Differentiating friends from foes in the fungal root microbiome

Date:
December 10, 2021
Source:
Max Planck Institute for Plant Breeding Research
Summary:
A collaborative project has shed light on the fungal genetic
determinants that explain why some fungi from the root microbiome
can colonize roots and cause disease more efficiently than others.



FULL STORY ========================================================================== Complex microbial communities inhabit plants and modulate their
development.

Roots especially, host a wide diversity of micro-organisms -including
bacteria and fungi -that directly influence plant health. Researchers
from the MPIPZ previously discovered that these fungi are important
members of the root microbiome that can promote plant growth, but only
when they are kept in check by the combined action of the host innate
immune system and root-inhabiting bacteria.


==========================================================================
In a new study published in Nature Communications, Fantin Mesny and
co-authors provide novel insights into how these fungi colonize roots, why
many of them are potentially harmful and what differentiates beneficial
from pathogenic fungi in the root mycobiome (i.e., the fungal component
of the root microbiota).

To address these questions, the researchers focused on the model plant Arabidopsis thaliana (Thale Cress), which cannot rely on beneficial
mycorrhizal fungi to acquire nutrients since it does not harbour the
genetic network needed to establish a functional symbiosis with these
fungi. A. thaliana likely relies on other fungi to compensate for
the loss of mycorrhizal partners and to survive in nature. To better characterize these root-colonizing fungi in their broad diversity,
researchers have isolated a variety of fungal strains from the roots of
healthy plants across Europe and selected 41 that are representative of
the root mycobiome of A.thaliana.

In collaboration with INRAE Nancy (France) and the JGI (USA), the
genomes of these fungi were sequenced and compared to other fungi that
were previously described as saprotrophic, pathogenic, endophytic or mycorrhizal. Surprisingly, the scientists found that most root mycobiota members -- isolated from the roots of healthy plants -- derived from
ancestors that were likely pathogenic, and have retained a battery of
genes that were previously shown to be lost in genomes of beneficial mycorrhizal fungi. These genes encode effector-like small secreted
proteins that could modulate the host immune system, and enzymes that can degrade a large number of plant cell-wall constituents including pectin, cellulose and hemicellulose. These findings raised the possibility that
many of these fungi may have retained at least part of their ancestral pathogenic capabilities.

To test this hypothesis, A. thaliana plants were grown in a closed system
in the absence of any microorganism, or re-colonized with each of the
selected 41 fungal isolates. This experiment identified a wide diversity
of fungal effects on plant growth, ranging from highly detrimental to beneficial. Notably, the authors observed that the strains most harmful
to the plant were colonizing roots much more aggressively than those
having beneficial effects. Furthermore, the fungi most often detected
in the roots of A. thaliana in nature were also the ones showing harmful effects on their host in mono-association experiments.

Previous work from the group of Ste'phane Hacquard had suggested
that the mycobiome of A. thaliana can become detrimental when the host
immune system and the root-inhabiting bacteria do not tightly control the proliferation of these fungi. These new results show that in nature, fungi
with a high root-colonizing potential have a high pathogenic potential, explaining the need to control their growth.

Using a combination of association methods, including machine-learning
models, the authors then associated the fungal effects on
A. thalianagrowth to genome compositions, and successfully identified
a candidate gene family that could explain the detrimental effects and
root colonization abilities. This family (pectate lyase PL1_7) encodes
enzymes that degrade pectin, an essential constituent of plant cell
walls, which is especially abundant in the roots of dicotyledonous plants
such as A. thaliana. To validate its involvement in fungal detrimental activity, a gene from this family was introduced into the genome of a
fungal species that naturally does not harbour it. The resulting mutant
strain was able to colonize roots more aggressively than the original
isolate and this increase in fungal load in roots was associated with
a penalty on plant performance.

According to the last author of the study Ste'phane Hacquard, "These
results indicate that repertoires of plant cell-wall degrading enzymes in fungal genomes are key genetic determinants driving access to the root endosphere and explaining why robust root colonizers can potentially
become harmful if they degrade roots too aggressively." This study
highlighted that the mycobiome of healthy plants in nature is composed
of both friends and foes. This finding offers a new perspective on
the effects of fungi on plant health, and possibly opens the door to
new exciting considerations and developments for agriculture. Taking
advantage of these results could potentially provide a rationale on how
to design and optimize synthetic fungal communities to obtain beneficial outcomes on plant performance.

========================================================================== Story Source: Materials provided by Max_Planck_Institute_for_Plant_Breeding_Research. Note: Content may be
edited for style and length.


========================================================================== Journal Reference:
1. Fantin Mesny, Shingo Miyauchi, Thorsten Thiergart, Brigitte
Pickel, Lea
Atanasova, Magnus Karlsson, Bruno Hu"ttel, Kerrie W. Barry,
Sajeet Haridas, Cindy Chen, Diane Bauer, William Andreopoulos,
Jasmyn Pangilinan, Kurt LaButti, Robert Riley, Anna Lipzen,
Alicia Clum, Elodie Drula, Bernard Henrissat, Annegret Kohler,
Igor V. Grigoriev, Francis M.

Martin, Ste'phane Hacquard. Genetic determinants of endophytism
in the Arabidopsis root mycobiome. Nature Communications, 2021;
12 (1) DOI: 10.1038/s41467-021-27479-y ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2021/12/211210092829.htm

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