Shoot-derived miR2111 controls legume root and nodule development

AbstractLegumes control their nodule numbers through the Autoregulation Of Nodulation (AON). Rhizobia infection stimulates the production of root-derived CLE peptide hormones that are translocated to the shoot where they regulate a new signal. We used soybean to demonstrate that this shoot-derived signal is miR2111, which is transported via phloem to the root where it targets transcripts of Too Much Love (TML), a negative regulator of nodulation. Shoot perception of rhizobia-induced CLE peptides suppresses miR2111 expression, resulting in TML accumulation in roots and subsequent inhibition of nodule organogenesis. Feeding synthetic mature miR2111 via the petiole increased nodule numbers per plant. Likewise, elevating miR2111 availability by over-expression promoted nodulation, while target mimicry of TML induced the opposite effect on nodule development in wild-type plants and alleviated the supernodulating and stunted root growth phenotypes of AON-defective mutants. Additionally, in non-nodulating wild-type plants, ectopic expression of miR2111 significantly enhanced lateral root emergence with a decrease in lateral root length and average root diameter. In contrast, hairy roots constitutively expressing the target mimic construct exhibited reduced lateral root density. Overall, these findings demonstrate that miR2111 is both the critical shoot-to-root factor that positively regulates root nodule development, and also acts to shape root system architecture via orchestrating the degree of root branching, as well as the length and thickness of lateral roots.

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CLE-CLAVATA1 Signaling Pathway Modulates Lateral Root Development under Sulfur Deficiency

Plants ◽

10.3390/plants8040103 ◽

2019 ◽

Vol 8 (4) ◽

pp. 103 ◽

Cited By ~ 8

Author(s):

Wei Dong ◽

Yinghua Wang ◽

Hideki Takahashi

Keyword(s):

Root Development ◽

Lateral Root ◽

Molecular Mechanisms ◽

Plant Root ◽

Root System Architecture ◽

Wild Type ◽

Lateral Root Development ◽

S Deficiency ◽

Cle Peptide ◽

Plant Root System

Plant root system architecture changes drastically in response to availability of macronutrients in the soil environment. Despite the importance of root sulfur (S) uptake in plant growth and reproduction, molecular mechanisms underlying root development in response to S availability have not been fully characterized. We report here on the signaling module composed of the CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION (CLE) peptide and CLAVATA1 (CLV1) leucine-rich repeat receptor kinase, which regulate lateral root (LR) development in Arabidopsis thaliana upon changes in S availability. The wild-type seedlings exposed to prolonged S deficiency showed a phenotype with low LR density, which was restored upon sulfate supply. In contrast, the clv1 mutant showed a higher daily increase rate of LR density relative to the wild-type under prolonged S deficiency, which was diminished to the wild-type level upon sulfate supply, suggesting that CLV1 directs a signal to inhibit LR development under S-deficient conditions. CLE2 and CLE3 transcript levels decreased under S deficiency and through CLV1-mediated feedback regulations, suggesting the levels of CLE peptide signals are adjusted during the course of LR development. This study demonstrates a fine-tuned mechanism for LR development coordinately regulated by CLE-CLV1 signaling and in response to changes in S availability.

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Analysis of lateral root growth in Arabidopsis in response to physiologically active auxin analogues

Acta Agronomica Hungarica ◽

10.1556/aagr.58.2010.1.1 ◽

2010 ◽

Vol 58 (1) ◽

pp. 1-10 ◽

Cited By ~ 3

Author(s):

L. Novickienė ◽

V. Gavelienė ◽

L. Miliuvienė ◽

D. Kazlauskienė ◽

L. Pakalniškytė

Keyword(s):

Lateral Root ◽

Apical Meristem ◽

Lateral Roots ◽

Root System Architecture ◽

Test Plant ◽

Wild Type ◽

Root Primordia ◽

Lateral Root Primordia ◽

Primary Roots ◽

The Impact

The aim of this work was to investigate the formation and development of lateral roots in model trials on Arabidopsis thaliana L. Heynh wild type (Col-0), the alf4-1 mutant and its allele by applying the physiologically active auxin analogues IBA, IAA, TA-12 and TA-14.Differences were observed between the alf4-1 mutant and its allele phenotype in the formation of lateral roots. The application of auxin analogues was unable to restore the formation of lateral roots in the alf4-1 mutant. In some cases, under the impact of IBA (1 μM), a cluster of xylem cells was activated in the pericycle of the primary roots and lateral root primordia were formed. The auxin analogues induced the growth of primary roots in the alf4-1 allele and the formation and growth of lateral roots. The impact of IBA (1 μM), TA-12 (1 mM) and IAA (1 μM) was particularly evident. The intense formation of lateral roots under the impact of IBA and TA-12 could be related with the ability of these compounds to intensify mitotic activity in the apical meristem cells of the lateral roots. New data were obtained, showing that IBA and other physiologically active auxin analogues can modify the root system architecture of the test-plant Arabidopsis .

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

10.1101/2020.05.31.126557 ◽

2020 ◽

Author(s):

Jordan M. Chapman ◽

Gloria K. Muday

Keyword(s):

Arabidopsis Thaliana ◽

Lateral Root ◽

Lateral Roots ◽

Negative Regulator ◽

Antioxidant Compounds ◽

Wild Type ◽

Root Primordia ◽

Lateral Root Primordia ◽

Lateral Root Development ◽

Genes Encoding

AbstractFlavonoids are plant-specific antioxidant compounds that modulate plant development, which include flavonols and anthocyanins subclasses. In Arabidopsis thaliana, mutants in genes encoding each step in the flavonoid biosynthetic pathway have been isolated. We used these mutants to examine the role of flavonols in initiation and emergence of lateral roots and asked whether this regulation occurs through scavenging ROS. The tt4 mutants have a defect in the first committed step of flavonoid biosynthesis and have increased lateral root emergence. This phenotype was reversed by both genetic and chemical complementation. Using these flavonoid biosynthetic mutants, we eliminated roles for anthocyanins and the flavonols, quercetin and isorhamnetin, in controlling lateral root development. The tt7-2 mutant has a defect in a branchpoint enzyme blocking quercetin biosynthesis that led to elevated levels of kaempferol and reduced lateral roots. Kaempferol accumulated within lateral root primordia and was significantly increased in tt7-2. Thee data are consistent with kaempferol acting as a negative regulator of lateral root emergence. We examined ROS accumulation above and within the primordia using a general ROS sensor and identified increased signal above the primordia of the tt4 and tt7-2 mutants compared to wild type. Using a superoxide specific sensor, we detected a decrease in signal within the primordia of tt7-2, but not the tt4 mutant, compared to wild type. Together, these results support a model in which increased level of kaempferol in tt7-2 leads to a reduction in superoxide concentration in the lateral root primordia thereby reducing ROS-stimulated lateral root emergence.

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Arabidopsis AZG2, an auxin induced putative cytokinin transporter, regulates lateral root emergence

10.1101/2020.01.31.927970 ◽

2020 ◽

Author(s):

Tomás M. Tessi ◽

Sabine Brumm ◽

Eva Winklbauer ◽

Benjamin Schumacher ◽

Carlos I. Lescano ◽

...

Keyword(s):

Lateral Root ◽

Lateral Roots ◽

Root System Architecture ◽

Fluorescence Signal ◽

Loss Of Function ◽

Wild Type ◽

Root Primordia ◽

Long Distance ◽

Lateral Root Primordia ◽

Transporter Family

ABSTRACTThe phytohormones cytokinin (CK) and auxin are key regulators of plant growth and development. During the last decade specialised transport mechanisms turned out to be the key for the control of local and long distance hormone distributions. In contrast to auxin, CK transport is poorly understood. Here we show that Arabidopsis thaliana AZG2, a member of the AZG purine transporter family, acts as CK transporter involved in the determination of the root system architecture. The expression of AtAZG2 is primarily auxin dependent and restricted to a small group of cells surrounding the lateral root primordia. Compared to wild type, mutants carrying loss-of-function alleles of Atazg2 have higher density of lateral roots, suggesting AZG2 as being part of a regulatory pathway in lateral root emergence. Moreover, azg2 mutants are partially insensitive to exogenously applied CK, which is consistent with the observation that the CK reporter gene TCSnpro:GFP showed lower fluorescence signal in the roots of azg2 mutants compared to those of wild type. These results indicate a defective CK signalling pathway in the region of lateral root primordia. By the integration of AtAZG2 subcellular localization and CK transport capacity data, our results allowed us to propose a local Auxin/CK signalling model for the regulation of lateral root emergence.

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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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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 System Architecture ◽

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.

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The Rhizobium leguminosarum biovar trifolii ANU794 Induces Novel Developmental Responses on the Subterranean Clover Cultivar Woogenellup

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-19-0471 ◽

2006 ◽

Vol 19 (5) ◽

pp. 471-479 ◽

Cited By ~ 25

Author(s):

Angela Carmen Morris ◽

Michael Anthony Djordjevic

Keyword(s):

Lateral Root ◽

Rhizobium Leguminosarum ◽

Root Formation ◽

Fluorescent Protein ◽

Lateral Roots ◽

Hybrid Structures ◽

Nodule Development ◽

Lateral Root Formation ◽

Low Efficiency ◽

Developmental Responses

The clover-nodulating Rhizobium leguminosarum bv. trifolii ANU794 initiates normal root-nodule development with abnormally low efficiency on the Trifolium subterraneum cv. Woogenellup. The cellular and developmental responses of Woogenellup roots to the site- and dose-defined inoculation of green fluorescent protein (gfp)-labeled cells of ANU843 (nodulation proficient) and ANU794 was investigated using light, fluorescence, and confocal microscopy. Strain ANU794-gfp induced three primordia types and four developmental responses at the inoculation site: true or aberrant nodules (on 5 and 25% of plants, respectively), hybrid structures (20% of plants), or lateral roots (50% of plants). The novel hybrid structures possessed nodule and lateral root-like features and unusual vascular patterning. Strain ANU794-gfp induces lateral root formation by stimulating pericycle cell divisions at all nearby protoxylem poles. Only true nodules induced by ANU794-gfp contained intracellular bacteria. In contrast, strain ANU843-gfp induced nodules only and lateral root formation was suppressed at spot inoculation sites. Primordium types were distinguishable by the emission spectrum characteristics of phenolic UV-absorbing and fluorescent compounds that accumulate in primordium cells. Hybrid primordia contained (at least) two fluorescent cell populations, suggesting that they are chimeric. The results suggest that ANU794 may produce both nodule- and lateral root-generating signals simultaneously.

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Expression Studies on AUX1-like Genes in Medicago truncatula Suggest That Auxin Is Required at Two Steps in Early Nodule Development

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2001.14.3.267 ◽

2001 ◽

Vol 14 (3) ◽

pp. 267-277 ◽

Cited By ~ 86

Author(s):

Françoise de Billy ◽

Cathy Grosjean ◽

Sean May ◽

Malcolm Bennett ◽

Julie V. Cullimore

Keyword(s):

Medicago Truncatula ◽

Lateral Root ◽

Sequence Similarity ◽

Lateral Roots ◽

Peripheral Region ◽

Nodule Development ◽

Central Position ◽

Root Tips ◽

High Sequence Similarity ◽

Primary Roots

Medicago truncatula contains a family of at least five genes related to AUX1 of Arabidopsis thaliana (termed MtLAX genes for Medicago truncatula-like AUX1 genes). The high sequence similarity between the encoded proteins and AUX1 implies that the MtLAX genes encode auxin import carriers. The MtLAX genes are expressed in roots and other organs, suggesting that they play pleiotropic roles related to auxin uptake. In primary roots, the MtLAX genes are expressed preferentially in the root tips, particularly in the provascular bundles and root caps. During lateral root and nodule development, the genes are expressed in the primordia, particularly in cells that were probably derived from the pericycle. At slightly later stages, the genes are expressed in the regions of the developing organs where the vasculature arises (central position for lateral roots and peripheral region for nodules). These results are consistent with MtLAX being involved in local auxin transport and suggest that auxin is required at two common stages of lateral root and nodule development: development of the primordia and differentiation of the vasculature.

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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 ◽

Developmental Plasticity ◽

Lateral Roots ◽

Time Lapse ◽

Root System Architecture ◽

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.

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