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

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

The Plant Cell ◽

10.1105/tpc.114.135210 ◽

2015 ◽

Vol 27 (3) ◽

pp. 806-822 ◽

Cited By ~ 22

Author(s):

Ming-Juan Lei ◽

Qi Wang ◽

Xiaolin Li ◽

Aimin Chen ◽

Li Luo ◽

...

Keyword(s):

Medicago Truncatula ◽

Root Hair ◽

Tip Growth ◽

Root Hairs ◽

Small Gtpase ◽

Nod Factor ◽

Root Hair Deformation

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Biological activity of Nod factors

Acta Biochimica Polonica ◽

10.18388/abp.2020_5353 ◽

2020 ◽

Author(s):

Dominika Kidaj ◽

Mikolaj Krysa ◽

Katarzyna Susniak ◽

Joanna Matys ◽

Iwona Komaniecka ◽

...

Keyword(s):

Molecular Level ◽

Root Nodules ◽

Cortical Cell ◽

Plant Tissues ◽

Nod Factors ◽

Nod Factor ◽

Expression Of Genes ◽

Root Hair Deformation ◽

Low Concentrations ◽

Genes Encoding

Chemically, the Nod factors (NFs) are lipochitooligosaccharides, produced mainly by bacteria of the Rhizobium genus. They are the main signaling molecules involved in the initiation of symbiosis between rhizobia and legume plants. Nod factors affect plant tissues at very low concentrations, even as low as 10–12 mol/L. They induce root hair deformation, cortical cell division, and root nodules’ formation in the host plant. At the molecular level, the cytoskeleton is reorganized and expression of genes encoding proteins called nodulins is induced in response to Nod factors in the cell. Action of Nod factors is highly specific because it depends on the structure of a particular Nod factor involved, as well as the plant receptor reacting with it.

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Structural and functional comparison of Frankia root hair deforming factor and rhizobia Nod factor

Canadian Journal of Botany ◽

10.1139/b99-060 ◽

1999 ◽

Vol 77 (9) ◽

pp. 1293-1301 ◽

Cited By ~ 13

Author(s):

Hélène Cérémonie ◽

Frédéric Debellé ◽

Maria P Fernandez

Keyword(s):

Root Hair ◽

Nod Factors ◽

Frankia Strain ◽

Nod Factor ◽

Combined Nitrogen ◽

Nitrogen Effect ◽

Root Hair Deformation ◽

Butanol Extraction ◽

Layer Chromatography

The infectious processes of the Frankia-Alnus and Rhizobium-legume symbioses present strong similarities, suggesting the existence of analogies between Frankia root hair deforming factor and rhizobia Nod factors. Biochemical and functional analogies were tested using ACoN24d Frankia strain. The putative chitin-like nature of the Frankia deforming factor was explored by (i) gas chromatography coupled to mass spectrometry and thin layer chromatography, after radioactive labeling of the culture for detection of chitin oligomers, and (ii) following the root hair deforming activity of the supernatant after discriminating treatments (temperature, chitinase, butanol extraction). In parallel, the functional analogy was questioned by testing the mitotic activity of the Frankia supernatant onAlnus glutinosa (L.) roots. The implication in the symbiotic process of the Frankia factor was indirectly explored by testing the effect of a nodulation inhibitor (combined nitrogen) on root hair deformation. The studies of the combined nitrogen effect on root hair deformation indicate that the deformation induced in vitro by the Frankia factor is linked to the symbiotic process. Moreover, the various approaches used suggest that rhizobia Nod factors and Frankia root hair deforming factor are two structurally divergent symbiotic factors. However, functionnal differences between Frankia root hair factor and the Nod factors have to be confirmed.Key words: Frankia, root hair deforming factor, Nod factor, actinorhizal plants.

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Nod Factors Alter the Microtubule Cytoskeleton in Medicago truncatula Root Hairs to Allow Root Hair Reorientation

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-18-1195 ◽

2005 ◽

Vol 18 (11) ◽

pp. 1195-1204 ◽

Cited By ~ 40

Author(s):

Björn J. Sieberer ◽

Antonius C. J. Timmers ◽

Anne Mie C. Emons

Keyword(s):

Medicago Truncatula ◽

Root Hair ◽

Tip Growth ◽

Root Hairs ◽

High Density ◽

Nod Factors ◽

Microtubule Cytoskeleton ◽

Nod Factor ◽

Set Up ◽

Drug Studies

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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Rhizobial Nod factors are required for cortical cell division in the nodule morphogenetic programme of the Aeschynomeneae legume Arachis

Plant Biology ◽

10.1111/j.1438-8677.2010.00439.x ◽

2011 ◽

Vol 13 (5) ◽

pp. 794-800 ◽

Cited By ~ 15

Author(s):

F. Ibáñez ◽

A. Fabra

Keyword(s):

Cell Division ◽

Cortical Cell ◽

Nod Factors

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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 plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

eLife ◽

10.7554/elife.38874 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 9

Author(s):

Anna Malolepszy ◽

Simon Kelly ◽

Kasper Kildegaard Sørensen ◽

Euan Kevin James ◽

Christina Kalisch ◽

...

Keyword(s):

Root Nodules ◽

Lotus Japonicus ◽

Positional Information ◽

Dependent Manner ◽

Nitrogen Fixing ◽

Nod Factors ◽

Nod Factor ◽

Infection Threads ◽

Bacterial Mutants ◽

Multicellular Organisms

Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.

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