Contributions to the Yearbook of the Max Planck Society

Disease outbreaks in crops reduce global yields by about 30% each year. Harnessing the natural capacity of plants to block microbial infections would help shift towards more environmentally sustainable agriculture. Researchers have made significant progress in understanding molecular mechanisms of pathogen detection by dedicated immune receptors and how, once activated, these proteins mobilize defence programs to stop disease. The discovery of a set of immune receptor-generated nucleotide signalling molecules and their modes of action clears a new path for engineering crop disease resistance.

Plants inhabit an enormous range of habitats. Studying how they adapted to their specific environments can provide fundamental biological insights as well as information that can help to reduce the impacts of climate change on natural and agricultural ecosystems. We investigate the mechanisms of adaptation in natural populations of the molecular and eco-evolutionary model plant, Arabidopsis thaliana. This system is ideal for connecting the biochemical and molecular bases of trait variation with its ecological and evolutionary context.

In the current era of big data, why do we still lack a complete molecular and physical understanding of how cells form tissues and develop into organisms? A simple answer is complexity across scales. Morphology is determined by a cascade of processes that take place at different scales of biological organization, and yield the final form through complex feedback loops of gene action, tissue growth and mechanics. Computational techniques are valuable to organize such data into mechanistic explanations. We describe two predictive, multi-scale studies of plant development and diversity.

Hybrid crops are favored in agriculture due to their increased vigor and yield. However, the offspring of hybrid plants is genetically variable due to sexual reproduction. Therefore, new hybrid seeds need to be generated by plant breeders year after year - a time consuming and costly process that is not amenable for all crops. Recent research has demonstrated that sexual reproduction can be avoided to produce clonal seeds maintaining the hybrid state. Here, we summarize novel approaches developed in hybrid Arabidopsis and rice promising a revolution in hybrid breeding and seed production.

Fungi and other filamentous microbial eukaryotes, i.e. oomycetes, cause many devastating plant diseases worldwide and are responsible for up to 10% of crop losses. Over the last decade, pesticide application, breeding for plant disease resistance or genetic manipulation of plant immune components have been primarily used to control microbial diseases. However, recent findings indicate that bacterial commensals living benignly inside or at the surface of plant root tissues can confer extended immune functions to the plant host, thereby restricting infection by filamentous microbes.

An epigenetic memory determines how strongly genes are expressed. Polycomb Group protein complexes stably shut down genes by compacting the packaging material of DNA. Recent studies in plants showed that two different and short DNA sequences, called teloboxes and RY motifs, are involved in this epigenetic process. Genes that are under epigenetic regulation are enriched in both motifs, often in combination. Specialized transcription factors, which recognize teloboxes and RY motifs, also directly bind to building blocks of the Polycomb Group and thus stabilize the memory of target genes.

To improve crop quality and yield, breeders need to control the fertility of stamens, the male organs that produce pollen within sacs called anthers. For example, it would be ideal to manipulate at will the release of pollen from anthers. However, this firstly requires a detailed understanding of how anther cells themselves activate pollen release. In barley, this activation seems to be triggered by the phytohormone auxin and requires enzymes to separate specific cells from each other to finally open the anthers.

Boundary zones were previously seen as physical barriers that separate plant tissues and thus allow the development of functional organs. However, recent studies revealed that boundaries, like those between the shoot apical meristem and leaf primordia and those between leaflets, also serve as launching pads for secondary meristem formation and play an important role in determining plant architecture. Interestingly, establishment of boundary zones during shoot branching and complex leaf development is regulated by homologous genes.

Plants sense microbial molecules to trigger innate immunity for protection from pathogens. However, microbes have evolved broad virulence factors that interfere with plant immune components. Therefore, immune mechanisms must be robust to cope with microbial perturbations. In addition, since too much immune response is detrimental for plant fitness, plant immune responses need to be tuned. The scientists study how plant immune signaling networks achieve the properties robustness and tunability using molecular genetics, genomics and computational modeling.

Individual genetic alterations can have direct impact on the phenotypes of the respective organisms. Such mutations can be useful for functional annotation of the respective regions of the genome and can be found between wildtype and mutant genomes, between distinct individuals of the same species, and between the genomic sequences of diverse species. The group develops new approaches to identify and to distinguish such differences from all other changes that do not affect the phenotypes.

Depending on the environmental conditions, plants can rapidly alter their metabolism. Post-translational modification of proteins seems to play key roles during this adaptation. Reversible acetylation of lysine residues in proteins has recently emerged as post-translational modification controlling many important cellular functions beyond transcription. The identification of acetylation sites on metabolic enzymes in plants is a first step to uncover its physiological role in metabolism.

Due to their potential risk for the genome integrity and thus the viability of an organism, transposable elements are kept inactive. Among others, the mechanism of RNA-directed DNA methylation facilitates this inactivation in plants. Recent investigations discovered a new shoot apical meristem specific function of this mechanism. It reinforces silencing of these elements during the early phase of vegetative growth and counteracts their drug-induced activation. It furthermore provides a checkpoint for correct epigenetic inheritance during the transition from vegetative to reproductive phase.

Morphogenesis and growth are processes driven by genetic and signaling networks. Although many genetic components controlling plant organ shape have been identified, how they control the mechanical properties of cells remains elusive. In animal systems recent studies have shown that mechanical forces can feed back on genetic programs and even appear to be capable of influencing cell fate. Do such feedbacks exist in plants? What is the role of mechanics in morphogenesis? We address these questions by combining the expertise of physicists, biologists and computational modelers.

RNA polymerase II transcribes protein coding and several classes of regulatory RNAs in multicellular organisms. The C-terminal domain of the RNAPII largest subunit, RNAPII-CTD, carries conserved heptapeptide repeats that are phosphorylated at different residues by a protein kinase cascade in Arabidopsis. Recent studies start to reveal how phosphorylation of the RNAPII-CTD by TFIIH-associated protein kinases regulates growth and development via coordinated control of transcription, cell cycle and biogenesis of microRNAs and small silencing siRNAs.

New plant diseases emerge regularly being a threat for food security. Some pathogens cause epidemics on living plants only and are called biotrophs. Comparative genomics revealed a loss of essential metabolic pathways leading to biotrophy. However, gene loss is only possible due to the ability to suppress host defense. Defense suppression and adaptability requires a large gene pool that is acquired by sexual recombination or interaction with other organisms. To get a comprehensive view on how new pathogens emerge it is important to dissect their interaction within natural habitats.

Plants display remarkable robustness against attempted pathogen infection and in their natural environment disease is the exception. Analysis of Arabidopsis plants is illuminating some fundamental processes by which plants recognize and resist microbial pathogen invasion. What emerges from recent studies is a set of distinct immune response branches in different parts of the host cell which are strictly coordinated to produce effective immunity.

Many traits that play important roles in plant breeding are complex, meaning that they are controlled by multiple genetic and environmental factors. Knowledge of the corresponding genes facilitates early diagnoses of complex traits and thereby increases the efficiency and precision of breeding new varieties of crop plants. To identify such genes, association-studies for complex traits of potato were conducted at the institute. Highly significant associations were identified between candidate genes and complex traits such as resistance to potato late blight disease.

Viable plant seeds are not always able to germinate and can cycle between a sleeping (dormant) and awake (non-dormant) state. Dormancy prevents germination during unfavourable seasons, an ability that has been lost in most of our crop species. The molecular regulation of seed dormancy is largely unknown. The Seed Dormancy Group has identified components of this control by isolating seed dormancy genes.

Most traits which are important for fitness and agricultural value of crops are so-called quantitative traits. A large number of genes which interact with each other and are influenced by environmental factors contribute to variation of these traits. Understanding the genetic architecture of quantitative traits is not only important with respect to basic science but will also dramatically facilitate practical plant breeding.

Each cell of higher organisms contains a nucleus where the genetic material is tightly packed. In order to utilize genes, parts of the genetic material need to be unpacked, and protein complexes are involved in the process. Other protein complexes, conversely, function to prevent access to genes disabling gene expression.

Modern molecular biology employs high-throughput methods, for example to determine genome sequences. Their analysis and interpretation increasingly requires integration of heterogeneous data. Standards for access to biological data and web service technologies can facilitate automated finding and invocation of bioinformatics resources.

MIKC* MADS-box proteins constitute a regulatory network controlling important processes in pollen development of Arabidopsis thaliana. Comparative analysis of function, evolution, and systems biology of the MIKC* transcription factor family may allow a deeper understanding of land plant gametophytes.

Global change threatens agricultural production and represents a challenge for plant breeding research. Consequently, research focuses on elucidating the genetic regulation of adaptation to drought stress in crop plants. Barley is a good model for analysing genetic adaptation mechanisms, as it is characterized by tolerance to abiotic stress and a high genetic diversity. Understanding the genetic regulation of flowering time, for example, will allow the targeted manipulation of development during the breeding process and hence adaptation to changing environments.

Cultivated barley ranks number four among the world cereals. Barley emerged about 10000 years ago from wild barley species. At the institute, the genetic diversity among cultivated and wild barley varieties is studied with novel genome research tools. The new results are exploited, on one hand, to support modern plant breeding. On the other hand, the data assist in unravelling the molecular regulation of growth and development in crop plants.

Plants synthesize a vast array of secondary compounds derived from phenylalanine, which fulfill defense functions against unfavorable environmental conditions. To understand the basis for this chemical diversity, the mechanism of substrate selection was unraveled for a key enzyme of phenylpropanoid metabolism. This knowledge may provide strategies of engineering natural product pathways aiming at targeted modifications of plant properties.

The activities of enzyme classes in a living organism can be displayed by activity-based profiling. This technology is based on the use of tagged small molecules, which covalently bind to enzymes in an activity-dependent manner. The Plant Chemetics group is developing and applying this technology and other novel chemistry tools to reveal the dynamics of enzyme activities during plant-pathogen interactions.

The architecture of flowering plants shows an enormous heterogeneity. This variability is, to a large extent, caused by the different branching patterns of the vegetative and flowering shoots. Side-shoots originate from secondary meristems, which are formed in the axils of leaves. In tomato and in Arabidopsis, the gene LATERAL SUPPRESSOR (Ls/LAS) encodes a transcription factor controlling the initiation of axillary meristems during vegetative development. The gene is expressed in a narrow domain of the leaf axil and conditions the competence of the meristem founder cells. Transcription factors of the MYB class are also required for axillary meristem formation in specific zones along the shoot axis. Furthermore, plant architecture is strongly influenced by differential outgrowth of the axillary buds. Recently, it has been demonstrated that, in addition to the archetypical plant hormones auxin and cytokinin, bud outgrowth is regulated by a new root derived signal.

The roxy1 mutant from Arabidopsis thaliana initiates a reduced number of petal primordia and exhibits abnormalities during further petal development. The defects are restricted to the second whorl of the flower and independent of the organ identity. ROXY1 is predominantly expressed in tissues that give rise to new flower organs, including petal precursor cells and petal primordia. Glutaredoxins (GRXs) are small, ubiquitous oxidoreductases that have been intensively studied in E. coli, yeast and humans and oxidize or reduce conserved, cysteine containing motifs. They are involved in a large variety of cellular processes and exert a crucial function in the response to oxidative stress. Our data demonstrate that, unexpectedly, a plant glutaredoxin is involved in flower development, likely by mediating posttranslational modifications and thus affecting the activity of target proteins required for normal petal organ initiation and morphogenesis. Surprisingly, ROXY1 belongs to a novel subgroup, the CC-type, being specific for land plants. The existence of large CC-type subfamilies in angiosperms supports the assumption that their capability to posttranslationally modify target protein activity has been integrated into crucial plant specific processes coinciding with the development of complex flowers. Further analysis of ROXY1 and other CC-type members aims for an understanding of their biochemical properties, the identification of target proteins and unraveling the intriguing connection between redox regulation and flower development.

Plant mutants that lack the so-called Mlo protein are highly resistant against powdery mildew fungi. It is assumed that the fungus exploits presence of this protein to suppress plant defense mechanisms.

Our long-term goal is the understanding of the genetic differences between Arabidopsis accessions affecting important adaptive traits such as seed dormancy and plant growth. We expect that understanding this genetic variation will help explaining why specific variants are adapted to specific environments and that knowledge of the genetic basis of these traits will help breeding crop plants.

Protein modifiers are small proteins that can be covalently attached to substrate proteins. The resulting change can influence the function of the substrate protein and can thereby play a role in cellular information transfer. Attachment of modifiers is part of many developmental processes in plants, including flower induction, which depends on an interplay between a genetic program and environmental input parameters for optimal timing and execution.

Since their discovery in plants, over a decade ago, the study of MADS-box genes has made a major contribution to our current understanding of flower development at the level of organogenesis. Less well understood, however, remain the molecular genetic mechanisms involved in differentiation at the cellular level within these floral organs. In particular, how the cell lineages giving rise to the sex cells, in a process known as sporogenesis, become specified within the anthers and ovules is not well understood. As an unexpected outcome of our research on MADS-box genes, we uncovered a novel and plant specific family of transcription factors and found one of its members to control the process of sporogenesis. Its future analysis may contribute to a better understanding of sexual reproduction of plants.

Genetic variability and environmental factors determine the phenotype of the individuals of the same species. The possibilities to identify genetic variability at the DNA level, the availability of partial or even complete DNA sequence information of a multitude of organisms and the knowledge of gene function make it possible to explore the molecular basis of complex traits of humans, animals or plants. Knowledge on the molecular basis of complex traits of crop plants can contribute to the efficient selection of new varieties that are better adapted to human needs. In a pilot experiment, an association was found between field resistance of potato varieties to the late blight disease and DNA variants in a particular segment of the genome of potato (Solanum tuberosum).Christiane Gebhardt