Skip to main content
SpringerLink
Log in

CDF family of zinc transporters ZRC-1, MSC-2, and ZRG-17 are involved in survival at high zinc conditions, vegetative development, and cellulase utilization in Neurospora crassa

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

The cation diffusion facilitator (CDF) family of zinc transporters plays a crucial role in zinc homeostasis in eukaryotes, including fungi. Here, we investigated the cell functions and genetic interactions of CDF zinc transporters zrc-1 and msc-2 in Neurospora crassa. The Δzrc-1 mutant could not grow in a high-zinc environment, indicating that the zinc transporter protein ZRC-1 was essential for growth in high-zinc conditions. However, the deletion of msc-2 did not show any severe phenotypic defects. Furthermore, we studied the genetic interactions of the zinc transporters using the CDF double mutants. Previously, zrg-17 was reported to be critical, where the Δzrg-17 mutant showed defects in both vegetative development and asexual sporulation. Interestingly, the Δmsc-2;Δzrg-17 double mutant showed phenotypes similar to the wild type, and restored the phenotypic defects of the Δzrg-17 mutation. However, the Δzrc-1;Δmsc-2 and Δzrc-1;Δzrg-17 double mutants continue to display phenotypic defects like their parental single mutants. The double mutant Δzrc-1;Δzrg-17 showed severe vegetative growth defects, including slow growth, short aerial hyphae, narrowed septation, and defective asexual sporulation. In addition, aerial hyphae development of the Δzrc-1;Δmsc-2 and Δzrc-1;Δzrg-17 double mutants were reduced under endoplasmic reticulum stress. Thus, this study revealed the cell functions and genetic interactions of zrc-1, msc-2, and zrg-17 for vegetative development and tolerance to stress conditions in N. crassa.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  • Amich J and Calera JA 2014 Zinc acquisition: a key aspect in Aspergillus fumigatus virulence. Mycopathologia 178 379–385

    Article  PubMed  Google Scholar 

  • Amico-Ruvio SA, Murthy SE, Smith TP, et al. 2011 Zinc effects on NMDA receptor gating kinetics. Biophys J. 100 1910–1918

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barba-Ostria C, Lledías F and Georgellis D 2011 The Neurospora crassa DCC-1 protein, a putative histidine kinase, is required for normal sexual and asexual development and carotenogenesis. Eukaryot. Cell 10 1733–1739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barman A and Tamuli R 2017 The pleiotropic vegetative and sexual development phenotypes of Neurospora crassa arise from double mutants of the calcium signaling genes plc-1, splA2, and cpe-1. Curr. Genet. 63 861–875

    Article  PubMed  CAS  Google Scholar 

  • Bellotti D, Miller A, Rowińska-Żyrek M, et al. 2022 Zn2+ and Cu2+ binding to the extramembrane loop of Zrt2, a zinc transporter of Candida albicans. Biomolecules 12 121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bird AJ and Wilson S 2020 Zinc homeostasis in the secretory pathway in yeast. Curr. Opin. Chem. Biol. 55 145–150

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boch A, Trampczynska A, Simm C, et al. 2008 Loss of Zhf and the tightly regulated zinc-uptake system SpZrt1 in Schizosaccharomyces pombe reveals the delicacy of cellular zinc balance. FEMS Yeast Res. 8 883–896

    Article  PubMed  CAS  Google Scholar 

  • Boyce KJ, Cao C, and Andrianopoulos A 2016 Two-component signaling regulates osmotic stress adaptation via sskA and the high-osmolarity glycerol MAPK pathway in the human pathogen Talaromyces marneffei. mSphere 1 e00086-15

  • Chao Y and Fu D 2004 Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J. Biol. Chem. 279 17173–17180

    Article  PubMed  CAS  Google Scholar 

  • Cho M, Hu G, Caza M, et al. 2018 Vacuolar zinc transporter Zrc1 is required for detoxification of excess intracellular zinc in the human fungal pathogen Cryptococcus neoformans. J. Microbiol. 56 65–71

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi S, Hu YM, Corkins ME, et al. 2018 Zinc transporters belonging to the Cation Diffusion Facilitator (CDF) family have complementary roles in transporting zinc out of the cytosol. PLoS Genet. 14 e1007262

    Article  PubMed  PubMed Central  Google Scholar 

  • Clemens S 2022 The cell biology of zinc. J. Exp. Bot. 73 1688–1698

    Article  PubMed  CAS  Google Scholar 

  • Clemens S, Bloss T, Vess C, et al. 2002 A transporter in the endoplasmic reticulum of Schizosaccharomyces pombe cells mediates zinc storage and differentially affects transition metal tolerance. J. Biol. Chem. 277 18215–18221

    Article  PubMed  CAS  Google Scholar 

  • Collier LA, Ghosh A and Borkovich KA 2020 Heterotrimeric G-protein signaling is required for cellulose degradation in Neurospora crassa. mBio 11 e02419–e02420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cousins RJ, Liuzzi JP and Lichten LA 2006 Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281 24085–24089

    Article  PubMed  CAS  Google Scholar 

  • Crawford AC, Lehtovirta-morley LE, Alamir O, et al. 2018 Biphasic zinc compartmentalisation in a human fungal pathogen. PLoS Pathog. 14 e1007013

    Article  PubMed  PubMed Central  Google Scholar 

  • Cuajungco MP and Lees GJ 1997 Zinc metabolism in the brain: Relevance to human neurodegenerative disorders. Neurobiol. Dis. 4 137–169

    Article  PubMed  CAS  Google Scholar 

  • Davis RH and de Serres FJ 1970 Metabolism of amino acids and amines Part A. Methods Enzymol. 17 79–143

    Article  Google Scholar 

  • Deka R, Kumar R, and Tamuli R 2011 Neurospora crassa homologue of Neuronal Calcium Sensor-1 has a role in growth, calcium stress tolerance, and ultraviolet survival. Genetica 139 885–894

  • Dodson G and Steiner D 1998 The role of assembly in insulin’s biosynthesis. Curr. Opin. Struct. Biol. 8 189–194

    Article  PubMed  CAS  Google Scholar 

  • Eide DJ 2006 Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta Mol. Cell Res. 1763 711–722

    Article  CAS  Google Scholar 

  • Eide DJ 2009 Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J. Biol. Chem. 284 18565–18568

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellis CD, Wang F, MacDiarmid CW, et al. 2004 Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J. Cell Biol. 166 325–335

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellis CD, MacDiarmid CW and Eide DJ 2005 Heteromeric protein complexes mediate zinc transport into the secretory pathway of eukaryotic cells. J. Biol. Chem. 280 28811–28818

    Article  PubMed  CAS  Google Scholar 

  • Fang Y, Sugiura R, Ma Y, et al. 2008 Cation diffusion facilitator Cis4 is implicated in golgi membrane trafficking via regulating zinc homeostasis in fission yeast. Mol. Biol. Cell 19 1295–1303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feige MJ and Hendershot LM 2011 Disulfide bonds in ER protein folding and homeostasis. Curr. Opin. Cell Biol. 23 167–175

    Article  PubMed  CAS  Google Scholar 

  • Freedman RB 1995 The formation of protein disulphide bonds. Curr. Opin. Struct. Biol. 5 85–91

    Article  PubMed  CAS  Google Scholar 

  • Gaither LA and Eide DJ 2001 Eukaryotic zinc transporters and their regulation. Biometals 14 251–270

    Article  PubMed  CAS  Google Scholar 

  • Harding HP, Zhang Y and Ron D 1999 Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397 271–274

    Article  PubMed  CAS  Google Scholar 

  • Hetz C 2012 The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13 89–102

    Article  PubMed  CAS  Google Scholar 

  • Holm L 2022 Dali server: structural unification of protein families. Nucleic Acids Res. 50 210–215

    Article  Google Scholar 

  • Kambe T, Weaver BP and Andrews GK 2008 The genetics of essential metal homeostasis during development. Genesis 46 214–228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kambe T, Matsunaga M and Takeda TA 2017 Understanding the contribution of zinc transporters in the function of the early secretory pathway. Int. J. Mol. Sci. 18 2179

    Article  PubMed  PubMed Central  Google Scholar 

  • Kambe T, Taylor KM and Fu D 2021 Zinc transporters and their functional integration in mammalian cells. J. Biol. Chem. 296 100320

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kamizono A, Nishizawa M, Teranishi Y, et al. 1989 Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 219 161–167

    Article  PubMed  CAS  Google Scholar 

  • Kays AM, Rowley PS, Baasiri RA, et al. 2000 Regulation of conidiation and adenylyl cyclase levels by the Galpha protein GNA-3 in Neurospora crassa. Mol. Cell. Biol. 20 7693–7705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim MJ, Kil M, Jung JH, et al. 2008 Roles of zinc-responsive transcription factor Csr1 in filamentous growth of the pathogenic yeast Candida albicans. J. Microbiol. Biotechnol. 18 242–247

    PubMed  CAS  Google Scholar 

  • Kiranmayi P and Mohan PM 2006 Metal transportome of Neurospora crassa. In Silico Biol. 6 169–180

    PubMed  CAS  Google Scholar 

  • Kiranmayi P, Tiwari A, Sagar KP, et al. 2009 Functional characterization of tzn1 and tzn2-zinc transporter genes in Neurospora crassa. Biometals 22 411–420

    Article  PubMed  CAS  Google Scholar 

  • Ko J, Park H, Heo L, et al. 2012 GalaxyWEB server for protein structure prediction and refinement. Nucleic Acids Res. 40 294–297

    Article  Google Scholar 

  • Koh JY 2001 Zinc and disease of the brain. Mol. Neurobiol. 24 99–106

    Article  PubMed  CAS  Google Scholar 

  • Laskowski RA, MacArthur MW, Moss DS, et al. 1993 PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 283–291

    Article  CAS  Google Scholar 

  • Linke K, Wolfram T, Bussemer J, et al. 2003 The roles of the two zinc binding sites in DnaJ. J. Biol. Chem. 278 44457–44466

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ and Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25 402–408

    Article  PubMed  CAS  Google Scholar 

  • López-Berges MS 2020 ZafA-mediated regulation of zinc homeostasis is required for virulence in the plant pathogen Fusarium oxysporum. Mol. Plant Pathol. 21 244–249

    Article  PubMed  Google Scholar 

  • Lu M and Fu D 2007 Structure of the zinc transporter YiiP. Science 317 1746–1748

    Article  PubMed  CAS  Google Scholar 

  • Lyons TJ, Gasch AP, Gaither LA, et al. 2000 Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc. Natl. Acad. Sci. USA 97 7957–7962

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • MacDiarmid CW, Gaither LA and Eide D 2000 Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J. 19 2845–2855

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • MacDiarmid CW, Milanick MA and Eide DJ 2003 Induction of the ZRC1 metal tolerance gene in zinc-limited yeast confers resistance to zinc shock. J. Biol. Chem. 278 15065–15072

    Article  PubMed  CAS  Google Scholar 

  • McCluskey K, Wiest A and Plamann M 2010 The fungal genetics stock center: A repository for 50 years of fungal genetics research. J. Biosci. 35 119–126

    Article  PubMed  CAS  Google Scholar 

  • Mishra C, Keskar S and Rao M 1984 Production and properties of extracellular endoxylanase from Neurospora crassa. Appl. Environ. Microbiol. 48 224–228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Miyabe S, Izawa S and Inoue Y 2000 Expression of ZRC1 coding for suppressor of zinc toxicity is induced by zinc-starvation stress in Zap1-dependent fashion in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 276 879–884

    Article  PubMed  CAS  Google Scholar 

  • Miyabe S, Izawa S and Inoue Y 2001 The Zrc1 is involved in zinc transport system between vacuole and cytosol in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 282 79–83

    Article  PubMed  CAS  Google Scholar 

  • Mocchegiani E, Bertoni-Freddari C, Marcellini F, et al. 2005 Brain, aging and neurodegeneration: Role of zinc ion availability. Prog. Neurobiol. 75 367–390

    Article  PubMed  CAS  Google Scholar 

  • Montanini B, Blaudez D, Jeandroz S, et al. 2007 Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: Improved signature and prediction of substrate specificity. BMC Genomics 8 107

    Article  PubMed  PubMed Central  Google Scholar 

  • Montenegro-Montero A, Goity A and Larrondo LF 2015 The bZIP transcription factor HAC-1 is involved in the unfolded protein response and is necessary for growth on cellulose in Neurospora crassa. PLoS One 10 e013141

    Article  Google Scholar 

  • Moreno MÁ, Ibrahim-Granet O, Vicentefranqueira R, et al. 2007 The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol. Microbiol. 64 1182–1197

    Article  PubMed  CAS  Google Scholar 

  • Mouriño-Pérez RR 2013 Septum development in filamentous ascomycetes. Fungal Biol. Rev. 27 1–9

  • Navarro-Sampedro L, Yanofsky C and Corrochano LM 2008 A genetic selection for Neurospora crassa mutants altered in their light regulation of transcription. Genetics 178 171–183

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nicolson TJ, Bellomo EA, Wijesekara N, et al. 2009 Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 58 2070–2083

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nies DH 2003 Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27 313–339

    Article  PubMed  CAS  Google Scholar 

  • Nobile CJ, Nett JE, Hernday AD, et al. 2009 Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 7 e1000133

    Article  PubMed  PubMed Central  Google Scholar 

  • Park HS and Yu JH 2012 Genetic control of asexual sporulation in filamentous fungi. Curr. Opin. Microbiol. 15 669–677

    Article  PubMed  CAS  Google Scholar 

  • Paulsen IT and Saier MH 1997 A novel family of ubiquitous heavy metal ion transport proteins. J. Membr. Biol. 156 99–103

    Article  PubMed  CAS  Google Scholar 

  • Potapova TV and Golyshev SA 2016 Revisiting a special structural order of a growing tip of the Neurospora crassa hypha. Fungal Genomics Biol. 6 3–6

    Article  Google Scholar 

  • Pound LD, Sarkar SA, Benninger RKP, et al. 2009 Deletion of the mouse Slc30a8 gene encoding zinc transporter-8 results in impaired insulin secretion. Biochem. J. 421 371–376

    Article  PubMed  CAS  Google Scholar 

  • Ramachandran GN and Sasisekharan V 1968 Conformation of polypeptides and proteins. Adv. Protein Chem. 23 283–437

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen CG and Glass NL 2007 Localization of RHO-4 indicates differential regulation of conidial versus vegetative septation in the filamentous fungus Neurospora crassa. Eukaryot. Cell 6 1097–1107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Raulin J 1869 Chemical studies on vegetation. Ann. Sci. Nat. 11 93–99

    Google Scholar 

  • Riquelme M and Bartnicki-Garcia S 2004 Key differences between lateral and apical branching in hyphae of Neurospora crassa. Fungal Genet. Biol. 41 842–851

    Article  PubMed  Google Scholar 

  • Roberts AN, Berlin V, Hager KM, et al. 1988 Molecular analysis of a Neurospora crassa gene expressed during conidiation. Mol. Cell Biol. 8 2411–2418

    PubMed  PubMed Central  CAS  Google Scholar 

  • Scheuner D, Song B, McEwen E, et al. 2001 Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7 1165–1176

    Article  PubMed  CAS  Google Scholar 

  • Seale T 1973 Life cycle of Neurospora crassa viewed by scanning electron microscopy. J. Bacteriol. 113 1015–1025

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seidel C, Moreno-Velásquez SD, Riquelme M, et al. 2013 Neurospora crassa NKIN2, a kinesin-3 motor, transports early endosomes and is required for polarized growth. Eukaryot. Cell 12 1020–1032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soares LW, Bailão AM, de Soares CMA, et al. 2020 Zinc at the host-fungus Interface: How to uptake the metal? J. Fungi 6 305

    Article  CAS  Google Scholar 

  • Springer ML and Yanofsky C 1989 A morphological and genetic analysis of conidiophore development in Neurospora crassa. Genes Dev. 3 559–571

    Article  PubMed  CAS  Google Scholar 

  • Starr TL and Gonc AP 2018 The major cellulases CBH-1 and CBH-2 of Neurospora crassa rely on distinct ER cargo adaptors for efficient ER-exit. Mol Microbiol. 107 229–248

    Article  PubMed  CAS  Google Scholar 

  • Takács T, Németh MT, Bohner F, et al. 2022 Characterization and functional analysis of zinc trafficking in the human fungal pathogen Candida parapsilosis. Open Biol. 12 220077

    Article  PubMed  PubMed Central  Google Scholar 

  • Tiwari A, Ngiilmei SD and Tamuli R 2018 The NcZrg-17 gene of Neurospora crassa encodes a cation diffusion facilitator transporter required for vegetative development, tolerance to endoplasmic reticulum stress and cellulose degradation under low zinc conditions. Curr. Genet. 64 811–819

    Article  PubMed  CAS  Google Scholar 

  • Vallee BL and Auld DS 1990 Zinc coordination, function, and structure of zinc enzymes and other proteins. Biochemistry 29 5647–5659

    Article  PubMed  CAS  Google Scholar 

  • Vicentefranqueira R, Amich J, Marín L, et al. 2018 The transcription factor ZafA regulates the homeostatic and adaptive response to zinc starvation in Aspergillus fumigatus. Genes 9 318

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogel HJ 1956 A convenient growth medium for Neurospora (Medium N). Microb. Genet. Bull. 13 42–43

    Google Scholar 

  • Vogel HJ 1964 Distribution of lysine pathways among fungi: evolutionary implications. Am. Nat. 98 435–446

    Article  CAS  Google Scholar 

  • Westergaard M and Mitchell HK 1947 Neurospora V. A synthetic medium favoring sexual reproduction. Am. J. Bot. 573–577

  • Wijesekara N, Dai FF, Hardy AB, et al. 2010 Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 53 1656–1668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wu CY, Bird AJ, Chung LM, et al. 2008 Differential control of Zap1-regulated genes in response to zinc deficiency in Saccharomyces cerevisiae. BMC Genomics 9 1–17

    Article  Google Scholar 

  • Xu C, Bailly-Maitre B and Reed JC 2005 Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Invest. 115 2656–2664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang J and Zhang Y 2015 I-TASSER server: New development for protein structure and function predictions. Nucleic. Acids Res. 43 174–181

    Article  Google Scholar 

  • Zhao H and Eide D 1996a The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc. Natl. Acad. Sci. USA 93 2454–2458

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao H and Eide D 1996b The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271 23203–23210

    Article  PubMed  CAS  Google Scholar 

  • Zhao H and Eide DJ 1997 Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol. Cell Biol. 17 5044–5052

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zheng W, Zhang C, Li Y, et al. 2021 Folding non-homologous proteins by coupling deep-learning contact maps with I-TASSER assembly simulations. Cell Rep. Methods 1 100014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We thank the Fungal Genetics Stock Center (FGSC), Kevin McCluskey, and Aric Wiest for generously waiving charges for some of the strains. We also thank Dr. Anand Tiwari for initial help in this work. SN was financially supported by a Research Fellowship from the Ministry of Human Resource Development (MHRD), Government of India. We acknowledge the MHRD, IIT Guwahati, Department of Biotechnology (DBT) NER twinning grant BT/PR24473/NER/95/737/2017 to RT, and Science and Engineering Research Board (SERB) Start-up grant for Young Scientists, YSS/2014/000174, to AT, for partial financial support.

Author information

Authors and Affiliations

  1. Department of Biosciences and Bioengineering, Indian Institute of Technology Guwahati, Guwahati, 781 039, India

    Serena Ngiimei D & Ranjan Tamuli

Authors
  1. Serena Ngiimei D
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ranjan Tamuli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ranjan Tamuli.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Corresponding editor: PN Rangarajan

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ngiimei D, S., Tamuli, R. CDF family of zinc transporters ZRC-1, MSC-2, and ZRG-17 are involved in survival at high zinc conditions, vegetative development, and cellulase utilization in Neurospora crassa. J Biosci 49, 12 (2024). https://doi.org/10.1007/s12038-023-00398-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12038-023-00398-4

Keywords

Search

Navigation