The Small GTPase ROP10 of Medicago truncatula Is Required for Both Tip Growth of Root Hairs and Nod Factor-Induced Root Hair Deformation

The microtubule (MT) cytoskeleton is an important part of the tip-growth machinery in legume root hairs. Here we report the effect of Nod factor (NF) on MTs in root hairs of Medicago truncatula. In tip-growing hairs, the ones that typically curl around rhizobia, NF caused a subtle shortening of the endoplasmic MT array, which recovered within 10 min, whereas cortical MTs were not visibly affected. In growth-arresting root hairs, endoplasmic MTs disappeared shortly after NF application, but reformed within 20 min, whereas cortical MTs remained present in a high density. After NF treatment, growth-arresting hairs were swelling at their tips, after which a new outgrowth formed that deviated with a certain angle from the former growth axis. MT depolymerization with oryzalin caused a growth deviation similar to the NF; whereas, combined with NF, oryzalin increased and the MT-stabilizing drug taxol suppressed NF-induced growth deviation. The NF-induced disappearance of the endoplasmic MTs correlated with a loss of polar cytoarchitecture and straight growth directionality, whereas the reappearance of endoplasmic MTs correlated with the new set up of polar cytoarchitecture. Drug studies showed that MTs are involved in determining root hair elongation in a new direction after NF treatment.

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Identical Accumulation and Immobilization of Sulfated and Nonsulfated Nod Factors in Host and Nonhost Root Hair Cell Walls

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.2003.16.10.884 ◽

2003 ◽

Vol 16 (10) ◽

pp. 884-892 ◽

Cited By ~ 15

Author(s):

Joachim Goedhart ◽

Jean-Jacques Bono ◽

Ton Bisseling ◽

Theodorus W. J. Gadella

Keyword(s):

Hair Cell ◽

Root Hair ◽

Cell Walls ◽

Root Hairs ◽

Sharp Decrease ◽

Biologically Active ◽

Nod Factors ◽

Nod Factor ◽

Root Hair Cell ◽

Root Hair Deformation

Nod factors are signaling molecules secreted by Rhizobium bacteria. These lipo-chitooligosaccharides (LCOs) are required for symbiosis with legumes and can elicit specific responses at subnanomolar concentrations on a compatible host. How plants perceive LCOs is unclear. In this study, using fluorescent Nod factor analogs, we investigated whether sulfated and nonsulfated Nod factors were bound and perceived differently by Medicago truncatula and Vicia sativa root hairs. The bioactivity of three novel sulfated fluorescent LCOs was tested in a root hair deformation assay on M. truncatula, showing bioactivity down to 0.1 to 1 nM. Fluorescence microscopy of plasmolyzed M. truncatula root hairs shows that sulfated fluorescent Nod factors accumulate in the cell wall of root hairs, whereas they are absent from the plasma membrane when applied at 10 nM. When the fluorescent Nod factor distribution in medium surrounding a root was studied, a sharp decrease in fluorescence close to the root hairs was observed, visualizing the remarkable capacity of root hairs to absorb Nod factors from the medium. Fluorescence correlation microscopy was used to study in detail the mobilities of sulfated and nonsulfated fluorescent Nod factors which are biologically active on M. truncatula and V. sativa, respectively. Remarkably, no difference between sulfated and nonsulfated Nod factors was observed: both hardly diffuse and strongly accumulate in root hair cell walls of both M. truncatula and V. sativa. The implications for the mode of Nod factor perception are discussed.

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The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation

The Plant Journal ◽

10.1046/j.1365-313x.2003.01743.x ◽

2003 ◽

Vol 34 (4) ◽

pp. 495-506 ◽

Cited By ~ 211

Author(s):

Besma Ben Amor ◽

Sidney L. Shaw ◽

Giles E. D. Oldroyd ◽

Fabienne Maillet ◽

R. Varma Penmetsa ◽

...

Keyword(s):

Signal Transduction ◽

Medicago Truncatula ◽

Root Hair ◽

Calcium Flux ◽

Early Step ◽

Nod Factor ◽

Root Hair Deformation

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Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction

Development ◽

10.1242/dev.124.9.1781 ◽

1997 ◽

Vol 124 (9) ◽

pp. 1781-1787 ◽

Cited By ~ 1

Author(s):

R. Heidstra ◽

W.C. Yang ◽

Y. Yalcin ◽

S. Peck ◽

A.M. Emons ◽

...

Keyword(s):

Cell Division ◽

Root Hair ◽

Rhizobium Leguminosarum ◽

Tip Growth ◽

Cortical Cell ◽

Acc Oxidase ◽

Positional Information ◽

Nod Factors ◽

Nod Factor ◽

Root Hair Deformation

Nod factors secreted by Rhizobium leguminosarum bv. viciae induce root hair deformation, involving a reinitiation of tip growth, and the formation of nodule primordia in Vicia sativa (vetch). Ethylene is a potent inhibitor of cortical cell division, an effect that can be counteracted by applying silver ions (Ag+) or aminoethoxy-vinylglycine (AVG). In contrast to the inhibitory effect on cortical cell division, ethylene promotes the formation of root hairs (which involves tip growth) in the root epidermis of Arabidopsis. We investigate the possible paradox concerning the action of ethylene, putatively promoting Nod factor induced tip growth whilst, at the same time, inhibiting cortical cell division. We show, by using the ethylene inhibitors AVG and Ag+, that ethylene has no role in the reinitiation of root hair tip growth induced by Nod factors (root hair deformation) in vetch. However, root hair formation is controlled, at least in part, by ethylene. Furthermore, we show that ACC oxidase, which catalizes the last step in ethylene biosynthesis, is expressed in the cell layers opposite the phloem in that part of the root where nodule primordia are induced upon inoculation with Rhizobium. Therefore, we test whether endogenously produced ethylene provides positional information controlling the site where nodule primordia are formed by determining the position of nodules formed on pea roots grown in the presence of AVG or Ag+.

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Faculty Opinions recommendation of Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1011879.190521 ◽

2003 ◽

Author(s):

Julian Schroeder

Keyword(s):

Medicago Truncatula ◽

Hair Cells ◽

Root Hair ◽

Nod Factor ◽

Root Hair Cells

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Root hair deformation in the infection process of Alnus rubra

Canadian Journal of Botany ◽

10.1139/b83-319 ◽

1983 ◽

Vol 61 (11) ◽

pp. 2863-2876 ◽

Cited By ~ 49

Author(s):

Alison M. Berry ◽

John G. Torrey

Keyword(s):

Root Hair ◽

Cell Walls ◽

Root Hairs ◽

Infection Process ◽

Alnus Rubra ◽

Pseudomonas Cepacia ◽

Developmental Studies ◽

Experimental Conditions ◽

Root Hair Cell ◽

Root Hair Deformation

Structural and cell developmental studies of root hair deformation in Alnus rubra Bong. (Betulaceae) were carried out following inoculation with the soil pseudomonad Pseudomonas cepacia 85, alone or in concert with Frankia, and using axenically grown seedlings. Deformational changes can be observed in elongating root hairs within 2 h of inoculation with P. cepacia 85. These growing root hairs become branched or multilobed and highly modified from the single-tip growth of axenic root hairs. The cell walls of deformed hairs are histologically distinctive when stained with the fluorochrome acridine orange. Filtrate studies using P. cepacia 85 suggest that the deforming substance is not a low molecular weight compound. Root hair deformation and the associated wall histology are host specific in that Betula root hairs show none of these responses when grown and inoculated in the experimental conditions described. The bacterially induced changes in root hair cell walls during deformation may create a chemically and physically modified substrate for Frankia penetration, and the deformation itself may serve to entrap and enclose the filamentous organism, allowing wall dissolution and entry. Thus these events represent a complex host response as a precondition to successful nodulation.

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Nod Factor-Induced Expression of Leghemoglobin to Study the Mechanism of NH4NO3 Inhibition on Root Hair Deformation

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.1997.10.2.215 ◽

1997 ◽

Vol 10 (2) ◽

pp. 215-220 ◽

Cited By ~ 52

Author(s):

Renze Heidstra ◽

Gerd Nilsen ◽

Francisco Martinez-Abarca ◽

Ab van Kammen ◽

Ton Bisseling

Keyword(s):

Gene Expression ◽

Root Hair ◽

Rhizobium Leguminosarum ◽

Cortical Cell ◽

Brefeldin A ◽

Marker Genes ◽

Nodule Formation ◽

Cdna Clones ◽

Nod Factor ◽

Root Hair Deformation

Nod factors secreted by Rhizobium leguminosarum bv. viciae induce root hair deformation, the formation of nodule primordia, and the expression of early nodulin genes in Vicia sativa (vetch). Root hair deformation is induced within 3 h in a small, susceptible zone (±2 mm) of the root. NH4NO3, known to be a potent blocker of nodule formation, inhibits root hair deformation, initial cortical cell divisions, and infection thread formation. To test whether NH4NO3 affects the formation of a component of the Nod factor perception-transduction system, we studied Nod factor-induced gene expression. The differential display technique was used to search for marker genes, which are induced within 1 to 3 h after Nod factor application. Surprisingly, one of the isolated cDNA clones was identified as a leghemoglobin gene (VsLb1), which is induced in vetch roots within 1 h after Nod factor application. By using the drug brefeldin A, it was then shown that VsLb1 activation does not require root hair deformation. The pVsLb1 clone was used as a marker to show that in vetch plants grown in the presence of NH4NO3 Nod factor perception and transduction leading to gene expression are unaffected.

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Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi.1999.12.9.829 ◽

1999 ◽

Vol 12 (9) ◽

pp. 829-832 ◽

Cited By ~ 58

Author(s):

Norbert C. A. de Ruijter ◽

Ton Bisseling ◽

Anne Mie C. Emons

Keyword(s):

Actin Cytoskeleton ◽

Actin Filaments ◽

Tip Growth ◽

Developmental Stages ◽

Root Hairs ◽

Vicia Sativa ◽

Nod Factors ◽

Nod Factor

We studied the response of the actin cytoskeleton in vetch root hairs after application of host-specific Nod factor. Within 3 to 15 min, the number of sub-apical fine bundles of actin filaments (FB-actin) increased in all developmental stages. Tip growth resumed only in hairs in which the FB-actin density and the length of the region with FB-actin exceeded a minimal value.

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A Mutation in MRH2 Kinesin Enhances the Root Hair Tip Growth Defect Caused by Constitutively Activated ROP2 Small GTPase in Arabidopsis

PLoS ONE ◽

10.1371/journal.pone.0001074 ◽

2007 ◽

Vol 2 (10) ◽

pp. e1074 ◽

Cited By ~ 39

Author(s):

Guohua Yang ◽

Peng Gao ◽

Hua Zhang ◽

Shanjin Huang ◽

Zhi-Liang Zheng

Keyword(s):

Root Hair ◽

Tip Growth ◽

Small Gtpase ◽

Growth Defect

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AtRBOHC/RHD2 vesicular delivery to the apical plasma membrane domain during root hair development

10.1101/2021.09.13.460100 ◽

2021 ◽

Author(s):

Lenka Kuběnová ◽

Michaela Tichá ◽

Jozef Šamaj ◽

Miroslav Ovečka

Keyword(s):

Plasma Membrane ◽

Quantitative Analysis ◽

Root Hair ◽

Tip Growth ◽

Root Hairs ◽

Apical Plasma Membrane ◽

Loss Of Function ◽

Short Root ◽

Early Endosomes ◽

Root Hair Initiation

AbstractArabidopsis root hairs develop as long tubular extensions from the rootward pole of trichoblasts and exert polarized tip growth. The establishment and maintenance of root hair polarity is a complex process involving the local apical production of reactive oxygen species (ROS) generated by NADPH oxidase RESPIRATORY BURST OXIDASE HOMOLOG PROTEIN C/ROOT HAIR DEFECTIVE 2 (AtRBOHC/RHD2). It has been shown that loss-of-function rhd2 mutants have short root hairs that are unable to elongate by tip growth, and this phenotype was fully complemented by GFP-RHD2 expressed under the RHD2 promoter. However, the spatiotemporal mechanism of AtRBOHC/RHD2 subcellular redistribution and delivery to the plasma membrane (PM) during root hair initiation and tip growth are still unclear. Here, we used advanced microscopy for detailed qualitative and quantitative analysis of vesicular compartments containing GFP-RHD2 and characterization of their movements in developing bulges and growing root hairs. These compartments, identified by an independent marker such as the trans-Golgi network (TGN), deliver GFP-RHD2 to the apical PM domain, the extent of which correlates with the stage of root hair formation. Movements of TGN/early endosomes, but not late endosomes, were affected in the bulging domains of the rhd2-1 mutant. Finally, we reveal that accumulation in the growing tip, docking, and incorporation of TGN compartments containing GFP-RHD2 to the apical PM of root hairs requires structural sterols. These results help clarify the mechanism of polarized AtRBOHC/RHD2 targeting, maintenance, and recycling at the apical PM domain, coordinated with different developmental stages of root hair initiation and growth.One-sentence summaryAdvanced microscopy and quantitative analysis of vesicular TGN compartments revealed that delivering GFP-RHD2 to the apical plasma membrane domains of developing bulges and growing root hairs requires structural sterols.

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