Bradyrhizobium japonicum IRAT FA3 alters Arabidopsis thaliana root architecture via regulation of auxin efflux transporters PIN2, PIN3, PIN7 and ABCB19

Beneficial rhizobacteria can stimulate changes in plant root development. While root system growth is mediated by multiple factors, the regulated distribution of the phytohormone auxin within root tissues plays a principal role. Auxin transport facilitators help to generate the auxin gradients and maxima that determine root structure. Here, we show that the plant growth-promoting rhizobacterial strain Bradyrhizobium japonicum IRAT FA3 influences specific auxin efflux transporters to alter Arabidopsis thaliana root morphology. Gene expression profiling of host transcripts in control and B. japonicum-inoculated roots of the wild type A. thaliana accession Col-0 confirmed upregulation of PIN2, PIN3, PIN7 and ABCB19 with B. japonicum and identified genes potentially contributing to a diverse array of auxin-related responses. Co-cultivation of the bacterium with loss-of-function auxin efflux transport mutants revealed that B. japonicum requires PIN3, PIN7 and ABCB19 to increase lateral root development and utilizes PIN2 to reduce primary root length. Accelerated lateral root primordia production due to B. japonicum was not observed in single pin3, pin7 or abcb19 mutants, suggesting independent roles for PIN3, PIN7 and ABCB19 during the plant-microbe interaction. Our work demonstrates B. japonicum’s influence over host transcriptional reprogramming during plant interaction with this beneficial microbe and the subsequent alterations to root system architecture.

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Nitrate Signaling, Functions, and Regulation of Root System Architecture: Insights from Arabidopsis thaliana

Genes ◽

10.3390/genes11060633 ◽

2020 ◽

Vol 11 (6) ◽

pp. 633 ◽

Cited By ~ 1

Author(s):

Muhammad Asim ◽

Zia Ullah ◽

Fangzheng Xu ◽

Lulu An ◽

Oluwaseun Olayemi Aluko ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Root System ◽

Root Development ◽

System Architecture ◽

Lateral Root ◽

Transcriptional Regulatory Network ◽

Primary Root ◽

Root System Architecture ◽

Nitrate Transporter ◽

Nitrate Transporters

Root system architecture (RSA) is required for the acquisition of water and mineral nutrients from the soil. One of the essential nutrients, nitrate (NO3−), is sensed and transported by nitrate transporters NRT1.1 and NRT2.1 in the plants. Nitrate transporter 1.1 (NRT1.1) is a dual-affinity nitrate transporter phosphorylated at the T101 residue by calcineurin B-like interacting protein kinase (CIPKs); it also regulates the expression of other key nitrate assimilatory genes. The differential phosphorylation (phosphorylation and dephosphorylation) strategies and underlying Ca2+ signaling mechanism of NRT1.1 stimulate lateral root growth by activating the auxin transport activity and Ca2+-ANR1 signaling at the plasma membrane and the endosomes, respectively. NO3− additionally functions as a signal molecule that forms a signaling system, which consists of a vast array of transcription factors that control root system architecture that either stimulate or inhibit lateral and primary root development in response to localized and high nitrate (NO3−), respectively. This review elucidates the so-far identified nitrate transporters, nitrate sensing, signal transduction, and the key roles of nitrate transporters and its downstream transcriptional regulatory network in the primary and lateral root development in Arabidopsis thaliana under stress conditions.

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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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Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana

Journal of Biological Chemistry ◽

10.1074/jbc.ra120.014543 ◽

2020 ◽

pp. jbc.RA120.014543

Author(s):

Jordan M. Chapman ◽

Gloria K. Muday

Keyword(s):

Arabidopsis Thaliana ◽

Root Development ◽

Lateral Root ◽

Lateral Roots ◽

Negative Regulator ◽

Wild Type ◽

Root Primordia ◽

Lateral Root Primordia ◽

Lateral Root Development ◽

Genes Encoding

Flavonoids are a class of specialized metabolites with subclasses including flavonols and anthocyanins, which have unique properties as antioxidants. Flavonoids modulate plant development, but whether and how they impact lateral root development is unclear. We examined potential roles for flavonols in this process using Arabidopsis thaliana mutants with defects in genes encoding key enzymes in flavonoid biosynthesis. We observed the tt4 and fls1 mutants, which produce no flavonols, have increased lateral root emergence. The tt4 root phenotype was reversed by genetic and chemical complementation. To more specifically define the flavonoids involved, we tested an array of flavonoid biosynthetic mutants, eliminating roles for anthocyanins and the flavonols quercetin and isorhamnetin in modulating root development. Instead, two tt7 mutant alleles, with defects in a branchpoint enzyme blocking quercetin biosynthesis, formed reduced numbers of lateral roots, and tt7-2 had elevated levels of kaempferol. Using a flavonol-specific dye, we observed that in the tt7-2 mutant, kaempferol accumulated within lateral root primordia at higher levels than wild-type. These data are consistent with kaempferol, or downstream derivatives, acting as a negative regulator of lateral root emergence. We examined ROS accumulation using ROS-responsive probes and found reduced fluorescence of a superoxide-selective probe within the primordia of tt7-2 compared to wild type, but not in the tt4 mutant, consistent with opposite effects of these mutants on lateral root emergence. These results support a model in which increased level of kaempferol in the lateral root primordia of tt7-2 reduces superoxide concentration and ROS-stimulated lateral root emergence.

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Cryptic variation in RNA-directed DNA-methylation controls lateral root development when auxin signalling is perturbed

Nature Communications ◽

10.1038/s41467-019-13927-3 ◽

2020 ◽

Vol 11 (1) ◽

Cited By ~ 3

Author(s):

Zaigham Shahzad ◽

Ross Eaglesfield ◽

Craig Carr ◽

Anna Amtmann

Keyword(s):

Dna Methylation ◽

Root Development ◽

Transcriptional Repression ◽

Lateral Root ◽

Developmental Plasticity ◽

Plant Root ◽

Negative Regulator ◽

Lateral Root Primordia ◽

Lateral Root Development ◽

Cryptic Variation

AbstractMaintaining the right balance between plasticity and robustness in biological systems is important to allow adaptation while maintaining essential functions. Developmental plasticity of plant root systems has been the subject of intensive research, but the mechanisms underpinning robustness remain unclear. Here, we show that potassium deficiency inhibits lateral root organogenesis by delaying early stages in the formation of lateral root primordia. However, the severity of the symptoms arising from this perturbation varies within a natural population of Arabidopsis and is associated with the genetic variation in CLSY1, a key component of the RNA-directed DNA-methylation machinery. Mechanistically, CLSY1 mediates the transcriptional repression of a negative regulator of root branching, IAA27, and promotes lateral root development when the auxin-dependent proteolysis pathway fails. Our study identifies DNA-methylation-mediated transcriptional repression as a backup system for post-translational protein degradation which ensures robust development and performance of plants in a challenging environment.

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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 ◽

Root System Architecture ◽

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.

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Utilization of a hydrate cellulose film for investigation of Arabidopsis thaliana L. root system growth and development

Biotekhnologiya ◽

10.21519/0234-2758-2020-36-1-36-43 ◽

2020 ◽

Vol 36 (1) ◽

pp. 36-43

Author(s):

I.O. Konovalova ◽

T.N. Kudelina ◽

S.O. Smolyanina ◽

A.I. Lilienberg ◽

T.N. Bibikova

Keyword(s):

Arabidopsis Thaliana ◽

Root System ◽

Life Support ◽

Higher Plants ◽

Plant Root ◽

Lateral Roots ◽

Basic Research ◽

Cellulose Film ◽

A New Technique ◽

Basic Research Project

A new technique for Arabidopsis thaliana cultivation has been proposed that combines the use of a phytogel-based nutrient medium and a hydrophilic membrane of hydrate cellulose film, separating the root system of the plant from the medium thickness. Growth rates of both main and lateral roots were faster in the plants cultivated on the surface of hydrate cellulose film than in the plants grown in the phytogel volume. The location of the root system on the surface of the transparent hydrate film simplifies its observation and analysis and facilitates plant transplantation with preservation of the root system configuration. The proposed technique allowed us to first assess the effect of exogenous auxin on the growth of lateral roots at the 5-6 developmental stage. methods to study plant root systems, hydrate cellulose film, A. thaliana, lateral roots, differential root growth rate, auxin The work was financially supported by the Russian Foundation for Basic Research (Project Bel_mol_a 19-54-04015) and the basic topic of the Russian Academy of Sciences - IBMP RAS «Regularities of the Influence of Extreme Environmental Factors on the Processes of Cultivation of Higher Plants and the Development of Japanese Quail Tissues at Different Stages of its Ontogenesis under the Conditions of Regenerative Life Support Systems».

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High throughput phenotyping of root growth dynamics, lateral root formation, root architecture and root hair development enabled by PlaRoM

Functional Plant Biology ◽

10.1071/fp09167 ◽

2009 ◽

Vol 36 (11) ◽

pp. 938 ◽

Cited By ~ 48

Author(s):

Nima Yazdanbakhsh ◽

Joachim Fisahn

Keyword(s):

Root Growth ◽

Growth Kinetics ◽

Lateral Root ◽

Root Architecture ◽

Imaging Techniques ◽

Plant Root ◽

Primary Root ◽

Growth Media ◽

Root Extension ◽

Lateral Root Development

Plant organ phenotyping by non-invasive video imaging techniques provides a powerful tool to assess physiological traits and biomass production. We describe here a range of applications of a recently developed plant root monitoring platform (PlaRoM). PlaRoM consists of an imaging platform and a root extension profiling software application. This platform has been developed for multi parallel recordings of root growth phenotypes of up to 50 individual seedlings over several days, with high spatial and temporal resolution. PlaRoM can investigate root extension profiles of different genotypes in various growth conditions (e.g. light protocol, temperature, growth media). In particular, we present primary root growth kinetics that was collected over several days. Furthermore, addition of 0.01% sucrose to the growth medium provided sufficient carbohydrates to maintain reduced growth rates in extended nights. Further analysis of records obtained from the imaging platform revealed that lateral root development exhibits similar growth kinetics to the primary root, but that root hairs develop in a faster rate. The compatibility of PlaRoM with currently accessible software packages for studying root architecture will be discussed. We are aiming for a global application of our collected root images to analytical tools provided in remote locations.

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Lateral root formation and nutrients: nitrogen in the spotlight

Plant Physiology ◽

10.1093/plphys/kiab145 ◽

2021 ◽

Author(s):

Pierre-Mathieu Pélissier ◽

Hans Motte ◽

Tom Beeckman

Keyword(s):

Signaling Pathways ◽

Root System ◽

Root Development ◽

Lateral Root ◽

Molecular Mechanisms ◽

Root Formation ◽

Lateral Roots ◽

Nutrient Use Efficiency ◽

Lateral Root Formation ◽

Lateral Root Development

Abstract Lateral roots are important to forage for nutrients due to their ability to increase the uptake area of a root system. Hence, it comes as no surprise that lateral root formation is affected by nutrients or nutrient starvation, and as such contributes to the root system plasticity. Understanding the molecular mechanisms regulating root adaptation dynamics towards nutrient availability is useful to optimize plant nutrient use efficiency. There is at present a profound, though still evolving, knowledge on lateral root pathways. Here, we aimed to review the intersection with nutrient signaling pathways to give an update on the regulation of lateral root development by nutrients, with a particular focus on nitrogen. Remarkably, it is for most nutrients not clear how lateral root formation is controlled. Only for nitrogen, one of the most dominant nutrients in the control of lateral root formation, the crosstalk with multiple key signals determining lateral root development is clearly shown. In this update, we first present a general overview of the current knowledge of how nutrients affect lateral root formation, followed by a deeper discussion on how nitrogen signaling pathways act on different lateral root-mediating mechanisms for which multiple recent studies yield insights.

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A 3D-printed, Arabidopsis Thaliana Root Imaging Platform

Lab on a Chip ◽

10.1039/d1lc00149c ◽

2021 ◽

Author(s):

Michel Moussus ◽

Matthias Meier

Keyword(s):

Molecular Dynamics ◽

Arabidopsis Thaliana ◽

High Resolution ◽

Root System ◽

Plant Root ◽

Microfluidic Platforms ◽

External Cues ◽

3D Printed ◽

Plant Root System ◽

Analytical Tools

High resolution live imaging promises new insights into the cellular and molecular dynamics of the plant root system in response to external cues. Microfluidic platforms are valuable analytical tools that...

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