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Environmental Research

Plant Symbioses: Fragile Partnerships

Symbioses between plants and nitrogen-fixing bacteria can be ecologically advantageous for both parties. Surprisingly, many partnerships, including some involving the ancestors of several modern fruits such as strawberries, blackberries and apples, have been dissolved during evolution. This is reported by scientists from the Helmholtz Zentrum München together with colleagues from the Ludwig-Maximilians-Universität München (LMU) in 'Science'.

Root nodules. Source: C. Cathebras, LMU

All plants require an adequate supply of inorganic nutrients, such as fixed nitrogen (usually in the form of ammonia or nitrate), for growth. A special group of flowering plants thus depend on close symbiotic relationships with nitrogen-fixing bacteria as a source of fixed nitrogen. The plant provides specialized root nodules as ‘housing’ for its bacterial benefactors, which allows them to make use of energy-rich organic carbon compounds in return for the ammonia they generate from atmospheric nitrogen. Thus, both partners reap advantages from the relationship. Nevertheless, a comparative study of 37 plant genomes carried out by Munich molecular biologists in cooperation with French and Chinese colleagues, demonstrates that the capacity to form root-nodule partnerships has repeatedly been lost during the course of evolution.

The ability to form root nodules in response to the presence of nitrogen-fixing bacteria is currently restricted to four orders of flowering plants (Fabales, Fagales, Cucurbitales and Rosales), to which many agriculturally significant species – including beans, peas and soy bean – belong. The authors of the new study therefore assumed that the genetic basis for this type of symbiosis initially evolved in a common ancestor of these groups. “However, only 10 of the 28 plant families that make up these four orders are now able to form nitrogen-fixing root nodules. Moreover most of the genera in nine of these families do not adopt the symbiotic lifestyle,” says LMU geneticist Professor Martin Parniske, who initiated the international collaboration.

In order to identify the genetic grounds for the relatively low incidence of root nodule symbioses among the plant families in which it occurs, the consortium collected DNA samples and the BGI in China sequenced the entire genome of 10 species that form distinct types of nodules with diverse bacterial symbionts, which in turn employ different infection strategies. In close cooperation with LMU and the Plant Genome and Systems Biology Research Unit (PGSB) at the Helmholtz Zentrum München, the genomic sequence data for these species were then included in a genome-wide comparison of 37 plant species representing the four orders mentioned above. Much to everyone’s surprise, the analyses revealed that many members of these groups – including well known cultivars such as strawberries, blackberries and apples – had once possessed, but subsequently lost the capacity to form symbioses.

“We discovered that the gene NODULE INCEPTION (NIN), which is an essential prerequisite for root nodule symbiosis, has been repeatedly and independently disabled by mutation in several different lineages. The functional gene was therefore most probably present in a common ancestor of these lines, but was later lost several times independently,” explains first author Maximilian Griesmann, doctoral student at LMU who worked closely together with Manuel Spannagl, Georg Haberer and Klaus F.X. Mayer, head of PGSB and also TUM professor, on the genetic analyses. “These findings were completely unexpected. In many terrestrial ecosystems, low nitrogen availability is a factor limiting plant growth, so that one would expect the symbiosis to be associated with a definite selective advantage,” adds Parniske.

According to the paper’s authors, one possible reason for the frequent breakdown of these symbioses is that root nodules can be invaded by parasitic bacteria which compete for, and consume the compounds provided by the plants without supplying nitrogen in return. In that case, loss of the symbiosis should effectively be favored as an evolutionary adaptation that enables the plant to escape this form of exploitation. Other scenarios in which the symbiosis no longer benefits the host are also conceivable, such as a persistent oversupply of nitrogen or situations in which the availability of other essential substances – like water or phosphates – constrains plant growth.

In the field of synthetic biology, efforts to equip non-symbiotic crop plants with the ability to establish root-nodule symbioses are underway, with a view to reducing the need to supply fixed nitrogen by applying environmentally problematic fertilizers. “Our results suggest that evolution exerts a selective pressure against the maintenance of root-nodules symbioses, and future studies need to take this factor into account,” Mayer points out.

“Moreover, the ten newly sequenced and annotated plant genomes in this study, close previous gaps in the genealogical tree of plants and thus for the first time permit comparative analyzes of a large evolutionary and physiological area”, says Spannagl.

Further Information

Original Publication:
Griesmann, M. et al. (2018): Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis. Science, DOI: 10.1126/science.aat1743

As German Research Center for Environmental Health, Helmholtz Zentrum München pursues the goal of developing personalized medical approaches for the prevention and therapy of major common diseases such as diabetes mellitus, allergies and lung diseases. To achieve this, it investigates the interaction of genetics, environmental factors and lifestyle. The Helmholtz Zentrum München has about 2,500 staff members and is headquartered in Neuherberg in the north of Munich. Helmholtz Zentrum München is a member of the Helmholtz Association, a community of 19 scientific-technical and medical-biological research centers with a total of about 37,000 staff members. 

The Research Unit Plant Genome and Systems Biology (PGSB) focuses on the analysis of plant genomes, using bioinformatic techniques. To store and manage the data, we developed a database, PlantsDB, that aims to provide a data and information resource for individual plant species. In addition PlantsDB provides a platform for integrative and comparative plant genome research. 

As one of Europe's leading research universities, LMU Munich is committed to the highest international standards of excellence in research and teaching. Building on its 500-year-tradition of scholarship, LMU covers a broad spectrum of disciplines, ranging from the humanities and cultural studies through law, economics and social studies to medicine and the sciences. 15 percent of LMU‘s 50,000 students come from abroad, originating from 130 countries worldwide. The know-how and creativity of LMU's academics form the foundation of the University's outstanding research record. This is also reflected in LMU‘s designation of as a "university of excellence" in the context of the Excellence Initiative, a nationwide competition to promote top-level university research.