The Phenotype Paradox: Lessons From Natural Transcriptome Evolution on How to Engineer Plants

Plants have evolved genome complexity through iterative rounds of single gene and whole genome duplication. This has led to substantial expansion in transcription factor numbers following preferential retention and subsequent functional divergence of these regulatory genes. Here we review how this s...

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Published inFrontiers in plant science Vol. 11; p. 75
Main Authors Law, Justin, Ng, Kangbo, Windram, Oliver P F
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 18.02.2020
Subjects
breeding and genomics
directed evolution
gene network analysis
Plant Science
synthetic biology
systems biology
systems biology
breeding and genomics
gene network analysis
synthetic biology
directed evolution
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Abstract Plants have evolved genome complexity through iterative rounds of single gene and whole genome duplication. This has led to substantial expansion in transcription factor numbers following preferential retention and subsequent functional divergence of these regulatory genes. Here we review how this simple evolutionary network rewiring process, regulatory gene duplication followed by functional divergence, can be used to inspire synthetic biology approaches that seek to develop novel phenotypic variation for future trait based breeding programs in plants.
AbstractList Plants have evolved genome complexity through iterative rounds of single gene and whole genome duplication. This has led to substantial expansion in transcription factor numbers following preferential retention and subsequent functional divergence of these regulatory genes. Here we review how this simple evolutionary network rewiring process, regulatory gene duplication followed by functional divergence, can be used to inspire synthetic biology approaches that seek to develop novel phenotypic variation for future trait based breeding programs in plants.
Author Windram, Oliver P F
Law, Justin
Ng, Kangbo
AuthorAffiliation 3 Institute for the Physics of Living Systems, University College London , London , United Kingdom
2 The Francis Crick Institute , London , United Kingdom
1 Grand Challenges in Ecosystems and the Environment, Imperial College London , Ascot , United Kingdom
AuthorAffiliation_xml – name: 2 The Francis Crick Institute , London , United Kingdom
– name: 1 Grand Challenges in Ecosystems and the Environment, Imperial College London , Ascot , United Kingdom
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Author_xml – sequence: 1
  givenname: Justin
  surname: Law
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  surname: Windram
  fullname: Windram, Oliver P F
  organization: Grand Challenges in Ecosystems and the Environment, Imperial College London, Ascot, United Kingdom
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Cites_doi 10.1111/j.1365-313X.2011.04647.x
10.1186/s13015-017-0100-5
10.1016/S1360-1385(98)01232-1
10.1016/j.pbi.2010.04.006
10.1073/pnas.0501102102
10.1038/386485a0
10.1126/scisignal.2001014
10.1093/genetics/160.4.1651
10.1104/pp.112.200147
10.1016/j.tplants.2016.01.014
10.1371/journal.pone.0096732
10.1104/pp.006478
10.1126/science.1126410
10.1016/j.bbagrm.2016.08.005
10.1371/journal.pgen.1000772
10.1146/annurev.bi.46.070177.003041
10.1098/rstb.2013.0353
10.1038/nature09534
10.1038/nrg1272
10.1016/j.artmed.2018.10.006
10.1016/S1369-5266(00)00107-2
10.1038/ng.942
10.1186/s13059-016-0908-1
10.1186/1471-2229-8-68
10.1093/bioinformatics/btx501
10.1126/science.1158684
10.1111/tpj.12434
10.1073/pnas.1201961109
10.1093/molbev/msv058
10.1126/science.290.5494.1151
10.1038/35075138
10.1111/j.1365-313X.2010.04459.x
10.1093/jxb/ers100
10.1186/s12859-017-1657-1
10.1371/journal.pone.0028646
10.1016/j.tplants.2005.11.002
10.1126/science.aar6089
10.1126/science.1248688
10.1016/j.copbio.2015.02.001
10.1105/tpc.15.00471
10.1073/pnas.1309606110
10.1093/bioinformatics/btr626
10.1038/nbt0597-436
10.1093/nar/gkx197
10.1371/journal.pcbi.0030059
10.1371/journal.pone.0068358
10.1038/nmeth.2016
10.1038/ng.2877
10.1103/PhysRevE.89.012702
10.1016/j.biosystems.2008.12.004
10.1104/pp.008532
10.1073/pnas.1719622115
10.1105/tpc.112.102046
10.1038/cr.2007.104
10.1007/978-3-642-86659-3
10.1073/pnas.252535999
10.1016/j.cell.2014.08.009
10.1016/S1360-1385(00)01600-9
10.1105/tpc.021410
10.1038/nature09916
10.1515/sagmb-2014-0082
10.1016/j.chom.2013.12.002
10.3389/fpls.2019.00560
10.1038/nature06847
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Keywords systems biology
breeding and genomics
gene network analysis
synthetic biology
directed evolution
Language English
License Copyright © 2020 Law, Ng and Windram.
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Reviewed by: Tsubasa Shoji, Nara Institute of Science and Technology (NAIST), Japan; Zhe Liang, Heidelberg University, Germany
This article was submitted to Plant Biotechnology, a section of the journal Frontiers in Plant Science
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References Weirauch (B55) 2014; 158
Lehti-Shiu (B30) 2017; 1860
Ohno (B37) 1970
Swanson-Wagner (B46) 2012; 109
Swinnen (B47) 2016; 21
Wendel (B56) 2016; 17
Crameri (B6) 1997; 15
Feller (B11) 2011; 66
Penfold (B38) 2015; 14
Mittler (B36) 2006; 11
Delgado (B7) 2019; 95
Marbach (B35) 2012; 9
Yu (B61) 2007; 3
Grandbastien (B13) 1998; 3
Kashkush (B23) 2002; 160
Grimaldi (B14) 2011; 6
Haake (B16) 2002; 130
Kreps (B28) 2002; 130
Riechmann (B41) 2000; 3
Maere (B34) 2005; 102
Rydenfelt (B42) 2014; 89
Tsuda (B49) 2010; 13
Barabási (B3) 2004; 5
Blanc (B5) 2004; 16
Zhang (B64) 2012; 28
Wei (B54) 2018; 115
Jeong (B19) 2001; 411
Koenig (B26) 2013; 110
Yokobayashi (B60) 2002; 99
Shoji (B44) 2019; 10
Kim (B25) 2014; 15
Tsuda (B50) 2009; 5
Studer (B45) 2011; 43
Hénaff (B15) 2014; 77
Hecker (B17) 2009; 96
Godsey (B12) 2013; 8
Thiagarajan (B48) 2017; 12
Jiang (B20) 2013; 161
Ramírez-González (B40) 2018; 361
Shoji (B43) 2011; 67
Lai (B29) 2008; 8
Yu (B62) 2008; 322
Deng (B8) 2017; 33
Jiao (B21) 2011; 473
Eulgem (B10) 2000; 5
Liu (B32) 2017; 18
Jin (B22) 2015; 32
Windram (B59) 2017; 45
Doebley (B9) 1997; 386
Voordeckers (B53) 2015; 34
Lynch (B33) 2000; 290
Lewis (B31) 2015; 27
Wilson (B57) 1977; 46
Atkinson (B2) 2012; 63
Altshuler (B1) 2010; 467
Isalan (B18) 2008; 452
Zhang (B63) 2008; 18
Bhardwaj (B4) 2010; 3
Windram (B58) 2012; 24
Plucain (B39) 2014; 343
Kim (B24) 2014; 46
Konishi (B27) 2006; 312
Vanneste (B51) 2014; 369
Villaverde (B52) 2014; 9
References_xml – volume: 67
  start-page: 949
  year: 2011
  ident: B43
  article-title: Recruitment of a duplicated primary metabolism gene into the nicotine biosynthesis regulon in tobacco
  publication-title: Plant J.
  doi: 10.1111/j.1365-313X.2011.04647.x
  contributor:
    fullname: Shoji
– volume: 12
  start-page: 8
  year: 2017
  ident: B48
  article-title: The feasibility of genome-scale biological network inference using graphics processing units
  publication-title: Algorithms Mol. Biol.
  doi: 10.1186/s13015-017-0100-5
  contributor:
    fullname: Thiagarajan
– volume: 3
  start-page: 181
  year: 1998
  ident: B13
  article-title: Activation of plant retrotransposons under stress conditions
  publication-title: Trends Plant Sci.
  doi: 10.1016/S1360-1385(98)01232-1
  contributor:
    fullname: Grandbastien
– volume: 13
  start-page: 459
  year: 2010
  ident: B49
  article-title: Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity
  publication-title: Curr. Opin. Plant Biol.
  doi: 10.1016/j.pbi.2010.04.006
  contributor:
    fullname: Tsuda
– volume: 102
  start-page: 5454
  year: 2005
  ident: B34
  article-title: Modeling gene and genome duplications in eukaryotes
  publication-title: Proc. Natl. Acad. Sci.
  doi: 10.1073/pnas.0501102102
  contributor:
    fullname: Maere
– volume: 386
  start-page: 485
  year: 1997
  ident: B9
  article-title: The evolution of apical dominance in maize
  publication-title: Nature
  doi: 10.1038/386485a0
  contributor:
    fullname: Doebley
– volume: 3
  start-page: ra79
  year: 2010
  ident: B4
  article-title: Rewiring of transcriptional regulatory networks: hierarchy, rather than connectivity, better reflects the importance of regulators
  publication-title: Sci. Signal.
  doi: 10.1126/scisignal.2001014
  contributor:
    fullname: Bhardwaj
– volume: 160
  start-page: 1651
  year: 2002
  ident: B23
  article-title: Gene loss, silencing and activation in a newly synthesized wheat allotetraploid
  publication-title: Genetics
  doi: 10.1093/genetics/160.4.1651
  contributor:
    fullname: Kashkush
– volume: 161
  start-page: 1844
  year: 2013
  ident: B20
  article-title: Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants
  publication-title: Plant Physiol.
  doi: 10.1104/pp.112.200147
  contributor:
    fullname: Jiang
– volume: 21
  start-page: 506
  year: 2016
  ident: B47
  article-title: Lessons from domestication: targeting cis-regulatory elements for crop improvement
  publication-title: Trends Plant Sci.
  doi: 10.1016/j.tplants.2016.01.014
  contributor:
    fullname: Swinnen
– volume: 9
  year: 2014
  ident: B52
  article-title: MIDER: network inference with mutual information distance and entropy reduction
  publication-title: PloS One
  doi: 10.1371/journal.pone.0096732
  contributor:
    fullname: Villaverde
– volume: 130
  start-page: 639
  year: 2002
  ident: B16
  article-title: Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis
  publication-title: Plant Physiol.
  doi: 10.1104/pp.006478
  contributor:
    fullname: Haake
– volume: 312
  start-page: 1392
  year: 2006
  ident: B27
  article-title: An SNP caused loss of seed shattering during rice domestication
  publication-title: Sci. (80-. )
  doi: 10.1126/science.1126410
  contributor:
    fullname: Konishi
– volume: 1860
  start-page: 3
  year: 2017
  ident: B30
  article-title: Diversity, expansion, and evolutionary novelty of plant DNA-binding transcription factor families
  publication-title: Biochim. Biophys. Acta - Gene Regul. Mech.
  doi: 10.1016/j.bbagrm.2016.08.005
  contributor:
    fullname: Lehti-Shiu
– volume: 5
  start-page: e1000772
  year: 2009
  ident: B50
  article-title: Network properties of robust immunity in plants
  publication-title: PloS Genet.
  doi: 10.1371/journal.pgen.1000772
  contributor:
    fullname: Tsuda
– volume: 46
  start-page: 573
  year: 1977
  ident: B57
  article-title: Biochemical Evolution
  publication-title: Annu. Rev. Biochem.
  doi: 10.1146/annurev.bi.46.070177.003041
  contributor:
    fullname: Wilson
– volume: 369
  year: 2014
  ident: B51
  article-title: Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution
  publication-title: Philos. Trans. R. Soc B Biol. Sci.
  doi: 10.1098/rstb.2013.0353
  contributor:
    fullname: Vanneste
– volume: 467
  start-page: 1061
  year: 2010
  ident: B1
  article-title: A map of human genome variation from population-scale sequencing
  publication-title: Nature
  doi: 10.1038/nature09534
  contributor:
    fullname: Altshuler
– volume: 5
  start-page: 101
  year: 2004
  ident: B3
  article-title: Network biology: understanding the cell's functional organization
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg1272
  contributor:
    fullname: Barabási
– volume: 95
  start-page: 133
  year: 2019
  ident: B7
  article-title: Computational methods for gene regulatory networks reconstruction and analysis: a review
  publication-title: Artif. Intell. Med.
  doi: 10.1016/j.artmed.2018.10.006
  contributor:
    fullname: Delgado
– volume: 3
  start-page: 423
  year: 2000
  ident: B41
  article-title: A genomic perspective on plant transcription factors
  publication-title: Curr. Opin. Plant Biol.
  doi: 10.1016/S1369-5266(00)00107-2
  contributor:
    fullname: Riechmann
– volume: 43
  start-page: 1160
  year: 2011
  ident: B45
  article-title: Identification of a functional transposon insertion in the maize domestication gene tb1
  publication-title: Nat. Genet.
  doi: 10.1038/ng.942
  contributor:
    fullname: Studer
– volume: 17
  year: 2016
  ident: B56
  article-title: Evolution of plant genome architecture
  publication-title: Genome Biol.
  doi: 10.1186/s13059-016-0908-1
  contributor:
    fullname: Wendel
– volume: 8
  start-page: 68
  year: 2008
  ident: B29
  article-title: Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens
  publication-title: BMC Plant Biol.
  doi: 10.1186/1471-2229-8-68
  contributor:
    fullname: Lai
– volume: 33
  start-page: 3964
  year: 2017
  ident: B8
  article-title: HiDi: an efficient reverse engineering schema for large-scale dynamic regulatory network reconstruction using adaptive differentiation
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btx501
  contributor:
    fullname: Deng
– volume: 322
  start-page: 104
  year: 2008
  ident: B62
  article-title: High-quality binary protein interaction map of the yeast interactome network
  publication-title: Sci. (80-. ).
  doi: 10.1126/science.1158684
  contributor:
    fullname: Yu
– volume: 77
  start-page: 852
  year: 2014
  ident: B15
  article-title: Extensive amplification of the E2F transcription factor binding sites by transposons during evolution of Brassica species
  publication-title: Plant J.
  doi: 10.1111/tpj.12434
  contributor:
    fullname: Hénaff
– volume: 109
  start-page: 11878
  year: 2012
  ident: B46
  article-title: Reshaping of the maize transcriptome by domestication
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1201961109
  contributor:
    fullname: Swanson-Wagner
– volume: 32
  start-page: 1767
  year: 2015
  ident: B22
  article-title: An Arabidopsis transcriptional regulatory map reveals distinct functional and evolutionary features of novel transcription factors
  publication-title: Mol. Biol. Evol.
  doi: 10.1093/molbev/msv058
  contributor:
    fullname: Jin
– volume: 290
  start-page: 1151
  year: 2000
  ident: B33
  article-title: The evolutionary fate and consequences of duplicate genes
  publication-title: Sci. (80-. ).
  doi: 10.1126/science.290.5494.1151
  contributor:
    fullname: Lynch
– volume: 411
  start-page: 41
  year: 2001
  ident: B19
  article-title: Lethality and centrality in protein networks
  publication-title: Nature
  doi: 10.1038/35075138
  contributor:
    fullname: Jeong
– volume: 66
  start-page: 94
  year: 2011
  ident: B11
  article-title: Evolutionary and comparative analysis of MYB and bHLH plant transcription factors
  publication-title: Plant J.
  doi: 10.1111/j.1365-313X.2010.04459.x
  contributor:
    fullname: Feller
– volume: 63
  start-page: 3523
  year: 2012
  ident: B2
  article-title: The interaction of plant biotic and abiotic stresses: from genes to the field
  publication-title: J. Exp. Bot.
  doi: 10.1093/jxb/ers100
  contributor:
    fullname: Atkinson
– volume: 18
  start-page: 241
  year: 2017
  ident: B32
  article-title: A time series driven decomposed evolutionary optimization approach for reconstructing large-scale gene regulatory networks based on fuzzy cognitive maps
  publication-title: BMC Bioinf.
  doi: 10.1186/s12859-017-1657-1
  contributor:
    fullname: Liu
– volume: 6
  year: 2011
  ident: B14
  article-title: Regnann: reverse engineering gene networks using artificial neural networks
  publication-title: PloS One
  doi: 10.1371/journal.pone.0028646
  contributor:
    fullname: Grimaldi
– volume: 11
  start-page: 15
  year: 2006
  ident: B36
  article-title: Abiotic stress, the field environment and stress combination
  publication-title: Trends Plant Sci.
  doi: 10.1016/j.tplants.2005.11.002
  contributor:
    fullname: Mittler
– volume: 361
  start-page: eaar6089
  year: 2018
  ident: B40
  article-title: The transcriptional landscape of polyploid wheat
  publication-title: Sci. (80-. )
  doi: 10.1126/science.aar6089
  contributor:
    fullname: Ramírez-González
– volume: 343
  start-page: 1366
  year: 2014
  ident: B39
  article-title: Epistasis and allele specificity in the emergence of a stable polymorphism in Escherichia coli
  publication-title: Sci. (80-. )
  doi: 10.1126/science.1248688
  contributor:
    fullname: Plucain
– volume: 34
  start-page: 180
  year: 2015
  ident: B53
  article-title: How do regulatory networks evolve and expand throughout evolution?
  publication-title: Curr. Opin. Biotechnol.
  doi: 10.1016/j.copbio.2015.02.001
  contributor:
    fullname: Voordeckers
– volume: 27
  start-page: 3038
  year: 2015
  ident: B31
  article-title: Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000
  publication-title: Plant Cell
  doi: 10.1105/tpc.15.00471
  contributor:
    fullname: Lewis
– volume: 110
  start-page: E2655
  year: 2013
  ident: B26
  article-title: Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1309606110
  contributor:
    fullname: Koenig
– volume: 28
  start-page: 98
  year: 2012
  ident: B64
  article-title: Inferring gene regulatory networks from gene expression data by path consistency algorithm based on conditional mutual information
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr626
  contributor:
    fullname: Zhang
– volume: 15
  start-page: 436
  year: 1997
  ident: B6
  article-title: Molecular evolution of an arsenate detoxification pathway by dna shuffling
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt0597-436
  contributor:
    fullname: Crameri
– volume: 45
  start-page: 4984
  year: 2017
  ident: B59
  article-title: Engineering microbial phenotypes through rewiring of genetic networks
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx197
  contributor:
    fullname: Windram
– volume: 3
  start-page: e59
  year: 2007
  ident: B61
  article-title: The Importance of Bottlenecks in Protein Networks: Correlation with Gene Essentiality and Expression Dynamics
  publication-title: PloS Comput. Biol.
  doi: 10.1371/journal.pcbi.0030059
  contributor:
    fullname: Yu
– volume: 8
  year: 2013
  ident: B12
  article-title: Improved inference of gene regulatory networks through integrated Bayesian clustering and dynamic modeling of time-course expression data
  publication-title: PloS One
  doi: 10.1371/journal.pone.0068358
  contributor:
    fullname: Godsey
– volume: 9
  start-page: 796
  year: 2012
  ident: B35
  article-title: Wisdom of crowds for robust gene network inference
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2016
  contributor:
    fullname: Marbach
– volume: 46
  start-page: 270
  year: 2014
  ident: B24
  article-title: Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2877
  contributor:
    fullname: Kim
– volume: 89
  start-page: 012702
  year: 2014
  ident: B42
  article-title: Statistical mechanical model of coupled transcription from multiple promoters due to transcription factor titration
  publication-title: Phys. Rev. E. Stat. Nonlin. Soft Matter Phys.
  doi: 10.1103/PhysRevE.89.012702
  contributor:
    fullname: Rydenfelt
– volume: 96
  start-page: 86
  year: 2009
  ident: B17
  article-title: Gene regulatory network inference: data integration in dynamic models-A review
  publication-title: BioSystems
  doi: 10.1016/j.biosystems.2008.12.004
  contributor:
    fullname: Hecker
– volume: 130
  start-page: 2129
  year: 2002
  ident: B28
  article-title: Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress
  publication-title: Plant Physiol.
  doi: 10.1104/pp.008532
  contributor:
    fullname: Kreps
– volume: 115
  start-page: E4151
  year: 2018
  ident: B54
  article-title: Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.1719622115
  contributor:
    fullname: Wei
– volume: 24
  start-page: 3530
  year: 2012
  ident: B58
  article-title: Arabidopsis defense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis
  publication-title: Plant Cell
  doi: 10.1105/tpc.112.102046
  contributor:
    fullname: Windram
– volume: 18
  start-page: 508
  year: 2008
  ident: B63
  article-title: Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants
  publication-title: Cell Res.
  doi: 10.1038/cr.2007.104
  contributor:
    fullname: Zhang
– volume-title: Evolution by gene duplication
  year: 1970
  ident: B37
  doi: 10.1007/978-3-642-86659-3
  contributor:
    fullname: Ohno
– volume: 99
  start-page: 16587
  year: 2002
  ident: B60
  article-title: Directed evolution of a genetic circuit
  publication-title: Proc. Natl. Acad. Sci. U. S. A.
  doi: 10.1073/pnas.252535999
  contributor:
    fullname: Yokobayashi
– volume: 158
  start-page: 1431
  year: 2014
  ident: B55
  article-title: Determination and inference of eukaryotic transcription factor sequence specificity
  publication-title: Cell
  doi: 10.1016/j.cell.2014.08.009
  contributor:
    fullname: Weirauch
– volume: 5
  start-page: 199
  year: 2000
  ident: B10
  article-title: The WRKY superfamily of plant transcription factors
  publication-title: Trends Plant Sci.
  doi: 10.1016/S1360-1385(00)01600-9
  contributor:
    fullname: Eulgem
– volume: 16
  start-page: 1679
  year: 2004
  ident: B5
  article-title: Functional divergence of duplicated genes formed by polyploidy during arabidopsis evolution
  publication-title: Plant Cell
  doi: 10.1105/tpc.021410
  contributor:
    fullname: Blanc
– volume: 473
  start-page: 97
  year: 2011
  ident: B21
  article-title: Ancestral polyploidy in seed plants and angiosperms
  publication-title: Nature
  doi: 10.1038/nature09916
  contributor:
    fullname: Jiao
– volume: 14
  start-page: 307
  year: 2015
  ident: B38
  article-title: CSI: a nonparametric Bayesian approach to network inference from multiple perturbed time series gene expression data
  publication-title: Stat. Appl. Genet. Mol. Biol.
  doi: 10.1515/sagmb-2014-0082
  contributor:
    fullname: Penfold
– volume: 15
  start-page: 84
  year: 2014
  ident: B25
  article-title: Mechanisms underlying robustness and tunability in a plant immune signaling network
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2013.12.002
  contributor:
    fullname: Kim
– volume: 10
  year: 2019
  ident: B44
  article-title: The recruitment model of metabolic evolution: jasmonate-responsive transcription factors and a conceptual model for the evolution of metabolic pathways
  publication-title: Front. Plant Sci.
  doi: 10.3389/fpls.2019.00560
  contributor:
    fullname: Shoji
– volume: 452
  start-page: 840
  year: 2008
  ident: B18
  article-title: Evolvability and hierarchy in rewired bacterial gene networks
  publication-title: Nature
  doi: 10.1038/nature06847
  contributor:
    fullname: Isalan
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StartPage 75
SubjectTerms breeding and genomics
directed evolution
gene network analysis
Plant Science
synthetic biology
systems biology
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Title The Phenotype Paradox: Lessons From Natural Transcriptome Evolution on How to Engineer Plants
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