Agrobacterium-Plant Interactions

Agrobacterium species are gram-negative, obligately aerobic soil bacteria capable of saprophytic or parasitic growth and are responsible for the crown gall and hairy root diseases of dicotyledonous plants (53). The genus contains two widely studied pathogenic species: Agrobacterium tumefaciens and A. rhizogenes (115). Both infect a broad variety of plants and infect only at wound sites. They infect individual cells at the site of infection and cause these cells to proliferate; A. tumefaciens causes either a gall of disorganized callus tissue or a teratoma containing stunted shoots, and A. rhizogenes causes a proliferation of morphologically distinctive roots. In each case, this is achieved by the transfer of a discrete fragment of bacterial DNA to the nuclei of plant cells, where it is integrated into genomic DNA and directs the overproduction of or hypersensitivity to plant growth hormones. This transferred DNA (T-DNA) also directs the production of novel compounds called opines, which provide a source of nutrients to the colonizing bacteria. The T-DNAs are localized prior to transfer on a family of large plasmids, called Ti (tumor-inducing) plasmids for A. tumefaciens or Ri (root-inducing) plasmids for A. rhizogenes. Ti and Ri plasmids also contain nontransferred genes which encode proteins that mediate T-DNA transfer and other nontransferred genes which direct opine catabolism. In addition to these diseases, some strains of A. tumefaciens can incite a root decay on susceptible grape vines (24). Since strains lacking the Ti plasmid can cause this disease, no DNA need be transferred during infection, but at least one degradative enzyme, a pectinase, is released by the bacteria. Agrobacterium is the only genus of bacteria that is thought to transfer DNA to higher organisms as a normal part of its behavioral repertoire. However, one of the more surprising and rewarding aspects of recent developments in the field is the finding that this ability most probably evolved from other, more widely distributed kinds of bacterial metabolism (208). First, the transfer of DNA probably evolved from a conjugal transfer system. Second, every Agrobacterium signal transduction system so far studied that is required to perceive plant-released molecules is homologous to some other bacterial regulatory system. Understanding how Agrobacterium spp. perceive wounded plants and transfer DNA to them has been aided immeasurably by uncovering and exploiting the similarities between this system and homologous bacterial systems. Just as students of Agrobacterium spp. have benefitted from developments in other fields of molecular biology, they have made a number of discoveries that are of interest to a wider audience. The notion that plant-associated bacteria might induce the genes required for association in response to host-released signal molecules originated with studies of A. tumefaciens. This phenomenon was later found to be true ofRhizobium species as well as a variety of other plant and animal pathogens (148). The regulatory system that controls this induction is arguably one of the best characterized of its gene family. A second example involves the mechanism of DNA transfer. Assuming that this transfer is essentially a type of bacterial conjugation, it arguably has been more completely characterized than any other conjugal transfer system. In this review I will attempt to describe various aspects of Agrobacterium-plant interactions and will place special emphasis on the exchange of chemical signals during infection. The word "signal" is taken in its broadest sense to denote any compound (including diffusible chemicals, polysaccharides, proteins, and DNA) which plays a role in this plantmicroorganism interaction. The first section will deal with plant-released compounds that are perceived by Agrobacterium spp. , and the second section will analyze signals transferred from the bacterium to the plant, especially the DNA which is transferred from bacteria to plant nuclei. This study also will strongly emphasize recent findings, including unpublished work presented at recent symposia and elsewhere. This rapidly moving field of research has been the subject of many other recent reviews: some have emphasized signal exchange (20, 52, 58, 83, 153, 154, 249, 258a); others have treated general aspects of crown gall tumorigenesis (16, 21, 75, 94, 109, 157, 196, 253, 258, 270-272) or mechanisms ofT-DNA transfer (119, 173, 208, 209); and still