Partial penetrance facilitates developmental evolution in bacteria
Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the unde...
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Published in | Nature (London) Vol. 460; no. 7254; pp. 510 - 514 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
23.07.2009
Nature Publishing Group |
Subjects | |
Online Access | Get full text |
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Abstract | Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve. Here we identify a stochastic cell fate determination process that operates in Bacillus subtilis sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an intercompartmental signalling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable 'twin' spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we can systematically tune the penetrance of each mutant fate. Furthermore, signalling and replication perturbations synergize to significantly increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type Clostridium oceanicum shows a strong resemblance to twin sporulation in these B. subtilis mutants. Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters. |
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AbstractList | The role of partial penetrance in development
Geneticists have long known that individuals with exactly the same genetic make-up can differ from one another in their development and resulting phenotype, but the developmental and evolutionary significance of the phenomenon are not clear. The nature of this 'partial penetrance', whereby the effects of a mutation are observed only in some individuals, even in an isogenic population, has been studied using
Bacillus subtilis
sporulation as a model developmental system. The results suggest how mutations affecting DNA replication and cell division may act in synergy to facilitate the evolution of twin sporulation as a new trait, through progressive increases in its penetrance.
Individuals with exactly the same genetic make-up can differ from one another in their development and resulting phenotype when the genome contains a mutation — a phenomenon called 'partial penetrance'. Exploration of the genetic and stochastic factors controlling the proportion of abnormal 'twin' spores in mutant populations of the bacterium
Bacillus subtilus
now reveals how mutations affecting DNA replication and cell division may act in synergy to significantly increase the penetrance of twin sporulation.
Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently
1
,
2
,
3
,
4
. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve
5
,
6
,
7
,
8
. Here we identify a stochastic cell fate determination process that operates in
Bacillus subtilis
sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an intercompartmental signalling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable ‘twin’ spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we can systematically tune the penetrance of each mutant fate. Furthermore, signalling and replication perturbations synergize to significantly increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type
Clostridium oceanicum
shows a strong resemblance to twin sporulation in these
B. subtilis
mutants
9
,
10
. Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters. Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve. Here we identify a stochastic cell fate determination process that operates in Bacillus subtilis sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an intercompartmental signalling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable 'twin' spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we can systematically tune the penetrance of each mutant fate. Furthermore, signalling and replication perturbations synergize to significantly increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type Clostridium oceanicum shows a strong resemblance to twin sporulation in these B. subtilis mutants. Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters. Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fate of individual organisms differently 1 - 4 . This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve 5 - 8 . Here, we identify a stochastic cell fate determination process that operates in Bacillus subtilis sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an inter-compartmental signaling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable “twin” spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we could systematically tune the penetrance of each mutant fate. Furthermore, signaling and replication perturbations synergize to dramatically increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type Clostridium oceanicum showed a strong resemblance to twin sporulation in these B. subtilis mutants 9 , 10 . Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters. Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms differently. This phenomenon, known as partial penetrance, has been observed in diverse developmental systems. However, it remains unclear how the underlying genetic network specifies the set of possible alternative fates and how the relative frequencies of these fates evolve. Here we identify a stochastic cell fate determination process that operates in Bacillus subtilis sporulation mutants and show how it allows genetic control of the penetrance of multiple fates. Mutations in an intercompartmental signalling process generate a set of discrete alternative fates not observed in wild-type cells, including rare formation of two viable 'twin' spores, rather than one within a single cell. By genetically modulating chromosome replication and septation, we can systematically tune the penetrance of each mutant fate. Furthermore, signalling and replication perturbations synergize to significantly increase the penetrance of twin sporulation. These results suggest a potential pathway for developmental evolution between monosporulation and twin sporulation through states of intermediate twin penetrance. Furthermore, time-lapse microscopy of twin sporulation in wild-type Clostridium oceanicum shows a strong resemblance to twin sporulation in these B. subtilis mutants. Together the results suggest that noise can facilitate developmental evolution by enabling the initial expression of discrete morphological traits at low penetrance, and allowing their stabilization by gradual adjustment of genetic parameters. [PUBLICATION ABSTRACT] |
Audience | Academic |
Author | Eldar, Avigdor Dworkin, Jonathan Xenopoulos, Panagiotis Fontes, Michelle E Piggot, Patrick J Chary, Vasant K Loson, Oliver C Elowitz, Michael B |
AuthorAffiliation | 2 Department of Microbiology and Immunology, Temple University School of Medicine, 3400 North Broad St., Philadelphia, PA 19140, USA 1 Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology, Pasadena, CA 91125 3 Department of Microbiology, College of Physicians and Surgeons, Columbia University, New York, New York 10032 |
AuthorAffiliation_xml | – name: 1 Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology, Pasadena, CA 91125 – name: 3 Department of Microbiology, College of Physicians and Surgeons, Columbia University, New York, New York 10032 – name: 2 Department of Microbiology and Immunology, Temple University School of Medicine, 3400 North Broad St., Philadelphia, PA 19140, USA |
Author_xml | – sequence: 1 givenname: Michael B surname: Elowitz fullname: Elowitz, Michael B organization: Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology – sequence: 2 givenname: Avigdor surname: Eldar fullname: Eldar, Avigdor organization: Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology – sequence: 3 givenname: Vasant K surname: Chary fullname: Chary, Vasant K organization: Department of Microbiology and Immunology, Temple University School of Medicine – sequence: 4 givenname: Panagiotis surname: Xenopoulos fullname: Xenopoulos, Panagiotis organization: Department of Microbiology and Immunology, Temple University School of Medicine – sequence: 5 givenname: Michelle E surname: Fontes fullname: Fontes, Michelle E organization: Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology – sequence: 6 givenname: Oliver C surname: Loson fullname: Loson, Oliver C organization: Howard Hughes Medical Institute and Division of Biology and Department of Applied Physics, California Institute of Technology – sequence: 7 givenname: Jonathan surname: Dworkin fullname: Dworkin, Jonathan organization: Department of Microbiology, College of Physicians and Surgeons, Columbia University – sequence: 8 givenname: Patrick J surname: Piggot fullname: Piggot, Patrick J organization: Department of Microbiology and Immunology, Temple University School of Medicine |
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ContentType | Journal Article |
Copyright | Macmillan Publishers Limited. All rights reserved 2009 2009 INIST-CNRS COPYRIGHT 2009 Nature Publishing Group Copyright Nature Publishing Group Jul 23, 2009 |
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Keywords | Development Bacteria Bacillales Bacillaceae Bacillus subtilis Sporulation |
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References | Ben-Yehuda, S., Losick, R. (b23) 2002; 109 Angert, E. R., Losick, R. M. (b20) 1998; 95 Harwood, C. R., Cutting, S. M. (b29) 1990 Suel, G. M., Garcia-Ojalvo, J., Liberman, L. M., Elowitz, M. B. (b31) 2006; 440 Becker, E. C., Pogliano, K. (b33) 2007; 66 Dworkin, J., Losick, R. (b18) 2005; 121 Rosenfeld, N., Young, J. W., Alon, U., Swain, P. S., Elowitz, M. B. (b30) 2005; 307 Sangster, T. A. (b3) 2008; 105 Zupancic, M. L., Tran, H., Hofmeister, A. E. (b13) 2001; 39 Paredes, C. J., Alsaker, K. V., Papoutsakis, E. T. (b19) 2005; 3 Zeigler, D. R. (b34) 2008; 190 Youngman, P., Perkins, J. B., Losick, R. (b28) 1984; 12 Khvorova, A., Chary, V. K., Hilbert, D. W., Piggot, P. J. (b12) 2000; 182 Pogliano, J. (b17) 1999; 31 West-Eberhard, M. J. (b7) 2005; 102 Angert, E. R. (b10) 2005; 3 Kirschner, M., Gerhart, J. (b8) 2005 Queitsch, C., Sangster, T. A., Lindquist, S. (b2) 2002; 417 Eichenberger, P., Fawcett, P., Losick, R. (b16) 2001; 42 Rutherford, S., Hirate, Y., Swalla, B. J. (b27) 2007; 42 Coote, J. G. (b4) 1972; 71 Lee, P. S., Lin, D. C., Moriya, S., Grossman, A. D. (b22) 2003; 185 Horvitz, H. R., Sulston, J. E. (b1) 1980; 96 Hilbert, D. W., Piggot, P. J. (b11) 2004; 68 Smith, L. D. (b9) 1970; 103 Suel, G. M., Kulkarni, R. P., Dworkin, J., Garcia-Ojalvo, J., Elowitz, M. B. (b32) 2007; 315 Felix, M. A., Wagner, A. (b6) 2008; 100 Noirot-Gros, M. F. (b24) 2006; 103 Keis, S., Shaheen, R., Jones, D. T. (b25) 2001; 51 Piggot, P. J., Coote, J. G. (b14) 1976; 40 Karow, M. L., Glaser, P., Piggot, P. J. (b15) 1995; 92 Rutherford, S. L., Henikoff, S. (b5) 2003; 33 Waddington, C. H. (b26) 1942; 150 Dworkin, J., Losick, R. (b21) 2002; 99 Felix, Wagner (CR6) 2008; 100 Zupancic, Tran, Hofmeister (CR13) 2001; 39 Piggot, Coote (CR14) 1976; 40 Pogliano (CR17) 1999; 31 Hilbert, Piggot (CR11) 2004; 68 Lee, Lin, Moriya, Grossman (CR22) 2003; 185 West-Eberhard (CR7) 2005; 102 Angert, Losick (CR20) 1998; 95 Dworkin, Losick (CR21) 2002; 99 Rosenfeld, Young, Alon, Swain, Elowitz (CR30) 2005; 307 Rutherford, Hirate, Swalla (CR27) 2007; 42 Angert (CR10) 2005; 3 Queitsch, Sangster, Lindquist (CR2) 2002; 417 Eichenberger, Fawcett, Losick (CR16) 2001; 42 Suel, Garcia-Ojalvo, Liberman, Elowitz (CR31) 2006; 440 Ben-Yehuda, Losick (CR23) 2002; 109 Coote (CR4) 1972; 71 Kirschner, Gerhart (CR8) 2005 Horvitz, Sulston (CR1) 1980; 96 Keis, Shaheen, Jones (CR25) 2001; 51 Karow, Glaser, Piggot (CR15) 1995; 92 Harwood, Cutting (CR29) 1990 Zeigler (CR34) 2008; 190 Waddington (CR26) 1942; 150 Sangster (CR3) 2008; 105 Suel, Kulkarni, Dworkin, Garcia-Ojalvo, Elowitz (CR32) 2007; 315 Smith (CR9) 1970; 103 Rutherford, Henikoff (CR5) 2003; 33 Noirot-Gros (CR24) 2006; 103 Dworkin, Losick (CR18) 2005; 121 Youngman, Perkins, Losick (CR28) 1984; 12 Khvorova, Chary, Hilbert, Piggot (CR12) 2000; 182 Paredes, Alsaker, Papoutsakis (CR19) 2005; 3 Becker, Pogliano (CR33) 2007; 66 LD Smith (BFnature08150_CR9) 1970; 103 MJ West-Eberhard (BFnature08150_CR7) 2005; 102 CJ Paredes (BFnature08150_CR19) 2005; 3 J Pogliano (BFnature08150_CR17) 1999; 31 JG Coote (BFnature08150_CR4) 1972; 71 P Eichenberger (BFnature08150_CR16) 2001; 42 ML Karow (BFnature08150_CR15) 1995; 92 A Khvorova (BFnature08150_CR12) 2000; 182 CR Harwood (BFnature08150_CR29) 1990 GM Suel (BFnature08150_CR32) 2007; 315 DR Zeigler (BFnature08150_CR34) 2008; 190 J Dworkin (BFnature08150_CR18) 2005; 121 TA Sangster (BFnature08150_CR3) 2008; 105 S Keis (BFnature08150_CR25) 2001; 51 EC Becker (BFnature08150_CR33) 2007; 66 P Youngman (BFnature08150_CR28) 1984; 12 MA Felix (BFnature08150_CR6) 2008; 100 HR Horvitz (BFnature08150_CR1) 1980; 96 J Dworkin (BFnature08150_CR21) 2002; 99 ER Angert (BFnature08150_CR10) 2005; 3 SL Rutherford (BFnature08150_CR5) 2003; 33 GM Suel (BFnature08150_CR31) 2006; 440 C Queitsch (BFnature08150_CR2) 2002; 417 M Kirschner (BFnature08150_CR8) 2005 S Ben-Yehuda (BFnature08150_CR23) 2002; 109 ER Angert (BFnature08150_CR20) 1998; 95 MF Noirot-Gros (BFnature08150_CR24) 2006; 103 PJ Piggot (BFnature08150_CR14) 1976; 40 CH Waddington (BFnature08150_CR26) 1942; 150 S Rutherford (BFnature08150_CR27) 2007; 42 ML Zupancic (BFnature08150_CR13) 2001; 39 DW Hilbert (BFnature08150_CR11) 2004; 68 PS Lee (BFnature08150_CR22) 2003; 185 N Rosenfeld (BFnature08150_CR30) 2005; 307 |
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Snippet | Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fates of individual organisms... The role of partial penetrance in development Geneticists have long known that individuals with exactly the same genetic make-up can differ from one another in... Development normally occurs similarly in all individuals within an isogenic population, but mutations often affect the fate of individual organisms differently... |
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SubjectTerms | Bacillus subtilis Bacillus subtilis - genetics Bacillus subtilis - physiology Bacteria Bacteriology Biological and medical sciences Biological Evolution Chromosomes Clostridium Developmental biology DNA Replication Evolution Fluorescence Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Bacterial Gene mutations Genetic aspects Growth, nutrition, cell differenciation Humanities and Social Sciences letter Methods Microbiology multidisciplinary Mutation Physiological aspects Science Science (multidisciplinary) Spores, Bacterial - growth & development Stochastic processes Twins |
Title | Partial penetrance facilitates developmental evolution in bacteria |
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