Subcellular Localization of a Plant Catalase-Phenol Oxidase, AcCATPO, from and Identification of a Non-canonical Peroxisome Targeting Signal

Overview

Journal Front Plant Sci

Date 2017 Aug 22

PMID 28824680

Citations 6

Authors

Ning Chen

Xiao-Lu Teng

Xing-Guo Xiao

Affiliations

Soon will be listed here.

Abstract

AcCATPO is a plant catalase-phenol oxidase recently identified from red amaranth. Its physiological function remains unexplored. As the starting step of functional analysis, here we report its subcellular localization and a non-canonical targeting signal. Commonly used bioinformatics programs predicted a peroxisomal localization for AcCATPO, but failed in identification of canonical peroxisomal targeting signals (PTS). The C-terminal GFP tagging led the fusion protein AcCATPO-GFP to the cytosol and the nucleus, but N-terminal tagging directed the GFP-AcCATPO to peroxisomes and nuclei, in transgenic tobacco. Deleting the tripeptide (PTM) at the extreme C-terminus almost ruled out the peroxisomal localization of GFP-AcCATPOΔ3, and removing the C-terminal decapeptide completely excluded peroxisomes as the residence of GFP-AcCATPOΔ10. Furthermore, this decapeptide as a targeting signal could import GFP-10aa to the peroxisome exclusively. Taken together, these results demonstrate that AcCATPO is localized to the peroxisome and the nucleus, and its peroxisomal localization is attributed to a non-canonical PTS1, the C-terminal decapeptide which contains an internal SRL motif and a conserved tripeptide P-S/T-I/M at the extreme of C-terminus. This work may further the study as to the physiological function of AcCATPO, especially clarify its involvement in betalain biosynthesis, and provide a clue to elucidate more non-canonic PTS.

Citing Articles

Investigation of how gate residues in the main channel affect the catalytic activity of Scytalidium thermophilum catalase.

Yuzugullu Karakus Y, Goc G, Zengin Karatas M, Balci Unver S, Yorke B, Pearson A Acta Crystallogr D Struct Biol. 2024; 80(Pt 2):101-112.

PMID: 38265876 PMC: 10836395. DOI: 10.1107/S2059798323011063.

ROS generated from biotic stress: Effects on plants and alleviation by endophytic microbes.

Sahu P, Jayalakshmi K, Tilgam J, Gupta A, Nagaraju Y, Kumar A Front Plant Sci. 2022; 13:1042936.

PMID: 36352882 PMC: 9638130. DOI: 10.3389/fpls.2022.1042936.

Virtual 2-D map of the fungal proteome.

Mohanta T, Mishra A, Khan A, Hashem A, Abd-Allah E, Al-Harrasi A Sci Rep. 2021; 11(1):6676.

PMID: 33758316 PMC: 7988114. DOI: 10.1038/s41598-021-86201-6.

Abiotic Stress and Reactive Oxygen Species: Generation, Signaling, and Defense Mechanisms.

Sachdev S, Ansari S, Ansari M, Fujita M, Hasanuzzaman M Antioxidants (Basel). 2021; 10(2).

PMID: 33670123 PMC: 7916865. DOI: 10.3390/antiox10020277.

Reactive oxygen species metabolism and photosynthetic performance in leaves of Hordeum vulgare plants co-infested with Heterodera filipjevi and Aceria tosichella.

Labudda M, Tokarz K, Tokarz B, Muszynska E, Gietler M, Gorecka M Plant Cell Rep. 2020; 39(12):1719-1741.

PMID: 32955612 PMC: 7502656. DOI: 10.1007/s00299-020-02600-5.

References

Zamocky M, Koller F . Understanding the structure and function of catalases: clues from molecular evolution and in vitro mutagenesis. Prog Biophys Mol Biol. 1999; 72(1):19-66. DOI: 10.1016/s0079-6107(98)00058-3. View

Petriv O, Tang L, Titorenko V, Rachubinski R . A new definition for the consensus sequence of the peroxisome targeting signal type 2. J Mol Biol. 2004; 341(1):119-34. DOI: 10.1016/j.jmb.2004.05.064. View

Goldberg I, HOCHMAN A . Purification and characterization of a novel type of catalase from the bacterium Klebsiella pneumoniae. Biochim Biophys Acta. 1989; 991(2):330-6. DOI: 10.1016/0304-4165(89)90124-4. View

Bononi A, Pinton P . Study of PTEN subcellular localization. Methods. 2014; 77-78:92-103. PMC: 4396696. DOI: 10.1016/j.ymeth.2014.10.002. View

Sunnadeniya R, Bean A, Brown M, Akhavan N, Hatlestad G, Gonzalez A . Tyrosine Hydroxylation in Betalain Pigment Biosynthesis Is Performed by Cytochrome P450 Enzymes in Beets (Beta vulgaris). PLoS One. 2016; 11(2):e0149417. PMC: 4758722. DOI: 10.1371/journal.pone.0149417. View

Reuter L, Ritala A, Linder M, Joensuu J . Novel Hydrophobin Fusion Tags for Plant-Produced Fusion Proteins. PLoS One. 2016; 11(10):e0164032. PMC: 5051927. DOI: 10.1371/journal.pone.0164032. View

Itzhak D, Tyanova S, Cox J, Borner G . Global, quantitative and dynamic mapping of protein subcellular localization. Elife. 2016; 5. PMC: 4959882. DOI: 10.7554/eLife.16950. View

Lametschwandtner G, Brocard C, Fransen M, Van Veldhoven P, Berger J, Hartig A . The difference in recognition of terminal tripeptides as peroxisomal targeting signal 1 between yeast and human is due to different affinities of their receptor Pex5p to the cognate signal and to residues adjacent to it. J Biol Chem. 1998; 273(50):33635-43. DOI: 10.1074/jbc.273.50.33635. View

Polturak G, Breitel D, Grossman N, Sarrion-Perdigones A, Weithorn E, Pliner M . Elucidation of the first committed step in betalain biosynthesis enables the heterologous engineering of betalain pigments in plants. New Phytol. 2015; 210(1):269-83. DOI: 10.1111/nph.13796. View

10.

Sutay Kocabas D, Bakir U, Phillips S, McPherson M, Ogel Z . Purification, characterization, and identification of a novel bifunctional catalase-phenol oxidase from Scytalidium thermophilum. Appl Microbiol Biotechnol. 2008; 79(3):407-15. DOI: 10.1007/s00253-008-1437-y. View

11.

Tanz S, Small I . In silico methods for identifying organellar and suborganellar targeting peptides in Arabidopsis chloroplast proteins and for predicting the topology of membrane proteins. Methods Mol Biol. 2011; 774:243-80. DOI: 10.1007/978-1-61779-234-2_16. View

12.

Thornton J, Taylor K, Ford D, Valentine R . Differential subcellular localization of the splice variants of the zinc transporter ZnT5 is dictated by the different C-terminal regions. PLoS One. 2011; 6(8):e23878. PMC: 3161073. DOI: 10.1371/journal.pone.0023878. View

13.

Nelson B, Cai X, Nebenfuhr A . A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 2007; 51(6):1126-36. DOI: 10.1111/j.1365-313X.2007.03212.x. View

14.

Cross L, Ebeed H, Baker A . Peroxisome biogenesis, protein targeting mechanisms and PEX gene functions in plants. Biochim Biophys Acta. 2015; 1863(5):850-62. DOI: 10.1016/j.bbamcr.2015.09.027. View

15.

Han L, Han Y, Xiao X . Truncated cotton subtilase promoter directs guard cell-specific expression of foreign genes in tobacco and Arabidopsis. PLoS One. 2013; 8(3):e59802. PMC: 3612094. DOI: 10.1371/journal.pone.0059802. View

16.

Steiner U, Schliemann W, Strack D . Assay for tyrosine hydroxylation activity of tyrosinase from betalain-forming plants and cell cultures. Anal Biochem. 1996; 238(1):72-5. DOI: 10.1006/abio.1996.0253. View

17.

Geldner N, Denervaud-Tendon V, Hyman D, Mayer U, Stierhof Y, Chory J . Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J. 2009; 59(1):169-78. PMC: 4854200. DOI: 10.1111/j.1365-313X.2009.03851.x. View

18.

Tanz S, Castleden I, Small I, Millar A . Fluorescent protein tagging as a tool to define the subcellular distribution of proteins in plants. Front Plant Sci. 2013; 4:214. PMC: 3690342. DOI: 10.3389/fpls.2013.00214. View

19.

Terlecky S, Nuttley W, McCollum D, Sock E, Subramani S . The Pichia pastoris peroxisomal protein PAS8p is the receptor for the C-terminal tripeptide peroxisomal targeting signal. EMBO J. 1995; 14(15):3627-34. PMC: 394437. DOI: 10.1002/j.1460-2075.1995.tb00032.x. View

20.

Huh W, Falvo J, Gerke L, Carroll A, Howson R, Weissman J . Global analysis of protein localization in budding yeast. Nature. 2003; 425(6959):686-91. DOI: 10.1038/nature02026. View