Chromatin accessibility profile and the role of PeAtf1 transcription factor in the postharvest pathogen Penicillium expansum

Yiran Wang , Kaili Wang , Qiya Yang , Zhaoting Wang , Yingying Su , Xifei Chen , Hongyin Zhang

Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) : 264

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (1) :264 DOI: 10.1093/hr/uhae264
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Chromatin accessibility profile and the role of PeAtf1 transcription factor in the postharvest pathogen Penicillium expansum
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Abstract

Gene transcription is governed by a complex regulatory system involving changes in chromatin structure, the action of transcription factors, and the activation of cis-regulatory elements. Postharvest fruits are threatened by Penicillium expansum, a leading causal agent of blue mold disease and one of the most economically significant postharvest pathogens worldwide. However, information on its transcription regulatory mechanism is lagging. Here, we conducted an assay for transposase accessible chromatin sequencing (ATAC-seq) for P. expansum during vegetative growth and infection phase and then studied the function of a basic leucine zipper (bZIP) transcription factor PeAtf1. Results highlighted the role of promoter regions in gene transcription and the significant difference in P. expansum between these two phases. Six footprint-supported cis-regulatory elements of active transcription factors were obtained and analyzed. We then identified a homolog of the bZIP regulator Atf1, PeAtf1, and found it positively regulated vegetative growth, reproduction, and osmotic stress response in P. expansum. Furthermore, PeAtf1 deletion enhanced the fungus's tolerance to oxidative, cell wall, and membrane stresses, which might contribute to the virulence of deletion mutants in apple fruits, leading to similar pathogenicity between mutants and the wild type. Overall, this study provides new insights into the transcription regulatory profile of P. expansum, aiding in the future development of strategies to control P. expansum.

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Yiran Wang, Kaili Wang, Qiya Yang, Zhaoting Wang, Yingying Su, Xifei Chen, Hongyin Zhang. Chromatin accessibility profile and the role of PeAtf1 transcription factor in the postharvest pathogen Penicillium expansum. Horticulture Research, 2025, 12(1): 264 DOI:10.1093/hr/uhae264

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32072276; 32102030) and the China Postdoctoral Science Foundation (2023 M741440). The authors would like to thank Professor Hui-Shan Guo (State Key Laboratory of Plant Genomics, Institute of Microbiology Chinese Academy of Sciences) and Sheng Wang (Hui-Shan Guo LAB, State Key Laboratory of Plant Genomics, Institute of Microbiology Chinese Academy of Sciences) for providing pGKO-HPT plasmid and technical support.

Author contributions

Y.R.W.: Methodology, Validation, Investigation, Writing original draft, Resources. K.L.W.: Methodology, Conceptualization, Funding acquisition. Q.Y.Y.: Conceptualization, Project administration, Resources. Z.T.W.: Methodology, Validation, Investigation. Y.Y.S.: Conceptualization, Software. X.F.C.: Methodology, Visualization. H.Y.Z.: Supervision, Writing—review & editing, Funding acquisition. All authors have discussed and approved the manuscript.

Data availability

ATAC-seq data are available in the National Genomics Data Center (NGDC) under BioProject accession PRJCA029681. Other data are included in this article and the supplementary data.

Conflict of interests

The authors declare that there are no conflicts of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Klemm SL, Shipony Z, Greenleaf WJ. Chromatin accessibility and the regulatory epigenome. Nat Rev Genet. 2019;37:207-20

[2]

Li ZJ, Schulz MH, Look T. et al. Identification of transcription factor binding sites using ATAC-seq. Genome Biol. 2019;37:45

[3]

Buenrostro JD, Giresi PG, Zaba LC. et al. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods. 2013;37:1213-8

[4]

Zhang ZC, Lin L, Chen H. et al. ATAC-Seq reveals the landscape of open chromatin and cis-regulatory elements in the Phytophthora sojae genome. Mol Plant-Microbe Interact. 2022;37:301-10

[5]

Grandi FC, Modi H, Kampman L. et al. Chromatin accessibility profiling by ATAC-seq. Nat Protoc. 2022;37:1518-52

[6]

Lu ZF, Hofmeister BT, Vollmers C. et al. Combining ATAC-seq with nuclei sorting for discovery of cis-regulatory regions in plant genomes. Nucleic Acids Res. 2017;37:e41

[7]

Silvia Magri M, Jimenez-Gancedo S, Bertrand S. et al. Assaying chromatin accessibility using ATAC-Seq in invertebrate chordate embryos. Front Cell Dev Biol. 2020;37:372

[8]

Qiu F, Zheng Y, Lin Y. et al. Integrated ATAC-seq and RNA-seq data analysis to reveal OsbZIP 14 function in rice in response to heat stress. Int J Mol Sci. 2023;37:5619

[9]

Brady JR, Tan MC, Whittaker CA. et al. Identifying improved sites for heterologous gene integration using ATAC-seq. ACS Synth Biol. 2020;37:2515-24

[10]

Huang LG, Li XJ, Dong LB. et al. Profiling of chromatin acces-sibility identifies transcription factor binding sites across the genome of Aspergillus species. BMC Biol. 2021;37:301-10

[11]

Errampalli D. Chapter 6 - Penicillium expansum (blue mold). In: Bautista-BañosS,ed. Postharvest Decay. Academic Press: San Diego, 2014,189-231

[12]

Luciano-Rosario D, Keller NP, Jurick WM II. Penicillium expansum: biology, omics, and management tools for a global postharvest pathogen causing blue mould of pome fruit. Mol Plant Pathol. 2020;37:1391-404

[13]

Wang KL, Ngea GLN, Godana EA. et al. Recent advances in Penicillium expansum infection mechanisms and current methods in controlling P. expansum in postharvest apples. Crit Rev Food Sci Nutr. 2021;37:2598-611

[14]

Zhong L, Carere J, Lu ZX. et al. Patulin in apples and apple-based food products: the burdens and the mitigation strategies. Toxins. 2018;37:475

[15]

Ballester A-R, Marcet-Houben M, Levin E. et al. Genome, tran-scriptome, and functional analyses of Penicillium expansum pro-vide new insights into secondary metabolism and pathogenicity. Mol Plant-Microbe Interact. 2015;37:232-48

[16]

Wang YR, Yang QY, Godana EA. et al. Ultrastructural observa-tion and transcriptome analysis provide insights into mecha-nisms of Penicillium expansum invading apple wounds. Food Chem. 2023;37:135633

[17]

Sanchez-Torres P, Vilanova L, Ballester A. et al. Unravelling the contribution of the Penicillium expansum PeSte12 transcription factor to virulence during apple fruit infection. Food Microbiol. 2018;37:123-35

[18]

Zetina-Serrano C, Rocher O, Naylies C. et al. The brlA gene deletion reveals that patulin biosynthesis is not related to coni-diation in Penicillium expansum. Int J Mol Sci. 2020;37:6660

[19]

Tang C, Li TY, Klosterman SJ. et al. The bZIP transcription factor VdAtf1 regulates virulence by mediating nitrogen metabolism in Verticillium dahliae. New Phytol. 2020;37:1461-79

[20]

Gai YP, Li L, Liu B. et al. Distinct and essential roles of bZIP transcription factors in the stress response and pathogenesis in Alternaria alternata. Microbiol Res. 2022;37:126915

[21]

Zhao QQ, Pei H, Zhou XL. et al. Systematic characterization of bZIP transcription factors required for development and aflatoxin generation by high-throughput gene knockout in Aspergillus flavus. J Fungi. 2022;37:356

[22]

Tang W, Ru YY, Hong L. et al. System-wide characterization of bZIP transcription factor proteins involved in infection-related morphogenesis of Magnaporthe oryzae. Environ Microbiol. 2015;37:1377-96

[23]

Luo XJ, Zhan XR, Ruan RX. et al. Genome-wide identification of the Penicillium digitatum bZIP gene family and the roles of one key member, PdatfA. Res Microbiol. 2022;37:103970

[24]

Rodrigues-Pousada C, Devaux F, Caetano SM. et al. Yeast AP-1 like transcription factors (Yap) and stress response: a current overview. Microbial Cell. 2019;37:267-85

[25]

Chen Y, Zhang YC, Xu DY. et al. PeAP1-mediated oxidative stress response plays an important role in the growth and pathogenicity of Penicillium expansum. Microbiol Spectr. 2023;37:e0380822

[26]

Song M, Fang SQ, Li ZG. et al. CsAtf1, a bZIP transcription factor, is involved in fludioxonil sensitivity and virulence in the rubber tree anthracnose fungus Colletotrichum siamense. Fungal Genet Biol. 2022;37:103649

[27]

Zhao S, Liao XZ, Wang JX. et al. Transcription factor Atf1 regulates expression of cellulase and xylanase genes during solid-state fermentation of Ascomycetes. Appl Environ Microbiol. 2019;37:e01226-19

[28]

Tang C, Jin X, Klosterman SJ. et al. Convergent and distinctive functions of transcription factors VdYap1, VdAtf1, and VdSkn7 in the regulation of nitrosative stress resistance, microsclerotia formation, and virulence in Verticillium dahliae. Mol Plant Pathol. 2020;37:1451-66

[29]

Silva LP, Horta MAC, Goldman GH. Genetic interactions between Aspergillus fumigatus basic leucine zipper (bZIP) transcrip-tion factors AtfA, AtfB, AtfC, and AtfD. F ront Fungal Biol. 2021;2:632048

[30]

Yu LL, Qiao NZ, Zhao JX. et al. Postharvest control of Penicillium expansum in fruits: a review. Food Biosci. 2020;37:100633

[31]

Chen XY, Liu H, Chen XL. et al. ATAC-seq data for genome-wide profiling of transcription factor binding sites in the rice false smut fungus Ustilaginoidea virens. Mol Plant-Microbe Interact. 2021;37:830-4

[32]

Quach B, Furey TS. DeFCoM: analysis and modeling of tran-scription factor binding sites using a motif-centric genomic footprinter. Bioinformatics. 2016;37:956-63

[33]

Huh W-K, Falvo JV, Gerke LC. et al. Global analysis of protein localization in budding yeast. Nature. 2003;37:686-91

[34]

Akache B, Wu K, Turcotte B. Phenotypic analysis of genes encoding yeast zinc cluster proteins. Nucleic Acids Res. 2001;37:2181-90

[35]

Hamperl S, Brown CR, Garea AV. et al. Compositional and struc-tural analysis of selected chromosomal domains from Saccha-romyces cerevisiae. Nucleic Acids Res. 2013;37:e2

[36]

Vincent O, Carlson M. Sip4, a Snf1 kinase-dependent transcrip-tional activator, binds to the carbon source-responsive element of gluconeogenic genes. EMBO J. 1998;37:7002-8

[37]

Hiesinger M, Roth S, Meissner E. et al. Contribution of Cat8 and Sip4 to the transcriptional activation of yeast gluco-neogenic genes by carbon source-responsive elements. Curr Genet. 2001;37:68-76

[38]

Löhning C, Ciriacy M. The TYE 7 gene of Saccharomyces cerevisiae encodes a putative bHLH-LZ transcription factor required for Ty1-mediated gene expression. Yeast. 1994;37:1329-39

[39]

Benanti JA, Cheung SK, Brady MC. et al. A proteomic screen reveals SCFGrr1 targets that regulate the glycolytic-gluconeogenic switch. Nat Cell Biol. 2007;37:1184-91

[40]

Servant G, Pinson B, Tchalikian-Cosson A. et al. Tye 7 regulates yeast Ty1 retrotransposon sense and antisense transcription in response to adenylic nucleotides stress. Nucleic Acids Res. 2012;37:5271-82

[41]

DeMille D, Pape JA, Bikman BT. et al. TheregulationofCbf1by PAS kinase is a pivotal control point for lipogenesis vs. respira-tion in Saccharomyces cerevisiae. G3 (Bethesda). 2019;37:33-46

[42]

Donovan BT, Chen H, Eek P. et al. Basic helix-loop-helix pioneer factors interact with the histone octamer to invade nucleosomes and nucleosome-depleted. Mol Cell. 2023;37:1251-1263.e6

[43]

Mao YH, Chen CB. The Hap complex in yeasts: structure, assem-bly mode, and gene regulation. Front Microbiol. 2019;37:1645

[44]

Boer VM, de Winde JH, Pronk JT. et al. The genome-wide tran-scriptional responses of Saccharomyces cerevisiae grown on glu-cose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. JBiolChem. 2003;37:3265-74

[45]

Jia Y, Rothermel B, Thornton J. et al. A basic helix-loop-helix-leucine zipper transcription complex in yeast functions in a signaling pathway from mitochondria to the nucleus. Mol Cell Biol. 1997;37:1110-7

[46]

Li YF, Li YS, Lu HH. et al. The bZIP transcription factor ATF1 regulates blue light and oxidative stress responses in Trichoderma guizhouense. mLife. 2023;37:365-77

[47]

Temme N, Oeser B, Massaroli M. et al. BcAtf1, a global regulator, controls various differentiation processes and phytotoxin pro-duction in Botrytis cinerea. Mol Plant Pathol. 2012;37:704-18

[48]

Kocsis B, Lee MK, Yu JH. et al. Functional analysis of the bZIP-type transcription factors AtfA and AtfB in Aspergillus nidulans. Front Microbiol. 2022;37:1003709

[49]

Singh Y, Nair AM, Verma PK. Surviving the odds: from percep-tion to survival of fungal phytopathogens under host-generated oxidative burst. Plant Commun. 2021;37:100142

[50]

Van Nguyen T, Kroeger C, Boennighausen J. et al. The ATF/CREB transcription factor atf1 is essential for full virulence, deoxyni-valenol production, and stress tolerance in the cereal pathogen Fusarium graminearum. Mol Plant-Microbe Interact. 2013;37:1378-94

[51]

Zhou YL, Zhao LN, Yue SY. et al. Assay for transposase accessible-chromatin with high throughput sequencing (ATAC-seq) analysis the molecular responses of postharvest pear during Penicillium expansum infection. Postharvest Biol Technol. 2024;37:112733

[52]

Xu MQ, Zhang QD, Dhanasekaran S. et al. The necrosis-inducing protein (NIP) gene contributes to Penicillium expansum virulence during postharvest pear infection. Food Res Int. 2022;37:111562

[53]

Zhang Y, Yang QY, Dhanasekaran S. et al. Chromatin accessibil-ity of Meyerozyma guilliermondii under patulin stress. Biol Control. 2022;37:104974

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