Strategies to protect crop plants against viruses: pathogen-derived resistance blossoms.

Abstract

Since 1986, the ability to confer resistance against an otherwise devastating virus by introducing a single pathogen-derived or virus-targeted sequence into the DNA of a potential host plant has had a marked influence on much of the research effort, focus, and shortterm objectives of plant virologists throughout the world. The vast literature on coat protein-mediated protection, for example, attests to our fascination for unraveling fundamental molecular mechanism(s), our (vain) Despite extensive and sometimes elegant experimentation, the molecular mechanism(s) of this viral "crossprotection" have remained elusive and controversial. In some cases, the coat protein (CP) of the protectant virus was thought to be primarily responsible, either by preventing particle disassembly or by re-encapsidating the incoming genome of the more severe challenge virus. However, viroids [240-to 380-nt-long, naked circular single-stranded (ss)RNA pathogens] and mutant viruses making assembly-defective or no detectable CP could also cross-protect against their more severe relatives. Such observations prompted models based on inhibitory interactions between sense and antisense RNAs or between the replicational machineries ofthe two competing pathogens (6). Controversy arose largely because available molecular technology could not resolve which regulatory or coding sequence(s) or polypeptide product(s) from the actively replicating genome of the primary (protectant) pathogen were responsible for interfering with the many replicative processes essential to establish infection by the secondary, related, and more severe virus. In contrast, multiple infections by unrelated viruses sharing a common host are very prevalent in nature. Many aspects of this older story have their parallels in current hypotheses and lack of a unified model for pathogenderived resistance in transgenic plants.The advent of improved cell and tissue culture techniques, efficient protocols for Agrobacterium tumefaciens-mediated transformation and plantlet regeneration in dicotyledonous species (7) [and more recent methods for monocot crops (8-10)], has permitted, among other applications (11,12), the theory of pathogenderived virus resistance to be tested in practice.Collaboration between researchers at Monsanto and Washington University (St. Louis) led to the first report of CPmediated protection (CPMP) against tobacco mosaic virus (TMV) in tobacco in 1986 (4). Since then, CPMP has been reported for over 20 viruses in at least 10 different taxonomic groups, in a wide 3134 variety of dicot plant species, and the list is increasing rapidly.

Transgenic accumulation of two plant virus coat proteins on a single self-processing polypeptide.

“…Pathogen-derived resistance (PDR) (Sanford & Johnston, 1985) against plant viruses has been demonstrated through genetic transformation of plants with genes that encode either wild-type or modified viral proteins (Fitchen & Beachy, 1993 ;Wilson, 1993). In many cases, the accumulation of transgenic viral proteins correlates with the level of resistance achieved, and protection has been proposed to involve protein interference with specific virus processes (Reimann-Philipp & Beachy, 1993).…”

Recombination between viral DNA and the transgenic coat protein gene of African cassava mosaic geminivirus.

“…Coat protein-mediated virus resistance has been successfully applied for a number of RNA plant viruses (Hull & Davies, 1992 ;Wilson, 1993). For the geminivirus tomato yellow leaf curl virus (TYLCV) Israel strain, Kunik et al (1994) observed a delay in the appearance of disease symptoms and subsequent recovery from symptoms in tomato plants expressing the TYLCV coat protein gene.…”

“…Coat protein-mediated resistance is, so far, the best studied method of protecting plants against virus infection (Hull & Davies, 1992 ;Wilson 1993). Two possible risks associated with viral coat proteinexpressing plants are conceivable : heterologous encapsidation and recombination.…”

Studies of coat protein-mediated resistance to tobacco mosaic virus (TMV). II. Challenge by a mutant with altered virion surface does not overcome resistance conferred by TMV coat protein

“…In contrast, TMV in which the CP was replaced by the SHMV CP overcame CP-MR to the same extent as did SHMV. We conclude that CP-MR conferred by TMV CP involves interactions between amino acid sequences of the challenge viruses and the transgene protein other than those on the surface of the challenge virus.Coat protein-mediated resistance (CP-MR) has been widely used to develop protection in monocots and dicots against a number of different viruses (see reviews by Fitchen & Beachy, 1993;Wilson, 1993). However, the molecular and cellular nature of the resistance has not been fully elucidated for any example of CP-MR. We have focused our studies of CP-MR on protection against tobacco mosaic tobamovirus (TMV) in tomato and tobacco plants.…”

“…Coat protein-mediated resistance (CP-MR) has been widely used to develop protection in monocots and dicots against a number of different viruses (see reviews by Fitchen & Beachy, 1993;Wilson, 1993). However, the molecular and cellular nature of the resistance has not been fully elucidated for any example of CP-MR. We have focused our studies of CP-MR on protection against tobacco mosaic tobamovirus (TMV) in tomato and tobacco plants.…”