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

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.

Download Full-text

The expa1-1 mutant reveals a new biophysical lateral root organogenesis checkpoint

10.1101/249961 ◽

2018 ◽

Cited By ~ 2

Author(s):

Priya Ramakrishna ◽

Graham A Rance ◽

Lam Dai Vu ◽

Evan Murphy ◽

Kamal Swarup ◽

...

Keyword(s):

Cell Division ◽

Root System ◽

Lateral Root ◽

Root Formation ◽

Lateral Roots ◽

Lateral Root Formation ◽

Asymmetric Cell Divisions ◽

Cell Divisions ◽

Root Organogenesis ◽

Pericycle Cells

ABSTRACTIn plants, post-embryonic 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 asymmetric cell division in adjacent pericycle cells. Characterization of an expansin a1 (expa1) mutant has revealed a novel checkpoint during lateral root formation. Specifically, a minimal pericycle width was found to be necessary and sufficient to trigger asymmetric pericycle cell divisions 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.SIGNFICANCE STATEMENTOrgan formation is an essential process in plants and animals, driven by cell division and cell identity establishment. Root branching, where lateral roots form along the primary root axis, increases the root system and aids capture of water and nutrients. We have discovered that tight control of cell width is necessary to co-ordinate asymmetric cell divisions in cells that give rise to a new lateral root organ. While biomechanical processes have been shown to play a role in plant organogenesis, including lateral root formation, our data give new mechanistic insights into the cell size checkpoint during lateral root initiation.

Download Full-text

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.

Download Full-text

Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0239 ◽

2012 ◽

Vol 367 (1595) ◽

pp. 1525-1533 ◽

Cited By ~ 39

Author(s):

Leentje Jansen ◽

Ianto Roberts ◽

Riet De Rycke ◽

Tom Beeckman

Keyword(s):

Lateral Root ◽

Vascular Tissue ◽

Lateral Roots ◽

Root Tip ◽

Root Initiation ◽

Auxin Response ◽

Lateral Root Initiation ◽

Evolutionarily Conserved ◽

Chemical Inhibition ◽

Pericycle Cells

In Arabidopsis thaliana , lateral-root-forming competence of pericycle cells is associated with their position at the xylem poles and depends on the establishment of protoxylem-localized auxin response maxima. In maize, our histological analyses revealed an interruption of the pericycle at the xylem poles, and confirmed the earlier reported proto-phloem-specific lateral root initiation. Phloem-pole pericycle cells were larger and had thinner cell walls compared with the other pericycle cells, highlighting the heterogeneous character of the maize root pericycle. A maize DR5::RFP marker line demonstrated the presence of auxin response maxima in differentiating xylem cells at the root tip and in cells surrounding the proto-phloem vessels. Chemical inhibition of auxin transport indicated that the establishment of the phloem-localized auxin response maxima is crucial for lateral root formation in maize, because in their absence, random divisions of pericycle and endodermis cells occurred, not resulting in organogenesis. These data hint at an evolutionarily conserved mechanism, in which the establishment of vascular auxin response maxima is required to trigger cells in the flanking outer tissue layer for lateral root initiation. It further indicates that lateral root initiation is not dependent on cellular specification or differentiation of the type of vascular tissue.

Download Full-text

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.

Download Full-text

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.

Download Full-text

Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species:Raphanus sativus, Helianthus annuus, Zea mays, andDaucus carota

PROTOPLASMA ◽

10.1007/bf01276795 ◽

1995 ◽

Vol 188 (1-2) ◽

pp. 49-58 ◽

Cited By ~ 45

Author(s):

P. J. Casero ◽

Ilda Casimiro ◽

P. G. Lloret

Keyword(s):

Zea Mays ◽

Helianthus Annuus ◽

Lateral Root ◽

Root Initiation ◽

Lateral Root Initiation ◽

Pericycle Cells

Download Full-text

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.

Download Full-text

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.

Download Full-text

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.

Download Full-text