The AreA Nitrogen Catabolite Repression Activator Balances Fungal Nutrient Utilization and Virulence in the Insect Fungal Pathogen Beauveria bassiana.

In many fungi, the AreA GATA-type transcription factor mediates nitrogen catabolite repression affecting fungal development and, where applicable, virulence. Here, we investigated the functions of AreA in the fungal entomopathogen and plant endophyte Beauveria bassiana using knockdown of gene expression. The antiAreA mutants were impaired in nitrogen utilization and showed increased sensitivities to osmotic stressors but increased tolerances to oxidative/hypoxia stresses. Repression of BbAreA caused overall minimal effects on fungal virulence. The minor effects on virulence appeared to be due in part to competing secondary effects where host defense phenoloxidase activity was significantly decreased, but production of the fungal metabolite oosporein was increased and hyphal body development was impaired. Knockdown of BbAreA expression also resulted in impairment in ability of the fungus to associate with host plants. These data implicate that BbAreA likely acts as a regulator to balance fungal nutrient utilization, pathogenicity, and mutualism, facilitating the fungal occupation of host niches.

[1]  Chengshu Wang,et al.  Inductive Production of the Iron-Chelating 2-Pyridones Benefits the Producing Fungus To Compete for Diverse Niches , 2021, mBio.

[2]  S. Ying,et al.  Genome-Wide Insight into Profound Effect of Carbon Catabolite Repressor (Cre1) on the Insect-Pathogenic Lifecycle of Beauveria bassiana , 2021, Journal of fungi.

[3]  Yongjun Zhang,et al.  Multifunctional role of a fungal pathogen-secreted laccase 2 in evasion of insect immune defense. , 2021, Environmental microbiology.

[4]  Yongjun Zhang,et al.  Pest management via endophytic colonization of tobacco seedlings by the insect fungal pathogen Beauveria bassiana. , 2020, Pest management science.

[5]  Yongjun Zhang,et al.  The fungal mitochondrial membrane protein, BbOhmm, antagonistically controls hypoxia tolerance. , 2020, Environmental microbiology.

[6]  J. F. Castro,et al.  Antifungal Activity of Beauveria bassiana Endophyte against Botrytis cinerea in Two Solanaceae Crops , 2019, Microorganisms.

[7]  Shihua Wang,et al.  Regulation of Morphology, Aflatoxin Production, and Virulence of Aspergillus flavus by the Major Nitrogen Regulatory Gene areA , 2019, Toxins.

[8]  L. Ries,et al.  Overview of carbon and nitrogen catabolite metabolism in the virulence of human pathogenic fungi , 2018, Molecular microbiology.

[9]  Yongjun Zhang,et al.  An aldo-keto reductase, Bbakr1, is involved in stress response and detoxification of heavy metal chromium but not required for virulence in the insect fungal pathogen, Beauveria bassiana. , 2018, Fungal genetics and biology : FG & B.

[10]  Guohong Li,et al.  A bifunctional catalase‐peroxidase, MakatG1, contributes to virulence of Metarhizium acridum by overcoming oxidative stress on the host insect cuticle , 2017, Environmental microbiology.

[11]  L. Ries,et al.  Filamentous fungal carbon catabolite repression supports metabolic plasticity and stress responses essential for disease progression , 2017, PLoS pathogens.

[12]  B. Tudzynski,et al.  Nitrate Assimilation in Fusarium fujikuroi Is Controlled by Multiple Levels of Regulation , 2017, Front. Microbiol..

[13]  Y. Pei,et al.  Regulatory cascade and biological activity of Beauveria bassiana oosporein that limits bacterial growth after host death , 2017, Proceedings of the National Academy of Sciences.

[14]  Yongjun Zhang,et al.  The PacC transcription factor regulates secondary metabolite production and stress response, but has only minor effects on virulence in the insect pathogenic fungus Beauveria bassiana , 2017, Environmental microbiology.

[15]  Chengshu Wang,et al.  Insect Pathogenic Fungi: Genomics, Molecular Interactions, and Genetic Improvements. , 2017, Annual review of entomology.

[16]  F. Vega,et al.  Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation , 2016, Biological control : theory and applications in pest management.

[17]  S. Ying,et al.  The Pal pathway required for ambient pH adaptation regulates growth, conidiation, and osmotolerance of Beauveria bassiana in a pH-dependent manner , 2016, Applied Microbiology and Biotechnology.

[18]  M. Bidochka,et al.  Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi , 2016, Plant Molecular Biology.

[19]  Jin-Rong Xu,et al.  The AreA transcription factor mediates the regulation of deoxynivalenol (DON) synthesis by ammonium and cyclic adenosine monophosphate (cAMP) signalling in Fusarium graminearum. , 2015, Molecular plant pathology.

[20]  Chengshu Wang,et al.  Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity , 2015, Proceedings of the National Academy of Sciences.

[21]  S. Ying,et al.  Distinct contributions of one Fe- and two Cu/Zn-cofactored superoxide dismutases to antioxidation, UV tolerance and virulence of Beauveria bassiana. , 2015, Fungal genetics and biology : FG & B.

[22]  N. Keyhani,et al.  Erratum to: Stress response signaling and virulence: insights from entomopathogenic fungi , 2015, Current Genetics.

[23]  Y. Pei,et al.  Bbmsn2 acts as a pH-dependent negative regulator of secondary metabolite production in the entomopathogenic fungus Beauveria bassiana. , 2015, Environmental microbiology.

[24]  S. Ying,et al.  Wee1 and Cdc25 control morphogenesis, virulence and multistress tolerance of Beauveria bassiana by balancing cell cycle-required cyclin-dependent kinase 1 activity. , 2015, Environmental microbiology.

[25]  S. Cheevadhanarak,et al.  Tenellin acts as an iron chelator to prevent iron-generated reactive oxygen species toxicity in the entomopathogenic fungus Beauveria bassiana. , 2015, FEMS microbiology letters.

[26]  Y. Pei,et al.  Ablation of the creA regulator results in amino acid toxicity, temperature sensitivity, pleiotropic effects on cellular development and loss of virulence in the filamentous fungus Beauveria bassiana. , 2014, Environmental microbiology.

[27]  Yuanyuan Pan,et al.  Disruption of the nitrogen regulatory gene AcareA in Acremonium chrysogenum leads to reduction of cephalosporin production and repression of nitrogen metabolism. , 2013, Fungal genetics and biology : FG & B.

[28]  H. Giese,et al.  The AreA transcription factor in Fusarium graminearum regulates the use of some nonpreferred nitrogen sources and secondary metabolite production. , 2013, Fungal biology.

[29]  J. Fraser,et al.  Nitrogen regulation of virulence in clinically prevalent fungal pathogens. , 2013, FEMS microbiology letters.

[30]  S. Ying,et al.  Insight into the transcriptional regulation of Msn2 required for conidiation, multi-stress responses and virulence of two entomopathogenic fungi. , 2013, Fungal genetics and biology : FG & B.

[31]  S. Ying,et al.  Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. , 2013, Environmental microbiology.

[32]  C. Scazzocchio,et al.  The GATA factors AREA and AREB together with the co-repressor NMRA, negatively regulate arginine catabolism in Aspergillus nidulans in response to nitrogen and carbon source. , 2012, Fungal genetics and biology : FG & B.

[33]  M. Brock,et al.  Nutrient acquisition by pathogenic fungi: nutrient availability, pathway regulation, and differences in substrate utilization. , 2011, International journal of medical microbiology : IJMM.

[34]  J. Fraser,et al.  Nitrogen Metabolite Repression of Metabolism and Virulence in the Human Fungal Pathogen Cryptococcus neoformans , 2011, Genetics.

[35]  Byong-Ki Kim,et al.  Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana , 2011, Molecular microbiology.

[36]  R. S. St. Leger,et al.  Mrt, a Gene Unique to Fungi, Encodes an Oligosaccharide Transporter and Facilitates Rhizosphere Competency in Metarhizium robertsii1[C][W] , 2010, Plant Physiology.

[37]  C. Keyser,et al.  CTC medium: a novel dodine-free selective medium for isolating entomopathogenic fungi, especially Metarhizium acridum, from soil. , 2010 .

[38]  N. Keyhani,et al.  Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. , 2009, Microbiology.

[39]  C. Woloshuk,et al.  Role of AREA, a regulator of nitrogen metabolism, during colonization of maize kernels and fumonisin biosynthesis in Fusarium verticillioides. , 2008, Fungal genetics and biology : FG & B.

[40]  R. Cox,et al.  Biosynthesis of the 2‐Pyridone Tenellin in the Insect Pathogenic Fungus Beauveria bassiana , 2007, Chembiochem : a European journal of chemical biology.

[41]  R. Fluhr,et al.  Nutrition acquisition strategies during fungal infection of plants. , 2007, FEMS microbiology letters.

[42]  C. Veneault-Fourrey,et al.  CLNR1, the AREA/NIT2‐like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle , 2003, Molecular microbiology.

[43]  C. Scazzocchio,et al.  Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter‐specific recognition by the Aspergillus nidulans GATA factor AreA , 1997, The EMBO journal.