Brassinosteroid coordinates cell layer interactions in plants via cell wall and tissue mechanics

Kelly-Bellow, Robert; Lee, Karen; Kennaway, Richard; Barclay, Elaine; Whibley, Annabel; Bushell, Claire; Spooner, Jamie; Yu, Min; Brett, Paul J.; Kular, Baldeep; Cheng, Shujing; Chu, Jinfang; Xu, Tao; Lane, Brendan; Fitzsimons, J. T.; Xue, Yongbiao; Smith, Richard S.; Whitewoods, Christopher D.; Coen, Enrico

doi:10.1126/science.adf0752

Cited by 22 publications

(9 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This finding suggests the existence of a directed stress arising from the inner cells that is transmitted to the epidermal cells. It has been observed previously in A. thaliana hypocotyls that the inner layers have highly aligned microtubules ( 43 , 48 ) and exert a stress on the outer layers ( 15 , 49 , 50 ).…”

Section: Characterization Of Growth and Cell Division In M Polymorpha...mentioning

confidence: 93%

Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

Bonfanti,

Smithers,

Bourdon

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Plant morphogenesis is governed by the mechanics of the cell wall—a stiff and thin polymeric box that encloses the cells. The cell wall is a highly dynamic composite material. New cell walls are added during cell division. As the cells continue to grow, the properties of cell walls are modulated to undergo significant changes in shape and size without breakage. Spatial and temporal variations in cell wall mechanical properties have been observed. However, how they relate to cell division remains an outstanding question. Here, we combine time-lapse imaging with local mechanical measurements via atomic force microscopy to systematically map the cell wall’s age and growth, with their stiffness. We make use of two systems, Marchantia polymorpha gemmae, and Arabidopsis thaliana leaves. We first characterize the growth and cell division of M. polymorpha gemmae. We then demonstrate that cell division in M. polymorpha gemmae results in the generation of a temporary stiffer and slower-growing new wall. In contrast, this transient phenomenon is absent in A. thaliana leaves. We provide evidence that this different temporal behavior has a direct impact on the local cell geometry via changes in the junction angle. These results are expected to pave the way for developing more realistic plant morphogenetic models and to advance the study into the impact of cell division on tissue growth.

show abstract

Section: Characterization Of Growth and Cell Division In M Polymorpha...mentioning

confidence: 93%

Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

Bonfanti,

Smithers,

Bourdon

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…For example, during the formation of chick intestinal villi, epithelium buckling creates small pockets underneath the villi tips, concentrating the morphogen, Shh (Shyer et al, 2015). Similarly, tissue geometry significantly influences plant growth and patterning by determining how mechanical stresses are distributed within the tissue (Green, 1999;Dumais & Kwiatkowska, 2002;Iida et al, 2023;Kelly-Bellow et al, 2023). At the level of individual cells, considering cell wall geometry helps us understand the influence of turgor pressure on cell wall stresses (Geitmann & Ortega, 2009).…”

Section: The Interplay Between Biochemistry Mechanics and Geometry Fo...mentioning

confidence: 99%

Multiple feedbacks on self‐organized morphogenesis during plant regeneration

Mathew,

Ganguly,

Prasad

2023

New Phytologist

View full text Add to dashboard Cite

SummaryDecades of research have primarily emphasized genetic blueprint as the driving force behind plant regeneration. The flow of information from genetics, which manifests as biochemical properties, including hormones, has been extensively implicated in plant regeneration. However, recent advancements have unveiled additional intrinsic modules within this information flow. Here, we explore the three core modules of plant regeneration: biochemical properties, mechanical forces acting on cells, and cell geometry. We debate their roles and interactions during morphogenesis, emphasizing the potential for multiple feedbacks between these core modules to drive pattern formation during regeneration. We propose that de novo organ regeneration is a self‐organized event driven by multidirectional information flow between these core modules.

show abstract

“…It is becoming clear that BR signaling functions at the crossroad between CWS and growth (Wolf 2022). Indeed, alteration of pectin methylation status triggers BR signaling (Wolf et al 2012, 2014), BR signaling modulates the expression of a multitude of cell wall-associated transcripts (Sun et al 2010; Yu et al 2011), as well as the activity of wall modifying enzymes (Qu et al 2011; Xie et al 2011; Sánchez-Rodríguez et al 2017), and the inhibition of BR signaling in a mutant affecting pectin modification leads to life-threatening defects in tissue and cellular integrity (Kelly-Bellow et al 2023). Despite the apparent vital importance of the interplay between the cell wall and BR signaling, little is known in regard to the underpinning molecular actors.…”

Section: Introductionmentioning

confidence: 99%

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

Biermann,

von Arx,

Xhelilaj

et al. 2024

Preprint

View full text Add to dashboard Cite

Plant cells survey and modulate their cell wall to control their shape and anisotropic growth. Signaling mediated by the plant steroid hormones brassinosteroids (BR) plays a central role in coordinating cell wall status and cell growth, and alterations in the cell wall BR feedback loop leads to life-threatening defects in tissue and cellular integrity. How the status of the cell wall is relayed to BR signaling remains largely unclear. Increasing evidence shows that RAPID ALKALANIZATION FACTORs (RALFs), a class of secreted peptides, play structural and signaling roles at the cell surface. Here we show that perception of RALF23 promotes the formation and signaling of the main BR receptor complex formed by BRASSINOSTEROID INSENSITIVE 1 (BRI1) and BRI1 BRASSINOSTEROID INSENSITIVE1 BRASSINOSTEROID ASSOCIATED KINASE 1 (BAK1). The loss of the plasma membrane localized RALF receptor complex FERONIA (FER) LORELEI LIKE GPI anchor protein 1 (LLG1) leads to defects in cell expansion and anisotropy, as well as uncontrolled BRI1 BAK1 complex formation and signaling. RALF23 bioactivity relies on pectin status and its perception induces changes in pectin composition and the activity of pectin-modifying enzymes. Our observations suggest a model in which RALF23 functions as a cell wall informed signaling cue initiating a feedback loop that solicits BR signaling, modifies the cell wall, and coordinates cell morphogenesis.

show abstract

Brassinosteroid coordinates cell layer interactions in plants via cell wall and tissue mechanics

Cited by 22 publications

References 51 publications

Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

Stiffness transitions in new walls post-cell division differ between Marchantia polymorpha gemmae and Arabidopsis thaliana leaves

Multiple feedbacks on self‐organized morphogenesis during plant regeneration

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

Contact Info

Product

Resources

About