Brassinosteroid signaling and BRI1 dynamics went underground

doi:10.1016/j.pbi.2016.06.014

Current Opinion in Plant Biology

Volume 33, October 2016, Pages 92-100

https://doi.org/10.1016/j.pbi.2016.06.014 Get rights and content

Highlights

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The root has become a model for studying BR signaling and BRI1 dynamics.
•
BRI1 relies on clathrin-dependent and -independent internalization processes.
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BRI1 ubiquitination and membrane lipids emerge as regulators of the BR complex.
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BRs and BR signaling factors control root vasculature development.
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Coherent root growth is balanced by opposite tissue-specific BR effects.

Brassinosteroids (BRs) are a group of steroid molecules perceived at the cell surface and that act as plant hormones. Since their discovery as crucial growth substances, BRs were mainly studied for their action in above ground organs and the BR signaling pathway was largely uncovered in the context of hypocotyl elongation. However, for the past two years, most of the exciting findings on BR signaling have been made using roots as a model. The Arabidopsis root is a system of choice for cell biology and allowed detailed characterization of BR perception at the cell membrane. In addition, a series of elegant articles dissected how BRs act in tissue specific manners to control root growth and development.

Graphical abstract

Introduction

Brassinosteroids (BRs) are perceived by combinatorial pairs of Receptor-Like Kinases (RLK) at the plasma membrane (PM). Binding of the ligand to the extracellular domain of BR-INSENSITIVE-1 (BRI1), BRI1-LIKE-1 (BRL1) and BRL3 triggers dimerization with BRI1-ASSOCIATED-KINASE-1 (BAK1) (or close family members from the SOMATIC-EMBRYOGENESIS-RECEPTOR-KINASE (SERK) family), which activates the trans-phosphorylation of their kinase domains. Activation of receptor complexes leads to a phosphorylation/de-phosphorylation cascade that inactivates GSK3 kinases from the BR-INSENSTIVE-2 (BIN2) family. This allows the accumulation of BRASSINAZOLE-RESISTANT-1 (BZR1) and BR-INSENSITIVE-EMS-SUPPRESSOR-1 (BES1) transcription factors in the nucleus where they bind to the promoter of thousands of genes and regulate their transcription (see recent reviews for more details on the molecular mechanism of BR signaling [1, 2]). Although much progress has been made over the past two decades on the canonical BR signaling pathway, several key questions in the BR field have started to be addressed only recently. These include how BRs are dynamically perceived by their receptor complexes at the cell surface, and how specific developmental or environmental contexts trigger different genomic responses to control growth and development. Interestingly, most of the recent advances in the BR field arose from work performed using roots. Indeed, the root has become the go-to model to study subcellular signaling mechanisms and here we highlight some recent findings made with this model, notably on the regulation of the BR receptor complex. We also review the emerging roles of BR signaling in root development, focusing on its effects on (1) tissue differentiation and (2) the control of the root meristem size.

Section snippets

Building of a BR receptor complex at the cell surface

After intensive endoplasmic reticulum (ER)-mediated quality control of BRI1 folding and degradation of misfolded BRI1 by the ER-associated degradation machinery [3, 4], BRI1 finds its way through the Golgi and the trans-Golgi Network/early endosome (TGN/EE) before cycling between the cell surface and brefeldin A (BFA)-sensitive endosomes (Figure 1) [5, 6]. Efficient exocytosis and endosomal recycling of BRI1 to the cell surface was recently shown to require the vacuolar ATPase subunit

Root development and the emergence of new paradigms in BR signaling

BRs control the final length of the root in complex manners that are sometimes antagonistic (Figure 3) [2]. BRs impact root growth by modulating the elongation of differentiated cells [33], but also by modulating meristem size [34, 35]. Indeed, BRs can either promote cell-cycle progression or cell differentiation, which have opposite effects on meristem size and final root length [34, 35]. In addition, BRs also promote cell division in the Quiescent Center (QC) and the differentiation of distal

Conclusions and perspectives

Recent advances made on BRI1 activation and deactivation mechanisms in roots greatly complexify our view on the dynamics of BR perception. The knowledge gained on EGFR must certainly serve as a blueprint for dissecting the interplay between BRI1 dynamics and signaling, but differences are very likely to arise. The development of high-resolution imaging is slowly emerging in plants and will certainly provide invaluable insights into the spatial and temporal control of BRI1 internalization by CME

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest
•• of outstanding interest

Acknowledgements

We thank Youssef Belkhadir, Matthieu Platre, Laia Armengot, and Sara Martins for critical comments on the manuscript. We apologize to researchers whose work could not be cited here due to space limitations. YJ is funded by grants from European Research Council (3363360-APPL) and Marie Curie Action (PCIG-GA-2011-303601); GV by grants from Marie Curie Action (PCIG-GA-2012-334021) and Agence Nationale de la Recherche (ANR-13-JSV2-0004-01).

References (53)

Y. Luo et al.
V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis
Nature Plants
(2015)
A. Gadeyne et al.
The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants
Cell
(2014)
L.K. Goh et al.
Multiple mechanisms collectively regulate clathrin-mediated endocytosis of the epidermal growth factor receptor
J Cell Biol
(2010)
M.A. Lemmon
Membrane recognition by phospholipid-binding domains
Nat Rev Mol Cell Biol
(2008)
M.L. Simon et al.
A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants
Nat Plants
(2016)
Y. Cheng et al.
Brassinosteroids control root epidermal cell fate via direct regulation of a MYB-bHLH-WD40 complex by GSK3-like kinases
Elife
(2014)
A. Cano-Delgado et al.
BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis
Development
(2004)
Y. Jaillais et al.
Unraveling the paradoxes of plant hormone signaling integration
Nat Struct Mol Biol
(2010)
Y. Belkhadir et al.
The molecular circuitry of brassinosteroid signaling
New Phytol
(2015)
A.P. Singh et al.
Growth control: brassinosteroid activity gets context
J Exp Bot
(2015)

Y. Liu et al.

Endoplasmic reticulum-mediated protein quality control in Arabidopsis

Front Plant Sci

(2014)

Y. Liu et al.

EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

Proc Natl Acad Sci U S A

(2015)

N. Geldner et al.

Endosomal signaling of plant steroid receptor kinase BRI1

Genes Dev

(2007)

E. Russinova et al.

Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1)

Plant Cell

(2004)

S. Di Rubbo et al.

The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis

Plant Cell

(2013)

X. Gou et al.

Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling

PLoS Genet

(2012)

M. Hothorn et al.

Structural basis of steroid hormone perception by the receptor kinase BRI1

Nature

(2011)

N.G. Irani et al.

Fluorescent castasterone reveals BRI1 signaling from the plasma membrane

Nat Chem Biol

(2012)

Y. Jaillais et al.

Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation

Proc Natl Acad Sci U S A

(2011)

J. Santiago et al.

Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases

Science

(2013)

C.A. Bucherl et al.

Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling

Plant Physiol

(2013)

Y. Jaillais et al.

Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor

Genes Dev

(2011)

X. Wang et al.

Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane

Science

(2006)

L. Wang et al.

Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells

Mol Plant

(2015)

S. Martins et al.

Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination

Nat Commun

(2015)

S. Sigismund et al.

Clathrin-independent endocytosis of ubiquitinated cargos

Proc Natl Acad Sci U S A

(2005)

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A germinating seedling incorporates environmental signals such as light into developmental outputs. Light is not only a source of energy, but also a central coordinative signal in plants. Traditionally, most research focuses on aboveground organs’ response to light; therefore, our understanding of photomorphogenesis in roots is relatively scarce. However, root development underground is highly responsive to light signals from the shoot and understanding these signaling mechanisms will give a better insight into early seedling development. Here, we review the central light signaling hubs and their role in root growth promotion of Arabidopsis thaliana seedlings.
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To maintain optimal growth and survival, plants balance complex developmental processes while simultaneously sensing and responding to both endogenous physiological factors and changes in their surroundings. Phytohormones are an important class of compounds, which regulate various aspects of plant development and responses to adverse environmental conditions. With the signaling pathways well worked out for most of the hormones, it is evident that these signaling pathways interact in a complex network to coordinate such processes. Besides the five established classical groups of phytohormones, brassinosteroids (BRs) have emerged as prominent phytohormones in recent times. BRs are not only strong modulators of cellular division, cellular elongation, and cellular differentiation across plant tissues but also they make a significant contribution in improving adaptation to various stresses. This chapter summarizes mechanisms regulating production, homeostasis, signaling of BR and their interconnections with different plant hormones to control plant growth and adaptation.
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We show the importance of cellular Ca2+ gradient for the BR-induced modulation of antioxidant enzymes activity. As soon as BR-perceiving receptor complex is localized in plasma membrane, its conformation and further availability for endocytosis after activation is under influence of the phospholipid composition around [20]. Phospholipid composition is a subject of fast change by phospholipases and lipid kinases activity.
Brassinosteroids (BRs) are steroid hormones regulating various aspects of plant metabolism, including growth, development and stress responses. However, little is known about the mechanism of their impact on antioxidant systems and phospholipid turnover. Using tobacco plants overexpressing H⁺/Ca²⁺vacuolar Arabidopsis antiporter CAX1, we showed the role of Ca²⁺ ion balance in the reactive oxygen species production and rapid phosphatidic acid accumulation induced by exogenous BR. Combination of our experimental results with public transcriptomic and proteomic data revealed a particular role of Ca²⁺-dependent phospholipid metabolizing enzymes in BR signaling. Here we provide novel insights into the role of calcium balance and lipid-derived second messengers in plant responses to exogenous BRs and propose a complex model integrating BR-mediated metabolic changes with phospholipid turnover.
Auxin-Regulated Reversible Inhibition of TMK1 Signaling by MAKR2 Modulates the Dynamics of Root Gravitropism
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Plants are able to orient their growth according to gravity, which ultimately controls both shoot and root architecture.¹ Gravitropism is a dynamic process whereby gravistimulation induces the asymmetric distribution of the plant hormone auxin, leading to asymmetric growth, organ bending, and subsequent reset of auxin distribution back to the original pre-gravistimulation situation.1, 2, 3 Differential auxin accumulation during the gravitropic response depends on the activity of polarly localized PIN-FORMED (PIN) auxin-efflux carriers.1, 2, 3, 4 In particular, the timing of this dynamic response is regulated by PIN2,⁵^,⁶ but the underlying molecular mechanisms are poorly understood. Here, we show that MEMBRANE ASSOCIATED KINASE REGULATOR2 (MAKR2) controls the pace of the root gravitropic response. We found that MAKR2 is required for the PIN2 asymmetry during gravitropism by acting as a negative regulator of the cell-surface signaling mediated by the receptor-like kinase TRANSMEMBRANE KINASE1 (TMK1).²^,7, 8, 9, 10 Furthermore, we show that the MAKR2 inhibitory effect on TMK1 signaling is antagonized by auxin itself, which triggers rapid MAKR2 membrane dissociation in a TMK1-dependent manner. Our findings suggest that the timing of the root gravitropic response is orchestrated by the reversible inhibition of the TMK1 signaling pathway at the cell surface.
Metabolic Cellular Communications: Feedback Mechanisms between Membrane Lipid Homeostasis and Plant Development
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Citation Excerpt :
This tyrosine phosphorylation triggers the rapid dissociation of BKI1 from the plasma membrane and allows further downstream BRI1 signaling. A likely mechanistic explanation for this membrane release is that the phosphorylation, which is negatively charged, creates a local electrostatic clash with the highly anionic plasma membrane, thereby releasing BKI1 into the cytosol (Jaillais and Vert, 2016). In favor of this hypothesis, a BKI1 mutant in which the tyrosine residue within the membrane hook is substituted for a negatively charged aspartic acid, is unable to bind to the plasma membrane (Jaillais et al., 2011).
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Plant growth relies on interconnected hormonal pathways, their corresponding transcriptional networks and mechanical signals. This work reviews recent brassinosteroid (BR) studies and integrates them with current growth models derived from research in roots. The relevance of spatiotemporal BR signaling in the longitudinal and radial root axes and its multifaceted interaction with auxin, the impact of BR on final cell size determination and its interplay with microtubules and the cell wall are discussed. Also highlighted are emerging variations of canonical BR signaling that could function in developmental-specific context.

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View full text

Brassinosteroid signaling and BRI1 dynamics went underground

Highlights

Graphical abstract

Introduction

Section snippets

Building of a BR receptor complex at the cell surface

Root development and the emergence of new paradigms in BR signaling

Conclusions and perspectives

References and recommended reading

Acknowledgements

Nature Plants

Cell

J Cell Biol

Nat Rev Mol Cell Biol

Nat Plants

Elife

Development

Nat Struct Mol Biol

The molecular circuitry of brassinosteroid signaling

New Phytol

Growth control: brassinosteroid activity gets context

J Exp Bot

Endoplasmic reticulum-mediated protein quality control in Arabidopsis

Front Plant Sci

EBS7 is a plant-specific component of a highly conserved endoplasmic reticulum-associated degradation system in Arabidopsis

Proc Natl Acad Sci U S A

Endosomal signaling of plant steroid receptor kinase BRI1

Genes Dev

Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1)

Plant Cell

The clathrin adaptor complex AP-2 mediates endocytosis of brassinosteroid insensitive1 in Arabidopsis

Plant Cell

Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling

PLoS Genet

Structural basis of steroid hormone perception by the receptor kinase BRI1

Nature

Fluorescent castasterone reveals BRI1 signaling from the plasma membrane

Nat Chem Biol

Extracellular leucine-rich repeats as a platform for receptor/coreceptor complex formation

Proc Natl Acad Sci U S A

Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases

Science

Visualization of BRI1 and BAK1(SERK3) membrane receptor heterooligomers during brassinosteroid signaling

Plant Physiol

Tyrosine phosphorylation controls brassinosteroid receptor activation by triggering membrane release of its kinase inhibitor

Genes Dev

Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane

Science

Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells

Mol Plant

Internalization and vacuolar targeting of the brassinosteroid hormone receptor BRI1 are regulated by ubiquitination

Nat Commun

Clathrin-independent endocytosis of ubiquitinated cargos

Proc Natl Acad Sci U S A