Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation

Toyokura, Koichi; Goh, Tatsuaki; Shinohara, Hidefumi; Shinoda, Akinori; Kondo, Yuki; Okamoto, Yoshie; Uehara, Tsuyoshi; Fujimoto, Koichi; Okushima, Yoko; Ikeyama, Yoshifumi; Nakajima, Keiji; Mimura, Tetsuro; Tasaka, Masao; Matsubayashi, Yoshikatsu; Fukaki, Hidehiro

doi:10.1016/j.devcel.2018.11.031

Cited by 74 publications

(105 citation statements)

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“…a,b). It was reported that the puchi mutation increases LR primordium density, but retards LR emergence (Hirota et al ., ; Kang et al ., ; Toyokura et al ., ), thereby the density of emerged LRs in puchi mutant was comparable to that of WT in 7‐d‐old seedlings without auxin treatment (control; Fig. c).…”

Section: Resultsmentioning

confidence: 74%

“…Among the candidate genes are several known LR regulators, including GATA23 (De Rybel et al ., ), MEMBRANE‐ASSOCIATED KINASE REGULATOR 4 ( MAKR4 ) (Jaillais et al ., ; Xuan et al ., ), PUCHI (Hirota et al ., ) and TOLS2/PIPL3 (Toyokura et al ., ; Table ). GATA23 encodes a transcription factor whose spatial expression pattern demarks LR founder cells and positively regulates the specification of LR founder cells (De Rybel et al ., ).…”

Section: Resultsmentioning

confidence: 95%

“…qPCR analysis confirmed that the expression of the candidate genes was activated in both LBD16‐GR lines upon DEX treatment in the presence of translation inhibitor CHX (Figs d,f,h,j, S1). Consistent with these results, the putative LBD16 targets were also upregulated by DEX treatment alone in the LBD16‐GR overexpression line ( 35Spro:LBD16‐GR arf7 arf19 ; Figs e,i, S1) (Toyokura et al ., ). In the gLBD16‐GR line, PUCHI showed over two‐fold upregulation by DEX treatment alone, but other genes were not significantly upregulated (Figs c,g, S1).…”

Section: Resultsmentioning

confidence: 97%

“…LBD16 expression is dependent on the SLR/IAA14‐ARF7‐ARF19 auxin signaling cascade (Fukaki et al ., ; Okushima et al ., ; Goh et al ., ). qPCR analysis confirmed that all potential LBD16 targets were activated in WT roots by 4 h auxin treatment (Figs a,b, S3; Toyokura et al ., ). By contrast, the auxin‐inducible expression of the identified LBD16 targets was lost in the arf7 arf19 and slr‐1 mutants (Figs a,b, S3).…”

Section: Resultsmentioning

confidence: 97%

“…Arabidopsis thaliana accession Columbia (Col) was used as the wild‐type (WT) plant in this study. The lbd16‐1 (SALK_095791), lbd18‐1 (SALK_038125), lbd33‐1 (SAIL_95_H10), LBD16‐GFP ( genomeLBD16‐GFP ), LBD16pro:NLS:GFP , LBD16‐SRDX ( genomeLBD16‐SRDX ), arf7‐2 arf19‐5 , arf7‐1 arf19‐1 (Goh et al ., ), 35Spro:LBD16‐GR arf7‐2 arf19‐5 (Toyokura et al ., ), ARF7pro:ARF7‐GR nph4‐1 arf19‐1 (Okushima et al ., ; Lavenus et al ., ), puchi‐1 , GFP‐PUCHI ( PUCHIpro:GFP‐PUCHI ), PUCHIpro:GUS (Hirota et al ., ), PUCHIpro:NLS‐VENUSx3 (Toyokura et al ., ), GATA23pro:NLS‐GUS‐GFP (De Rybel et al ., ), and DR5:GUS (Ulmasov et al ., ) lines have been described previously. Seeds were germinated under sterile conditions on 1× Murashige & Skoog (MS) medium containing 1.0% sucrose solidified with 0.5% gellan gum as described by Goh et al .…”

Section: Methodsmentioning

confidence: 99%

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Lateral root initiation requires the sequential induction of transcription factors LBD16 and PUCHI in Arabidopsis thaliana

et al. 2019

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Summary Lateral root (LR) formation in Arabidopsis thaliana is initiated by asymmetric division of founder cells, followed by coordinated cell proliferation and differentiation for patterning new primordia. The sequential developmental processes of LR formation are triggered by a localized auxin response. LATERAL ORGAN BOUNDARIES‐DOMAIN 16 (LBD16), an auxin‐inducible transcription factor, is one of the key regulators linking auxin response in LR founder cells to LR initiation. We identified key genes for LR formation that are activated by LBD16 in an auxin‐dependent manner. LBD16 targets identified include the transcription factor gene PUCHI, which is required for LR primordium patterning. We demonstrate that LBD16 activity is required for the auxin‐inducible expression of PUCHI. We show that PUCHI expression is initiated after the first round of asymmetric cell division of LR founder cells and that premature induction of PUCHI during the preinitiation phase disrupts LR primordium formation. Our results indicate that LR initiation requires the sequential induction of transcription factors LBD16 and PUCHI.

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Section: Resultsmentioning

confidence: 74%

Section: Resultsmentioning

confidence: 95%

Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

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Lateral root initiation requires the sequential induction of transcription factors LBD16 and PUCHI in Arabidopsis thaliana

et al. 2019

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Pericycle

Dubrovsky

Rost

2023

Encyclopedia of Life Sciences

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Pericycle is a primary tissue of plant roots with meristematic properties and is the site for the initiation of lateral roots and two secondary meristems, the vascular cambium and phellogen (cork cambium). Pericycle pluripotent cell properties are also revealed during cultivation of root explants in shoot regeneration media. In this article, the characteristics of the pericycle related to each of its functions are reviewed. During lateral root development, five important and coordinated events take place in the pericycle: founder cell identity acquisition, cell division competence, asymmetric cell division, new organ growth axis establishment and lateral inhibition. Cellular and molecular bases of these processes as well as transcriptomic insights in pericycle cell identity are discussed. Cell cycle and related genetic control in pericycle development are also addressed. Cellular and molecular bases of participation of pericycle in the formation of lateral meristems, vascular cambium and phellogen (cork cambium), differences among eudicots and monocots in pericycle development, as well as participation of pericycle in loading of mineral nutrients and unloading of organic compounds are also reviewed. Key Concepts The pericycle is a primary tissue with pluripotent properties that participates in lateral root (LR) formation. In eudicots, it also gives rise to two lateral meristems: vascular cambium and cork cambium (phellogen). Pericycle is typical of plant roots and is the most external cell layer (or layers) of the vascular cylinder. In other plant organs, pericycle or pericycle‐like cell layers can also be present depending on taxon. Outside the root apical meristem, in the root differentiation zone of eudicots, the xylem pole pericycle (XPP) maintains its proliferation activity. Due to its proliferation activity, pericycle possesses high regenerative properties involved in regeneration of shoots from roots. The XPP and phloem pole pericycle (PPP) are characterised by distinct transcriptomic profiles related to their adjacent vascular tissues. Pericycle cells committed for LR development in monocots and eudicots retain the common features related to cell cycle, active auxin synthesis, transport and signalling, and responsiveness to nitrates. LR formation starts from pericycle founder cell specification which is auxin dependent and implies drastic developmental changes in genetic programs involved in asymmetric cell division, new organ growth axis establishment and lateral inhibition. The first founder cell specification is followed by the recruitment of neighbouring pericycle cells that leads to the formation of a morphogenetic field of founder cells giving rise to a LR. The transition from primary to secondary growth starts in the pericycle and procambium and leads to the formation of vascular cambium and phellogen which are coordinated processes dependent on auxin and cytokinin. Pericycle maintains high metabolic activity and participates in loading phloem and xylem and in unloading phloem and thus is involved in shoot‐to‐root and root‐to‐shoot long‐distance transport.

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Design Principles of Branching Morphogenesis in Filamentous Organisms

2019

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The radiation of life on Earth was accompanied by the diversification of multicellular body plans in the eukaryotic kingdoms Animalia, Plantae, Fungi and Chromista. Branching forms are ubiquitous in nature and evolved repeatedly in the above lineages. The developmental and genetic basis of branch formation is well studied in the three-dimensional shoot and root systems of land plants, and in animal organs such as the lung, kidney, mammary gland, vasculature, etc. Notably, recent thought-provoking studies combining experimental analysis and computational modeling of branching patterns in whole animal organs have identified global patterning rules and proposed unifying principles of branching morphogenesis. Filamentous branching forms represent one of the simplest expressions of the multicellular body plan and constitute a key step in the evolution of morphological complexity. Similarities between simple and complex branching forms distantly related in evolution are compelling, raising the question whether shared mechanisms underlie their development. Here, we focus on filamentous branching organisms that represent major study models from three distinct eukaryotic kingdoms, including the moss Physcomitrella patens (Plantae), the brown alga Ectocarpus sp. (Chromista), and the ascomycetes Neurospora crassa and Aspergillus nidulans (Fungi), and bring to light developmental regulatory mechanisms and design principles common to these lineages. Throughout the review we explore how the regulatory mechanisms of branching morphogenesis identified in other models, and in particular animal organs, may inform our thinking on filamentous systems and thereby advance our understanding of the diverse strategies deployed across the eukaryotic tree of life to evolve similar forms. Gross morphology of single clones (A-C) and dissected branching filaments (D-F) in the moss Physcomitrella patens (A,D), the brown alga Ectocarpus sp. (B,E), and the filamentous fungus Aspergillus nidulans (C,F). Fungal hyphae were fixed and stained with Hoechst 33258 and Calcofluor to visualize nuclei and septa, respectively.

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Lateral Inhibition by a Peptide Hormone-Receptor Cascade during Arabidopsis Lateral Root Founder Cell Formation

Cited by 74 publications

References 63 publications

Lateral root initiation requires the sequential induction of transcription factors LBD16 and PUCHI in Arabidopsis thaliana

Lateral root initiation requires the sequential induction of transcription factors LBD16 and PUCHI in Arabidopsis thaliana

Pericycle

Design Principles of Branching Morphogenesis in Filamentous Organisms

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