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A non-canonical fungal peroxisome PTS-1 signal, SYM, and its evolutionary aspects

Ámon, Judit and Nemuuzaya, Suren and Alczheimer, Kevin and Kocsubé, Sándor and Farkas, Zoltán and Svorenj, Gergő and Gácser, Attila and Tyagi, Chetna and Kozma-Bognár, László and Kozma-Bognárné Hamari, Zsuzsanna (2025) A non-canonical fungal peroxisome PTS-1 signal, SYM, and its evolutionary aspects. SCIENTIFIC REPORTS, 15 (1). No. 28088. ISSN 2045-2322

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Abstract

Proteins localized to peroxisomes, particularly those expressed under specific conditions or in low abundance, are often undetected by routine proteomics methods due to detection sensitivity limits. In silico identification and experimental validation of peroxisomal targeting signals (PTSs) offer a reliable alternative. We demonstrate that SYM, a non-canonical plant PTS-1 signal, functions similarly in Aspergillus nidulans , as GFP tagged with a SYM C-terminal tripeptide localizes to peroxisomes. One of two native A. nidulans proteins with C-terminal SYM tripeptide shows weak peroxisomal localization alongside cytoplasmic presence, indicating that only a subset of proteins with non-canonical signals access peroxisomes. In silico analysis of 1,010 fungal genomes identified diverse SYM-proteins with variable functions, suggesting that non-canonical PTS-1 signals may evolve spontaneously. Two-thirds of SYM-proteins are predicted to localize to specific intracellular compartments other than the peroxisome. We propose that despite their predicted localization, these proteins possessing SYM as a non-canonical peroxisomal signal might also have peroxisomal presence. Among SYM-proteins, pectinesterases, known plant pathogen virulence factors, were frequent. Notably, 25% of fungal pectinesterases harbor non-canonical PTS-1 signals, suggesting that partial peroxisomal localization of pectinesterases has evolved convergently. This suggests that partial peroxisomal localization may enhance protein functional flexibility, contributing to the organism’s adaptability.

Item Type: Article
Additional Information: Funding Agency and Grant Number: University of Szeged [DE-AC02-05CH11231]; DOE Office of Science [261572, 675858, 777536, 101017567, INFN-LNL-2, IN2P3-CPPM]; FP7 WeNMR; NIKHEF; US Open Science Grid; National Academy of Scientist Education Program of the National Biomedical Foundation under the sponsorship of the Hungarian Ministry of Culture and Innovation [AN-128740, K-134567]; National Research, Development and Innovation Office Funding text: JGI Sequences used in the SYM-protein analysis and pectinesterase localization analysis were from the US Department of Energy Joint Genome Institute in collaboration with the user community. We acknowledge the 1000 Fungal Genomes project consortium (PI's: F. Martin, R. Vilgalys, S.E. Baker, I.V. Grigoriev, J. Spatafora, M.R. Andersen, L-J. Ma, R. Proctor, R. Hamelin, G. Bonito, J.J. Coleman, H.C. Kistler, A. Eichmeier, A. Owensby Quandt, (A) Kohler, (B) Min, (C) Hori, C. Hittinger, C. Hansel, D.C. Eastwood, (D) Lindner, D. Raudabaugh, D. Catcheside, D. Salvachua, I-G. Choi, J.E. Stajich, J. Gladden, J. Vogel, J.W. Taylor, K. Peay, K. Solomon, L. Nagy, M.C. Aime, M. Kluge, M-N. Rosso, M. Campbell, M. Freitag, N. Nguyen, O. Yarden, P. Chain, P. Inderbitzin, P. Crous, P. Gladieux, P.E. Busby, S. Duplessis, S.W. Singer, T.D. Bruns, T.Y. James, T. Ward, and V. Subramanian) for providing access to unpublished genome data and permitting us to publish our analysis. The genome sequence data were conducted by the U.S. Department of Energy (DOE) Joint Genome Institute (http://www.jgi.doe.gov/) (https://ror.org/04xm1d337), a DOE Office of Science User Facility, was supported by the DOE Office of Science under contract number DE-AC02-05CH11231. he FP7 WeNMR (project# 261572), H2020 West-Life (project# 675858), the EOSC-hub (project# 777536) and the EGI-ACE (project# 101017567) European e-Infrastructure projects are acknowledged for the use of their web portals, which make use of the EGI infrastructure with the dedicated support of CESNET-MCC, INFN-LNL-2, NCG-INGRID-PT, TW-NCHC, IFCA-LCG2, UA-BITP, TR-FC1-ULAKBIM, CSTCLOUD-EGI, IN2P3-CPPM, SURFsara and NIKHEF, and the additional support of the national GRID Initiatives of Belgium, France, Italy, Germany, the Netherlands, Poland, Portugal, Spain, UK, Taiwan and the US Open Science Grid. Research work of AG and GS were conducted with the support of the National Academy of Scientist Education Program of the National Biomedical Foundation under the sponsorship of the Hungarian Ministry of Culture and Innovation. LKB's work was supported by the National Research, Development and Innovation Office (grant numbers AN-128740 and K-134567).
Subjects: Q Science / természettudomány > QH Natural history / természetrajz > QH301 Biology / biológia > QH3015 Molecular biology / molekuláris biológia
SWORD Depositor: MTMT SWORD
Depositing User: MTMT SWORD
Date Deposited: 08 Feb 2026 15:02
Last Modified: 08 Feb 2026 15:02
URI: https://real.mtak.hu/id/eprint/233500

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