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

2019 ◽  
Vol 70 (15) ◽  
pp. 3927-3940 ◽  
Author(s):  
Rémi Branco ◽  
Josette Masle

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.

2019 ◽  
Author(s):  
Rémi Branco ◽  
Josette Masle

AbstractAs in animals, the plant body plan and primary organs are established during embryogenesis. However, plants have the ability to generate new organs and functional units throughout their whole life. These are produced through the specification, initiation and differentiation of secondary meristems, governed by the intrinsic genetic program and cues from the environment. They give plants 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 still largely elusive. In particular the mechanisms regulating the iterative formation of lateral roots along the primary root remain little known. A pivotal role of auxin is well established and recently the role of local mechanical signals and oscillations in transcriptional activity has emerged. Here we provide evidence for a role of Translationally Controlled Tumor Protein (TCTP), a vital ubiquitous protein in eukaryotes. We show that Arabidopsis AtTCTP1 controls root system architecture through a dual function: as a general constitutive growth promoter locally, and as a systemic signalling agent via mobility from the shoot. Our data indicate that this signalling function is specifically targeted to the pericycle and modulates the frequency of lateral root initiation and emergence sites along the primary root, and the compromise between branching and elongating, independent of shoot size. Plant TCTP genes show high similarity among species. TCTP messengers and proteins have been detected in the vasculature of diverse species. This suggests that the mobility and extracellular signalling function of AtTCTP1 to control root organogenesis might be widely conserved within the plant kingdom, and highly relevant to a better understanding of post-embryonic formation of lateral organs in plants, and the elusive coordination of shoot and root morphogenesis.


Author(s):  
Marek Šírl ◽  
Tereza Šnajdrová ◽  
Dolores Gutiérrez-Alanís ◽  
Joseph G. Dubrovsky ◽  
Jean Phillipe Vielle-Calzada ◽  
...  

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.


2020 ◽  
Author(s):  
Hardik P. Gala ◽  
Amy Lanctot ◽  
Ken Jean-Baptiste ◽  
Sarah Guiziou ◽  
Jonah C. Chu ◽  
...  

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.


1979 ◽  
Vol 6 (2) ◽  
pp. 195 ◽  
Author(s):  
PB Goodwin ◽  
SC Morris

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.


2020 ◽  
Author(s):  
Moutasem Omary ◽  
Naama Gil-Yarom ◽  
Chen Yahav ◽  
Evyatar Steiner ◽  
Idan Efroni

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.


2020 ◽  
Vol 21 (5) ◽  
pp. 1886 ◽  
Author(s):  
Marek Širl ◽  
Tereza Šnajdrová ◽  
Dolores Gutiérrez-Alanís ◽  
Joseph G. Dubrovsky ◽  
Jean Phillipe Vielle-Calzada ◽  
...  

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.


Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3303-3310 ◽  
Author(s):  
M.J. Laskowski ◽  
M.E. Williams ◽  
H.C. Nusbaum ◽  
I.M. Sussex

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.


1991 ◽  
Vol 69 (1) ◽  
pp. 123-135 ◽  
Author(s):  
Bai-Ling Lin ◽  
V. Raghavan

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.


2012 ◽  
Vol 367 (1595) ◽  
pp. 1509-1516 ◽  
Author(s):  
S. Guyomarc'h ◽  
S. Léran ◽  
M. Auzon-Cape ◽  
F. Perrine-Walker ◽  
M. Lucas ◽  
...  

Root system architecture plays an important role in determining nutrient and water acquisition and is modulated by endogenous and environmental factors, resulting in considerable developmental plasticity. The orientation of primary root growth in response to gravity (gravitropism) has been studied extensively, but little is known about the behaviour of lateral roots in response to this signal. Here, we analysed the response of lateral roots to gravity and, consistently with previous observations, we showed that gravitropism was acquired slowly after emergence. Using a lateral root induction system, we studied the kinetics for the appearance of statoliths, phloem connections and auxin transporter gene expression patterns. We found that statoliths could not be detected until 1 day after emergence, whereas the gravitropic curvature of the lateral root started earlier. Auxin transporters modulate auxin distribution in primary root gravitropism. We found differences regarding PIN3 and AUX1 expression patterns between the lateral root and the primary root apices. Especially PIN3, which is involved in primary root gravitropism, was not expressed in the lateral root columella. Our work revealed new developmental transitions occurring in lateral roots after emergence, and auxin transporter expression patterns that might explain the specific response of lateral roots to gravity.


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