Plant Physiol, December 2001, Vol. 127, pp. 1476-1483

UPDATE ON MOLECULAR PLANT-MICROBE INTERACTIONS
Molecular Plant-Microbe Interactions That Cut the Mustard¹

Department of Plant Pathology and Microbiology, Texas A&M University, 2132 TAMU, College Station, Texas 77843-2132

	INTRODUCTION

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While browsing this special Plant Physiology issue on the Diversity of Plant Systems, one must be impressed, albeit perhaps not surprised, by the numerous examples showing that research on various plants often leads to fascinating discoveries in several plant science subdisciplines. This Update aims to continue on this course while simultaneously introducing additional levels of complexity in the form of microbes that infect plants. Rather than serving as a standard literature review, the objective is to provide a broad conceptual introduction to the field of molecular plant-microbe interactions.

This is not an attempt at Arabidopsis bashing; in fact, it is quite the opposite because it is very clearly recognized that the tiny wild mustard has provided an enormously powerful genetic model system. Arabidopsis has contributed substantially to the elevation of molecular plant microbe studies as a respected specialty in the life sciences and it provides valuable information to spice up research on other plant systems. With that in mind, the major focus of this Update aims to provide persuasive arguments that diverse plant model systems are required to further our understanding of the fascinating area of plant microbial biology.

	PLANTS AND MICROBES

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Why study microorganisms that infect plants? As with all scientific endeavors, a major driving force is to gain fundamental information, in this case about the plant-microbial world around us. As in medical research, the consensus among scientists working with plant-infecting microbes is that scientific treasures will be revealed once mechanisms are elucidated that explain what exactly occurs at the molecular level when a plant becomes infected with fungi, viruses, or bacteria. However, interests are often also dictated by more immediate socio-economic impulses because microbes are responsible for many plant diseases that cause substantial economic losses in agriculture or have a substantial esthetic impact in our urban areas. These harmful effects are often manifested directly through pathogen-mediated damage to the plant and a consequent reduction in plant vigor and yield or quality of crops. Perhaps less well known is that several plant pathogens also produce toxins that are harmful to humans, which is of great public health concern (Scholthof, 1999).

Because plant pathogen populations are under constant selective pressure from changing agricultural practices, their genetic makeup changes over time to remain competitive, a variation of the "Red Queen" hypothesis (Ridley, 1993). These continual shifts in the population genetics of the pathogen require detailed molecular studies and a continuous attention to the development of new or improved measures to control harmful pathogens. However, the infection of plants with certain microbes (e.g. symbiotic microorganisms) can also have beneficial effects on plant health. Continued studies are needed to understand such systems and to explore ways to expand their benefits. Therefore, the area of plant-microbe interactions is important because it addresses fundamental questions in biology while it also is of practical value for the application of beneficial microbes and the control of harmful pathogens in an environmentally responsible manner.

	RESISTANCE AND SUSCEPTIBILITY

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Despite the negative economic consequences of plant diseases and benefits of symbiotic interactions, most plants resist infection by most microbes. This phenomenon has generated variations on the same fundamental question ever since scientists started studying plant-infecting microbes: How do plants protect themselves from pathogen attack? One particularly intriguing resistance phenotype first recognized by Flor (1955) is the gene-for-gene phenomenon. In this interaction, the product of a single resistance gene (R gene) in the plant specifically recognizes the product of a pathogen avirulence (avr) gene. This sets off a hypersensitive response (HR) that culminates in rapid cell death around the site of infection to effectively prevent further spread of the pathogen. Since the advent of molecular biology, a major goal has been to identify and isolate microbe and plant genes controlling the interactions that occur upon infection, especially those that are involved in the HR. One can easily imagine the excitement that was generated by reports in the mid-1990s when cloning of R genes was first reported (for review, see Dangl and Jones, 2001; also discussed in detail elsewhere in this issue).

Because of recent research advances with Arabidopsis and R genes, it is not surprising that these are popular "hot" topics in many recent scientific treatises. However impressive and useful these findings are, plant-microbe interactions involving Arabidopsis and R genes represent only a fraction of the immense pool of diverse associations between plants and microbes in nature. A more complete understanding of plant-microbe interactions will be achieved through the use of natural hosts and by tackling systems that are more complex than those conferred by single dominant R genes.

Plants can also effectively protect themselves against pathogen attack through action of nonspecific resistance mechanisms that are not mediated by R genes. For example, the plant environment may be incompatible for a microbe to thrive, or the pathogen may induce a broad spectrum of defense responses that combat the infection. Often such impediments can be major factors in a phenomenon recognized as non-host resistance that places severe restrictions on the host range for a pathogen (Heath, 2000). Broad-spectrum defenses include physical barriers (Walton, 1994), activation of defense-related proteins (Heath, 2000), or induction of viral RNA-degrading systems (Waterhouse et al., 2001). Plants also produce secondary metabolites and other natural products that can confer disease resistance (Dixon, 2001). Systemic acquired resistance is a nonspecific protective mechanism that can be activated when plants are challenged with a pathogen (Sticher et al., 1997).

In addition to the value of investigating resistance mechanisms, much can be learned from studying fully compatible interactions that lead to systemic infection. Such investigations may elucidate why certain plants develop only mild symptoms (tolerance), whereas other plants suffer severe or even lethal symptoms. These are very important aspects that should not be underestimated because in fact systemic infections create most of the disease problems (Agrios, 1997), and they are necessary to achieve the beneficial effects of symbiotic interactions (Smith and Goodman, 1999).

	A PLEA FOR DIVERSITY

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Biological research benefits greatly from development of specific genetic model systems. Human HeLa cells, hamster kidney cells, the nematode Caenorhabditis elegans, the fruitfly (Drosophila melanogaster), bakers' yeast (Sacharromyces cerevisiae), and the bacterium Escherichia coli, are well known examples of organismal model systems. For plant sciences, this role is currently fulfilled by Arabidopsis. Why use a model system and how is it defined? Most scientists would probably agree that model systems are genetically well characterized and stable, and represent reliable and adaptable experimental systems that consistently yield novel and important results. Information and materials obtained through studies on model systems are extremely important to provide direction for research on other systems.

Due to the inherently complex nature of plant-microbe interactions, studies must be pursued on taxonomically diverse species of plants. For example, considering that the host range of a microbe is genetically controlled, useful information can be obtained by simultaneous molecular analyses on several different plants instead of centralized efforts on a single model system. Despite the philosophical incentives, there is a practical impediment to the development and acceptance of additional valuable experimental systems. In this era of limited funding for plant sciences, it becomes increasingly difficult to be competitive with less popular, yet superb, peripheral biological systems. Therefore, it is of the utmost importance that every appropriate opportunity be utilized to impress upon funding decision makers the scientific importance of studying diverse plant systems, in this case to further our understanding of molecular plant-microbe interactions. In essence, every plant-microbe interaction is unique and represents a bipartite model system with the potential to yield novel information. Convincing evidence for these arguments should be apparent from the examples described in the following sections.

	SPECIFIC EXAMPLES OF MODEL SYSTEMS TO STUDY PLANT-MICROBE INTERACTIONS

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This section briefly describes examples of systems that are used to study the molecular basis for infection of plants by microbes. For a more general and complete introduction to plant-microbe interactions, the interested reader may consider consulting a standard plant pathology textbook (Agrios, 1997), recent issues of the Annual Review of Phytopathology (http://www.annualreviews.org), and various publications by the American Phytopathological Society (http://www.apsnet.org). The reader is referred to other reviews for information on molecular interactions of plants with nematodes (Williamson and Hussey, 1996).

	FUNGI AND RELATED MULTICELLULAR MICROORGANISMS

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Historically, plant pathogens have been studied because they cause disease symptoms that have a severe negative effect on the yield or quality of crops. A classic example is provided by Phytophthora infestans, which causes late blight on potatoes (Solanum tuberosum). P. infestans attained notoriety in the middle of the 19th century because for many years it single-handedly destroyed potato crops in Europe, and most dramatically, in Ireland. This resulted in the infamous potato famine that caused the starvation of millions, and many survivors emigrated in desperation to North America. To date, the late-blight pathogen remains a continuous threat for potato growers worldwide because of its adaptive abilities, recently emphasized in the western hemisphere by the emergence of strains that can reproduce sexually instead of solely relying on an asexual cycle (Gavino et al., 2000). Although many R genes have been incorporated into potatoes through traditional breeding strategies, the ability to rapidly adapt allows the fungus to overcome restrictions imposed by defense genes and chemical control measures. This example illustrates that research on the natural host plant is mandatory and that the current emphasis on cloning and deployment of R genes might benefit from the integration of efforts to develop broad-spectrum non-R gene defenses. Research on Phytophthora spp. remains at the forefront of our understanding of plant-microbe interactions, but it also illustrates that much work remains to be done (Judelson, 1997).

Our understanding of the molecular basis for pathogenicity benefits from studies on the plant pathogenic fungus Magnaporthe grisea, the causal agent of rice blast. This disease can devastate rice (Oryza sativa) crops and is a severe and ongoing threat in developing nations where rice is a staple food. Rice blast has served as a model system for the isolation and characterization of R genes (Jia et al., 2000), but it also has provided useful information on factors that are involved in the ability of a fungus to establish a systemic infection. Among other systems, this fungus and its host have served as a good model to study the signaling pathways that control how fungi may attach to the leaf surface, penetrate, and cause an infection (Dean, 1997). It is anticipated that with the ongoing efforts to sequence the genomes of M. grisea and rice, this system will soon unveil many molecular secrets of plant-pathogen interactions.

The systems described thus far are important from a fundamental and practical perspective to understand and control the disease symptoms caused by pathogens. Of immediate importance to public health is the study on toxins produced by plant-infecting fungi (i.e. mycotoxins). For example, several Fusarium and Aspergillus spp. infect many important crop plants. During infection these fungi produce secondary metabolites and in the case of Aspergillus parasiticus and Aspergillus flavus this culminates in the production of aflatoxins. Aflatoxins are acutely toxic to mammals and they also have potent carcinogenic properties. Animals and humans that consume food (e.g. corn [Zea mays] and peanuts [Arachis hypogaea]) contaminated with these pathogens can suffer serious health effects. A fungal model system is provided by Aspergillus nidulans because this fungus has a secondary metabolite pathway that is very similar to that in A. flavus, but A. nidulans does not produce the final aflatoxin product. Recent molecular studies with A. nidulans have yielded insights into the cluster of genes and enzymes (e.g. oxygenases) that control the production of secondary metabolites (Keller et al., 2000). These ongoing studies, aided by genomics efforts on this system, should elucidate the secondary metabolism pathway and its genetic control. This will be instrumental for the development of molecular strategies to safeguard the food supply from mycotoxin-producing fungi.

Plant pathogenic fungi also cause problems on trees. A good illustrative example is Cryphonectria parasitica, the causal agent of chestnut blight that has essentially eliminated chestnut (Castanea dentata) trees from U.S. forests. This fungus and its host have served as a very good model system to examine signaling pathways that control pathogenicity. C. parasitica is used as an example in this review because it introduces another level of complexity, in addition to the host and the pathogen. In nature, this fungus can be infected with viruses termed mycoviruses. Mycoviruses can cause various effects on the virulence of fungal pathogens and in the case of C. parasitica, these molecular parasites cause the fungus to be less virulent, i.e. hypovirulent (Nuss, 1996). This is a trait that is being evaluated for development of biological control strategies.

Another interesting conceptual question is how some fungi are able to coexist in close contact with plant cells for the uptake of essential nutrients without destroying the host tissue. Such intimate subtle interactions are established by some very important pathogens that cause rust or powdery mildew. These names accurately describe the rust-colored pustules and mycelial mats that can be seen following infection of wheat (Triticum aestivum) with Puccinia graminis or Erisyphe graminis, respectively. The stem rust pathogen P. graminis f. sp. tritici is a terrific example to illustrate another level of plant diversity because the fungus needs two taxonomically very different hosts, barberry (Berberis vulgaris) and wheat, to complete different stages of the life cycle (Peterson, 2001). Rust pathogens provide fundamental models for detailed investigation on the structures and interfaces between the fungi and their hosts necessary for exchange of nutrients and minerals, while avoiding the activation nonspecific plant defenses (Heath, 1997).

Not all compatible plant-microbe interactions are necessarily harmful to the plant. There are a number of fungi that can establish a symbiotic interaction that is mutually beneficial to pathogen and host (Smith and Goodman, 1999). In simplistic terms, many symbiotic interactions create a niche where the microbe provides the plant with extra nutrients or growth stimulators, or suppresses disease, and in turn, the plant provides a suitable habitat and photosynthates for the microbe. One example of successful symbionts are arbuscular mycorrhizal fungi that mobilize minerals from the soil in exchange for carbon nutrients provided by the plant. Within this context, it should be mentioned that certain soilborne microorganisms interfere with the ability of specific pathogens to infect plants; although not symbiotic, this also contributes to plant health (Handelsman and Stabb, 1996). Such complex microbe-pathogen-plant interactions are difficult to dissect at a molecular level but they are essential for the development of effective biological control strategies (Baek et al., 1999).

There are also many endosymbiotic fungi, most notably in grasses, that increase plant growth and they have an added interesting feature in that many produce alkaloids with insecticidal activity (Wilkinson et al., 2000). This again illustrates the intricate and diverse complexity of plant-microbe interactions because it suggests that plant endosymbionts can have an added evolutionary advantage for the plant by deterring insect attack. However, some of the alkaloids are harmful to cattle feeding on grasses. Molecular analyses to dissect the beneficial aspects from the harmful effects should improve the utility of these agronomically important symbiotic interactions (Panaccione et al., 2001).

	BACTERIA

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Many plant pathogenic bacteria are the subject of intense study (Alfano and Collmer, 1996) but one model system that consistently has yielded novel and valuable information on the molecular basis for bacterial diseases is represented by Pseudomonas spp. A popular research topic in bacteriology is quorum sensing, in which bacteria communicate with each other through the release and perception of signal molecules. Such studies on the quorum sensing signals produced by pathogenic phytobacteria may lead to a greater understanding of how leaf surfaces are colonized (Beattie and Lindow, 1999). This is also important in context of the regulation of gene expression for proteins that are necessary for the bacteria to infect plants, which also includes the production of bacterial toxins that influence pathogenicity (Bender et al., 1999).

Molecular studies on pseudomonads have identified a cluster of regulatory genes that are involved in the HR and in infection of plants, the so-called hrp genes. These hrp genes of phytobacteria are similar to genes that encode type III secretion factors produced by animal-infecting bacteria (Staskawicz et al., 2001). In this regard, it is quite intriguing that certain plant-infecting bacteria have apparently sufficiently conserved these features to provide them with the ability to be opportunistic human pathogens.

At present, agricultural plant biotechnology is largely dependent on our ability to create transgenic plants. This recent technological application is the result of earlier plant pathology research that addressed the question: How does Agrobacterium tumefaciens cause crown gall disease? It is now known that A. tumefaciens perceives wounded plant cells and this triggers the transfer of a DNA segment (T-DNA) that resides on an endogenous plasmid to the plant nucleus. The T-DNA is integrated into the chromosome to express genes that are responsible for formation of tumors. This ability to translocate DNA has been successfully exploited for customized transfer of DNA to many different plant species to regenerate transgenic plants with new genetic traits. The mechanism that A. tumefaciens uses to move its DNA is intriguing from a fundamental perspective because it is not only active in plants and fungi, but can also transform human cell lines (Kunik et al., 2001). This suggests that basic intercellular and intracellular transport mechanisms are conserved across kingdoms.

Just as there are fungi that provide nutrients for their hosts, there are also beneficial bacteria that infect plants. A classic example is represented by Rhizobium spp. that infect plants belonging to the legume family. The communication between the two organisms involves finely tuned signals (Long, 2001). Rhizobium spp. bacteria produce certain nodulation factors and these stimulate expression of plant proteins that induce the formation of nodules and are necessary for bacterial colonization and nitrogen fixation. Thus, the bacteria establish a symbiotic relationship with many important crop plants by supplying the ability for nitrogen fixation in exchange for the habitat and sugars provided by the plant.

Various plant systems are used to study symbiotic bacteria, and recently Medicago truncatula has become the Arabidopsis equivalent of legumes (Frugoli and Harris, 2001). Future research will benefit substantially from efforts to sequence the genomes of Rhizobium spp. and M. truncatula. Ultimately, our understanding of the symbiotic interaction may permit adaptation of various crop species to provide them with properties that are compatible for symbiotic interactions. This could substantially reduce the input of nitrogen fertilizer. Such a development would greatly benefit the environment by reducing contamination of ground water.

	VIRUSES

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The first pathogenic microbial agent to be recognized and classified as a virus was isolated over a hundred years ago from tobacco (Nicotiana tabacum) plants showing mosaic symptoms. The virus now known as Tobacco mosaic virus (TMV) has served as a model system in microbiology and has been instrumental for many scientific discoveries of biological principles (Creager et al., 1999). From a molecular plant virus perspective, a variety of different hosts for TMV and closely related viruses have been used to identify plant genes important for replication, movement, resistance, and symptom induction (Scholthof et al., 1999). One of the breakthroughs in the plant sciences in the past decade was the characterization of the TMV-specific N gene, one of the first R genes to be cloned and characterized (Whitham et al., 1994). The N gene was isolated after years of work on tobacco; Arabidopsis does not harbor this gene. However, certain strains of viruses similar to TMV infect Arabidopsis and it is anticipated that important complementary discoveries lie ahead.

Because viruses (and other subviral agents) are entirely dependent on their hosts, they provide excellent model systems to study basic molecular mechanisms that occur in plants with regards to regulatory interactions between nucleic acids and/or proteins. Many economically important viruses do not readily infect Arabidopsis and therefore basic research often relies on other host systems. It is impossible for me to summarize all the achievements made in recent years with the many virus host model systems that yielded insights into the mechanisms associated with different phases of the virus life cycle. Instead, I will focus on one particularly interesting question that has been a point of inquiry for decades, but until recently has been technically too challenging to address: What host proteins are involved in the different aspects of the virus infection?

All virus-like agents share the property that they are replicated inside host plant cells and it is generally assumed that this process involves the participation of host factors. Various laboratories are "hunting" for these host factors using a variety of plant systems. Particularly interesting is that some viruses can be transcribed and translated or even replicated in bakers' yeast (Sha et al., 1995; Noueiry et al., 2000). This feature is in itself interesting from an evolutionary standpoint. In addition, considering the vast genetic resources that are available for yeast, it is expected that this may yield many novel insights into molecular virus-host interactions. For example, recent investigations with this system have shown that eukaryotic translation factors may be involved in the replication of Brome mosaic virus (Noueiry et al., 2000). This would lend support to the speculation that translation of viral RNAs and their replication may be intricately linked.

Many viruses are transmitted from one plant to the next by insects or other biological vectors, and much information has been obtained through research with transmission of viruses by various species of aphids and thrips on numerous crop plants. An intriguing aspect with regards to replication has emerged in an indirect fashion through research on Tomato spotted wilt virus. This is an economically important virus that causes disease on numerous crops worldwide. However, not only can the virus replicate in many different plant species in diverse families, Tomato spotted wilt virus can also replicate in its thrips vector (Nagata et al., 1997). This implies that certain processes and host factors for virus replication must be extremely well conserved in different organisms. Within the context of virus transmission and "host" factors, recent studies have revealed other surprising new interactions. In particular, it was shown that proteins produced by endosymbiotic bacteria inside aphids may play a crucial role for virus transmission (Hogenhout et al., 2000). These proteins may protect the virus particles from degradation by the hostile proteolytic environment inside the insect hemolymph.

About a decade ago, it was firmly established that plant viruses encode specialized proteins that play a role in transporting virus ribonucleoprotein complexes through the plasmodesmata from one cell to the next. Biochemical studies on the TMV-tobacco model system were used to identify pectin methylesterase as the first known host protein that interacts with several virus movement proteins (Chen et al., 2000). How pectin methylesterase is involved in virus movement remains to be elucidated, but one possibility is that it guides the viral ribonucleoprotein complex to the cell periphery to permit subsequent passage through plasmodesmata for cell-to-cell movement.

Following cell-to-cell movement, the next phase in a virus life cycle includes vascular spread through the phloem (and perhaps xylem). A number of virus proteins might be involved in this process including the coat protein and nonstructural proteins. How these function is mostly unclear, but recent discoveries with different tobacco-virus combinations suggest a new avenue of exploration. At least some of the virus proteins that are required for spread can suppress posttranscriptional gene silencing, which is suspected to represent a plant defense strategy against viral invaders (Waterhouse et al., 2001). The question to be addressed is whether the posttranscriptional gene silencing suppression activity of virus proteins is directly responsible for virus spread or if these events are indirectly related, or perhaps unrelated.

A basic question with regards to virus infections is: What determines the host range of a virus? In other words, why are certain plant species susceptible to a particular virus whereas the same virus fails to infect other species? A related question is: Why is a given plant susceptible to one virus but not to another? These questions relate to host range determinants and reiterate the particular importance of host proteins. For example, studies with satellite panicum mosaic virus have shown that a small RNA element conveys a host-specific contribution to virus movement (Qiu and Scholthof, 2000), perhaps through its interaction with a host factor. Research with Tomato Bushy stunt virus on various plants showed that certain amino acids of a movement-associated protein need to be retained for activity in all its hosts but other residues have host-dependent activities (Chu et al., 2000). Future studies to isolate the corresponding host factors that interact with viral RNA or viral proteins should be very informative and may assist in developing novel control strategies.

	INCOMING THREATS

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Within the context of diversity, it is interesting to mention a few examples of emerging diseases that are (on the verge of) creating havoc in agriculture. The bacterial pathogen Xanthomonas axonopodis pv citri, which causes citrus canker, recently surfaced in Florida. There is no cure for this canker disease, and in an attempt to control spread of the disease an eradication program is in place to destroy all infected trees within a certain radius. However, this measure has been met with substantial resistance from local communities. This situation is reminiscent of the recent animal foot-and-mouth disease virus epidemic in Europe, and illustrates that diseases and their control have complex socioeconomic effects that provoke emotional responses unforeseen by designers of prevention schemes and economic models.

New variants of plant geminiviruses, which are whitefly-transmitted viruses with twin particles that contain single-stranded DNA, have surfaced in various parts of the world with devastating consequences, especially to small subsistence farmers. Additional viral threats (Simon-Moffat, 2001) are Plum pox virus, which causes severe symptoms on several stone fruits, Citrus tristeza virus on citrus trees, and a new virus transmitted by an eriophyid mite (Aceria tosichella Keifer) that causes disease in corn and wheat. These viruses, just like the well-studied economically important cucumoviruses, potyviruses, luteoviruses, and tospoviruses, are all transmitted by arthropod vectors. To battle virus spread in the absence of resistant plants, the vectors are often targeted through repetitive applications of pesticides, oftentimes with limited success. Therefore, fundamental research on the "old" and "new" viruses and their hosts is necessary for the development of new, environmentally responsible, and durable control measures.

	PLANTING AHEAD

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Arabidopsis has probably not yet been sufficiently explored for many plant-pathogen combinations, perhaps due to unfamiliarity of scientists with the system. In addition, some may harbor a preconceived bias against Arabidopsis-associated research, or other model-based systems. However, this will most likely dissipate, and many more of us will reap the benefits of the available Arabidopsis tools and information. Nevertheless, to more completely understand plant-microbe interactions on different crops and to develop durable and broad-spectrum control measures, functional genomics efforts on diverse plant systems will be instrumental.

The genomic sequence of numerous viruses is known and recently the genome of the first nonviral plant pathogen Xylella fastidiosa was determined (Simpson et al., 2000). Many others will hopefully follow. Obvious targets for plant genomics efforts are represented by bananas (Musa spp.), cotton (Gossypium hirsutum), cassava (Manihot esculenta), and various solanaceous crops (e.g. potatoes, tomatoes [Lycopersicon esculentum], and peppers [Capsicum annuum]). The rice genome sequence should soon be available, but other very important monocotyledonous systems (i.e. maize, millet [Setcria italica], wheat, barley [Hordeum vulgare], sorghum [Sorghum vulgare], and sugarcane [Saccharum officinarum]) await these efforts. Research on monocot systems is essential because these include primary food crops and they suffer from many diseases that cannot be studied using Arabidopsis. Furthermore, fundamental mechanisms that may be of practical value (i.e. gene silencing against viruses) may be conserved and operational in monocots, e.g. sugarcane (Ingelbrecht et al., 1999), but it is likely that unique monocot-specific factors are involved. Therefore, basic molecular plant-microbe studies need to be performed on model monocot systems most appropriate for the pathogen of study.

Considering the anticipated genomic initiatives on various plants, suitable alternative molecular genetic monocot and dicot model systems should become available in the coming decade. In anticipation of this information, the scenario in Figure 1 aims to illustrate a simplified applied molecular course of action to implement when an important disease problem (re-) emerges. Most disease problems are first noticed in the field and depending on the scope and urgency, this will immediately be followed by applied efforts to contain, control, or eradicate the pathogen. If the problem is sufficiently relevant from an economic perspective and interesting from a fundamental viewpoint, research on molecular interactions most likely will be performed on a model host system (Fig. 1). This can be the natural host or an alternative suitable plant species. Aided by genomics and functional genomics data, genes will be identified and/or manipulated to eliminate the pathogen, or protect the plant from either the infection or the symptoms. These modified genes can then be introduced into the natural host for performance evaluation. Independent of the source (Arabidopsis or other plants), and independent of the mechanism (e.g. R gene or gene silencing), all molecular genetic adaptations transferred to a new plant will have to be evaluated in the field under natural conditions. In the case of plant disease programs, this should include epidemiology and ecology studies, and integrate existing control measures to ensure that the most effective, durable, and environmentally responsible strategies will be practiced. Recent developments with genetically engineered foods have illustrated that it is also crucial to monitor societal acceptance of this modified agricultural system (Scholthof, 2001). The above scenario also applies to research on beneficial microbes to improve their positive contribution or adapt their use to a new host.

View larger version (33K): [in this window] [in a new window]   Figure 1.   Molecular strategy for studying plant-microbe interactions and developing control strategies.

It is anticipated that a rational systems approach with various model and crop plants will become possible in the future. This will substantially accelerate our ongoing efforts to understand complex susceptibility determinants in diverse plant species. This should, in turn, lead to an expanded use of beneficial microbes and the development of very effective and durable control measures against harmful pathogens.

	ACKNOWLEDGMENTS

I thank Karen-Beth G. Scholthof and Jim Schoelz for critically reading the manuscript and providing very good suggestions.

	FOOTNOTES

Received August 28, 2001; returned for revision September 10, 2001; accepted September 17, 2001.

¹ This work was supported by the Texas Agricultural Experiment Station (TEX08387), by the U.S. Department of Agriculture/Cooperative State Research, Education, and Extension Service-National Research Institute Competitive Grants Program (grant no. 99-35303-8022), by the Texas Higher Education Coordinating Board Advanced Technology Program (grant no. 000517-0070-1999), and by The S.R. Noble Foundation, Inc. (Ardmore, OK).

^* E-mail herscho{at}tamu.edu; fax 979-845-6483.

www.plantphysiol.org/cgi/doi/10.1104/pp.010789.

	LITERATURE CITED

TOP INTRODUCTION PLANTS AND MICROBES RESISTANCE AND SUSCEPTIBILITY A PLEA FOR DIVERSITY SPECIFIC EXAMPLES OF MODEL... FUNGI AND RELATED MULTICELLULAR... BACTERIA VIRUSES INCOMING THREATS PLANTING AHEAD LITERATURE CITED

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