Downregulation of chloroplast protease AtDeg5 leads to changes in chronological progression of ontogenetic stages, leaf morphology and chloroplast ultrastructure in Arabidopsis

Małgorzata Baranek, Tomasz P. Wyka, Grzegorz Jackowski

Abstract


The chloroplast protein AtDeg5 is a serine-type protease peripherally attached to thylakoid membrane at its lumenal side. Since reliable data regarding the role of AtDeg5 in controlling the course of growth and developmental processes are extremely limited, two independent T-DNA insertional lines with different extent of AtDeg5 reduction were prepared and ontogenesis stage-based analysis performed. Both mutant lines displayed a compensatory overaccumulation of AtDeg8. The repression of AtDeg5 protease altered a range of phenotypic features in at least one of the mutants, with the most prominent being changes in chronological progression of development and growth of individual rosette leaves, flower production and silique ripening as well as in the area of fully expanded leaves and chloroplast ultrastructure. By analyzing the results of parallel-mutant screening we conclude that AtDeg8 overdose may rescue 23% of AtDeg5 deficiency with regard to some AtDeg5-controlled traits; alternatively AtDeg5 may have catalytic sites in excess so that these traits might remain unaltered when AtDeg5 pool is reduced by 23%. For some other AtDeg5-dependent traits the absence of excessive amount of AtDeg5 catalytic sites, lack of AtDeg5 dosage effect and inability of AtDeg8 to compensate deficiency or absence of AtDeg5 occurred.

Keywords


AtDeg5 protease; chronological progression; leaf morphology; chloroplast ultrastructure; starch grains

Full Text:

PDF

References


Pesquet E. Plant proteases – from detection to function. Physiol Plant. 2012;145(1):1–4. http://dx.doi.org/10.1111/j.1399-3054.2012.01614.x

Lipińska B, Ang D, Georgopoulos C. Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein. Nucl Acids Res. 1988;16(15):7545–7562. http://dx.doi.org/10.1093/nar/16.15.7545

Strauch KL, Beckwitt J. An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc Natl Acad Sci USA. 1988;85(5):1576–1580. http://dx.doi.org/10.1073/pnas.85.5.1576

Wilken C, Kitzing K, Kurzbauer R, Ehrmann M, Clausen T. Crystal structure of the DegS stress sensor: how a PDZ domain recognizes misfolded protein and activates a protease. Cell. 2004;117(4):483–494. http://dx.doi.org/10.1016/S0092-8674(04)00454-4

Jiang J, Zhang X, Chen Y, Wu Y, Zhou ZH, Chang Z, Sui SF. Activation of DegP chaperone-protease via formation of large cage-like oligomers upon binding to substrate proteins. Proc Natl Acad Sci USA. 2008;105(33):11939–11944. http://dx.doi.org/10.1073/pnas.0805464105

Bai XC, Pan XI, Wang XJ, Ye YY, Chang LF, Leng D, et al. Characterization of the structure and function of Escherichia coli DegQ as a representative of the DegQ-like proteases of bacterial HtrA family proteins. Structure. 2011;19(9):1328–1337. http://dx.doi.org/10.1016/j.str.2011.06.013

Ortega J, Iwańczyk J, Jomaa A. Escherichia coli DegP: a structure-driven functional model. J Bacteriol. 2009;191(15):4705–4713. http://dx.doi.org/10.1128/JB.00472-09

Schuhmann H, Huesgen PF, Adamska I. The family of Deg/HtrA proteases in plants. BMC Plant Biol. 2012;12(1):1–14. http://dx.doi.org/10.1186/1471-2229-12-52

Schuhmann H, Adamska I. Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell. Physiol Plant. 2012;145(1):224–234. http://dx.doi.org/10.1111/j.1399-3054.2011.01533.x

Schuhmann H, Mogg U, Adamska I. A new principle of oligomerization of plant DEG7 protease based on interactions of degenerated protease domains. Biochem J. 2011;435(1):167–174. http://dx.doi.org/10.1042/BJ20101613

Kley J, Schmidt B, Boyanov B, Stolt-Bergner PC, Kirk R, Ehrmann M, et al. Structural adaptation of the plant protease Deg1 to repair photosystem II during light exposure. Nat Struct Mol Biol. 2011;18(6):728–731. http://dx.doi.org/10.1038/nsmb.2055

Sun XW, Fu TJ, Chen N, Guo JK, Ma JF, Zou MJ, et al. The stromal chloroplast Deg7 protease participates in the repair of photosystem II after photoinhibition in Arabidopsis. Plant Physiol. 2010;152(3):1263–1273. http://dx.doi.org/10.1104/pp.109.150722

Sun W, Gao F, Fan H, Shan X, Sun R, Liu L, et al. The structures of Arabidopsis Deg5 and Deg8 reveal new insights into HtrA proteases. Acta Crystallogr D Biol Crystallogr. 2013;69(5):830–837. http://dx.doi.org/10.1107/S0907444913002023

Sun XW, Peng L, Guo J, Chi W, Ma J, Lu C, et al. Formation of DEG5 and DEG8 and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell. 2007;19(4):1347–1361. http://dx.doi.org/10.1105/tpc.106.049510

Kapri-Pardes E, Naveh L, Adam Z. The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell. 2007;19(3):1039–1047. http://dx.doi.org/10.1105/tpc.106.046573

Luciński R, Misztal L, Samardakiewicz S, Jackowski G. The thylakoid protease Deg2 is involved in stress-related degradation of the photosystem II light-harvesting protein Lhcb6 in Arabidopsis thaliana. New Phytol. 2011;192(1):174–186. http://dx.doi.org/10.1111/j.1469-8137.2011.03782.x

Kato Y, Sun X, Zhang L, Sakamoto W. Cooperative D1 degradation in the photosystem II repair mediated by chloroplastic proteases in Arabidopsis. Plant Physiol. 2012;159(4):1428–1439. http://dx.doi.org/10.1104/pp.112.199042

Zienkiewicz M, Ferenc A, Wasilewska W, Romanowska E. High light stimulates Deg1-dependent cleavage of the minor LHCII antenna proteins CP26 and CP29 and the PsbS protein in Arabidopsis thaliana. Planta. 2012235(2):279–288. http://dx.doi.org/10.1007/s00425-011-1505-x

Luciński R, Misztal L, Samardakiewicz S, Jackowski G. Involvement of Deg5 protease in wounding-related disposal of PsbF apoprotein. Plant Physiol Biochem. 2011;49(3):311–320. http://dx.doi.org/10.1016/j.plaphy.2011.01.001

Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 1962;15(3):473–497. http://dx.doi.org/10.1111/j.1399-3054.1962.tb08052.x

Grabsztunowicz M, Jackowski G. Isolation of intact and pure chloroplasts from leaves of Arabidopsis thaliana plants acclimated to low irradiance for studies on Rubisco regulation. Acta Soc Bot Pol. 2013;82(1):91–95. http://dx.doi.org/10.5586/asbp.2012.043

Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227(5259):680–685. http://dx.doi.org/10.1038/227680a0

Luciński R, Jackowski G. AtFtsH heterocomplex-mediated degradation of apoproteins of the major light harvesting complex of photosystem II (LHCII) in response to stresses. J Plant Physiol. 2013;170(12):1082–1089. http://dx.doi.org/10.1016/j.jplph.2013.03.008

Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, et al. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell. 2001;13(7):1499–1510. http://dx.doi.org/10.2307/3871382

Kincaid DT, Schneider RB. Quantification of leaf shape with a microcomputer and Fourier transform. Can J Bot. 1983;61(9):2333–2342. http://dx.doi.org/10.1139/b83-256

Western TL, Skinner DJ, Haughn GW. Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol. 2000;122(2):345–355. http://dx.doi.org/10.1104/pp.122.2.345

Chow PS, Landhausser SM. A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol. 2004;24(10):1129–1136. http://dx.doi.org/10.1093/treephys/24.10.1129

Farquhar GD, von Caemmerer S, Berry JA. A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta. 1980;149(1):78–90. http://dx.doi.org/10.1007/BF00386231

Tanaka Y, Sugano SS, Shimada T, Nishimura I. Enhancement of leaf photosynthetic capacity through increased stomatal density in Arabidopsis. New Phytol. 2013;198(3):757–764. http://dx.doi.org/10.1111/nph.12186

Long SP, Bernacchi CJ. Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot. 2003;54(392):2393–2401. http://dx.doi.org/10.1093/jxb/erg262

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL. Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant Cell Environ. 2007;30(9):1035–1040. http://dx.doi.org/10.1111/j.1365-3040.2007.01710.x

Arnon D. Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 1949;24(1):1–15. http://dx.doi.org/10.1104/pp.24.1.1

Lancashire PD, Bleiholder H, van der Boom T, Langeluddeke P, Stauss R, Weber E, et al. A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol. 1991;119(3):561–601. http://dx.doi.org/10.1111/j.1744-7348.1991.tb04895.x

Telfer A, Bollman KM, Poethig RS. Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development. 1997;124(3):645–654.

Yu F, Park S, Rodermel SR. The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J. 2004;37(6):864–876. http://dx.doi.org/10.1111/j.1365-313X.2003.02014.x

Yu F, Park S, Rodermel SR. Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol. 2005;138(4):1957–1966. http://dx.doi.org/10.1104/pp.105.061234

Stanne TM, Sjögren LL, Koussevitzky S, Clarke AK. Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem J. 2009;417(1):257–268. http://dx.doi.org/10.1042/BJ20081146

Tisné S, Reymond M, Vile D, Fabre J, Dauzat M, Koornneef M, et al. Combined genetic and modeling approaches reveal that epidermal cell area and number in leaves are controlled by leaf and plant developmental processes in Arabidopsis. Plant Physiol. 2008;148(2):1117–1127. http://dx.doi.org/10.1104/pp.108.124271

Massonnet C, Vile D, Fabre J, Hannah MA, Caldana C, Lisec J, et al. Probing the reproducibility of leaf growth and molecular phenotypes: a comparison of three Arabidopsis accessions cultivated in ten laboratories. Plant Physiol. 2010;152(4):2142–2157. http://dx.doi.org/10.1104/pp.109.148338

Cookson SJ, Chenu K, Granier C. Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. Ann Bot. 2007;99(4):703–711. http://dx.doi.org/10.1093/aob/mcm005

Huijser P, Schmid M. The control of developmental phase transitions in plants. Development. 2011;138(19):4117–4129. http://dx.doi.org/10.1242/dev.063511

Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, et al. Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell. 2007;19(4):1362–1375. http://dx.doi.org/10.1105/tpc.106.042911




DOI: https://doi.org/10.5586/asbp.2015.001

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society