A Model Relating the Probability of Foliar Disease Incidence to the Population Frequencies of Bacterial Plant Pathogens

Rouse, D. I.

doi:10.1094/phyto-75-505

Cited by 81 publications

(50 citation statements)

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“…Characterization of bacteria isolated from the lesions confirmed that the hrcC and hrpJ mutants were the causal agents of the lesions detected in the field plots inoculated with these strains. The small amounts of disease caused by the secretion mutants are generally consistent with the dose-response experiments of Rouse et al (246). The observation that hrp mutants are able to cause some disease in the field is also consistent with findings reported in the initial publication on hrp genes (174).…”

Section: Genes Associated With Pathogenicitysupporting

confidence: 89%

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Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

Hirano

Upper

2000

Microbiol Mol Biol Rev

834

610

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SUMMARY The extremely large number of leaves produced by terrestrial and aquatic plants provide habitats for colonization by a diversity of microorganisms. This review focuses on the bacterial component of leaf microbial communities, with emphasis on Pseudomonas syringae—a species that participates in leaf ecosystems as a pathogen, ice nucleus, and epiphyte. Among the diversity of bacteria that colonize leaves, none has received wider attention than P. syringae, as it gained notoriety for being the first recombinant organism (Ice− P. syringae) to be deliberately introduced into the environment. We focus on P. syringae to illustrate the attractiveness and somewhat unique opportunities provided by leaf ecosystems for addressing fundamental questions of microbial population dynamics and mechanisms of plant-bacterium interactions. Leaf ecosystems are dynamic and ephemeral. The physical environment surrounding phyllosphere microbes changes continuously with daily cycles in temperature, radiation, relative humidity, wind velocity, and leaf wetness. Slightly longer-term changes occur as weather systems pass. Seasonal climatic changes impose still a longer cycle. The physical and physiological characteristics of leaves change as they expand, mature, and senesce and as host phenology changes. Many of these factors influence the development of populations of P. syringae upon populations of leaves. P. syringae was first studied for its ability to cause disease on plants. However, disease causation is but one aspect of its life strategy. The bacterium can be found in association with healthy leaves, growing and surviving for many generations on the surfaces of leaves as an epiphyte. A number of genes and traits have been identified that contribute to the fitness of P. syringae in the phyllosphere. While still in their infancy, such research efforts demonstrate that the P. syringae-leaf ecosystem is a particularly attractive system with which to bridge the gap between what is known about the molecular biology of genes linked to pathogenicity and the ecology and epidemiology of associated diseases as they occur in natural settings, the field.

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Section: Genes Associated With Pathogenicitysupporting

confidence: 89%

“…The P. syringae pv. syringae-snap bean-bacterial brown spot disease is one such system (111,112,167,246). The experimental approaches used by Lindemann et al (167) and Rouse et al (246) were similar in the sense that the relationship between epiphytic population sizes of P. syringae pv.…”

Section: Relationship Between Epiphytic Bacterial Population Sizes Anmentioning

confidence: 99%

Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

Hirano

Upper

2000

Microbiol Mol Biol Rev

834

610

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“…Bacterial alteration of the host plant environment has been traditionally associated with plantpathogenic bacteria. The ability of plant-pathogenic bacteria such as P. syringae to cause disease is strongly correlated with their epiphytic population sizes on leaves (66,97,105) and probably also with that subset of the population that is within symptomless leaves and, thus, in more intimate contact with plant cells (8,118). Considerable attention has been given to the characterization of the molecular determinants that are involved in the interaction of P. syringae with its host, particularly the hypersensitive response and pathogenicity (hrp) genes.…”

Section: Microbial Modification Of the Leaf Habitatmentioning

confidence: 99%

Microbiology of the Phyllosphere

Lindow

Brandl

2003

Appl Environ Microbiol

1,819

1,418

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2The above-ground parts of plants are normally colonized by a variety of bacteria, yeasts, and fungi. While a few microbial species can be isolated from within plant tissues, many more are recovered from the surfaces of healthy plants. The aerial habitat colonized by these microbes is termed the phyllosphere, and the inhabitants are called epiphytes. While there has been some investigation of the colonists of buds and flowers (1, 48), most work on phyllosphere microbiology has focused on leaves, a more dominant aerial plant structure. Bacteria are by far the most numerous colonists of leaves, often being found in numbers averaging 10 6 to 10 7 cells/cm 2 (up to 10 8 cells/g) of leaf (1,7,41). Because of their numerical dominance on leaves, and because more information is available on the process of bacterial colonization of leaves, we focus on this group of microbes in this review.Compared to most other bacterial habitats, there has been relatively little examination of phyllosphere microbiology. This is somewhat surprising given the abundance of plants in the world and the roles of various phyllosphere bacteria in the important processes discussed below. Leaves constitute a very large microbial habitat. It is estimated that the terrestrial leaf surface area that might be colonized by microbes is about 6.4 ϫ 10 8 km 2 (83). Given the large number of bacteria on leaves in temperate regions of the world and that populations in tropical regions are probably even larger, the planetary phyllosphere bacterial population may be as large as 10 26 cells (83). Clearly, in aggregate, these bacteria are sufficiently numerous to contribute in many processes of importance to global processes, as well as to the behavior of the individual plants on which they live.In the following sections we review available information on the identities and properties of the bacterial colonists of plant surfaces as well as describe the nature of the leaf surface habitat that these bacteria colonize. We emphasize the results of studies using new molecular and microscopic tools that have provided new insights into both the identity and the behavior of epiphytes, as well as into the nature of the plant surfaces that they inhabit. Also, we review recent studies of the interactions of various epiphytic bacteria with plants, which suggest that there is much more interaction between them than in a strict commensalistic relationship, in which they have been traditionally considered to coexist. The interactions that occur between bacteria on leaves have also received considerable attention. We attempt to illustrate how new approaches to defining the nature of leaf surface habitats have helped us to understand the behavior and interactions of epiphytic bacteria as well as why leaves are a particularly suitable habitat for exploring processes in microbial ecology. More comprehensive reviews of phyllosphere microbiology also address other important features of this interesting association (1,7,8,41,47,55,73). MICROBIAL COMMUNITIES ON LEAVESThe microbial ...

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“…syringae (Pss), the causal agent of brown spot disease of bean and frost injury to plants (12). Pss can multiply to high population sizes on the surface of healthy leaves, and these large epiphytic populations precede disease (13). Pss forms aggregates of various sizes while growing on leaves, presumably in response to local differences in nutrient availability on the leaf.…”

mentioning

confidence: 99%

Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface

Dulla

Lindow

2008

Proc. Natl. Acad. Sci. U.S.A.

111

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The paradigm of bacterial quorum sensing (QS), which mediates cell-density-dependent gene expression, usually has been studied in high-cell-density planktonic liquid cultures or in biofilms in which signal concentrations accumulate to sufficiently high levels to induce QS. Presumably under conditions with restricted diffusion of the signal molecule, smaller population sizes could achieve such a state of QS induction. The plant-pathogenic bacterium Pseudomonas syringae, in which QS controls traits involved in epiphytic fitness and virulence, occurs on leaf surfaces in aggregates of various sizes. Because leaves often harbor limited surface water, we investigated the size of aggregates that would permit QS in a nonsaturated environment. QS induction was visualized via dual fluorescence of P. syringae cells harboring a transcriptional fusion of mRFP1 with ahlI, which exhibits N-acyl homoserine lactone-dependent transcriptional activity, and a constitutive GFP marker to account for all P. syringae cells on a leaf. Confocal microscopy revealed that, on wet leaves, no QS induction was evident within 2 days after inoculation, but it increased rapidly with increasing aggregate sizes >40 and 22 cells per aggregate by 3 and 4 days, respectively. In contrast, QS induction was common in aggregates >33 cells by 2 days after inoculation on dry leaves and increased rapidly with increasing aggregate sizes >35 and 13 cells after 3 and 4 days, respectively. These observations demonstrate that small groups of cells experience QS conditions on dry leaves where signal diffusion is restricted. Quorum size of bacteria in non-water-saturated environments such as on leaves is small, and QS induction may be commonly operative.aggregate ͉ diffusion ͉ quorum sensing ͉ epiphyte ͉ bioreporter

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A Model Relating the Probability of Foliar Disease Incidence to the Population Frequencies of Bacterial Plant Pathogens

Cited by 81 publications

References 0 publications

Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

Bacteria in the Leaf Ecosystem with Emphasis onPseudomonas syringae—a Pathogen, Ice Nucleus, and Epiphyte

Microbiology of the Phyllosphere

Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface

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