Regulation of antimicrobial and host-targeting effector proteins in beneficial and pathogenic root-associated fungi

The project will be supervised by Alga Zuccaro at the University of Cologne.

Abstract:

In nature, plants associate with a multitude of microorganisms collectively referred to as the plant
microbiome. The composition of this microbiome varies between different plant species and
depends on environmental factors such as soil quality, humidity and temperature. A balanced
microbiome confers numerous benefits to its host, including protection against pathogens,
improved nutrient acquisition and resilience to abiotic stress. These remarkable symbiotic
interactions have evolved over millions of years leading to finely tuned relationships not only
between microbes and their hosts but also among the microbiome's diverse members. Notably,
these intricate inter-microbial relationships have direct repercussions on plant health. This is
vividly illustrated by microorganisms which exhibit a high pathogenic potential in mono-culture but
can be effectively restrained as part of a balanced microbial community. In order to maintain this
balance, microbiome members have developed mechanisms to defend their niche, and by
extension their host, against outsiders. The beneficial root endophyte Serendipita vermifera (S.
vermifera) for instance acts synergistically with bacterial members of the plant microbiome to
protect barley against the pathogenic fungus Bipolaris sorokininana (B. sorokiniana). While
microbes employ diverse strategies to outcompete their rivals, including interference with host
immunity and resource sequestration, S. vermifera seems to take a more direct approach. Its
beneficial effects are not intricately linked with extensive host transcriptional reprogramming.
Instead, they are associated with the modulation of the expression of secreted microbial effectors.

Originally, effectors were described in the context of host colonization. Their secretion was
observed to play a role in suppressing host defences and disrupting the host cell machinery to
facilitate colonization and microbial reproduction. However, recent discoveries have unveiled an
intriguing addition to our understanding of microbial competition: the deployment of specialized
antimicrobial effectors. The aggressive soil-born pathogen Verticiullium dahlia for instance
secretes the virulence effector VdAve1 which displays antimicrobial activity and facilitates
colonization of tomato and cotton through the manipulation of their microbiomes by suppressing
antagonistic bacteria.

The revelation that effectors can be directed against other microbes presents exciting prospects
for sustainable agriculture. Understanding how beneficial fungi employ effectors to defend their
niches against pathogens could lead to innovative strategies for crop protection and might help
to fully harness the potential of synthetic microbial communities. While more and more effectors
are identified in both pathogenic and beneficial microbes, two pivotal questions remain
unanswered:

Which transcriptional regulatory mechanisms control effector expression in response to
host colonization or the presence of competing microbes?
Are these mechanisms conserved among microbes with different lifestyles?

Key publication: Mahdi LK, Miyauchi S, Uhlmann C, Garrido-Oter R, Langen G, Zuccaro A (2021). The fungal
root endophyte Serendipita vermifera displays inter-kingdom synergistic beneficial effects with
the microbiota in Arabidopsis thaliana and barley. The ISME Journal 16, 1-14.
doi:10.1038/s41396-021-01138-y.

Link to the Zuccaro group homepage: https://ag-zuccaro.botanik.uni-koeln.de/