The RNAi machinery controls distinct responses to environmental signals in the basal fungus Mucor circinelloides

Nicolas, Francisco E.; Vila, Ana; Moxon, Simon; Cascales, Maria D.; Torres-Martinez, Santiago; Ruiz-Vazquez, Rosa M.; Garre, Victoriano

doi:10.1186/s12864-015-1443-2

Title: The RNAi machinery controls distinct responses to environmental signals in the basal fungus Mucor circinelloides

Journal Article · Wed Mar 25 00:00:00 EDT 2015 · BMC Genomics

DOI: https://doi.org/10.1186/s12864-015-1443-2 · OSTI ID:1345508

Nicolas, Francisco E. ^[1]; Vila, Ana ^[2]; Moxon, Simon ^[3]; Cascales, Maria D. ^[2]; Torres-Martinez, Santiago ^[2]; Ruiz-Vazquez, Rosa M. ^[2]; Garre, Victoriano ^[2]

Univ. of Murcia, Murcia (Spain); DOE Office of Scientific and Technical Information (OSTI)
Univ. of Murcia, Murcia (Spain)
The Genome Analysis Centre, Norwich (United Kingdom)

Here, RNA interference (RNAi) is a conserved mechanism of genome defence that can also have a role in the regulation of endogenous functions through endogenous small RNAs (esRNAs). In fungi, knowledge of the functions regulated by esRNAs has been hampered by lack of clear phenotypes in most mutants affected in the RNAi machinery. Mutants of Mucor circinelloides affected in RNAi genes show defects in physiological and developmental processes, thus making Mucor an outstanding fungal model for studying endogenous functions regulated by RNAi. Some classes of Mucor esRNAs map to exons (ex-siRNAs) and regulate expression of the genes from which they derive. To have a broad picture of genes regulated by the silencing machinery during vegetative growth, we have sequenced and compared the mRNA profiles of mutants in the main RNAi genes by using RNA-seq. In addition, we have achieved a more complete phenotypic characterization of silencing mutants Deletion of any main RNAi gene provoked a deep impact in mRNA accumulation at exponential and stationary growth. Genes showing increased mRNA levels, as expected for direct ex-siRNAs targets, but also genes with decreased expression were detected, suggesting that, most probably, the initial ex-siRNA targets regulate the expression of other genes, which can be up- or down-regulated. Expression of 50% of the genes was dependent on more than one RNAi gene in agreement with the existence of several classes of ex-siRNAs produced by different combinations of RNAi proteins. These combinations of proteins have also been involved in the regulation of different cellular processes. Besides genes regulated by the canonical RNAi pathway, this analysis identified processes, such as growth at low pH and sexual interaction that are regulated by a dicer-independent non-canonical RNAi pathway. In conclusion, this work shows that the RNAi pathways play a relevant role in the regulation of a significant number of endogenous genes in M. circinelloides during exponential and stationary growth phases and opens up an important avenue for in-depth study of genes involved in the regulation of physiological and developmental processes in this fungal model.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1345508

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 16; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Origins and Mechanisms of miRNAs and siRNAs Carthew, Richard W.; Sontheimer, Erik J. Cell, Vol. 136, Issue 4 https://doi.org/10.1016/j.cell.2009.01.035	journal	February 2009
Photobiology in the Zygomycota: Multiple photoreceptor genes for complex responses to light Corrochano, Luis M.; Garre, Victoriano Fungal Genetics and Biology, Vol. 47, Issue 11 https://doi.org/10.1016/j.fgb.2010.04.007	journal	November 2010
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Diverse Pathways Generate MicroRNA-like RNAs and Dicer-Independent Small Interfering RNAs in Fungi Lee, Heng-Chi; Li, Liande; Gu, Weifeng Molecular Cell, Vol. 38, Issue 6 https://doi.org/10.1016/j.molcel.2010.04.005	journal	June 2010
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Small GTP-binding proteins are associated with chitosomes and vesicles carrying glucose oxidase from Mucor circinelloides Moreno-Jiménez, Rocío; García-Soto, Jesús; Martínez-Cadena, Guadalupe Microbiology, Vol. 154, Issue 3 https://doi.org/10.1099/mic.0.2007/012179-0	journal	March 2008
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A Single dicer Gene Is Required for Efficient Gene Silencing Associated with Two Classes of Small Antisense RNAs in Mucor circinelloides de Haro, Juan P.; Calo, Silvia; Cervantes, María Eukaryotic Cell, Vol. 8, Issue 10 https://doi.org/10.1128/ec.00191-09	journal	August 2009
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Fission Yeast Rho5p GTPase Is a Functional Paralogue of Rho1p That Plays a Role in Survival of Spores and Stationary-Phase Cells Rincón, Sergio A.; Santos, Beatriz; Pérez, Pilar Eukaryotic Cell, Vol. 5, Issue 3 https://doi.org/10.1128/ec.5.3.435-446.2006	journal	March 2006
High-frequency heterokaryon formation by Mucor racemosus. Lasker, B. A.; Borgia, P. T. Journal of Bacteriology, Vol. 141, Issue 2 https://doi.org/10.1128/jb.141.2.565-569.1980	journal	January 1980
Nutrition, Growth, and Morphogenesis of Mucor Rouxii Bartnicki-Garcia, S.; Nickerson, Walter J. Journal of Bacteriology, Vol. 84, Issue 4 https://doi.org/10.1128/jb.84.4.841-858.1962	journal	January 1962
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A Single Argonaute Gene Participates in Exogenous and Endogenous RNAi and Controls Cellular Functions in the Basal Fungus Mucor circinelloides Cervantes, María; Vila, Ana; Nicolás, Francisco E. PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069283	journal	July 2013
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Regulation of Autolysis in Aspergillus nidulans Emri, Tamás; Molnár, Zsolt; Szilágyi, Melinda Applied Biochemistry and Biotechnology, Vol. 151, Issue 2-3 https://doi.org/10.1007/s12010-008-8174-7	journal	March 2008
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Photobiology in the Zygomycota: Multiple photoreceptor genes for complex responses to light Corrochano, Luis M.; Garre, Victoriano Fungal Genetics and Biology, Vol. 47, Issue 11 https://doi.org/10.1016/j.fgb.2010.04.007	journal	November 2010
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Diverse Pathways Generate MicroRNA-like RNAs and Dicer-Independent Small Interfering RNAs in Fungi Lee, Heng-Chi; Li, Liande; Gu, Weifeng Molecular Cell, Vol. 38, Issue 6 https://doi.org/10.1016/j.molcel.2010.04.005	journal	June 2010
Antifungal drug resistance evoked via RNAi-dependent epimutations Calo, Silvia; Shertz-Wall, Cecelia; Lee, Soo Chan Nature, Vol. 513, Issue 7519 https://doi.org/10.1038/nature13575	journal	July 2014
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One of the Two Dicer-like Proteins in the Filamentous Fungi Magnaporthe oryzae Genome Is Responsible for Hairpin RNA-triggered RNA Silencing and Related Small Interfering RNA Accumulation Kadotani, Naoki; Nakayashiki, Hitoshi; Tosa, Yukio Journal of Biological Chemistry, Vol. 279, Issue 43 https://doi.org/10.1074/jbc.M408259200	journal	August 2004
Mnt1p and Mnt2p of Candida albicans Are Partially Redundant α-1,2-Mannosyltransferases That Participate in O -Linked Mannosylation and Are Required for Adhesion and Virulence Munro, Carol A.; Bates, Steven; Buurman, Ed T. Journal of Biological Chemistry, Vol. 280, Issue 2 https://doi.org/10.1074/jbc.M411413200	journal	November 2004
Epidemiology and Outcome of Zygomycosis: A Review of 929 Reported Cases Roden, M. M.; Zaoutis, T. E.; Buchanan, W. L. Clinical Infectious Diseases, Vol. 41, Issue 5 https://doi.org/10.1086/432579	journal	September 2005
Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes Nicolas, F. E. The EMBO Journal, Vol. 22, Issue 15 https://doi.org/10.1093/emboj/cdg384	journal	August 2003
Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides Nicolas, Francisco Esteban; Moxon, Simon; de Haro, Juan P. Nucleic Acids Research, Vol. 38, Issue 16 https://doi.org/10.1093/nar/gkq301	journal	April 2010
Small GTP-binding proteins are associated with chitosomes and vesicles carrying glucose oxidase from Mucor circinelloides Moreno-Jiménez, Rocío; García-Soto, Jesús; Martínez-Cadena, Guadalupe Microbiology, Vol. 154, Issue 3 https://doi.org/10.1099/mic.0.2007/012179-0	journal	March 2008
Protein O-mannosylation is crucial for cell wall integrity, septation and viability in fission yeast: S. pombe PMT family Willer, Tobias; Brandl, Martin; Sipiczki, Matthias Molecular Microbiology, Vol. 57, Issue 1 https://doi.org/10.1111/j.1365-2958.2005.04692.x	journal	June 2005
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The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride: Function of sRNAs in Trichoderma Carreras-Villaseñor, Nohemi; Esquivel-Naranjo, Edgardo U.; Villalobos-Escobedo, J. Manuel Molecular Microbiology, Vol. 89, Issue 1 https://doi.org/10.1111/mmi.12261	journal	June 2013
Two Components of a velvet -Like Complex Control Hyphal Morphogenesis, Conidiophore Development, and Penicillin Biosynthesis in Penicillium chrysogenum Hoff, Birgit; Kamerewerd, Jens; Sigl, Claudia Eukaryotic Cell, Vol. 9, Issue 8 https://doi.org/10.1128/EC.00077-10	journal	June 2010
A Single dicer Gene Is Required for Efficient Gene Silencing Associated with Two Classes of Small Antisense RNAs in Mucor circinelloides de Haro, Juan P.; Calo, Silvia; Cervantes, María Eukaryotic Cell, Vol. 8, Issue 10 https://doi.org/10.1128/EC.00191-09	journal	August 2009
LaeA, a Regulator of Morphogenetic Fungal Virulence Factors Bok, Jin Woo; Balajee, S. Arunmozhi; Marr, Kieren A. Eukaryotic Cell, Vol. 4, Issue 9 https://doi.org/10.1128/EC.4.9.1574-1582.2005	journal	September 2005
Fission Yeast Rho5p GTPase Is a Functional Paralogue of Rho1p That Plays a Role in Survival of Spores and Stationary-Phase Cells Rincón, Sergio A.; Santos, Beatriz; Pérez, Pilar Eukaryotic Cell, Vol. 5, Issue 3 https://doi.org/10.1128/EC.5.3.435-446.2006	journal	March 2006
High-frequency heterokaryon formation by Mucor racemosus. Lasker, B. A.; Borgia, P. T. Journal of Bacteriology, Vol. 141, Issue 2 https://doi.org/10.1128/JB.141.2.565-569.1980	journal	January 1980
Nutrition, Growth, and Morphogenesis of Mucor Rouxii Bartnicki-Garcia, S.; Nickerson, Walter J. Journal of Bacteriology, Vol. 84, Issue 4 https://doi.org/10.1128/JB.84.4.841-858.1962	journal	January 1962
High-frequency heterokaryon formation by Mucor racemosus. Lasker, B. A.; Borgia, P. T. Journal of Bacteriology, Vol. 141, Issue 2 https://doi.org/10.1128/jb.141.2.565-569.1980	journal	January 1980
Nutrition, Growth, and Morphogenesis of Mucor Rouxii Bartnicki-Garcia, S.; Nickerson, Walter J. Journal of Bacteriology, Vol. 84, Issue 4 https://doi.org/10.1128/jb.84.4.841-858.1962	journal	January 1962
RNA Interference Pathways in Fungi: Mechanisms and Functions Chang, Shwu-Shin; Zhang, Zhenyu; Liu, Yi Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-092611-150138	journal	October 2012
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome Li, Bo; Dewey, Colin N. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-323	journal	August 2011
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
Differentiation-Dependent Expression of 17β-Hydroxysteroid Dehydrogenase, Type 10, in the Rodent Testis: Effect of Aging in Leydig Cells Ivell, Richard; Balvers, Marga; Anand, Ravinder J. K. Endocrinology, Vol. 144, Issue 7 https://doi.org/10.1210/en.2002-0082	journal	July 2003
The Putative Protein Methyltransferase LAE1 of Trichoderma atroviride Is a Key Regulator of Asexual Development and Mycoparasitism Aghcheh, Razieh Karimi; Druzhinina, Irina S.; Kubicek, Christian P. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0067144	journal	June 2013
A Single Argonaute Gene Participates in Exogenous and Endogenous RNAi and Controls Cellular Functions in the Basal Fungus Mucor circinelloides Cervantes, María; Vila, Ana; Nicolás, Francisco E. PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069283	journal	July 2013
Sporangiospore Size Dimorphism Is Linked to Virulence of Mucor circinelloides Li, Charles H.; Cervantes, Maria; Springer, Deborah J. PLoS Pathogens, Vol. 7, Issue 6 https://doi.org/10.1371/journal.ppat.1002086	journal	June 2011
Calcineurin Plays Key Roles in the Dimorphic Transition and Virulence of the Human Pathogenic Zygomycete Mucor circinelloides Lee, Soo Chan; Li, Alicia; Calo, Silvia PLoS Pathogens, Vol. 9, Issue 9 https://doi.org/10.1371/journal.ppat.1003625	journal	September 2013
Functional Analyses of Trichoderma reesei LAE1 Reveal Conserved and Contrasting Roles of This Regulator Karimi-Aghcheh, Razieh; Bok, Jin Woo; Phatale, Pallavi A. G3: Genes\|Genomes\|Genetics, Vol. 3, Issue 2 https://doi.org/10.1534/g3.112.005140	journal	February 2013
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Functional Diversity of RNAi-Associated sRNAs in Fungi Nicolás, Francisco; Ruiz-Vázquez, Rosa International Journal of Molecular Sciences, Vol. 14, Issue 8 https://doi.org/10.3390/ijms140815348	journal	July 2013

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A Non-canonical RNA Silencing Pathway Promotes mRNA Degradation in Basal Fungi Trieu, Trung Anh; Calo, Silvia; Nicolás, Francisco E. PLOS Genetics, Vol. 11, Issue 4 https://doi.org/10.1371/journal.pgen.1005168	journal	April 2015
A non-canonical RNAi pathway controls virulence and genome stability in Mucorales Pérez-Arques, Carlos; Navarro-Mendoza, María Isabel; Murcia, Laura PLOS Genetics, Vol. 16, Issue 7 https://doi.org/10.1371/journal.pgen.1008611	journal	July 2020
RNAi-Based Functional Genomics Identifies New Virulence Determinants in Mucormycosis Trieu, Trung Anh; Navarro-Mendoza, María Isabel; Pérez-Arques, Carlos PLOS Pathogens, Vol. 13, Issue 1 https://doi.org/10.1371/journal.ppat.1006150	journal	January 2017
The interaction of fungi with the environment orchestrated by RNAi Villalobos-Escobedo, José Manuel; Herrera-Estrella, Alfredo; Carreras-Villaseñor, Nohemí Mycologia, Vol. 108, Issue 3 https://doi.org/10.3852/15-246	journal	May 2016

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59 BASIC BIOLOGICAL SCIENCES
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esRNAs
mRNA profiling
non-canonical RNAi pathway
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sexual interaction

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