731
Views
3
CrossRef citations to date
0
Altmetric
Research Paper

Peroxin 14 tags peroxisomes and interacts with Nbr1 for pexophagy in the filamentous insect pathogenic fungus Beauveria bassiana

, , , , , & ORCID Icon show all
Article: 2168337 | Received 03 Aug 2022, Accepted 10 Jan 2023, Published online: 29 Jan 2023

References

  • Reggiori F Klionsky DJ. Autophagic processes in yeast: mechanism, machinery and regulation. Genetics. 2013; 194:314–24.
  • Mahalingam SS, Shukla N, Farré JC, et al. Balancing the opposing principles that govern peroxisome homeostasis. Trends Biochem Sci. 2021; 46:200–212.
  • Kiel JA, Veenhuis M, van der Klei IJ. PEX genes in fungal genomes: common, rare or redundant. Traffic. 2006; 7:1291–1303.
  • Farré JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol. 2016; 17:537–552.
  • Farré JC, Manjithaya R, Mathewson RD, et al. PpAtg30 tags peroxisomes for turnover by selective autophagy. Dev Cell. 2008; 14:365–376.
  • Motley AM, Nuttall JM, Hettema EH. Pex3‑anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 2012; 31:2852–2868.
  • Burnett SF, Farré JC, Nazarko TY, et al. Peroxisomal Pex3 activates selective autophagy of peroxisomes via interaction with the pexophagy receptor Atg30. J Biol Chem. 2015; 290:8623–8631.
  • Klein DA, Paschke MW. Filamentous fungi: the indeterminate lifestyle and Microbial ecology. Microb Ecol. 2004; 47:224–235.
  • Ying SH, Feng MG. Insight into vital role of autophagy in sustaining biological control potential of fungal pathogens against pest insects and nematodes. Virulence. 2019; 10: 429–437.
  • Werner A, Herzog B, Voigt O, et al. NBR1 is involved in selective pexophagy in filamentous ascomycetes and can be functionally replaced by a tagged version of its human homolog. Autophagy. 2019; 15:78–97.
  • Kirkin V, Lamark T, Sou YS, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell. 2009; 33:505–516.
  • Pieuchot L, Jedd G. Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu Rev Microbiol. 2012; 66:237–263.
  • Bellu AR, Komori M, van der Klei IJ, et al. Peroxisome biogenesis and selective degradation converge at Pex14p. J Biol Chem. 2001; 276: 44570–4457.
  • Deng Y, Qu Z, Naqvi NI. The role of snx41-based pexophagy in Magnaporthe development. PLoS One. 2013; 8:e79128.
  • Lopez-Perez M, Rodriguez-Gomez D, Loera O. Production of conidia of Beauveria bassiana in solid-state culture: current status and future perspectives. Crit Rev Biotechnol. 2015; 35: 334–341.
  • Ortiz-Urquiza A, Keyhani NO. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects. 2013; 4: 357–374.
  • Wanchoo A, Lewis MW, Keyhani NO. Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology-SGM. 2009; 155:3121–3133.
  • Ding JL, Hou J, Feng MG, et al. Transcriptomic analyses reveal comprehensive responses of insect hemocytes to mycopathogen Beauveria bassiana, and fungal virulence-related cell wall protein assists pathogen to evade host cellular defense. Virulence. 2020; 11:1352–1365.
  • Hou J, Lin HY, Ding JL, et al. Peroxins in peroxisomal receptor export system contribute to development, stress response, and virulence of insect pathogenic fungus Beauveria bassiana. J Fungi (Basel). 2022; 8:622.
  • Ding JL, Peng YJ, Chu XL, et al. Autophagy-related gene BbATG11 is indispensable for pexophagy and mitophagy, and contributes to stress response, conidiation and virulence in the insect mycopathogen Beauveria bassiana. Environ Microbiol. 2018; 20:3309–3324.
  • Pang MY, Lin HY, Hou J, et al. Different contributions of the peroxisomal import protein Pex5 and Pex7 to development, stress response and virulence of insect fungal pathogen Beauveria bassiana. J Appl Microbiol. 2022; 132:509–519.
  • Johnson MA, Snyder WB, Cereghino JL, et al. Pichia pastoris Pex14p, a phosphorylated peroxisomal membrane protein, is part of a PTS-receptor docking complex and interacts with many peroxins. Yeast. 2001; 18:621–641.
  • Bergin D, Reeves EP, Renwick J, et al. Superoxide production in Galleria mellonella hemocytes: Identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun. 2005; 73:4161–4170.
  • Wang JY, Li L, Chai RY, et al. Pex13 and Pex14, the key components of the peroxisomal docking complex, are required for peroxisome formation, host infection and pathogenicity-related morphogenesis in Magnaporthe oryzae. Virulence. 2019; 10:292–314.
  • Chen Y, Zheng S, Ju Z, et al. Contribution of peroxisomal docking machinery to mycotoxin biosynthesis, pathogenicity and pexophagy in the plant pathogenic fungus Fusarium graminearum. Environ Microbiol. 2018; 20:3224–3245.
  • Jiang L, Hara-Kuge S, Yamashita S, et al. Peroxin Pex14p is the key component for coordinated autophagic degradation of mammalian peroxisomes by direct binding to LC3-II. Genes Cells. 2015; 20:36–49.
  • Nazarko TY, Ozeki K, Till A, et al. Peroxisomal Atg37 binds Atg30 or palmitoyl-CoA to regulate phagophore formation during pexophagy. J Cell Biol. 2014; 204:541–557.
  • Deosaran E, Larsen KB, Hua R, et al. NBR1 acts as an autophagy receptor for peroxisomes. J Cell Sci. 2013;126:939–952.
  • Noda NN, Kumeta H, Nakatogawa H, et al. Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells. 2008; 13:1211–1218.
  • Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011; 7:279–296.
  • Svenning S, Lamark T, Krause K, et al. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy. 2011; 7:993–1010.
  • Zientara-Rytter K, Subramani S. Mechanistic insights into the role of Atg11 in selective autophagy. J Mol Biol. 2020; 432:104–122.
  • Farré JC, Burkenroad A, Burnett SF, et al. Phosphorylation of mitophagy and pexophagy receptors coordinates their interaction with Atg8 and Atg11. EMBO Rep. 2013; 14:441–449.
  • Xiao G, Ying SH, Zheng P, et al. Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep. 2012; 2:483.
  • Letunic I, Khedkar S, Bork P. SMART: recent updates, new developments and status in 2020. Nucleic Acids Res. 2021; 49:D458–460−.
  • Ding JL, Hou J, Li XH, et al. Transcription activator Swi6 interacts with Mbp1 in MluI cell cycle box-binding complex and regulates hyphal differentiation and virulence in Beauveria bassiana. J Fungi (Basel). 2021; 7:411.
  • Lin HY, Ding JL, Peng YJ, et al. Proteomic and phosphoryproteomic investigations reveal that autophagy-related protein 1, a protein kinase for autophagy initiation, synchronously deploys phosphoregulation on the ubiquitin-like conjugation system in the mycopathogen Beauveria bassiana. mSystems. 2022; 7:e0146321.
  • Wang JJ, Peng YJ, Feng MG, et al. Functional analysis of the mitochondrial gene mitofilin in the filamentous entomopathogenic fungus Beauveria bassiana. Fungal Genet Biol. 2019; 132:103250.