Plant-Plant Communications: Rhizosphere Signaling between Parasitic Angiosperms and Their Hosts

Plants are in constant communication with a multitude of diverse organisms. Some symbioses, such as the association of nitrogen-fixing bacteria and mycorrhizal fungi with plant roots, are beneficial to the plant. Others, such as the interaction of plants with viral, microbial, fungal, and nematode pathogens, are harmful. Most plant-organism interactions go unnoticed simply because they are underground. A single gram of fertile soil can contain 10 bacteria, 10 actinomycetes, and 10 fungi, as well as several millimeters of roots. Populations in the rhizosphere, the narrow zone of soil surrounding a root, may be 1 or 2 orders of magnitude higher. Plants are not passive targets for associating organisms but, rather, actively affect the structure of rhizosphere communities by releasing attractants and repellents from their roots. As much as 20% of a plant’s net photosynthate is released into the rhizosphere. Large quantities of phenolic compounds are also released from plant roots; approximately 120 kg/ha plant-derived phenolics can be added into grassland soil annually. Many of these strongly affect neighboring plant and microbial communities (Siqueira et al., 1991). Other signals released from plant roots are more subtle and are specifically directed toward attracting or repelling particular colonizers. An important conclusion from several recent studies is that interactions between plants and other organisms are mediated by signal molecules that cue developmental and physiological events critical in the interaction (Baker et al., 1997). In natural environments plants are intimately associated with other plants. Epiphytes such as orchids, bromeliads, and Spanish moss grow on other plants, using them for support. Plants such as Indian pipe (Monotropa uniflora) indirectly obtain nutrients from other plants via mycorrhizal bridges that connect them with host roots. A more direct plant-plant interaction is between parasitic plants and their hosts (Press and Graves, 1995). Parasitian originated at least eight times independently in the evolution of higher plants and about 3000 species of angiosperms (approximately 1%) are parasites (Kuijt, 1969; Parker and Riches, 1993). Parasitic plants have different modes of invading host plants; some invade host root, whereas others invade aerial parts of the plant. In all cases invasion of host tissues and extraction of host resources is mediated by haustoria, specialized multifunctional organs that uniquely define parasitic plants. In this review we will discuss how haustorium development in root-parasitic plants is cued by host plant signals. Several parasitic plants are significant agricultural pests. For example, dwarf mistletoes (Arceuthobium spp.) are responsible for the annual loss of more than 3.2 billion board feet of lumber in the United States because of reduced and deformed growth of infected conifers (Parker and Riches, 1993). However, the parasitic plants with the greatest impact worldwide are the root parasites in the Scrophulariaceae and closely related Orobanchaceae families. Crops susceptible to these parasites include important cereals such as maize, sorghum, millet, and rice, as well as legumes and other vegetables. Striga spp. are particularly notorious, infecting more than two-thirds of the 73 million ha of cereals and legumes in Africa. Yield losses by infection with these parasites often reach 100%, and levels of infestation are frequently so great that continued crop production becomes impossible. The Food and Agriculture Organization of the United Nations estimates that the lives of more than 100 million Africans in 25 countries are threatened by crop losses due to Striga spp. Because of their significance to agriculture, most parasitic plant research, and consequently most of this review, concerns plants of the parasitic genera Scrophulariaceae.