<i>Casuarina glauca</i> Prenodule Cells Display the Same Differentiation as the Corresponding Nodule Cells

Laplaze, Laurent; Duhoux, Emile; Franche, Claudine; Frutz, Thierry; Svistoonoff, Sergio; Bisseling, Ton; Bogusz, Didier; Pawlowski, Katharina

doi:10.1094/mpmi.2000.13.1.107

Cited by 58 publications

(27 citation statements)

References 33 publications

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“…involve the formation of a prenodule so that the initial epidermal infection and lateral organ development programs are separate both temporally and spatially. It has been proposed that these independent processes present in actinorhizal nodulation have been merged together in legumes (Gualtieri and Bisseling, 2000;Laplaze et al, 2000). Our finding that physical separation of infection from the emerging nodule leads to the development of nodules with a central vascular arrangement supports this hypothesis.…”

Section: Implications For Nodule Evolutionsupporting

confidence: 82%

Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules ofMedicago truncatula

et al. 2013

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Nodulation in legumes involves the coordination of epidermal infection by rhizobia with cell divisions in the underlying cortex. During nodulation, rhizobia are entrapped within curled root hairs to form an infection pocket. Transcellular tubes called infection threads then develop from the pocket and become colonized by rhizobia. The infection thread grows toward the developing nodule primordia and rhizobia are taken up into the nodule cells, where they eventually fix nitrogen. The epidermal and cortical developmental programs are synchronized by a yet-to-be-identified signal that is transmitted from the outer to the inner cell layers of the root. Using a new allele of the Medicago truncatula mutant Lumpy Infections, lin-4, which forms normal infection pockets but cannot initiate infection threads, we show that infection thread initiation is required for normal nodule development. lin-4 forms nodules with centrally located vascular bundles similar to that found in lateral roots rather than the peripheral vasculature characteristic of legume nodules. The same phenomenon was observed in M. truncatula plants inoculated with the Sinorhizobium meliloti exoY mutant, and the M. truncatula vapyrin-2 mutant, all cases where infections arrest. Nodules on lin-4 have reduced expression of the nodule meristem marker MtCRE1 and do not express root-tip markers. In addition, these mutant nodules have altered patterns of gene expression for the cytokinin and auxin markers CRE1 and DR5. Our work highlights the coordinating role that bacterial infection exerts on the developing nodule and allows us to draw comparisons with primitive actinorhizal nodules and rhizobia-induced nodules on the nonlegume Parasponia andersonii.

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Section: Implications For Nodule Evolutionsupporting

confidence: 82%

Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules ofMedicago truncatula

et al. 2013

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“…The Frankia CcI3 genome is completely sequenced (22), and it represents a narrow-host-range symbiont. The relationship between the plant host and symbiont, including the nodulation process, is well studied (17,18,27,35,41). The purpose of this study was to develop a system to identify chemical signaling between the microbe and its host plant.…”

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confidence: 99%

Casuarina Root Exudates Alter the Physiology, Surface Properties, and Plant Infectivity of Frankia sp. Strain CcI3

Beauchemin

Furnholm

Lavenus

et al. 2012

Appl Environ Microbiol

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The actinomycete genus Frankia forms nitrogen-fixing symbioses with 8 different families of actinorhizal plants, representing more than 200 different species. Very little is known about the initial molecular interactions between Frankia and host plants in the rhizosphere. Root exudates are important in Rhizobium-legume symbiosis, especially for initiating Nod factor synthesis. We measured differences in Frankia physiology after exposure to host aqueous root exudates to assess their effects on actinorhizal symbioses. Casuarina cunninghamiana root exudates were collected from plants under nitrogen-sufficient and -deficient conditions and tested on Frankia sp. strain CcI3. Root exudates increased the growth yield of Frankia in the presence of a carbon source, but Frankia was unable to use the root exudates as a sole carbon or energy source. Exposure to root exudates caused hyphal "curling" in Frankia cells, suggesting a chemotrophic response or surface property change. Exposure to root exudates altered Congo red dye binding, which indicated changes in the bacterial surface properties at the fatty acid level. Fourier transform infrared spectroscopy (FTIR) confirmed fatty acid changes and revealed further carbohydrate changes. Frankia cells preexposed to C. cunninghamiana root exudates for 6 days formed nodules on the host plant significantly earlier than control cells. These data support the hypothesis of early chemical signaling between actinorhizal host plants and Frankia in the rhizosphere.A ctinorhizal symbioses are mutualistic interactions that occur between actinorhizal plants and the actinomycete genus Frankia (27,38). Frankia exists either in a free-living state in the soil or in symbiosis with actinorhizal plants (2, 4, 31). Actinorhizal plants consist of 8 different plant families, including over 200 different species of woody dicotyledonous trees and shrubs (31,38,42). The globally distributed actinorhizal plants are found on every continent except Antarctica and are able to grow in a diverse set of natural habitats, including arid lands, plains, tundra, and temperate forests. Actinorhizal plants are pioneer plant species that are able to grow in extremely nutrient-poor soil conditions and, with the aid of Frankia, are able to reclaim surrounding soil in disrupted environments. Actinorhizal plants are important in agroforestry, in soil reclamation, and as a fuel source.While actinorhizal symbiosis has been well studied at a morphological level since the 1970s, very little is known about the molecular interactions that occur between the plant hosts and Frankia during the establishment of the association. The establishment of the symbiosis encompasses the infection and nodulation processes (23,27,38). In general, the bacterium needs to recognize a host plant and the host needs to identify the bacterium as a friend, not a foe. The bacteria enter the plant and establish the association after several steps. The infection ultimately leads to the formation of the mature nodule.There is a paucity of information o...

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“…At the same time, limited cell divisions are triggered in the cortex, creating a so-called prenodule. Prenodule function is not known, but it is an obligatory step of intracellular infection (Laplaze et al, 2000). Concomitantly, cell divisions occur in the pericycle in front of the xylem pole leading to the formation of a nodule lobe primordium.…”

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confidence: 99%

Auxin Influx Activity Is Associated with Frankia Infection during Actinorhizal Nodule Formation in Casuarina glauca

et al. 2007

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Plants from the Casuarinaceae family enter symbiosis with the actinomycete Frankia leading to the formation of nitrogen-fixing root nodules. We observed that application of the auxin influx inhibitor 1-naphtoxyacetic acid perturbs actinorhizal nodule formation. This suggests a potential role for auxin influx carriers in the infection process. We therefore isolated and characterized homologs of the auxin influx carrier (AUX1-LAX) genes in Casuarina glauca. Two members of this family were found to share high levels of deduced protein sequence identity with Arabidopsis (Arabidopsis thaliana) AUX-LAX proteins. Complementation of the Arabidopsis aux1 mutant revealed that one of them is functionally equivalent to AUX1 and was named CgAUX1. The spatial and temporal expression pattern of CgAUX1 promoter:b-glucuronidase reporter was analyzed in Casuarinaceae. We observed that CgAUX1 was expressed in plant cells infected by Frankia throughout the course of actinorhizal nodule formation. Our data suggest that auxin plays an important role during plant cell infection in actinorhizal symbioses.

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Casuarina glauca Prenodule Cells Display the Same Differentiation as the Corresponding Nodule Cells

Cited by 58 publications

References 33 publications

Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules ofMedicago truncatula

Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules ofMedicago truncatula

Casuarina Root Exudates Alter the Physiology, Surface Properties, and Plant Infectivity of Frankia sp. Strain CcI3

Auxin Influx Activity Is Associated with Frankia Infection during Actinorhizal Nodule Formation in Casuarina glauca

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