Abstract
Microsclerotia (MS) formation was successfully induced in Nomuraea rileyi in liquid amended medium (AM) culture. To investigate how N. rileyi senses growth stress and regulates MS differentiation, based on transcriptome library, sho1 and sln1 genes were cloned. The transcription levels of sho1 and sln1 were upregulated in response to the changing culture conditions. To determine the functions of sho1 and sln1, gene-silencing mutants (sholi, sln1i and shol&sln1i) were generated using RNA silencing technology. The significant phenotypic changes in the mutants included reduced conidial yields by 22.72, 40.27, and 63.67 % and virulence by 24.53, 25.74, and 59.04 %, respectively. Furthermore, the mutants presented decreased MS yields by approximately 96 % under changing culture conditions. Our results confirmed the crucial role of Sho1p and Sln1p in sensing growth stress due to changing culture conditions and regulating MS differentiation.
Similar content being viewed by others
References
Boisnard S, Ruprich-Robert G, Florent M, Da Sliva B, Chapeland-Leclerc F, Papon N (2008) Role of Sho1p adaptor in the pseudohyphal development, drugs sensitivity, osmotolerance and oxidant stress adaptation in the opportunistic yeast Candida lusitaniae. Yeast 25:849–859
Boucias DG, Tigano MS, Sosa-Gomez DR, Glare TR, Inglis PW (2000) Genotypic properties of the entomopathogenic fungus Nomuraea rileyi. Biocontrol 19:124–138
Boyce KL, Schreider L, Kirszenblat L, Andrianopoulos A (2011) The two-component histidine kinases DrkA and SlnA are required for in vivo growth in the human pathogen Penicillium mameffei. Mol Microbiol 82:1164–1184
Chen CB, Harel A, Gorovoits R, Yarden O, Dickman MB (2004) MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing. MPMI 17(4):404–413
Chen H, Yin YP, Li Y, Mahmud MS, Wang ZK (2012) Identification and analysis of gene differentially expressed in the Spodoptera litura fat body in response to the biocontrol fungus, Nomuraea rileyi. Comp Biochem Physiol B: Biochem Mol Biol 163:203–210
Dang YK, Yang QY, Xue ZH, Liu Y (2011) RNA interference in fungi: pathways, functions, and applications. Eukaryot Cell 10(9):1148–1155
Dragosits M, Stadlmann J, Graf A, Gasser B, Maurer M, Sauer M, Kreil DP, Altmann F, Mattanovish D (2010) The response to unfolded protein is involved in osmotolerance of Pichia pastoris. BMC Genom 11:207
Faria MR, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256
Furukawa K, Hoshi Y, Maeda T, Nakajima T, Abe K (2005) Aspergillus nidulans HOG pathway is activated only by two-component signalling pathway in response to osmotic stress. Mol Microbiol 56(5):1246–1261
Gasch AP, Spellman PT, Kao CM, Carmel-harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257
Hagiwara D, Asano Y, Marui J, Yoshimi A, Mizuno T, Abe K (2009) Transcriptional profiling for Aspergillus nidulans HogA MAPK signaling pathway in response to fludioxonil and osmotic stress. Fungal Genet Biol 46:868–878
Jackson MA, Jaronski ST (2009) Production of microsclerotia of the fungal entomopathogen Metarhizium anisopliae and their potential for use as a biocontrol agent for soil-inhabiting insects. Mycol Res 113:842–850
Jiang SS, Yin YP, Song ZY, Zhou GL, Wang ZK (2014) RacA and Cdc42 regulate polarized growth and microsclerotium formation in the dimorphic fungus Nomuraea rileyi. Res Microbiol 165:233–242
Kanamaru K (2011) Roles of the His-Asp phosphorelay signal transduction system in controlling cell growth and development in Aspergillus nidulans. Biosic Biotechnol Biochem 75(1):1–6
Konte T, Plemenitas A (2013) The HOG signal transduction pathway in the halophilic fungus Wallemia ichthyophaga: identification and characterisation of MAP kinases WiHog1A and WiHog1B. Extremophiles 17:623–636
Lackner DH, Schmidt MW, Wu SD, Wolf DA, Bahler J (2012) Regulation of transcriptome, translation, and proteome in response to environmental stress in fission yeast. Genome Biol 13:R25
Li S, Ault A, Malone CL, Raitt D, Dean S, Johnston LH, Deschenes RJ, Fassler JS (1998) The yeast histidine protein kinase, Sln1p, mediates phosphtransfer to two response regulators, Ssk1p and Skn7p. EMBO J 17(23):6952–6962
Liu JJ, Yin YP, Song ZY, Li Y, Jiang SS, Shao CW, Wang ZK (2014) NADH: flavin oxidoreductase/NADH oxidase and ROS regulate microsclerotium development in Nomuraea rileyi. World J Microbiol Biotechnol 30:1927–1935
Miskei M, Karányi Z, Pócsi I (2009) Annotation of stress-response proteins in the aspergilla. Fungal Genet Biol 46:S105–S120
Mollapour M, Piper PW (2007) Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquglyceroprin for endocytosis, thereby rendering cells resistant to acetic acid. Mol Cell Biol 27(18):6446–6456
Monge RA, Román E, Nombela C, Pla J (2006) The MAP kinase signal transduction network in Candida albicans. Microbiology 152:905–912
Nikolaou E, Agrafioti I, Stumpf M, Quinn J, Stansfield I, Brown AJ (2009) Phylogenetic diversity of stress signaling pathways in fungi. BMC Evol Biol 9:44
O’Rourke SM, Herskowitz I (2004) Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15:532–542
Pillet F, Lemonier S, Schiavone M, Formosa C, Martin-Yken H, Francois JM, Dague E (2014) Uncovering by atomic force microscopy of an original circular structure at the yeast cell surface in response to heat shock. BMC Biol 12:6
Raymond M (1985) Presentation d’un programme d’analyse logprobit pour micro-orinateur. Cah ORSTOM Entomol Med Parasitol 22:117–121
Román E, Nombela C, Pla J (2005) The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candica albicans. Mol Cell Biol 25(23):10611–10627
Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192:289–318
Saito H, Tatebayashi K (2004) Regulation of the osmoregulatory HOG MAPK cascade in yeast. J Biolchem 136:267–272
Smith DA, Morgan BA, Quinn J (2010) Stress signalling to fungal stress-activated protein kinase pathways. FEMS Microbiol Lett 306:1–8
Song ZY, Yin YP, Jiang SS, Liu JJ, Chen H, Wang ZK (2013) Comparative transcriptome analysis of microsclerotia development in Nomuraea rileyi. BMC Genom 14:411
Song ZY, Yin YP, Jiang SS, Liu JJ, Wang ZK (2014) Optimization of culture medium for microsclerotia production by Nomuraea rileyi and analysis of their viability for use as a mycoinsecticide. Biocontrol 59:597–605
Srinivasa K, Kim J, Yee S, Kim W, Choi W (2012) A MAP kinase pathway is implicated in the Pseudohyphal induction by hydrogen peroxide in Candica albicans. Mol Cell 33:183–193
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Vandesompele J, De Preter K, Pattyn F, Poppe B, Roy NV, Paepe AD, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:research0034
Vylkova S, Jiang WS, Li WS, Nayyar N, Edgerton M (2007) Histatin 5 initiates osmotic stress response in Candida albicans via avtivation of the Hog1 mitogen-activated protein kinase pathway. Eukaryot Cell 6:1876–1888
Wang CS, Duan ZB, Leger RJS (2008) MOS1 osmosensor of Metarhizum anisopliae is required for adaptation to insect host hemolymph. Eukaryot Cell 7(2):302–309
Wang F, Tao J, Qian J, You S, Dong H, Shen H, Chen X, Tang S, Ren S (2009) A histidine kinase PmHHK1 regulates polar growth, sporulation and cell wall composition in the dimorphic fungus Penicillium marneffi. Mycol Res 113:915–923
Xiao GH, Ying SH, Zheng P, Wang ZL, Zhang SW, Xie XQ, Shang YF, Leger RJS, Zhao GP, Wang CS, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483
Yin YP, Huang S, Song ZY, Wang ZK (2012) Microsclerotia artificial inductions of Nomuraea rileyi CQNr01. Scientia Agricultura Sinica 45(23):4801–4807 (In Chinese)
Zheng P, Xia YL, Xiao GH, Xiong C, Hu X, Zhang SW, Zheng HJ, Huang Y, Zhou Y, Wang SY, Zhao GP, Liu XZ, Leger RJS, Wang CS (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12:R116
Acknowledgments
Financial support for this study was provided by Special Fund for Agro-scientific in the Public Interest (Project 201103002) and State 863 Project of China (Project 2011AA10A201).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Song, Z., Shen, L., Yin, Y. et al. Role of two Nomuraea rileyi transmembrane sensors Sho1p and Sln1p in adaptation to stress due to changing culture conditions during microsclerotia development. World J Microbiol Biotechnol 31, 477–485 (2015). https://doi.org/10.1007/s11274-015-1801-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11274-015-1801-x