Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum

Abstract

Summary Specific antibodies and enzyme–gold probes were used to study the structure and development of infection threads in nodules induced by Rhizobium leguminosarum on the roots of Vicia, Pisum and Phaseolus. In Pisum nodules, the tubular infection thread wall contains polysaccharides antigenically similar to those of the cell wall, including cellulose, xyloglucan, methyl‐esterified pectin and non‐esterified pectin, but none of these wall components is present around the infection droplet structures from which bacteria are internalized by plant plasma membrane. As reported previously for pea nodules, the luminal matrix of infection threads and infection droplets contains a plant glycoprotein; this glycoprotein is also secreted by infected and uninfected cortical cells of a Vicia root at the earliest stages of nodule initiation. Synthesis of a transcellular infection thread apparently involves reorganized deposition of components normally targeted to the cell wall, and infection thread growth is orientated anticlinally through the outer cortex in the same plane observed for the deposition of new cell walls following mitosis. Both the development of infection threads in the outer cortex and the initiation of cell division in the inner cortex are preceded by a similar process of cell reactivation involving centralization of nuclei and the development of anticlinal transvacuolar strands. It is therefore suggested that the two Rhizobium‐induced processes of infection thread growth and cortical cell division may both be consequences of a similar plant cell response in the inner and outer root cortex, respectively. Phaseolus nodules contained only short intracellular infection structures which terminated within individual cells and contained no luminal matrix material. The differences in infection thread structure between Pisum and Phaseolus nodules may reflect differences in ontogeny between “indeterminate” and “determinate” nodule meristems.

Development of N2‐fixing nodules on the wetland legume Lotus uliginosus exposed to conditions of flooding

“…As a very low O # concentration is necessary for the expression and function of nitrogenase (Gallon, 1992), it is essential that an O # -diffusion barrier be formed in young nodules before N # fixation can occur within them (Sheehy & Thornley, 1988) potential role of the MAC236\MAC265 glycoprotein in the formation of such a barrier has previously been shown in terrestrially grown lupin nodules by James et al (1997), and the pattern of localization shown by the present study suggests that it may have a similar function in Lotus nodules, even under the low O # concentrations created by flooding. Although large infection threads have been recently reported by Szczyglowski et al (1998) in young nodules of L. japonicus, most previous studies of the development of nodules on Lotus (Pankhurst et al, 1979 ;Vance et al, 1982 ;Wood et al, 1985) have suggested that infection threads and infection droplets are relatively scarce and fairly small structures, at least in comparison to indeterminate nodules such as those found on pea (Newcomb et al, 1979 ;Rae et al, 1992). However, the present study has shown that, for a short period during nodule development, there is massive proliferation of quite large infection threads within L. uliginosus, with many of them releasing MAC236-labelled material into host cells more or less simultaneously, and hence producing the dense immunolabelling shown in Fig.…”

“…3a-d. The amounts of MAC236-labelled material seen in the meristematic L. uliginosus nodules are reminiscent of the dense labelling (by MAC236 and\or MAC265) of infection threads and\or infection droplets observed in the invasion zone of indeterminate nodules on pea (VandenBosch et al, 1989 ;Rae et al, 1992) and Neptunia (James et al, 1992b), rather than the rather sparse labelling seen in other determinate nodules, such as those on soybean (VandenBosch et al, 1989), P. vulgaris (Rae et al, 1992) and Vigna subterranea (Gueye et al, 1998). In Lotus, the MAC236-labelled material released from infection threads along with the rhizobia probably corresponded to the material observed by Vance et al (1982), and Wood et al (1985), and which Vance et al (1982) considered to be at least partly composed of polysaccharide.…”

“…Particular attention has been focussed on the formation of N # -fixing nodules on flooded roots and stems, but the monoclonal antibodies MAC236 and MAC265 have also been used to examine the role of host-derived glycoprotein(s) in the development of determinate Lotus nodules. Until now these glycoproteins have been shown to be of importance only in the infection and development of indeterminate nodules (VandenBosch et al, 1989 ;Rae et al, 1992 ;James et al, 1992b).…”

“…MAC236 and MAC265 were first shown to recognize epitopes on a glycoprotein component of the infection thread matrix and the infection droplet of pea and soybean nodules, as well as material within cortical intercellular spaces (VandenBosch et al, 1989 ;Rae et al, 1991Rae et al, , 1992James et al, 1991James et al, , 1992b. VandenBosch et al (1989) and Rae et al Fig.…”

Tansley Review No. 82. Strategies of arbuscular mycorrhizal fungi when infecting host plants

“…The interfacial membrane in AMs seems to retain synthetic activity as indicated by the deposition of /?-l,4 glucans around the fungus (see IV.2), whereas the peribacteroid membrane surrounding rhizobia ceases its synthetic activity and no glucans are found at the interface with the bacterium (Rae, Bonfante & Brewin, 1992).…”