Increased gene expression variability hinders the formation of regional mechanical conflicts leading to reduced organ shape robustness

• Verfasst von: Trinh, Duy Chi [VerfasserIn]
• Verfasst von: Martin, Marjolaine [VerfasserIn]
• Verfasst von: Bald, Lotte [VerfasserIn]
• Verfasst von: Maizel, Alexis [VerfasserIn]
• Verfasst von: Trehin, Christophe [VerfasserIn]
• Verfasst von: Hamant, Olivier [VerfasserIn]
• Titel: Increased gene expression variability hinders the formation of regional mechanical conflicts leading to reduced organ shape robustness
• Verf.angabe: Duy-Chi Trinh, Marjolaine Martin, Lotte Bald, Alexis Maizel, Christophe Trehin, and Olivier Hamant
• E-Jahr: 2023
• Jahr: July 17, 2023
• Umfang: 12 S.
• Fussnoten: Gesehen am 06.02.2024
• Titel Quelle: Enthalten in: National Academy of Sciences (Washington, DC)Proceedings of the National Academy of Sciences of the United States of America
• Ort Quelle: Washington, DC : National Acad. of Sciences, 1915
• Jahr Quelle: 2023
• Band/Heft Quelle: 120(2023), 30, Artikel-ID e2302441120, Seite 1-12
• ISSN Quelle: 1091-6490
• DOI: doi:10.1073/pnas.2302441120
• Datenträger: Online-Ressource
• Sprache: eng
• K10plus-PPN: 1880074389

Abstract

To relate gene networks and organ shape, one needs to address two wicked problems: i) Gene expression is often variable locally, and shape is reproducible globally; ii) gene expression can have cascading effects on tissue mechanics, with possibly counterintuitive consequences for the final organ shape. Here, we address such wicked problems, taking advantage of simpler plant organ development where shape only emerges from cell division and elongation. We confirm that mutation in VERNALIZATION INDEPENDENCE 3 (VIP3), a subunit of the conserved polymerase-associated factor 1 complex (Paf1C), increases gene expression variability in Arabidopsis. Then, we focused on the Arabidopsis sepal, which exhibits a reproducible shape and stereotypical regional growth patterns. In vip3 sepals, we measured higher growth heterogeneity between adjacent cells. This even culminated in the presence of negatively growing cells in specific growth conditions. Interestingly, such increased local noise interfered with the stereotypical regional pattern of growth. We previously showed that regional differential growth at the wild-type sepal tip triggers a mechanical conflict, to which cells resist by reinforcing their walls, leading to growth arrest. In vip3, the disturbed regional growth pattern delayed organ growth arrest and increased final organ shape variability. Altogether, we propose that gene expression variability is managed by Paf1C to ensure organ robustness by building up mechanical conflicts at the regional scale, instead of the local scale.