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Priority Programme: Deconstruction and Reconstruction of the Plant Microbiota, DECRyPT

 

Coordinator:

Prof. Alga Zuccaro, Ecological Genetics of Microbes, University of Cologne. Molecular Plant-Microbe Interactions.

Programme committee:

1. Prof. Oliver Bossdorf, Institute of Evolution and Ecology, University of Tübingen. Plant Evolutionary Ecology.
2. Prof. Jane Parker, Max Planck Institute for Plant Breeding Research, Cologne. Plant Immunity.
3. Prof. Martin Parniske, LMU Munich. Symbiotic Interactions.
4. Prof. Paul Schulze-Lefert, Max Planck Institute for Plant Breeding Research, Cologne. Microbiota Reconstitution Biology.
5. Prof. Detlef Weigel, Max Planck Institute for Developmental Biology, Tübingen. Evolutionary Genomics.
6. Prof. Alga Zuccaro, Ecological Genetics of Microbes, University of Cologne. Molecular Plant-Microbe Interactions.

External advisor:

Prof. Corné Pieterse, University of Utrecht.

Summary

The central scientific objectives of this priority programme (SPP) are to obtain deep and potentially predictive insights into plant-microbiota associations and to develop pioneering reductionist approaches towards a molecular understanding of plant microbiota functions. This SPP will elucidate genetic factors underlying plant microbiota establishment, test presumed community adaptation in ecological contexts and define community-associated emergent properties. Computational and genomic tools will guide hypothesis-testing and the design of microbiota reconstitution experiments in controlled environments.

Justification of an SPP on Deconstruction and Reconstruction of the Plant Microbiota

In nature, root and leaf organs of healthy plants engage in intimate associations with an enormous diversity of microbes belonging to different classes, including bacteria, fungi, oomycetes, viruses and protists. Collectively, the microbial assemblage of a healthy plant is called the ‘plant microbiota’ and the sum of the microbial genomes denoted the ‘plant microbiome’. It is widely believed that plant-derived photosynthates and other organic metabolites serve as substrates for proliferation of the plant associated microbial communities, by root exudation into the surrounding soil and extracellular transport into the apoplastic space or by provision of cell wall carbohydrates. Numerous reports have shown beneficial functions of individual members of these microbial assemblages for the plant host, including nutrient mobilization and uptake from marginal soils, and indirect protection against plant pathogens or abiotic stress tolerance, e.g. drought tolerance. However, lack of fundamental knowledge on microbe-microbe and microbe-host associations in these assemblages makes it currently impossible to predict whether individual members of the microbiota retain their beneficial activities in a microbial community context. Plant health and performance-related fitness phenotypes mediated by members of the plant microbiota challenge current concepts of plant-microbe co-evolution. Selection operates on phenotypes, which raises the question whether plants evolve as individuals by individual selection or with their associated microbes. Although extensive evidence supports the co-evolution of binary interactions between hosts and individual pathogenic microbes, it remains contentious whether genomic signatures exist for microbial community–related fitness phenotypes in the host genome and its associated microbiome. One proposal is to consider the multicellular host plus its associated microbes as a functional entity called the ‘holobiont’ to better understand plant fitness and plant adaptation in ecological contexts. Accordingly, the hologenome theory of evolution posits that evolution acts on the collective genomes of holobionts.


To establish compatibility with a multicellular host, plant-associated microbes have evolved diverse colonization strategies with distinct morphological, functional and genomic specializations as well as different degrees of interdependence. Microbes in these binary interactions can be host-specific or display a broad host range and the interactions are usually stable. To establish and maintain a compatible interaction, the plant host as well as the microbes must respond to and adapt to different signals. Alternative lifestyle and colonization strategies (e.g. symbiotic/mutualistic, commensalistic, exploitative, cooperative, antagonistic) may be a consequence of this adaptation to variable environments. The existence of a microbiota associated with healthy plants poses an apparent paradox in view of the widely accepted concept of the plant innate immune system which recognizes and actively defends against proliferation of diverse pathogens and parasites. Thus, an important unanswered question is how the innate immune system tolerates colonization of plant hosts by individual beneficial microbes or microbial communities. One idea we will test is that the innate immune system functions as microbial ‘management’ system that can simultaneously discriminate friends from foes to ensure plant survival and maximize plant fitness.


Recent findings indicate that both abiotic factors and host genotype interact to influence plant colonization by microbes and that a small number of microbial taxa, termed microbial “hubs”, are strongly interconnected and help shape community structure. The ease with which plant and microbial genomes can now be assembled and annotated, together with rapid technological advances in computational biology, metagenomics, cultureindependent microbial community characterization, as well as targeted manipulation of plantmicrobe interactions, offers unprecedented opportunities to synthesize and re-interpret knowledge on binary beneficial or pathogenic plant-microbe interactions in the context of plantassociated microbial communities. This knowledge is likely to have profound implications for the development of novel strategies for crop protection against pathogens, improved plant productivity and more sustainable food production systems, e.g. by reducing synthetic fertilizer inputs in agricultural settings.


The proposed SPP aims at a pragmatic understanding of the plant microbiota by application of systematic reductionist approaches, including the deconstruction and reconstruction of microbial assemblages. The deconstruction phase involves establishment of model microbial culture collections from plants grown in contrasting natural environments and microbial whole-genome sequencing of pure strains. The reconstruction phase includes microbiota reconstitution experiments using gnotobiotic plant systems to test the impact of different microbial microcosms on plant fitness parameters such as disease resistance, nutrient acquisition and abiotic stress tolerance under laboratory conditions, to ultimately understand their impact in nature.

Research areas:

Central to the SPP is an integrated analysis of microbiota functions and their ecological and evolutionary relevance, taking advantage of comparative approaches that employ the dicotyledonous model Arabidopsis thaliana, the legume symbiosis model Lotus japonicus and the monocotyledonous cereal crop Hordeum vulgare as references.

Four research areas reflect the scientific aims described above:
A. Community-level assembly of plant-microbe interactions
B. Role of the plant immune system in shaping resident microbial consortia
C. Ecological relevance of plant-microbiota
D. Collective toolkit development in the SPP

Publications:

Koprivova A, Schuck S, Jacoby R, Klinkhammer I, Welter B, Leson L, Martyn A, Nauen J, Grabenhorst N, Mandelkow JF, Zuccaro A, Zeier J, Kopriva S (accepted) Root-specific camalexin biosynthesis controls the plant growth promoting effects of multiple bacterial strains. PNAS

Sarkar D, Rovenich H, Jeena G, Nizam S, Tissier A, Balcke GU, Mahdi L, Bonkowski M, Langen G, Zuccaro A (2019) The inconspicuous gatekeeper: endophytic Serendipita vermifera acts as extended plant protection barrier in the rhizosphere. New Phytologist doi:10.1111/nph.15904