Robust organ size requires robust timing of initiation orchestrated by focused auxin and cytokinin signalling.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
17
10
2019
accepted:
15
04
2020
pubmed:
27
5
2020
medline:
4
3
2021
entrez:
27
5
2020
Statut:
ppublish
Résumé
Organ size and shape are precisely regulated to ensure proper function. The four sepals in each Arabidopsis thaliana flower must maintain the same size throughout their growth to continuously enclose and protect the developing bud. Here we show that DEVELOPMENT RELATED MYB-LIKE 1 (DRMY1) is required for both timing of organ initiation and proper growth, leading to robust sepal size in Arabidopsis. Within each drmy1 flower, the initiation of some sepals is variably delayed. Late-initiating sepals in drmy1 mutants remain smaller throughout development, resulting in variability in sepal size. DRMY1 focuses the spatiotemporal signalling patterns of the plant hormones auxin and cytokinin, which jointly control the timing of sepal initiation. Our findings demonstrate that timing of organ initiation, together with growth and maturation, contribute to robust organ size.
Identifiants
pubmed: 32451448
doi: 10.1038/s41477-020-0666-7
pii: 10.1038/s41477-020-0666-7
pmc: PMC7299778
mid: NIHMS1585329
doi:
Substances chimiques
AT1G58220 protein, Arabidopsis
0
Arabidopsis Proteins
0
Cytokinins
0
DNA-Binding Proteins
0
Indoleacetic Acids
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
686-698Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM134037
Pays : United States
Organisme : NIH HHS
ID : S10 OD010693
Pays : United States
Références
Williams, R. W. Mapping genes that modulate mouse brain development: a quantitative genetic approach. Mouse Brain Dev. 30, 21–49 (2000).
Mizukami, Y. A matter of size: developmental control of organ size in plants. Curr. Opin. Plant Biol. 4, 533–539 (2001).
pubmed: 11641070
Gomez, M., Gomez, V. & Hergovich, A. The Hippo pathway in disease and therapy: cancer and beyond. Clin. Transl. Med. 3, 22 (2014).
pubmed: 25097725
pmcid: 4107774
Zygulska, A. L., Krzemieniecki, K. & Pierzchalski, P. Hippo pathway – brief overview of its relevance in cancer. J. Physiol. Pharmacol. 68, 311–335 (2017).
pubmed: 28820389
Nicodème Fassinou Hotegni, V., Lommen, W. J. M., Agbossou, E. K. & Struik, P. C. Heterogeneity in pineapple fruit quality results from plant heterogeneity at flower induction. Front. Plant Sci. 5, 670 (2014).
pubmed: 25538714
pmcid: 4260489
Félix, M. A. & Wagner, A. Robustness and evolution: concepts, insights and challenges from a developmental model system. Heredity 100, 132–140 (2008).
pubmed: 17167519
Waddington, C. H. Canalization of development and the inheritance of acquired characters. Nature 150, 563–565 (1942).
Vogel, G. How do organs know when they have reached the right size? Science 340, 1156–1157 (2013).
pubmed: 23744919
Garelli, A., Gontijo, A. M., Miguela, V., Caparros, E. & Dominguez, M. Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 336, 579–582 (2012).
pubmed: 22556250
Colombani, J., Andersen, D. S. & Léopol, P. Secreted peptide dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336, 582–585 (2012).
pubmed: 22556251
Roeder, A. H. Sepals in Encyclopedia of Life Sciences (John Wiley & Sons, 2010).
Wolpert, L. Arms and the man: the problem of symmetric growth. PLoS Biol. 8, e1000477 (2010).
pubmed: 20838659
pmcid: 2935459
Katsanos, D. et al. Stochastic loss and gain of symmetric divisions in the C. elegans epidermis perturbs robustness of stem cell number. PLoS Biol. 15, e2002429 (2017).
pubmed: 29108019
pmcid: 5690688
Hong, L. et al. Variable cell growth yields reproducible organ development through spatiotemporal averaging. Dev. Cell 38, 15–32 (2016).
pubmed: 27404356
Wu, P. et al. DRMY1, a Myb-Like protein, regulates cell expansion and seed production in Arabidopsis thaliana. Plant Cell Physiol. 60, 285–302 (2019).
pubmed: 30351427
Dubos, C. et al. MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573–581 (2010).
pubmed: 20674465
Peaucelle, A. et al. Arabidopsis phyllotaxis Is controlled by the methyl-esterification status of cell wall pectins. Curr. Biol. 18, 1943–1948 (2008).
pubmed: 19097903
Peaucelle, A. et al. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr. Biol. 21, 1720–1726 (2011).
pubmed: 21982593
Arsuffi, G. & Braybrook, S. A. Acid growth: an ongoing trip. J. Exp. Bot. 69, 137–146 (2018).
pubmed: 29211894
Heisler, M. G. et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15, 1899–1911 (2005).
pubmed: 16271866
Jönsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M. & Mjolsness, E. An auxin-driven polarized transport model for phyllotaxis. Proc. Natl Acad. Sci. USA 103, 1633–1638 (2006).
pubmed: 16415160
Smith, R. S. et al. A plausible model of phyllotaxis. Proc. Natl Acad. Sci. USA 103, 1301–1306 (2006).
pubmed: 16432192
Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003).
pubmed: 14628043
Chandler, J. W., Jacobs, B., Cole, M., Comelli, P. & Werr, W. DORNRÖSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima. Plant Mol. Biol. 76, 171–185 (2011).
pubmed: 21547450
Cheng, Y., Dai, X. & Zhao, Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 20, 1790–1799 (2006).
pubmed: 16818609
pmcid: 1522075
Billou, I. et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44 (2005).
Goh, T., Kasahara, H., Mimura, T., Kamiya, Y. & Fukaki, H. Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos. Trans. R. Soc. B 367, 1461–1468 (2012).
Besnard, F. et al. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505, 417–421 (2014).
pubmed: 24336201
Besnard, F., Rozier, F. & Vernoux, T. The AHP6 cytokinin signaling inhibitor mediates an auxin–cytokinin crosstalk that regulates the timing of organ initiation at the shoot apical meristem. Plant Signal. Behav. 9, e28788 (2014).
pubmed: 24732036
pmcid: 4091322
Müller, B. & Sheen, J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094–1097 (2008).
pubmed: 18463635
pmcid: 2601652
Gordon, S. P., Chickarmane, V. S., Ohno, C. & Meyerowitz, E. M. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc. Natl Acad. Sci. USA 106, 16529–16534 (2009).
pubmed: 19717465
Bartrina, I., Otto, E., Strnad, M., Werner, T. & Schmülling, T. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23, 69–80 (2011).
pubmed: 21224426
pmcid: 3051259
Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005).
Weijers, D., Nemhauser, J. & Yang, Z. Auxin: small molecule, big impact. J. Exp. Bot. 69, 133–136 (2018).
pubmed: 29309681
pmcid: 5853209
Wybouw, B. & De Rybel, B. Cytokinin – a developing story. Trends Plant Sci. 24, 177–185 (2019).
pubmed: 30446307
Kwiatkowska, D. Flower primordium formation at the Arabidopsis shoot apex: quantitative analysis of surface geometry and growth. J. Exp. Bot. 57, 571–580 (2006).
pubmed: 16377735
Kwiatkowska, D. Flowering and apical meristem growth dynamics. J. Exp. Bot. 59, 187–201 (2008).
pubmed: 18256052
Bhatia, N. et al. Auxin acts through MONOPTEROS to regulate plant cell polarity and pattern phyllotaxis. Curr. Biol. 26, 3202–3208 (2016).
pubmed: 27818174
pmcid: 5154752
Braybrook, S. A. & Peaucelle, A. Mechano-chemical aspects of organ formation in Arabidopsis thaliana: The relationship between auxin and pectin. PLoS ONE 8, e57813 (2013).
pubmed: 23554870
pmcid: 3595255
Spartz, A. K. et al. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H
pubmed: 24858935
pmcid: 4079373
Ebisuya, M. & Briscoe, J. What does time mean in development? Development 145, dev164368 (2018).
pubmed: 29945985
pmcid: 6031406
Mara, A. & Holley, S. A. Oscillators and the emergence of tissue organization during zebrafish somitogenesis. Trends Cell Biol. 17, 593–599 (2007).
pubmed: 17988868
Lukowitz, W., Gillmor, C. S. & Scheible, W. R. Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol. 123, 795–805 (2000).
pubmed: 10889228
pmcid: 1539260
Neff, M. M., Turk, E. & Kalishman, M. Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18, 613–615 (2002).
pubmed: 12446140
Smyth, D. R., Bowman, J. L. & Meyerowitz, E. M. Early flower development in Arabidopsis. Plant Cell 2, 755–767 (1990).
pubmed: 2152125
pmcid: 159928
Hamant, O., Das, P. & Burian, A. Time-lapse imaging of developing shoot meristems using a confocal laser scanning microscope. Methods Mol. Biol. 1992, 257–268 (2019).
Roeder, A. H. K. et al. Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol. 8, e1000367 (2010).
pubmed: 20485493
pmcid: 2867943
Robinson, D. O. et al. Ploidy and size at multiple scales in the Arabidopsis sepal. Plant Cell 30, 2308–2329 (2018).
pubmed: 30143539
pmcid: 6241276
Müller, B. & Sheen, J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453, 1094–1097 (2008).
pubmed: 18463635
pmcid: 2601652
Barbier de Reuille, P. et al. MorphoGraphX: a platform for quantifying morphogenesis in 4D. eLife 4, e05864 (2015).
pmcid: 4421794