Dynamic evolution of small signalling peptide compensation in plant stem cell control.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
received:
09
09
2021
accepted:
24
02
2022
pubmed:
30
3
2022
medline:
26
4
2022
entrez:
29
3
2022
Statut:
ppublish
Résumé
Gene duplications are a hallmark of plant genome evolution and a foundation for genetic interactions that shape phenotypic diversity
Identifiants
pubmed: 35347264
doi: 10.1038/s41477-022-01118-w
pii: 10.1038/s41477-022-01118-w
doi:
Substances chimiques
Peptides
0
Protein Sorting Signals
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
346-355Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Conrad, B. & Antonarakis, S. E. Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu. Rev. Genom. Hum. Genet. 8, 17–35 (2007).
doi: 10.1146/annurev.genom.8.021307.110233
Carretero-Paulet, L. & Fares, M. A. Evolutionary dynamics and functional specialization of plant paralogs formed by whole and small-scale genome duplications. Mol. Biol. Evol. 29, 3541–3551 (2012).
pubmed: 22734049
doi: 10.1093/molbev/mss162
Panchy, N., Lehti-Shiu, M. & Shiu, S.-H. Evolution of gene duplication in plants1[OPEN]. Plant Physiol. 171, 2294–2316 (2016).
pubmed: 27288366
pmcid: 4972278
doi: 10.1104/pp.16.00523
Copley, S. D. Evolution of new enzymes by gene duplication and divergence. FEBS J. 287, 1262–1283 (2020).
pubmed: 32250558
doi: 10.1111/febs.15299
Kuzmin, E., Taylor, J. S. & Boone, C. Retention of duplicated genes in evolution. Trends Genet. 38, 59–72 (2022).
pubmed: 34294428
doi: 10.1016/j.tig.2021.06.016
Diss, G., Ascencio, D., DeLuna, A. & Landry, C. R. Molecular mechanisms of paralogous compensation and the robustness of cellular networks. J. Exp. Zool. B 322, 488–499 (2014).
doi: 10.1002/jez.b.22555
Kafri, R., Springer, M. & Pilpel, Y. Genetic redundancy: new tricks for old genes. Cell 136, 389–392 (2009).
pubmed: 19203571
doi: 10.1016/j.cell.2009.01.027
DeLuna, A., Springer, M., Kirschner, M. W. & Kishony, R. Need-based up-regulation of protein levels in response to deletion of their duplicate genes. PLoS Biol. 8, e1000347 (2010).
pubmed: 20361019
pmcid: 2846854
doi: 10.1371/journal.pbio.1000347
Somssich, M., Je, B. I., Simon, R. & Jackson, D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143, 3238–3248 (2016).
pubmed: 27624829
doi: 10.1242/dev.133645
Fletcher, J. C. The CLV-WUS stem cell signaling pathway: a roadmap to crop yield optimization. Plants 7, 87 (2018).
pmcid: 6313860
doi: 10.3390/plants7040087
Soyars, C. L., James, S. R. & Nimchuk, Z. L. Ready, aim, shoot: stem cell regulation of the shoot apical meristem. Curr. Opin. Plant Biol. 29, 163–168 (2016).
pubmed: 26803586
doi: 10.1016/j.pbi.2015.12.002
Rodriguez-Leal, D. et al. Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nat. Genet. 51, 786–792 (2019).
pubmed: 30988512
pmcid: 7274162
doi: 10.1038/s41588-019-0389-8
Jiao, W.-B. et al. The evolutionary dynamics of genetic incompatibilities introduced by duplicated genes in Arabidopsis thaliana. Mol. Biol. Evol. 38, 1225–1240 (2021).
pubmed: 33247726
doi: 10.1093/molbev/msaa306
Innan, H. & Kondrashov, F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97–108 (2010).
pubmed: 20051986
doi: 10.1038/nrg2689
Albalat, R. & Cañestro, C. Evolution by gene loss. Nat. Rev. Genet. 17, 379–391 (2016).
pubmed: 27087500
doi: 10.1038/nrg.2016.39
El-Brolosy, M. A. & Stainier, D. Y. R. Genetic compensation: a phenomenon in search of mechanisms. PLoS Genet. 13, e1006780 (2017).
pubmed: 28704371
pmcid: 5509088
doi: 10.1371/journal.pgen.1006780
Hanada, K. et al. Functional compensation of primary and secondary metabolites by duplicate genes in Arabidopsis thaliana. Mol. Biol. Evol. 28, 377–382 (2011).
pubmed: 20736450
doi: 10.1093/molbev/msq204
Kafri, R., Bar-Even, A. & Pilpel, Y. Transcription control reprogramming in genetic backup circuits. Nat. Genet. 37, 295–299 (2005).
pubmed: 15723064
doi: 10.1038/ng1523
DeLuna, A. et al. Exposing the fitness contribution of duplicated genes. Nat. Genet. 40, 676–681 (2008).
pubmed: 18408719
doi: 10.1038/ng.123
Freeling, M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60, 433–453 (2009).
pubmed: 19575588
doi: 10.1146/annurev.arplant.043008.092122
Vavouri, T., Semple, J. I. & Lehner, B. Widespread conservation of genetic redundancy during a billion years of eukaryotic evolution. Trends Genet. 24, 485–488 (2008).
pubmed: 18786741
doi: 10.1016/j.tig.2008.08.005
Goad, D. M., Zhu, C. & Kellogg, E. A. Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function. New Phytol. 216, 605–616 (2017).
pubmed: 27911469
doi: 10.1111/nph.14348
Fletcher, J. C. Recent advances in Arabidopsis CLE peptide signaling. Trends Plant Sci. 25, 1005–1016 (2020).
pubmed: 32402660
doi: 10.1016/j.tplants.2020.04.014
Hirakawa, Y. & Sawa, S. Diverse function of plant peptide hormones in local signaling and development. Curr. Opin. Plant Biol. 51, 81–87 (2019).
pubmed: 31132657
doi: 10.1016/j.pbi.2019.04.005
Whitewoods, C. D. et al. CLAVATA was a genetic novelty for the morphological innovation of 3D growth in land plants. Curr. Biol. 28, 2365–2376 (2018).
pubmed: 30033333
pmcid: 6089843
doi: 10.1016/j.cub.2018.05.068
Stuttmann, J. et al. Highly efficient multiplex editing: one-shot generation of 8× Nicotiana benthamiana and 12× Arabidopsis mutants. Plant J. 106, 8–22 (2021).
pubmed: 33577114
doi: 10.1111/tpj.15197
Fiers, M. et al. The CLAVATA3/ESR Motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol. 141, 1284–1292 (2006).
pubmed: 16751438
pmcid: 1533954
doi: 10.1104/pp.106.080671
Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294–294 (2008).
pubmed: 18202283
doi: 10.1126/science.1150083
Zhang, H., Lin, X., Han, Z., Qu, L.-J. & Chai, J. Crystal structure of PXY–TDIF complex reveals a conserved recognition mechanism among CLE peptide–receptor pairs. Cell Res. 26, 543–555 (2016).
pubmed: 27055373
pmcid: 4856767
doi: 10.1038/cr.2016.45
Li, Z., Chakraborty, S. & Xu, G. Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF–TDR interactions. PLoS ONE 12, e0175317 (2017).
pubmed: 28384649
pmcid: 5383425
doi: 10.1371/journal.pone.0175317
Lemmon, Z. H. et al. Rapid improvement of domestication traits in an orphan crop by genome editing. Nat. Plants 4, 766–770 (2018).
pubmed: 30287957
doi: 10.1038/s41477-018-0259-x
Thompson, A., Zakon, H. H. & Kirkpatrick, M. Compensatory drift and the evolutionary dynamics of dosage-sensitive duplicate genes. Genetics 202, 765–774 (2016).
pubmed: 26661114
doi: 10.1534/genetics.115.178137
Rodríguez-Leal, D., Lemmon, Z. H., Man, J., Bartlett, M. E. & Lippman, Z. B. Engineering quantitative trait variation for crop improvement by genome editing. Cell 171, 470–480 (2017).
pubmed: 28919077
doi: 10.1016/j.cell.2017.08.030
Wang, X. et al. Dissecting cis-regulatory control of quantitative trait variation in a plant stem cell circuit. Nat. Plants 7, 419–427 (2021).
pubmed: 33846596
doi: 10.1038/s41477-021-00898-x
Liu, L. et al. Enhancing grain-yield-related traits by CRISPR–Cas9 promoter editing of maize CLE genes. Nat. Plants 7, 287–294 (2021).
pubmed: 33619356
doi: 10.1038/s41477-021-00858-5
Alonge, M. et al. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell 182, 145–161 (2020).
pubmed: 32553272
pmcid: 7354227
doi: 10.1016/j.cell.2020.05.021
Xu, C. et al. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet. 47, 784–792 (2015).
pubmed: 26005869
doi: 10.1038/ng.3309
Samuels, J. Biodiversity of food species of the Solanaceae family: a preliminary taxonomic inventory of subfamily Solanoideae. Resources 4, 277–322 (2015).
doi: 10.3390/resources4020277
Leiboff, S. et al. Genetic control of morphometric diversity in the maize shoot apical meristem. Nat. Commun. 6, 8974 (2015).
pubmed: 26584889
doi: 10.1038/ncomms9974
Leiboff, S., DeAllie, C. K. & Scanlon, M. J. Modeling the morphometric evolution of the maize shoot apical meristem. Front. Plant Sci. 7, 1651 (2016).
pubmed: 27867389
pmcid: 5095129
doi: 10.3389/fpls.2016.01651
Schnablová, R., Herben, T. & Klimešová, J. Shoot apical meristem and plant body organization: a cross-species comparative study. Ann. Bot. 120, 833–843 (2017).
pubmed: 29136411
pmcid: 5737494
doi: 10.1093/aob/mcx116
Yang, Y. et al. Precise editing of CLAVATA genes in Brassica napus L. regulates multilocular silique development. Plant Biotechnol. J. 16, 1322–1335 (2018).
pubmed: 29250878
pmcid: 5999189
doi: 10.1111/pbi.12872
Khan, A. W. et al. Super-pangenome by integrating the wild side of a species for accelerated crop improvement. Trends Plant Sci. 25, 148–158 (2020).
pubmed: 31787539
pmcid: 6988109
doi: 10.1016/j.tplants.2019.10.012
Della Coletta, R., Qiu, Y., Ou, S., Hufford, M. B. & Hirsch, C. N. How the pan-genome is changing crop genomics and improvement. Genome Biol. 22, 3 (2021).
pubmed: 33397434
pmcid: 7780660
doi: 10.1186/s13059-020-02224-8
Bayer, P. E., Golicz, A. A., Scheben, A., Batley, J. & Edwards, D. Plant pan-genomes are the new reference. Nat. Plants 6, 914–920 (2020).
pubmed: 32690893
doi: 10.1038/s41477-020-0733-0
Sherman, R. M. & Salzberg, S. L. Pan-genomics in the human genome era. Nat. Rev. Genet. 21, 243–254 (2020).
pubmed: 32034321
pmcid: 7752153
doi: 10.1038/s41576-020-0210-7
Paaby, A. B. & Rockman, M. V. Cryptic genetic variation: evolution’s hidden substrate. Nat. Rev. Genet. 15, 247–258 (2014).
pubmed: 24614309
pmcid: 4737706
doi: 10.1038/nrg3688
Wagner, A. The molecular origins of evolutionary innovations. Trends Genet. 27, 397–410 (2011).
pubmed: 21872964
doi: 10.1016/j.tig.2011.06.002
Zheng, J., Payne, J. L. & Wagner, A. Cryptic genetic variation accelerates evolution by opening access to diverse adaptive peaks. Science 365, 347–353 (2019).
pubmed: 31346060
doi: 10.1126/science.aax1837
Kwon, C.-T. et al. Rapid customization of Solanaceae fruit crops for urban agriculture. Nat. Biotechnol. 38, 182–188 (2020).
pubmed: 31873217
doi: 10.1038/s41587-019-0361-2
Brooks, C., Nekrasov, V., Lippman, Z. B. & Van Eck, J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiol. 166, 1292–1297 (2014).
pubmed: 25225186
pmcid: 4226363
doi: 10.1104/pp.114.247577
Swartwood, K. & Van Eck, J. Development of plant regeneration and Agrobacterium tumefaciens-mediated transformation methodology for Physalis pruinosa. Plant Cell Tissue Organ Cult. 137, 465–472 (2019).
doi: 10.1007/s11240-019-01582-x
Van Eck, J., Keen, P. & Tjahjadi, M. in Transgenic Plants: Methods and Protocols (eds Kumar, S. et al.) 225–234 (Springer, 2019).
Zhang, B., Yang, X., Yang, C., Li, M. & Guo, Y. Exploiting the CRISPR/Cas9 System for targeted genome mutagenesis in petunia. Sci. Rep. 6, 20315 (2016).
pubmed: 26837606
pmcid: 4738242
doi: 10.1038/srep20315
Zhang, B. et al. CRISPR/Cas9-mediated targeted mutation reveals a role for AN4 rather than DPL in regulating venation formation in the corolla tube of Petunia hybrida. Hortic. Res. 8, 116 (2021).
Jiang, W. et al. Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic Acids Res. 41, e188 (2013).
pubmed: 23999092
pmcid: 3814374
doi: 10.1093/nar/gkt780
Gantner, J., Ordon, J., Kretschmer, C., Guerois, R. & Stuttmann, J. An EDS1–SAG101 complex is essential for TNL-mediated immunity in Nicotiana benthamiana. Plant Cell 31, 2456–2474 (2019).
pubmed: 31266900
pmcid: 6790086
doi: 10.1105/tpc.19.00099
Werner, S., Engler, C., Weber, E., Gruetzner, R. & Marillonnet, S. Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system. Bioeng. Bugs 3, 38–43 (2012).
pubmed: 22126803
van der Meer, I. M. in Plant Cell Culture Protocols (eds Loyola-Vargas, V. M. & Vázquez-Flota, F.) 265–272 (Humana Press, 2006).
Park, S. J., Jiang, K., Schatz, M. C. & Lippman, Z. B. Rate of meristem maturation determines inflorescence architecture in tomato. Proc. Natl Acad. Sci. USA 109, 639–644 (2012).
pubmed: 22203998
doi: 10.1073/pnas.1114963109
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
pubmed: 27043002
doi: 10.1038/nbt.3519
Pimentel, H., Bray, N. L., Puente, S., Melsted, P. & Pachter, L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 14, 687–690 (2017).
pubmed: 28581496
doi: 10.1038/nmeth.4324
Bombarely, A. et al. Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat. Plants 2, 16074 (2016).
Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).
pubmed: 25751142
pmcid: 4655817
doi: 10.1038/nmeth.3317
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).
pubmed: 25690850
pmcid: 4643835
doi: 10.1038/nbt.3122
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).
LoVerso, P. R. & Cui, F. A computational pipeline for cross-species analysis of RNA-seq data using R and bioconductor. Bioinforma. Biol. Insights 9, 165–174 (2015).
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Weber, E., Engler, C., Gruetzner, R., Werner, S. & Marillonnet, S. A modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6, e16765 (2011).
pubmed: 21364738
pmcid: 3041749
doi: 10.1371/journal.pone.0016765
Nakagawa, T. et al. Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095–2100 (2007).
pubmed: 17690442
doi: 10.1271/bbb.70216
Hendelman, A. et al. Conserved pleiotropy of an ancient plant homeobox gene uncovered by cis-regulatory dissection. Cell 184, 1724–1739 (2021).
pubmed: 33667348
doi: 10.1016/j.cell.2021.02.001
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010