | PubMed |
Schuhmann H, Huesgen PF, Adamska I (2012) The family of Deg/HtrA proteases in plants. BMC Plant Biology 12, 52.
| Crossref | Google Scholar | PubMed |
Shang H, Li M, Pan X (2023) Dynamic regulation of the light-harvesting system through state transitions in land plants and green algae. Plants 12, 1173.
| Crossref | Google Scholar | PubMed |
Shen JR (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annual Review of Plant Biology 66, 23-48.
| Crossref | Google Scholar | PubMed |
Telfer A, Bishop SM, Philips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. Journal of Biological Chemistry 269, 13244-13253.
| Crossref | Google Scholar | PubMed |
Tylor CR, Vanleperen W, Harbison J (2019) Demonstration of a relationship between state transitions and photosynthetic efficiency in a higher plant. Journal of Biochemistry 476, 3295-3312.
| Crossref | Google Scholar | PubMed |
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55-60.
| Crossref | Google Scholar | PubMed |
Vass I (2012) Molecular mechanism of photodamage in the photosystem II complex. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1817, 209-217.
| Crossref | Google Scholar |
Yamamoto Y (2016) Quality control of photosystem II: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids. Frontiers in Plant Science 7, 1136.
| Crossref | Google Scholar | PubMed |
Zhang S, Chen C, Dai S, Yang M, Meng Q, Lv W, Ma N (2022) A tomato putative metalloprotease SlEGY2 plays a positive role in thermotolerance. Agriculture 12, 940.
| Crossref | Google Scholar |
