Growth models from a brassinosteroid perspective
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).
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2023, Hormonal Cross-Talk, Plant Defense and Development: Plant Biology, Sustainability and Climate ChangeCytokinin promotes growth cessation in the Arabidopsis root
2022, Current BiologyCitation 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, iScienceCitation 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 ScienceCitation 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 ScienceCitation 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.