Plants and pathogenic agents, a refined and dangerous relationship: the example of fungi

Plant-fungus interactions are highly diverse, either being beneficial to the host plant such as those leading to mycorhizal symbiosis, or very detrimental when leading to severe diseases. Since the beginning of agriculture, improvement of plant resistance to pathogens has remained a major challenge. Breeding for resistance, first conducted empirically in the past centuries, was then performed on a more theoretical basis after the statement of heredity laws by Mendel at the end of the XIXth century. As a result, most cultivated species contain various cultivars whose resistance or susceptibility to a given pathogen species depend on their interaction with various races of that pathogen. Such highly specific race-cultivar systems are particularly suited for understanding the molecular dialogue which underlies compatible (host susceptible/pathogen virulent) or incompatible (host resistant/pathogen avirulent) interactions. During the twentieth century, one of the major events that paved the way for future research was the statement by Flor 1946, 1947] of the gene-for-gene concept. Studying inheritance of the disease phenotype in the interaction between flax and Melampsora lini he showed that resistance in the host and avirulence in the pathogen are dictated by single dominant genes which correspond one to one, i.e. one resistance gene for one avirulence gene. The fact that incompatibility may depend on the presence of only one resistance (R) gene in the host and one avirulence (Avr) gene in the pathogen was fully confirmed about 40 years later. Molecular genetics and complementation experiments have allowed to isolate numerous R and Avr genes from various plant-pathogen systems, and to verify the gene-for-gene concept. These studies have enlightened the elicitor/receptor concept, formerly introduced to account for the specificity of the compatible and incompatible interactions. The present knowledge of R and Avr genes also allows to predict how such genes have evolved and how they could be used to improve disease resistance. At the beginning of the twenty first century, this remains a major challenge in view of the severe losses caused by pests and pathogens to most crops on the earth.