Rewiring of transcriptional networks as a major event leading to the diversity of asexual multicellularity in fungi

Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of se...

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Published inCritical reviews in microbiology Vol. 45; no. 5-6; pp. 548 - 563
Main Authors Etxebeste, Oier, Otamendi, Ainara, Garzia, Aitor, Espeso, Eduardo A., Cortese, Marc S.
Format Journal Article
LanguageEnglish
Published England Taylor & Francis 02.11.2019
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ISSN1040-841X
1549-7828
1549-7828
DOI10.1080/1040841X.2019.1630359

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Abstract Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class Eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.
AbstractList Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class Eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.
Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class Eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at least five times in evolution, one of them in fungi. There are two types of CM programs in fungi, leading, respectively, to the formation of sexual or asexual spores. Asexual spores foment the spread of mycoses, as they are the main vehicle for dispersion. In spite of this key dependence, there is great morphological diversity of asexual multicellular structures in fungi. To advance the understanding of the mechanisms that control initiation and progression of asexual CM and how they can lead to such a remarkable morphological diversification, we studied 503 fungal proteomes, representing all phyla and subphyla, and most known classes. Conservation analyses of 33 regulators of asexual development suggest stepwise emergence of transcription factors. While velvet proteins constitute one of the most ancient systems, the central regulator BrlA emerged late in evolution (with the class Eurotiomycetes). Some factors, such as MoConX4, seem to be species-specific. These observations suggest that the emergence and evolution of transcriptional regulators rewire transcriptional networks. This process could reach the species level, resulting in a vast diversity of morphologies.
Author Cortese, Marc S.
Espeso, Eduardo A.
Etxebeste, Oier
Garzia, Aitor
Otamendi, Ainara
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Cites_doi 10.1038/nature10947
10.1128/MCB.7.9.3113
10.1111/brv.12418
10.1016/j.fgb.2010.05.008
10.1007/s00294-015-0556-0
10.1371/journal.pone.0089883
10.1038/nmicrobiol.2017.120
10.1371/journal.pgen.1002816
10.1016/j.funbio.2018.01.004
10.1111/j.1365-2958.1993.tb01565.x
10.1371/journal.pone.0040292
10.1371/journal.pbio.1001750
10.1111/geb.12214
10.1099/13500872-142-11-3211
10.1016/0012-1606(90)90215-5
10.1093/cid/ciw691
10.1002/j.1460-2075.1993.tb05899.x
10.1038/srep28874
10.1101/gad.4.9.1473
10.1046/j.1365-2958.2001.02472.x
10.1007/978-3-319-25844-7_12
10.1128/microbiolspec.FUNK-0053-2016
10.1126/science.1163225
10.1007/s00294-017-0692-9
10.1093/nar/gky1085
10.1093/genetics/143.1.155
10.1111/1462-2920.13431
10.1534/genetics.115.174342
10.3389/fmicb.2017.01837
10.1046/j.1365-2958.2000.01874.x
10.1002/j.1460-2075.1996.tb00903.x
10.1016/0092-8674(88)90198-5
10.1111/j.1365-2958.2010.07282.x
10.1007/s12275-014-4384-6
10.1111/j.1365-2958.2008.06520.x
10.1111/1462-2920.12618
10.1111/j.1600-0706.2005.14101.x
10.1016/j.tim.2010.09.007
10.3389/fmicb.2018.01859
10.1111/j.1365-2958.2010.07063.x
10.1534/genetics.109.101667
10.1074/jbc.M310840200
10.1186/s12915-016-0309-7
10.1007/BF01637246
10.1038/ncomms14444
10.1128/mBio.01130-18
10.1016/j.cub.2017.04.032
10.1093/nar/gkv1248
10.1038/nmicrobiol.2016.39
10.1016/j.fgb.2017.06.002
10.1038/msb.2009.52
10.1186/s40694-016-0024-8
10.1111/j.1365-2672.2009.04237.x
10.1371/journal.pone.0000970
10.1534/genetics.114.161430
10.1128/EC.00192-06
10.1093/genetics/78.2.679
10.1128/MCB.14.4.2503
10.1128/MCB.11.1.55
10.1111/mmi.13156
10.1016/j.cub.2008.01.061
10.1128/microbiolspec.FUNK-0055-2016
10.1111/j.1365-2958.1994.tb01293.x
10.1128/mSphere.00050-18
10.1111/j.1365-2958.2004.04065.x
10.1128/microbiolspec.FUNK-0052-2016
10.1146/annurev.micro.112408.134000
10.1038/nature.2017.21424
10.1534/genetics.114.165688
10.1007/s00253-015-6823-7
10.1371/journal.pone.0137554
10.1128/EC.00274-12
10.1016/S0169-5347(00)89050-3
10.1371/journal.pone.0048134
10.1111/j.1574-6976.2011.00285.x
10.1111/j.1365-2958.2006.05506.x
10.1093/molbev/msx148
10.1128/EC.00207-07
10.1016/j.simyco.2018.10.002
10.1016/j.mib.2012.09.006
10.1094/PDIS-05-16-0666-PDN
10.1101/gad.6.9.1770
10.1007/BF00326580
10.1186/s13059-017-1151-0
10.1111/j.1365-2958.2003.03961.x
10.1126/science.1155888
10.1073/pnas.1817822116
10.1038/532421a
10.1371/journal.pone.0017505
10.1111/nph.13948
10.1128/MMBR.62.1.35-54.1998
10.1007/3-540-28135-5_14
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References CIT0072
CIT0071
CIT0030
CIT0074
CIT0073
CIT0032
CIT0076
CIT0031
CIT0075
CIT0034
CIT0078
CIT0033
CIT0077
CIT0070
CIT0036
CIT0035
Kirk P (CIT0049) 2008
CIT0079
CIT0038
CIT0037
CIT0039
CIT0083
CIT0082
CIT0041
CIT0085
CIT0040
CIT0084
CIT0043
CIT0087
CIT0042
CIT0086
CIT0001
CIT0045
CIT0089
CIT0044
CIT0088
CIT0081
CIT0003
CIT0047
CIT0002
CIT0046
CIT0005
CIT0004
CIT0048
CIT0007
CIT0009
CIT0008
CIT0050
CIT0094
CIT0093
CIT0052
CIT0051
CIT0010
CIT0054
CIT0053
CIT0012
CIT0056
CIT0011
CIT0055
CIT0090
CIT0092
CIT0091
CIT0014
CIT0058
CIT0013
CIT0057
CIT0016
CIT0015
CIT0059
CIT0018
CIT0017
Selitrennikoff CP (CIT0080) 1974; 78
Andrianopoulos A (CIT0006) 1991; 3
CIT0061
CIT0060
CIT0063
CIT0062
CIT0021
CIT0065
CIT0020
CIT0064
CIT0023
CIT0067
CIT0022
CIT0066
Busby TM (CIT0019) 1996; 143
CIT0025
CIT0069
CIT0024
CIT0068
CIT0027
CIT0026
CIT0029
CIT0028
References_xml – ident: CIT0032
  doi: 10.1038/nature10947
– ident: CIT0017
  doi: 10.1128/MCB.7.9.3113
– ident: CIT0067
  doi: 10.1111/brv.12418
– ident: CIT0012
  doi: 10.1016/j.fgb.2010.05.008
– ident: CIT0072
  doi: 10.1007/s00294-015-0556-0
– ident: CIT0074
  doi: 10.1371/journal.pone.0089883
– ident: CIT0027
  doi: 10.1038/nmicrobiol.2017.120
– ident: CIT0010
  doi: 10.1371/journal.pgen.1002816
– ident: CIT0016
  doi: 10.1016/j.funbio.2018.01.004
– ident: CIT0003
  doi: 10.1111/j.1365-2958.1993.tb01565.x
– ident: CIT0029
  doi: 10.1371/journal.pone.0040292
– ident: CIT0004
  doi: 10.1371/journal.pbio.1001750
– ident: CIT0014
  doi: 10.1111/geb.12214
– ident: CIT0047
  doi: 10.1099/13500872-142-11-3211
– ident: CIT0081
  doi: 10.1016/0012-1606(90)90215-5
– ident: CIT0058
  doi: 10.1093/cid/ciw691
– ident: CIT0038
  doi: 10.1002/j.1460-2075.1993.tb05899.x
– ident: CIT0055
  doi: 10.1038/srep28874
– ident: CIT0066
  doi: 10.1101/gad.4.9.1473
– volume: 3
  start-page: 747
  year: 1991
  ident: CIT0006
  publication-title: Plant Cell
– ident: CIT0037
  doi: 10.1046/j.1365-2958.2001.02472.x
– ident: CIT0051
  doi: 10.1007/978-3-319-25844-7_12
– ident: CIT0083
  doi: 10.1128/microbiolspec.FUNK-0053-2016
– ident: CIT0009
  doi: 10.1126/science.1163225
– ident: CIT0018
  doi: 10.1007/s00294-017-0692-9
– ident: CIT0043
  doi: 10.1093/nar/gky1085
– volume: 143
  start-page: 155
  year: 1996
  ident: CIT0019
  publication-title: Genetics
  doi: 10.1093/genetics/143.1.155
– ident: CIT0023
  doi: 10.1111/1462-2920.13431
– ident: CIT0071
  doi: 10.1534/genetics.115.174342
– ident: CIT0036
  doi: 10.3389/fmicb.2017.01837
– volume-title: Dictionary of the Fungi
  year: 2008
  ident: CIT0049
– ident: CIT0090
  doi: 10.1046/j.1365-2958.2000.01874.x
– ident: CIT0094
  doi: 10.1002/j.1460-2075.1996.tb00903.x
– ident: CIT0001
  doi: 10.1016/0092-8674(88)90198-5
– ident: CIT0052
  doi: 10.1111/j.1365-2958.2010.07282.x
– ident: CIT0082
  doi: 10.1007/s12275-014-4384-6
– ident: CIT0033
  doi: 10.1111/j.1365-2958.2008.06520.x
– ident: CIT0086
  doi: 10.1111/1462-2920.12618
– ident: CIT0025
  doi: 10.1111/j.1600-0706.2005.14101.x
– ident: CIT0028
  doi: 10.1016/j.tim.2010.09.007
– ident: CIT0087
  doi: 10.3389/fmicb.2018.01859
– ident: CIT0034
  doi: 10.1111/j.1365-2958.2010.07063.x
– ident: CIT0048
  doi: 10.1534/genetics.109.101667
– ident: CIT0088
  doi: 10.1074/jbc.M310840200
– ident: CIT0044
  doi: 10.1186/s12915-016-0309-7
– ident: CIT0065
  doi: 10.1007/BF01637246
– ident: CIT0069
  doi: 10.1038/ncomms14444
– ident: CIT0093
  doi: 10.1128/mBio.01130-18
– ident: CIT0068
  doi: 10.1016/j.cub.2017.04.032
– ident: CIT0042
  doi: 10.1093/nar/gkv1248
– ident: CIT0045
  doi: 10.1038/nmicrobiol.2016.39
– ident: CIT0079
  doi: 10.1016/j.fgb.2017.06.002
– ident: CIT0046
  doi: 10.1038/msb.2009.52
– ident: CIT0063
  doi: 10.1186/s40694-016-0024-8
– ident: CIT0076
  doi: 10.1111/j.1365-2672.2009.04237.x
– ident: CIT0070
  doi: 10.1371/journal.pone.0000970
– ident: CIT0054
  doi: 10.1534/genetics.114.161430
– ident: CIT0059
  doi: 10.1128/EC.00192-06
– volume: 78
  start-page: 679
  year: 1974
  ident: CIT0080
  publication-title: Genetics
  doi: 10.1093/genetics/78.2.679
– ident: CIT0007
  doi: 10.1128/MCB.14.4.2503
– ident: CIT0061
  doi: 10.1128/MCB.11.1.55
– ident: CIT0040
  doi: 10.1111/mmi.13156
– ident: CIT0077
  doi: 10.1016/j.cub.2008.01.061
– ident: CIT0084
  doi: 10.1128/microbiolspec.FUNK-0055-2016
– ident: CIT0053
  doi: 10.1111/j.1365-2958.1994.tb01293.x
– ident: CIT0057
  doi: 10.1128/mSphere.00050-18
– ident: CIT0091
  doi: 10.1111/j.1365-2958.2004.04065.x
– ident: CIT0039
  doi: 10.1128/microbiolspec.FUNK-0052-2016
– ident: CIT0078
  doi: 10.1146/annurev.micro.112408.134000
– ident: CIT0015
  doi: 10.1038/nature.2017.21424
– ident: CIT0021
  doi: 10.1534/genetics.114.165688
– ident: CIT0056
  doi: 10.1007/s00253-015-6823-7
– ident: CIT0005
  doi: 10.1371/journal.pone.0137554
– ident: CIT0035
  doi: 10.1128/EC.00274-12
– ident: CIT0062
  doi: 10.1016/S0169-5347(00)89050-3
– ident: CIT0008
  doi: 10.1371/journal.pone.0048134
– ident: CIT0011
  doi: 10.1111/j.1574-6976.2011.00285.x
– ident: CIT0085
  doi: 10.1111/j.1365-2958.2006.05506.x
– ident: CIT0041
  doi: 10.1093/molbev/msx148
– ident: CIT0030
  doi: 10.1128/EC.00207-07
– ident: CIT0073
  doi: 10.1016/j.simyco.2018.10.002
– ident: CIT0075
  doi: 10.1016/j.mib.2012.09.006
– ident: CIT0060
  doi: 10.1094/PDIS-05-16-0666-PDN
– ident: CIT0064
  doi: 10.1101/gad.6.9.1770
– ident: CIT0092
  doi: 10.1007/BF00326580
– ident: CIT0026
  doi: 10.1186/s13059-017-1151-0
– ident: CIT0089
  doi: 10.1111/j.1365-2958.2003.03961.x
– ident: CIT0013
  doi: 10.1126/science.1155888
– ident: CIT0050
  doi: 10.1073/pnas.1817822116
– ident: CIT0020
  doi: 10.1038/532421a
– ident: CIT0024
  doi: 10.1371/journal.pone.0017505
– ident: CIT0022
  doi: 10.1111/nph.13948
– ident: CIT0002
  doi: 10.1128/MMBR.62.1.35-54.1998
– ident: CIT0031
  doi: 10.1007/3-540-28135-5_14
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Snippet Complex multicellularity (CM) is characterized by the generation of three-dimensional structures that follow a genetically controlled program. CM emerged at...
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SubjectTerms asexual development
asexual spore
complex multicellularity
Eurotiomycetes
evolution
Fungal Proteins - genetics
Fungal Proteins - metabolism
Fungi
Fungi - genetics
Fungi - growth & development
Fungi - physiology
Gene Expression Regulation, Fungal
Gene Regulatory Networks
mycoses
proteome
Reproduction, Asexual
spores
Spores, Fungal - genetics
Spores, Fungal - growth & development
Spores, Fungal - metabolism
transcription factors
Transcription Factors - genetics
Transcription Factors - metabolism
transcriptional network
Title Rewiring of transcriptional networks as a major event leading to the diversity of asexual multicellularity in fungi
URI https://www.tandfonline.com/doi/abs/10.1080/1040841X.2019.1630359
https://www.ncbi.nlm.nih.gov/pubmed/31267819
https://www.proquest.com/docview/2251691196
https://www.proquest.com/docview/2477621931
Volume 45
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