Systemic signalling through TCTP1 controls lateral root formation in Arabidopsis

Lateral Roots ◽

Primary Root ◽

Dual Function ◽

Growth Promoter ◽

Lateral Organs ◽

Root Organogenesis

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.

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 ◽

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.

Early development and gravitropic response of lateral roots in Arabidopsis thaliana

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0231 ◽

2012 ◽

Vol 367 (1595) ◽

pp. 1509-1516 ◽

Cited By ~ 30

Author(s):

S. Guyomarc'h ◽

S. Léran ◽

M. Auzon-Cape ◽

F. Perrine-Walker ◽

M. Lucas ◽

...

Keyword(s):

Lateral Root ◽

Lateral Roots ◽

Expression Patterns ◽

Primary Root ◽

Specific Response ◽

Root Induction ◽

Root Gravitropism ◽

Auxin Transporter

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.

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 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.

Disruption of CYCLOPHILIN 38 function reveals a photosynthesis-dependent systemic signal controlling lateral root emergence

10.1101/2020.03.11.985820 ◽

2020 ◽

Author(s):

Lina Duan ◽

Juan Manuel Pérez-Ruiz ◽

Francisco Javier Cejudo ◽

José R. Dinneny

Keyword(s):

Root Growth ◽

Root System ◽

Lateral Root ◽

System Development ◽

Lateral Roots ◽

Primary Root ◽

Minor Effect ◽

Low Light ◽

Primary Root Growth

AbstractPhotosynthesis in leaves generates the fixed-carbon resources and essential metabolites that support sink tissues, such as roots [1]. One of these products, sucrose, is known to promote primary root growth, but it is not clear what other molecules may be involved and whether other stages of root system development are affected by photosynthate levels [2]. Through a mutant screen to identify pathways regulating root system architecture, we identified a mutation in the CYCLOPHILIN 38 (CYP38) gene, which causes an accumulation of pre-emergent stage lateral roots, with a minor effect on primary root growth. CYP38 was previously reported to maintain the stability of Photosystem II (PSII) in chloroplasts [3]. CYP38 expression is enriched in the shoot and grafting experiments show that the gene acts non-cell autonomously to promote lateral root emergence. Growth of wild-type plants under low light conditions phenocopied the cyp38 lateral root emergence phenotype as did the inhibition of PSII-dependent electron transport or NADPH production. Importantly, the cyp38 root phenotype is not rescued by exogenous sucrose, suggesting the involvement of another metabolite. Auxin (IAA) is an essential hormone promoting root growth and its biosynthesis from tryptophan is dependent on reductant generated during photosynthesis [4,5]. Both WT seedlings grown under low light and cyp38 mutants have highly diminished levels of IAA in root tissues. The cyp38 lateral root defect is rescued by IAA treatment, revealing that photosynthesis promotes lateral root emergence partly through IAA biosynthesis. Metabolomic profiling shows that the accumulation of several defense-related metabolites are also photosynthesis-dependent, suggesting that the regulation of a number of energy-intensive pathways are down-regulated when light becomes limiting.

Same same, but different: growth responses of primary and lateral roots

Journal of Experimental Botany ◽

10.1093/jxb/eraa027 ◽

2020 ◽

Vol 71 (8) ◽

pp. 2397-2411 ◽

Cited By ~ 9

Author(s):

Sascha Waidmann ◽

Elizabeth Sarkel ◽

Jürgen Kleine-Vehn

Keyword(s):

Root System ◽

Lateral Root ◽

Growth Regulation ◽

Lateral Roots ◽

Primary Root ◽

Spatial Arrangement ◽

Growth Responses ◽

Lateral Root Primordia ◽

Organ Growth

Abstract The root system architecture describes the shape and spatial arrangement of roots within the soil. Its spatial distribution depends on growth and branching rates as well as directional organ growth. The embryonic primary root gives rise to lateral (secondary) roots, and the ratio of both root types changes over the life span of a plant. Most studies have focused on the growth of primary roots and the development of lateral root primordia. Comparably less is known about the growth regulation of secondary root organs. Here, we review similarities and differences between primary and lateral root organ growth, and emphasize particularly how external stimuli and internal signals differentially integrate root system growth.

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 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.

Strigolactones Control Root System Architecture and Tip Anatomy in Solanum lycopersicum L. Plants under P Starvation

Plants ◽

10.3390/plants9050612 ◽

2020 ◽

Vol 9 (5) ◽

pp. 612 ◽

Cited By ~ 2

Author(s):

Veronica Santoro ◽

Michela Schiavon ◽

Francesco Gresta ◽

Andrea Ertani ◽

Francesca Cardinale ◽

...

Keyword(s):

Solanum Lycopersicum ◽

Lateral Root ◽

Primary Root ◽

Root Traits ◽

Root Tip ◽

Root Number ◽

Wild Type ◽

Solanum Lycopersicum L ◽

P Supply

The hormones strigolactones accumulate in plant roots under phosphorus (P) shortage, inducing variations in plant phenotype. In this study, we aimed at understanding whether strigolactones control morphological and anatomical changes in tomato (Solanum lycopersicum L.) roots under varying P supply. Root traits were evaluated in wild-type seedlings grown in high vs. low P, with or without exogenous strigolactones, and in wild-type and strigolactone-depleted plants grown first under high vs. no P, and then under high vs. no P after acclimation on low P. Exogenous strigolactones stimulated primary root and lateral root number under low P. Root growth was reduced in strigolactone-depleted plants maintained under continuous P deprivation. Total root and root hair length, lateral root number and root tip anatomy were impaired by low strigolactone biosynthesis in plants grown under low P or transferred from low to no P. Under adequate P conditions, root traits of strigolactone-depleted and wild-type plants were similar. Concluding, our results indicate that strigolactones (i) control macro- and microscopic changes of root in tomato depending on P supply; and (ii) do not affect root traits significantly when plants are supplemented with adequate P, but are needed for acclimation to no P and typical responses to low P.

Repression of early lateral root initiation events by transient water deficit in barley and maize

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2011.0240 ◽

2012 ◽

Vol 367 (1595) ◽

pp. 1534-1541 ◽

Cited By ~ 27

Author(s):

Aurélie Babé ◽

Tristan Lavigne ◽

Jean-Philippe Séverin ◽

Kerstin A. Nagel ◽

Achim Walter ◽

...

Keyword(s):

Water Deficit ◽

Lateral Roots ◽

Time Lapse ◽

Negative Control ◽

Root Branching ◽

Branching Patterns ◽

Primary Determinant ◽

Key Driver

The formation of lateral roots (LRs) is a key driver of root system architecture and developmental plasticity. The first stage of LR formation, which leads to the acquisition of founder cell identity in the pericycle, is the primary determinant of root branching patterns. The fact that initiation events occur asynchronously in a very small number of cells inside the parent root has been a major difficulty in the study of the molecular regulation of branching patterns. Inducible systems that trigger synchronous lateral formation at predictable sites have proven extremely valuable in Arabidopsis to decipher the first steps of LR formation. Here, we present a LR repression system for cereals that relies on a transient water-deficit treatment, which blocks LR initiation before the first formative divisions. Using a time-lapse approach, we analysed the dynamics of this repression along growing roots and were able to show that it targets a very narrow developmental window of the initiation process. Interestingly, the repression can be exploited to obtain negative control root samples where LR initiation is absent. This system could be instrumental in the analysis of the molecular basis of drought-responsive as well as intrinsic pathways of LR formation in cereals.

GDSL-domain containing proteins mediate suberin biosynthesis and degradation, enabling developmental plasticity of the endodermis during lateral root emergence

10.1101/2020.06.25.171389 ◽

2020 ◽

Cited By ~ 1

Author(s):

Robertas Ursache ◽

Cristovao De Jesus Vieira-Teixeira ◽

Valérie Dénervaud Tendon ◽

Kay Gully ◽

Damien De Bellis ◽

...

Keyword(s):

Lateral Root ◽

Lateral Roots ◽

Transcriptional Response ◽

Soil Conditions ◽

Data Set ◽

Subsequent Formation ◽

Suberin Lamellae ◽

Casparian Strips ◽

Endodermal Cells

ABSTRACTRoots anchor plants and deliver water and nutrients from the soil. The root endodermis provides the crucial extracellular diffusion barrier by setting up a supracellular network of lignified cell walls, called Casparian strips, supported by a subsequent formation of suberin lamellae. Whereas lignification is thought to be irreversible, formation of suberin lamellae was demonstrated to be dynamic, facilitating adaptation to different soil conditions. Plants shape their root system through the regulated formation of lateral roots emerging from within the endodermis, requiring local breaking and re-sealing of the endodermal diffusion barriers. Here, we show that differentiated endodermal cells have a distinct auxin-mediated transcriptional response that regulates cell wall remodelling. Based on this data set we identify a set of GDSL-lipases that are essential for suberin formation. Moreover, we find that another set of GDSL-lipases mediates suberin degradation, which enables the developmental plasticity of the endodermis required for normal lateral root emergence.

Cytokinin functions as an asymmetric and anti-gravitropic signal in lateral roots

10.1101/572941 ◽

2019 ◽

Author(s):

Sascha Waidmann ◽

Michel Ruiz Rosquete ◽

Maria Schöller ◽

Heike Lindner ◽

Therese LaRue ◽

...

Keyword(s):

Root System ◽

Lateral Root ◽

Genome Wide Association Study ◽

Negative Impact ◽

Lateral Roots ◽

Primary Root ◽

Cytokinin Oxidase ◽

Cytokinin Signaling ◽

Organ Growth ◽

A Genome

AbstractDirectional organ growth allows the plant root system to strategically cover its surroundings. Intercellular auxin transport is aligned with the gravity vector in the primary root tips, facilitating downward organ bending at the lower root flank. Here we show that cytokinin signaling functions as a lateral root specific anti-gravitropic component, promoting the radial distribution of the root system. We performed a genome-wide association study and revealed that signal peptide processing of Cytokinin Oxidase 2 (CKX2) affects its enzymatic activity and, thereby, determines the degradation of cytokinins in naturalArabidopsis thalianaaccessions. Cytokinin signaling interferes with growth at the upper lateral root flank and thereby prevents downward bending. Our interdisciplinary approach revealed that two phytohormonal cues at opposite organ flanks counterbalance each other’s negative impact on growth, suppressing organ growth towards gravity and allow for radial expansion of the root system.