A conserved superlocus regulates above- and belowground root initiation

AbstractDuring plant post-embryonic growth new meristems and associated stem cells form in different development contexts in order to respond to environmental cues. While underground lateral roots initiate from designated cells in the main root, an unknown mechanism allows cells to bypass the root/shoot identity trajectory and generate shoot-borne-roots. Using single-cell profiling of tomato (Solanum lycoperiscum) stems we isolated a rare transient cell population that serve as progenitors for shoot-borne-root meristems. Analysis of this population identified a transcription factor required for the formation of shoot-borne-roots which we named SHOOT BORNE ROOTLESS (SBRL). Evolutionary analysis revealed that SBRL function is deeply conserved in angiosperms and that it arose as part of an ancient duplicated superlocus, only lost in root-less plants, containing both shoot-borne and lateral root initiation regulators. We propose that the ability to activate a common transition state with context-specific regulators allows the remarkable developmental plasticity found in plants.One Sentence SummaryHighly conserved superlocus of LBD genes, acting within an early transition identity, regulates shoot-borne and lateral root formation.

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Systemic signalling through translationally controlled tumour protein controls lateral root formation in Arabidopsis

Journal of Experimental Botany ◽

10.1093/jxb/erz204 ◽

2019 ◽

Vol 70 (15) ◽

pp. 3927-3940 ◽

Cited By ~ 9

Author(s):

Rémi Branco ◽

Josette Masle

Keyword(s):

Lateral Root ◽

Root Elongation ◽

Developmental Plasticity ◽

Lateral Roots ◽

Primary Root ◽

Dual Function ◽

Growth Promoter ◽

Root Initiation ◽

Long Distance ◽

Lateral Root Initiation

Abstract The plant body plan and primary organs are established during embryogenesis. However, in contrast to animals, plants have the ability to generate new organs throughout their whole life. These give them an extraordinary developmental plasticity to modulate their size and architecture according to environmental constraints and opportunities. How this plasticity is regulated at the whole-organism level is elusive. Here we provide evidence for a role for translationally controlled tumour protein (TCTP) in regulating the iterative formation of lateral roots in Arabidopsis. AtTCTP1 modulates root system architecture through a dual function: as a general constitutive growth promoter enhancing root elongation and as a systemic signalling agent via mobility in the vasculature. AtTCTP1 encodes mRNAs with long-distance mobility between the shoot and roots. Mobile shoot-derived TCTP1 gene products act specifically to enhance the frequency of lateral root initiation and emergence sites along the primary root pericycle, while root elongation is controlled by local constitutive TCTP1 expression and scion size. These findings uncover a novel type for an integrative signal in the control of lateral root initiation and the compromise for roots between branching more profusely or elongating further. They also provide the first evidence in plants of an extracellular function of the vital, highly expressed ubiquitous TCTP1.

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Formation of lateral root meristems is a two-stage process

Development ◽

10.1242/dev.121.10.3303 ◽

1995 ◽

Vol 121 (10) ◽

pp. 3303-3310 ◽

Cited By ~ 8

Author(s):

M.J. Laskowski ◽

M.E. Williams ◽

H.C. Nusbaum ◽

I.M. Sussex

Keyword(s):

Lateral Root ◽

Lateral Roots ◽

Initial Period ◽

Subsequent Stage ◽

Root Initiation ◽

Root Meristems ◽

Lateral Root Initiation ◽

Cell Layers ◽

Stage Process ◽

Pericycle Cells

In both radish and Arabidopsis, lateral root initiation involves a series of rapid divisions in pericycle cells located on the xylem radius of the root. In Arabidopsis, the number of pericycle cells that divide to form a primordium was estimated to be about 11. To determine the stage at which primordia are able to function as root meristems, primordia of different stages were excised and cultured without added hormones. Under these conditions, primordia that consist of 2 cell layers fail to develop while primordia that consist of at least 3–5 cell layers develop as lateral roots. We hypothesize that meristem formation is a two-step process involving an initial period during which a population of rapidly dividing, approximately isodiametric cells that constitutes the primordium is formed, and a subsequent stage during which meristem organization takes place within the primordium.

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AT-HOOK MOTIF NUCLEAR LOCALISED PROTEIN 18 as a Novel Modulator of Root System Architecture

10.20944/preprints202003.0046.v1 ◽

2020 ◽

Author(s):

Marek Šírl ◽

Tereza Šnajdrová ◽

Dolores Gutiérrez-Alanís ◽

Joseph G. Dubrovsky ◽

Jean Phillipe Vielle-Calzada ◽

...

Keyword(s):

Root System ◽

System Architecture ◽

Lateral Root ◽

Apical Meristem ◽

Lateral Roots ◽

Primary Root ◽

Root System Architecture ◽

Root Apical Meristem ◽

Root Initiation ◽

Lateral Root Initiation

The AT-HOOK MOTIF NUCLEAR LOCALIZED PROTEIN (AHL) gene family encodes embryophyte-specific nuclear proteins with DNA binding activity. They modulate gene expression and affect various developmental processes in plants. We identify AHL18 (At3G60870) as a developmental modulator of root system architecture and growth. AHL18 regulates the length of the proliferation domain and number of dividing cells in the root apical meristem and thereby, cell production. Both primary root growth and lateral root development respond according to AHL18 transcription level. The ahl18 knock-out plants show reduced root systems due to a shorter primary root and a lower number of lateral roots. This change results from a higher number of arrested and non-developing lateral root primordia (LRP) rather than from decreased initiation. Overexpression of AHL18 results in a more extensive root system, longer primary roots, and increased density of lateral root initiation events. Formation of lateral roots is affected during the initiation of LRP and later development. AHL18 regulate root apical meristem activity, lateral root initiation and emergence, which is in accord with localization of its expression.

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Lateral root initiation in Marsilea quadrifolia. I. Origin and histogenesis of lateral roots

Canadian Journal of Botany ◽

10.1139/b91-018 ◽

1991 ◽

Vol 69 (1) ◽

pp. 123-135 ◽

Cited By ~ 14

Author(s):

Bai-Ling Lin ◽

V. Raghavan

Keyword(s):

Lateral Root ◽

Single Cells ◽

Lateral Roots ◽

Central Axis ◽

Root Initiation ◽

Vascular Connection ◽

Lateral Root Initiation ◽

Marsilea Quadrifolia ◽

Lateral Root Primordium ◽

Root Primordium

In Marsilea quadrifolia, lateral roots arise from modified single cells of the endodermis located opposite the protoxylem poles within the meristematic region of the parent root. The initial cell divides in four specific planes to establish a fivecelled lateral root primordium, with a tetrahedral apical cell in the centre and the oldest merophytes and the root cap along the sides. The cells of the merophyte divide in a precise pattern to give rise to the cells of the cortex, endodermis, pericycle, and vascular tissues of the emerging lateral root. Although the construction of the parent root is more complicated than that of lateral roots, patterns of cell division and tissue formation are similar in both types of roots, with the various tissues being arranged in similar positions in relation to the central axis. Vascular connection between the lateral root primordium and the parent root is derived from the pericycle cells lying between the former and the protoxylem members of the latter. It is proposed that the central axis of the root is not only a geometric centre, but also a physiological centre which determines the fate of the different cell types. Key words: lateral root initiation, Marsilea quadrifolia, root histogenesis.

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A single cell view of the transcriptome during lateral root initiation in Arabidopsis thaliana

10.1101/2020.10.02.324327 ◽

2020 ◽

Author(s):

Hardik P. Gala ◽

Amy Lanctot ◽

Ken Jean-Baptiste ◽

Sarah Guiziou ◽

Jonah C. Chu ◽

...

Keyword(s):

Single Cell ◽

Root Development ◽

Lateral Root ◽

Lateral Roots ◽

Primary Root ◽

Root Initiation ◽

Lateral Root Primordia ◽

Lateral Root Development ◽

Lateral Root Initiation ◽

Molecular Events

AbstractRoot architecture is a major determinant of fitness, and is under constant modification in response to favorable and unfavorable environmental stimuli. Beyond impacts on the primary root, the environment can alter the position, spacing, density and length of secondary or lateral roots. Lateral root development is among the best-studied examples of plant organogenesis, yet there are still many unanswered questions about its earliest steps. Among the challenges faced in capturing these first molecular events is the fact that this process occurs in a small number of cells with unpredictable timing. Single-cell sequencing methods afford the opportunity to isolate the specific transcriptional changes occurring in cells undergoing this fate transition. Using this approach, we successfully captured the transcriptomes of initiating lateral root primordia, and discovered many previously unreported upregulated genes associated with this process. We developed a method to selectively repress target gene transcription in the xylem pole pericycle cells where lateral roots originate, and demonstrated that expression of several of these targets was required for normal root development. We also discovered novel subpopulations of cells in the pericycle and endodermal cell files that respond to lateral root initiation, highlighting the coordination across cell files required for this fate transition.One sentence summarySingle cell RNA sequencing reveals new molecular details about lateral root initiation, including the transcriptional impacts of the primordia on bordering cells.

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Application of Phytohormones to Pea Roots After Removal of the Apex: Effect on Lateral Root Production

Functional Plant Biology ◽

10.1071/pp9790195 ◽

1979 ◽

Vol 6 (2) ◽

pp. 195 ◽

Cited By ~ 9

Author(s):

PB Goodwin ◽

SC Morris

Keyword(s):

Lateral Root ◽

Lateral Roots ◽

Primary Root ◽

Root Production ◽

Root Tip ◽

Naphthaleneacetic Acid ◽

Root Initiation ◽

Lateral Root Initiation ◽

Lateral Bud ◽

Bud Growth

Removal of 2 mm of the primary root tip of Pisum sativum caused a complete halt to primary root elongation, but did not alter the total number of laterals formed. The auxins indole-3-acetic acid and 1-naphthaleneacetic acid, when applied to the stump in a lanolin emulsion, increased the number of lateral roots. High levels of abscisic acid and low levels of the cytokinins N6-benzylaminopurine and N6-(γ, γ-dimethylallylamino)purine, and of the gibberellins GA3 and GA7, resulted in decreased lateral root production. Kinetin was without effect. There appears to be an inverse relationship between auxins and cytokinins in root/shoot growth coordination. Auxins, which are produced in the shoot tip, inhibit lateral bud growth but promote lateral root initiation. Cytokinins, which are produced in the root tip, inhibit lateral root initiation, but promote lateral stem growth.

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At-Hook Motif Nuclear Localised Protein 18 as a Novel Modulator of Root System Architecture

International Journal of Molecular Sciences ◽

10.3390/ijms21051886 ◽

2020 ◽

Vol 21 (5) ◽

pp. 1886 ◽

Cited By ~ 3

Author(s):

Marek Širl ◽

Tereza Šnajdrová ◽

Dolores Gutiérrez-Alanís ◽

Joseph G. Dubrovsky ◽

Jean Phillipe Vielle-Calzada ◽

...

Keyword(s):

Root System ◽

System Architecture ◽

Lateral Root ◽

Apical Meristem ◽

Lateral Roots ◽

Primary Root ◽

Root System Architecture ◽

Root Apical Meristem ◽

Root Initiation ◽

Lateral Root Initiation

The At-Hook Motif Nuclear Localized Protein (AHL) gene family encodes embryophyte-specific nuclear proteins with DNA binding activity. They modulate gene expression and affect various developmental processes in plants. We identify AHL18 (At3G60870) as a developmental modulator of root system architecture and growth. AHL18 is involved in regulation of the length of the proliferation domain and number of dividing cells in the root apical meristem and thereby, cell production. Both primary root growth and lateral root development respond according to AHL18 transcription level. The ahl18 knock-out plants show reduced root systems due to a shorter primary root and a lower number of lateral roots. This change results from a higher number of arrested and non-developing lateral root primordia (LRP) rather than from a decreased LRP initiation. The over-expression of AHL18 results in a more extensive root system, longer primary roots, and increased density of lateral root initiation events. AHL18 is thus involved in the formation of lateral roots at both LRP initiation and their later development. We conclude that AHL18 participates in modulation of root system architecture through regulation of root apical meristem activity, lateral root initiation and emergence; these correspond well with expression pattern of AHL18.

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EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1820882116 ◽

2019 ◽

Vol 116 (17) ◽

pp. 8597-8602 ◽

Cited By ~ 22

Author(s):

Priya Ramakrishna ◽

Paola Ruiz Duarte ◽

Graham A. Rance ◽

Martin Schubert ◽

Vera Vordermaier ◽

...

Keyword(s):

Lateral Root ◽

Asymmetric Cell Division ◽

Lateral Roots ◽

Root Initiation ◽

Asymmetric Cell Divisions ◽

Cell Divisions ◽

Lateral Root Initiation ◽

Root Organogenesis ◽

A Cell ◽

Pericycle Cells

In plants, postembryonic formation of new organs helps shape the adult organism. This requires the tight regulation of when and where a new organ is formed and a coordination of the underlying cell divisions. To build a root system, new lateral roots are continuously developing, and this process requires the tight coordination of asymmetric cell division in adjacent pericycle cells. We identified EXPANSIN A1 (EXPA1) as a cell wall modifying enzyme controlling the divisions marking lateral root initiation. Loss ofEXPA1leads to defects in the first asymmetric pericycle cell divisions and the radial swelling of the pericycle during auxin-driven lateral root formation. We conclude that a localized radial expansion of adjacent pericycle cells is required to position the asymmetric cell divisions and generate a core of small daughter cells, which is a prerequisite for lateral root organogenesis.

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Root growth in corn and soybeans: effects of cadmium and lead on lateral root initiation

Canadian Journal of Botany ◽

10.1139/b78-034 ◽

1978 ◽

Vol 56 (3) ◽

pp. 277-281 ◽

Cited By ~ 19

Author(s):

Carl P. Malone ◽

Raymond J. Miller ◽

D. E. Koeppe

Keyword(s):

Root Growth ◽

Lateral Root ◽

Lateral Roots ◽

Toxic Effects ◽

Root Initiation ◽

Inhibitory Effects ◽

Lateral Root Initiation ◽

Primary Roots ◽

Cadmium And Lead

This study examines the previously reported inhibitory effects of Cd on root growth. In hydroponic experiments, 100 μg Cd/ℓ effected a 33% inhibition of lateral root initiation of corn. The growth of corn and soybean primary roots was not reduced at Cd concentrations of 1 mg/ℓ, and the number of lateral root initials in soybeans was not reduced at 2 mg Cd/ℓ. The toxic effects of Cd were ameliorated by additions of Zn or by additions of Fe citrate to nutrient growth solutions. While both Zn and Fe additions did result in increased lateral root initiation, the number of initials was significantly lower than the controls. Lead had no effect on the initiation of soybean lateral roots at a concentration of 100 μg Pb/ℓ. However, 5 mg Pb/ℓ did effect a 21% decrease in corn lateral root initials, but this decrease could not be demonstrated with higher Pb concentrations.

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Indolebutyric acid and ectomycorrhizal inoculation increase lateral root initiation and development of container-grown black oak seedlings

Canadian Journal of Forest Research ◽

10.1139/x87-007 ◽

1987 ◽

Vol 17 (1) ◽

pp. 36-39 ◽

Cited By ~ 9

Author(s):

C. M. Baser ◽

H. E. Garrett ◽

R. J. Mitchell ◽

G. S. Cox ◽

C. J. Starbuck

Keyword(s):

Growth Medium ◽

Growth And Development ◽

Lateral Root ◽

Acid Treatment ◽

Lateral Roots ◽

Root Initiation ◽

Indolebutyric Acid ◽

Lateral Root Initiation ◽

Black Oak ◽

Oak Seedlings

Containerized black oak seedlings in which the growth medium was inoculated with Pisolithustinctorius (Pers.) Coker Couch or left uninoculated were grown for 16 weeks with or without a polyacrylic starch containing 1000 μg indolebutyric acid per gram mixed throughout the growth medium. Seedlings treated with indolebutyric acid developed more than twice as many lateral roots as control seedlings which did not receive indolebutyric acid. Indolebutyric acid reduced the percentage of primary laterals colonized by P. tinctorius; however, the total number of colonized lateral roots was not affected. The combination of ectomycorrhizal inoculation with the indolebutyric acid treatment significantly increased the growth and development of black oak seedlings.

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