Elsevier

Current Opinion in Plant Biology

Volume 53, February 2020, Pages 90-97
Current Opinion in Plant Biology

Growth models from a brassinosteroid perspective

https://doi.org/10.1016/j.pbi.2019.10.008Get rights and content

Highlights

  • Core BR signaling components involve BR ligand-dependent and ligand-independent regulation.

  • Spatiotemporal BR activity controls both longitudinal and radial root growth.

  • BR and auxin occurrence is both similar and opposing.

  • Microtubule organization and cell wall composition are modulated by BR.

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.

Introduction

Organ growth is a result of a directional expansion and division of its constituent cells; communication between distinct cell types and tissues is an inherent coordinator of these processes. Accumulating evidence has demonstrated distinct effects of brassinosteroid (BR) on these growth parameters, depending on hormone level and on how the hormone is decoded in distinct root zones, tissues and cell-types. Thus, the study of BR signaling has gained momentum in the past decade, particularly in developmental studies using the Arabidopsis root [1,2,3••] (Box 1).

Here, we highlight recent advances related to understanding of the distribution of BR activity, demonstrating tissue-specific interpretation of its occurrence that impacts root zonation in the longitudinal axis, as well as the radial growth of the meristem. We discuss the multifaceted interaction of BR with the auxin gradient to dictate root zonation, where BR and auxin have opposing but also similar distribution (or response) patterns in the root tip, depending on the tissue type. In addition, works demonstrating the promoting effect of BR on cellular growth and differentiation are reviewed. These include regulation of microtubule organization and cell wall composition, which also feedback on the pathway, and a conceptual mechanism underlying termination of cell elongation. This review begins by highlighting recent discoveries of variations on the well establish canonical BR signaling scheme that could dictate physiologically and developmentally specific outputs.

Section snippets

The BR signaling pathway and emerging twists

The well-established core BR signaling pathway initiates when the steroid hormone directly binds to the extracellular domain of the main LRR receptor kinase (RK) BRASSINOSTEROID INSENSITIVE 1 (BRI1) and to its LRR-RK co-receptor BRI1-ASSOCIATED RECEPTOR KINASE (BAK1). The hormone similarly binds BRI1′s homologues BRI1-LIKE 1 and 3 (BRL1 and BRL3). A series of downstream interactions involving several regulatory proteins, lead to the inhibition and degradation of GSK3-like kinase BRASSINOSTEROID

The spatiotemporal relevance of BR during root growth

Knowledge regarding the extent and directionality of BR distribution within the organ remains fragmented [27••,28,29,30]. It is also unclear if available tools could determine the levels of the hormones in a tissue-specific manner. Reporters directly informing about BR perception at the plasma membrane (i.e. input) and transcriptional reporters (i.e. output) are lacking. However, relative spatiotemporal changes in the nuclear accumulation of BES1/BZR1 serve as a proxy for BR levels and

Final cell size determination and BR

How final cell size is determined is a fundamental question in developmental biology. Various mathematical models of the root system have been applied to describe mechanisms underlying the onset and duration of cell division and cell elongation (e.g. [45,47,55,56]). More recently, three models evaluated the possibility of measurement of distance from a reference point (positional cue), time spent elongating (‘timer’ model) and size (‘sizer’ model) as a means of controlling cell elongation

The bottom line: BR control of microtubules and the cell wall

Cell expansion relies on the extensibility properties of its surrounding primary wall. The primary cell wall is composed of cellulose microfibrils embedded in a hydrated matrix of hemicellulose and pectins. It remains unclear how the primary cell wall structure is linked to directionality (anisotropy) of cell expansion [58]. However, it was demonstrated in hypocotyls that modulation of its cell wall constituents impacts cell size and shape [59, 60, 61]. In agreement with the crucial role of BR

Conclusions and perspectives

This review highlighted BR-regulated growth processes in roots. These involve distinct tissue-specific BR responses and effects on the longitudinal and radial axes, contributing to coherent growth. Both positive and negative interactions with auxin, dictated by their relative levels and the tissues where they coincide, likely integrate to form multilayered feedback circuits. BR controls cell wall genes via a gene regulatory network but also has non-genomic influences on the organization of

Conflict of interest statement

Nothing declared.

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 Dr. Amar Pal Singh and members of the Savaldi-Goldstein lab for comments on the manuscript. This research is supported by the Israel Science Foundation (grant No. 1725/18).

References (84)

  • K. Caesar et al.

    A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana

    Plant J

    (2011)
  • A.P. Singh et al.

    Growth control: brassinosteroid activity gets context

    J Exp Bot

    (2015)
  • A. Planas-Riverola et al.

    Brassinosteroid signaling in plant development and adaptation to stress

    Development

    (2019)
  • L. Dolan et al.

    Cellular organisation of the Arabidopsis thaliana root

    Development

    (1993)
  • T. Denyer et al.

    Spatiotemporal developmental trajectories in the Arabidopsis root revealed using high-throughput single-cell RNA sequencing

    Dev Cell

    (2019)
  • T.Q. Zhang et al.

    A single-cell RNA sequencing profiles the developmental landscape of Arabidopsis root

    Mol Plant

    (2019)
  • K.H. Ryu et al.

    Single-cell RNA sequencing resolves molecular relationships among individual plant cells

    Plant Physiol

    (2019)
  • C.N. Shulse et al.

    High-throughput single-cell transcriptome profiling of plant cell types

    Cell Rep

    (2019)
  • V.V. Lavrekha et al.

    3D analysis of mitosis distribution highlights the longitudinal zonation and diarch symmetry in proliferation activity of the Arabidopsis thaliana root meristem

    Plant J

    (2017)
  • B. De Rybel et al.

    Plant vascular development: from early specification to differentiation

    Nat Rev Mol Cell Biol

    (2016)
  • S. Miyashima et al.

    Mobile PEAR transcription factors integrate positional cues to prime cambial growth

    Nature

    (2019)
  • Y. Belkhadir et al.

    The molecular circuitry of brassinosteroid signaling

    New Phytol

    (2015)
  • Y.C. Tian et al.

    Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor

    Nat Commun

    (2018)
  • Y. Yin et al.

    A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis

    Cell

    (2005)
  • Y. Yin et al.

    BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation

    Cell

    (2002)
  • W.Y. Chen et al.

    BES1 is activated by EMS1-TPD1-SERK1/2-mediated signaling to control tapetum development in Arabidopsis thaliana

    Nat Commun

    (2019)
  • E. Holzwart et al.

    BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling

    Proc Natl Acad Sci U S A

    (2018)
  • E. Smakowska-Luzan et al.

    An extracellular network of Arabidopsis leucine-rich repeat receptor kinases

    Nature

    (2018)
  • V. Amorim-Silva et al.

    TTL proteins scaffold brassinosteroid signaling components at the plasma membrane to optimize signal transduction in Arabidopsis

    Plant Cell

    (2019)
  • H. Ren et al.

    BRASSINOSTEROID-SIGNALING KINASE 3, a plasma membrane-associated scaffold protein involved in early brassinosteroid signaling

    PLoS Genet

    (2019)
  • J.S. Gui et al.

    OsREM4.1 interacts with OsSERK1 to coordinate the interlinking between abscisic acid and brassinosteroid signaling in rice

    Dev Cell

    (2016)
  • A. Houbaert et al.

    POLAR-guided signalling complex assembly and localization drive asymmetric cell division

    Nature

    (2018)
  • N. Vukasinovic et al.

    BRexit: possible brassinosteroid export and transport routes

    Trends Plant Sci

    (2018)
  • G.M. Symons et al.

    Brassinosteroids do not undergo long-distance transport in pea. Implications for the regulation of endogenous brassinosteroid levels

    Plant Physiol

    (2004)
  • G.M. Symons et al.

    Brassinosteroid transport

    J Exp Bot

    (2008)
  • S. Savaldi-Goldstein et al.

    The epidermis both drives and restricts plant shoot growth

    Nature

    (2007)
  • J. Chaiwanon et al.

    Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots

    Curr Biol

    (2015)
  • K. Vragovic et al.

    Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation

    Proc Natl Acad Sci U S A

    (2015)
  • M.P. Gonzalez-Garcia et al.

    Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots

    Development

    (2011)
  • H.S. Lee et al.

    Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation

    J Exp Bot

    (2015)
  • J. Vilarrasa-Blasi et al.

    Regulation of plant stem cell quiescence by a brassinosteroid signaling module

    Dev Cell

    (2014)
  • J. Heyman et al.

    ERF115 controls root quiescent center cell division and stem cell replenishment

    Science

    (2013)
  • Cited by (27)

    • Brassinosteroids: perspective of biosynthesis, crosstalk, and role in plant development

      2023, Hormonal Cross-Talk, Plant Defense and Development: Plant Biology, Sustainability and Climate Change
    • Cytokinin promotes growth cessation in the Arabidopsis root

      2022, Current Biology
      Citation Excerpt :

      This idea is consistent with our observations that cytokinin broadly affects root growth (Figures 2 and 5). Future work will need to determine the specific tissue layers that are required for cytokinin-mediated growth control.65–68 However, because layers must grow in synchrony during development to avoid tissue tearing, determining the primacy of external versus internal layers as “growth controllers” will be non-trivial to address.

    • Brassinosteroids Regulate Circadian Oscillation via the BES1/TPL-CCA1/LHY Module in Arabidopsisthaliana

      2020, iScience
      Citation Excerpt :

      Dephosphorylated BES1 and BZR1 then enter the nucleus, where they regulate the expression of BR-responsive genes by binding directly to their promoters (He et al., 2005; Yin et al., 2005; Sun et al., 2010). BRs regulate a variety of developmental and physiological processes in plants including cell division, photomorphogenesis, reproductive organ development, stomata development, leaf senescence, and biotic and abiotic stress responses (Wang et al., 2012; Gruszka, 2013; Zhiponova et al., 2013; Wang et al., 2001; Planas-Riverola et al., 2019; Yu et al., 2018; Ackerman-Lavert and Savaldi-Goldstein, 2020). Consistently, the molecular crosstalk between the BR signaling pathway and other hormonal and developmental signaling pathways is starting to emerge.

    • Emerging Connections between Small RNAs and Phytohormones

      2020, Trends in Plant Science
      Citation Excerpt :

      In turn, sRNAs are able to directly regulate GA biosynthesis and signaling via miR156-SPL, miR171-SCL, and miR159-GAMYB(L)s modules, respectively. BRs are steroid hormones mainly involved in plant growth, vascular differentiation, and stomatal development [35]. In arabidopsis, miRNAs from 48 known families and 23 unknown miRNAs are differentially expressed upon BR treatment [36] (Table 1).

    • Review: Emerging roles of brassinosteroid in nutrient foraging

      2020, Plant Science
      Citation Excerpt :

      Recently, the role of scaffold proteins, TETRATRICOPEPTIDE THIOREDOXIN-LIKE (TTL) in mediating the specific interaction of BR pathway components revealed another complexity in the pathway that could potentially regulate specific developmental process [35]. Genetic and molecular approaches have also revealed the BR receptor-dependent and independent regulation of BZR1 and BES1/BZR2 transcription factors, thus distinguishing the receptor-independent function of these transcription factors in regulating the various processes [36,37]. Similar to the independent activity of BZR1/BES1, the receptor complex can activate the downstream events independent of the known downstream components.

    View all citing articles on Scopus
    View full text