To kill or not to kill: the genetic relationship between a parasite and an endophyte

Abstract

N utritional strategies among plant pathogenic microbes range from necrotrophy, in which the pathogen rapidly kills the tissue that it is invading and draws its nutrition from it, to biotrophy, in which the pathogen draws its nutrition from living tissue. The most aggressive necrotrophs typically have very wide host ranges and attack young seedlings or stressed or otherwise defense-compromised plants. The most specialized biotrophs typically have very narrow host ranges, develop special differentiated structures for obtaining nutrition from the plant, and are often unable to grow except on the plant. Many pathogens fall between these two extremes. Some necrotrophic fungi and bacteria, called hemibiotrophs, initially proliferate at the site of infection and may spread some distance from it prior to the onset of tissue destruction. In contrast to the pathogenic microbes, many other microbes colonize plant tissues without damaging their hosts. These nonpathogenic endophytes include commensals, which may share a benign coexistence with their hosts, and mutualists or symbionts, which provide benefits for themselves and their hosts. Some notable examples are: fungal endophytes of tall fescue and rye grass, which produce feeding deterrents that protect the grasses from weevilsl; vesicular-arbuscular mycorrhizal fungi, which are obligate symbionts within the roots of many plants, and which enhance phosphorus and water use and provide some disease resistance2; and nitrogen-fixing bacteria, which form symbiotic associations with the roots of legumes 3. A fundamental question regarding both pathogens and endophytes is how to evade, suppress or defeat the defense mechanisms of the plant host. Plants have a broad spectrum of defense mechanisms including preformed and microbe-inducible physical and chemical barriers, as well as a rapid necrotic response at a site of infection (hypersensitive response) 4. As a consequence, all plants are resistant to most potential colonists, and the ability of ~,. microbe to colonize a particular plant is a specific function often specialized to a limited number of host species. Are there essential differences between the ways in which pathogens and endophytes colonize plant tissue, or are there common mechanisms for this process? The similarities between the growth habits of endophytes and biotrophs seem fairly obvious. There is some evi.dence for common plant mechanisms involved in symbiotic colonization by diverse organisms: mutations in five complementation groups in pea interfere with colonization both by nitrogen-fixing bacteria and by vesicular-arbuscular mycorrhizae s. Such pathways might also be exploited by biotrophic pathogens. There is also growing evidence that some pathogens produce specific substances, such as toxins or suppressors, that render plant tissue amenable to colonization 6-~. However, what about necrotrophs, which kill plant tissue ahead of the growing hyphae or cells? Does necrotrophy represent an extreme form of suppression of host responses, or is it mech-