Figure 1.
Lotus japonicus plants
with (left) and
without (right) nitrogen fixing root nodules, showing the growth improvement caused by symbiosis with the Rhizobia bacteria.

A new discovery of a simpler single-cell infection mechanism may improve our understanding of how legumes control infection by the beneficial bacteria called Rhizobium and how they build root nodules in which the bacteria fix atmospheric nitrogen that can be used by the plants. This discovery may lead to the development of sustainable agriculture with reduced use of artificial fertilisers.

2010.04.13

Scientists from the Danish National Research Foundation's Centre for Carbohydrate Recognition and Signalling (CARB) at the Department of Molecular Biology, Aarhus University, have used the model legume Lotus japonicus to reveal how legume plants use three different mechanisms to control infection by symbiotic bacteria. Like other organisms, plants have mechanisms to fight pathogenic bacterial infection, but in this beneficial symbiotic interaction, entry of the bacteria is accepted. The bacteria are accommodated inside the plant cells, where they convert atmospheric nitrogen into ammonium, which is used by the plant as a nitrogen source. Consequently, this symbiotic interaction enables legumes to grow without nitrogen fertiliser (Figure 1).

High-resolution photos:

Fig. 1a

Fig. 1b

Most cultivated crop legumes normally allow a stringently controlled, sophisticated entry of bacteria through their root hair infection threads to infect the root tissue during the development of nitrogen fixing root nodules (Figure 2). The new research reveals a simpler single-cell infection mechanism that may be the first mechanism evolved for symbiosis in primitive legumes at the evolutionary emergence of the legume plant family. A detailed analysis of this simple single-cell infection therefore contributes to understanding the evolution of symbiotic nitrogen fixation. It also facilitates a step by step approach in future biotechnological strategies that investigate the possibilities for transferring symbiotic nitrogen fixation to crops such as cereals. In the long-term perspective, this could conserve reserves of fossil fuels and contribute to sustainable agriculture with less use of expensive nitrogen fertiliser.

Figure 2.

Left:
Cross section of a root nodule showing the Rhizobia bacteria (blue) accommodated inside the nodule.

Right:
Close-up of a root hair with an infection thread containing bacteria (blue) progressing towards the root nodule cells.
High-resolution photos:

Fig. 2a

Fig. 2b

Online with Nature Communications

The CARB scientists have just published their results in Nature Communications, a new journal launched by the Nature Publishing Group. Nature Communications is the first of the classical high impact journals to skip the paper print, and it represents a new concept for online-only publication of biological, physical and chemical science research results. The first online issue on 12 April 2010 features the work presented here.

Background

Nitrogen fixing symbiosis between legumes and the soil bacteria Rhizobium is established as a non-pathogenic bacterial infection of cells in the developing root nodule organ. This developmental process is controlled by the host legume, which has a genetic programme that synchronises two processes running in parallel: organ formation and bacterial infection. For the experimental scientists, this coordination made it difficult to separate the molecular mechanisms underlying these two very different plant developmental processes, and it especially limited the assignment of the specific role of plant genes governing the bacterial infection and organ formation.

Genetic dissection of symbiosis

The use of genetics has now made it possible to obtain an overall picture of a decade of gene discoveries identifying the legume genes required for symbiosis. The mechanistic role of a total of sixteen receptors and signal transduction components has been brought together in a functional framework coordinating infection and root nodule organ formation. Further studies focusing on the role of individual genes in the infection process revealed how the legume plant possesses three different mechanisms for controlling bacterial infection. The simplest and least effective version is an intercellular invasion followed by single-cell endocytosis, and this mechanism is proposed to be the ancient entry mechanism that founded symbiosis in the legume plants. Identifying the gene set that regulates single-cell infection may be the key to "the biotechnological jewel in the crown" - the design of symbiosis in plants such as cereals, which are currently unable to interact with rhizobial bacteria. The central questions that can now be addressed are: how many genes does the legume plant use to host the symbiotic bacteria, and what is the minimum gene set needed to build a primitive symbiotic system in a non-legume plant? These questions will be addressed by the CARB scientists in future studies.

Title of the article: The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus

Authors: Lene H. Madsen, Leïla Tirichine, Anna Jurkiewicz, John T. Sullivan, Anne B. Heckmann, Anita S. Bek, Clive W. Ronson, Euan K. James and Jens Stougaard

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