Some plants can survive without nitrogen fertilizer. Where does this amazing ability come from? – The conversation

Nitrogen fertilizers form one of the pillars of the agricultural revolution of the 20th century and have become essential for maintaining current high agricultural yields.

These fertilizers are made by removing gaseous nitrogen from the air. Since nitrogen gas is a very stable chemical molecule, its conversion into fertilizer requires an enormous amount of energy, which is provided through the use of hydrocarbons, thus contributing to the creation of greenhouse gases. In addition, fertilizers added to the soil are often washed away by heavy rainfall and carried into bodies of water, where they promote algae growth and suffocate other living organisms (eutrophication phenomenon).

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Soybean field. Paulo Nabas

Therefore, the environmental costs of nitrogen fertilizers – whether industrial or in the form of manure – are significant, which is why reducing their use by 2030 is a priority for global agriculture.

However, some plants can survive without nitrogen fertilizer. These plants belong to four major botanical groups, including the legume group, which includes plants such as peas, beans, lentils, soy, peanuts, but also certain trees (acacia, mimosa or other locusts). As in the industrial chemical process, these plants obtain much of the nitrogen they need directly from the air… thanks to symbiosis with bacteria that live on the roots.

For many years, scientists have wondered how this connection between plants and bacteria might have evolved. Although such an understanding might make it possible in the future to transfer the ability to spontaneously absorb nitrogen to other species – and thus massively limit the use of fertilizers while maintaining high yields – the feasibility of such an approach has not yet been proven.

In our study recently published in Nature Plants, we analyzed the way several legumes interact with their symbiotic bacteria to trace the evolutionary history of these interactions.

A symbiosis within a committed committee

In legumes, bacteria live in symbiosis with these plants and convert gaseous nitrogen into ammonium that the plant can use. This type of symbiosis, called “mutualistic,” generally occurs in all living things and results from the interaction between two organisms that mutually enhances their growth and development.

This symbiosis takes place in a specific organ at the root of the plant, a so-called “nodule,” which houses the bacteria and supplies ammonium. The partners also exchange complex chemical signals.

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Nodule formed on the root system of Mimosa pudica plant. Catherine Masson

In search of the origin of nodulating symbiotic plants

Given the diversity of current symbiotic plants, it is difficult to know which physiological and genetic properties are necessary and sufficient for nitrogen-fixing symbiosis. Distinguishing ancestral traits from those that appeared more recently in symbiotic plants should make it possible to determine the “genetic recipe” of this association.

By comparing the genomes of several plants capable or not of achieving nitrogen fixation symbiosis, previous work has shown that all symbiotic plants share a group of common genes that are essential for this association… However, these genes are also present in certain plants that are unable to fix nitrogen. symbiotic.

Over the course of evolution, the emergence of a symbiosis would therefore not be associated with the acquisition of new genes, but rather with a change in the expression (or activity) of this group of common symbiotic genes.

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Peanuts. Sahil Ghosh

Even if all cells in an organism have the same genes, their activity varies greatly from cell to cell, depending on environmental conditions (including, for example, the proximity of microorganisms) and depending on the stage of development. Thus, legumes would have acquired the ability to achieve nitrogen-fixing symbiosis by reusing genes involved in various physiological processes (formation of lateral roots, interaction with beneficial fungi, etc.) and by increasing their expression during interaction with symbiotic ones Bacteria activated.

We tried to trace this process of “molecular tinkering,” as the biologist François Jacob called it.

When plants develop from a common ancestor thanks to “molecular tinkering”.

We therefore decided to compare the genes that are specifically activated in the nodules of nine plant species that can enter into this symbiosis.

More specifically, our aim was to identify genes that are commonly expressed during symbiosis in all of these species.

We observed that nearly a thousand genes were co-expressed in the nodules of the nine symbiotic plants examined. The most likely explanation for this similarity is that these different species inherited this genetic program that enables nodule formation and function from their common ancestor, a “symbiotic ancestor” that lived on Earth about 90 million years ago.

Thanks to the knowledge of these symbioses acquired elsewhere, we have been able to identify in this list numerous plant genes that allow plants to sense the chemical signals produced by their symbiotic bacteria, welcome them into their tissues and carry out the molecular processes that supply nitrogen to the air revoke.

Thus, the “symbiotic ancestor” was certainly able to carry out these three steps, essential for the functioning of the symbiosis, through molecular mechanisms based on the activity of this group of shared genes.

family tree

Simplified phylogenetic tree representing the major events associated with the evolution of nodulation. Pierre-Marc Delaux, provided by the author

Improvements that have arisen independently of each other over the course of evolution

But evolution never stops: certain plants that descended from this common symbiotic ancestor have lost the ability to enter into this symbiosis. Others, however, have developed special symbiotic abilities, symbiotic “adaptations,” which allow them, for example, to enter into symbiosis with different types of bacteria or under certain environmental conditions.

We therefore wondered whether we could tell when these adaptations had occurred in evolution.

To do this, we focused on two plants (Mimosa pudica and Medicago truncatula) and examined the genes involved in the symbiosis of these plants without being expressed in the common ancestor. In fact, plants belonging to the two largest legume families (represented by M. pudica and M. truncatula) have lost very little of their symbiotic ability and are still able to form nodules today.

Recently, it has been proposed that the stability of this symbiotic ability throughout the evolution of these plants is related to the ability of these plants to host bacteria within plant cells themselves, in structures called “symbiosomes.”

For these two plants, we have a detailed description of the gene expression associated with each step of the process of nodulation, symbiosome formation, and nitrogen fixation.

We found that a large number of genes associated with symbiosome formation are specific to each of these two plant species. In other words, these genes were not present in the nodule of their common ancestor, and so the ability to accommodate bacteria into nodule cells arose (evolved) independently in M. pudica and M. truncatula.

These symbiotic “adaptations” may therefore have converged on the same mechanism, control of the symbiont, but using different molecular processes. Future work should make it possible to test this hypothesis.