Unravelling new immunity-independent mechanisms for durable resistance to blast fungi using MAX effectors

Project Information

ii-MAX

Grant agreement ID: 852482

DOI

10.3030/852482

Project closed

EC signature date 11 October 2019

Start date 1 June 2020

End date 31 May 2026

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 499 875,00

EU contribution

€ 1 499 875,00

Coordinated by

INSTITUT NATIONAL DE RECHERCHE POUR L'AGRICULTURE, L'ALIMENTATION ET L'ENVIRONNEMENT
France

Periodic Reporting for period 3 - ii-MAX (Unravelling new immunity-independent mechanisms for durable resistance to blast fungi using MAX effectors)

Reporting period: 2023-06-01 to 2024-11-30

Summary of the context and overall objectives of the project

Crop diseases induced by plant pathogens (bacteria, viruses, fungi, etc.) are a major problem in agriculture. A typical example is the blast disease, which is caused by the fungus Magnaporthe oryzae and is recognised as the most destructive disease of rice and a major threat to wheat production and global food security. Facing the challenge of a growing world population, it is essential to improve crop protection against these diseases and thereby increase crop yield.

Helping our crops stay healthy requires a thorough understanding of their immune systems and the strategies deployed by pathogens to attack them. The ii-MAX project is making a significant contribution to this by elucidating the biological function and molecular mode of action of key fungal virulence factors called effectors. Effectors of plant pathogenic fungi are small proteins secreted during plant infection that act as molecular weapons to disrupt host defences and metabolism to promote host colonisation and disease development.

A few years ago, our team discovered a large family of effectors that represents so far the most diversified and important arsenal of molecular weapons identified in M. oryzae: the MAX effector family. MAX effectors may play a key role in the infectious process of M. oryzae, but this role is still unknown and the mechanisms of the host plant targeted by these effectors have not been defined.

In this context, the ii-MAX project aims to elucidate the biological function of MAX effectors by characterising the cellular and molecular processes they target in cereals. To this end, we are identifying and studying the plant proteins that are targeted during infection by MAX effectors. These target proteins will be characterised structurally and functionally to uncover the plant cellular mechanisms required for fungal disease development and identify new ways to protect cereal crops against these diseases. The results of this research will contribute to better protection of crops against fungal pathogens, thus promoting sustainable agriculture.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

Since the start of the project, we have collaborated with the group of Pierre Gladieux (PHIM, France) to identify the arsenal of MAX effectors present in the genomes of more than a hundred strains of M. oryzae capable of infecting different cereal species in a specific manner. This work has allowed us to study how MAX effectors evolve and diversify in M. oryzae. In particular, it shows that MAX effectors constitute a very dynamic compartment of the M. oryzae genome, potentially reflecting intense co-evolutionary interactions with host proteins. It also enabled the identification of MAX effectors that are present in all strains of M. oryzae, and that are potentially crucial to the infectious process.

We have also identified the MAX effectors that are deployed during the early stages of rice colonisation. Thus, we know that more than half of the MAX effectors present in a M. oryzae isolate are specifically expressed during this phase. MAX effectors are therefore largely deployed during infection.

For many of these effectors, we have identified, through several complementary experimental approaches, potential targets in the host plant, i.e. rice proteins that interact with MAX effectors and may be manipulated by the pathogen to promote infection. These targets could play a role in plant immunity or susceptibility. Our results indicate that MAX effectors interact with a wide variety of host proteins and thereby potentially target many molecular processes in rice, and potentially in other cereals. We also show that several MAX effectors appear to play redundant roles in the infection process.

We are now initiating the validation of the most interesting targets and their functional analysis in order to define their role in the establishment of the blast disease. We are also conducting, together with the group of André Padilla (CBS, France), modelling analyses of the 3D structure of MAX effectors interacting with their host targets to gain a better understanding of how MAX effectors, which have a conserved 3D structure, can interact with a wide range of host proteins.

These analyses will allow us to identify the rice proteins targeted during infection by MAX effectors and necessary for disease development. Specific modification of these targets will allow to improve rice resistance to blast.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Knowledge of the role of fungal effectors, and in particular that of M. oryzae effectors, is currently limited. The extreme diversity of effector sequences has prevented the identification of defined effector families and hindered the investigation of their function since there were no good selection criteria for prioritising the effectors.

Recent analyses of the resolution and/or prediction of the three-dimensional structure of fungal effectors have highlighted a small number of fungal effector families, such as the MAX family. It therefore appears that behind their extreme sequence diversity lies a limited number of effector families that can be defined according to a 3D structure conservation criterion.

The reasons for this diversification are currently not understood, but the structural conservation of MAX effectors indicates that they share a common origin. Due to their diverse surface properties, we believe that MAX effectors may interact with different proteins within the host and alter multiple mechanisms of plant immunity or susceptibility. That is why the ii-MAX project is ambitious and goes beyond the state of the art, as it is the first study that aims to elucidate the function of an entire family of fungal effectors.

The data acquired so far in the project indicate that MAX effectors interact with a variety of host proteins that could play very diverse roles during infection. In the next steps of the project, we will study the function of these host proteins as well as their structure in order to modify those required for disease development and thereby improve rice resistance to blast.

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