Occurrence of Indole-3-Acetic Acid-Producing Bacteria on Pear Trees and Their Association with Fruit Russet

Lindow, Steven E.; Desurmont, Caroline; Elkins, Rachel; McGourty, Glenn; Clark, Elizabeth G.; Brandl, Maria T.

doi:10.1094/phyto.1998.88.11.1149

Cited by 76 publications

(46 citation statements)

References 33 publications

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“…Bacterial strains that were tested for their ability to degrade IAA were originally isolated from Bartlett pear trees in orchards located near Healdsburg, CA (25). Erwinia herbicola 299R (3) served as a positive control for IAA production and as a negative control for IAA degradation.…”

Section: Methodsmentioning

confidence: 99%

“…Later, BIPs were identified as the cause of symptoms associated with severe plant diseases such as gypsophila gall (26), knot disease of olive and oleander (43), and russet of pear fruit (25), or, in other cases, as benefactors of plants, e.g., nitrogen-fixing Bradyrhizobium japonicum in root nodules (9) and plant-growth-promoting rhizobacteria such as Pseudomonas putida (33). Since the initial discovery of BIPs, an impressive body of scientific information has been established on the biology, ecology, and pathology of these bacteria, and much of the genetics and biochemistry of bacterial IAA production has been elucidated (20,32).…”

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confidence: 99%

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Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290

Leveau

Lindow

2005

Appl Environ Microbiol

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269

146

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We have isolated from plant surfaces several bacteria with the ability to catabolize indole-3-acetic acid (IAA). One of them, isolate 1290, was able to utilize IAA as a sole source of carbon, nitrogen, and energy. The strain was identified by its 16S rRNA sequence as Pseudomonas putida. Activity of the enzyme catechol 1,2-dioxygenase was induced during growth on IAA, suggesting that catechol is an intermediate of the IAA catabolic pathway. This was in agreement with the observation that the oxygen uptake by IAA-grown P. putida 1290 cells was elevated in response to the addition of catechol. The inability of a catR mutant of P. putida 1290 to grow at the expense of IAA also suggests a central role for catechol as an intermediate in IAA metabolism. Besides being able to destroy IAA, strain 1290 was also capable of producing IAA in media supplemented with tryptophan. In root elongation assays, P. putida strain 1290 completely abolished the inhibitory effect of exogenous IAA on the elongation of radish roots. In fact, coinoculation of roots with P. putida 1290 and 1 mM concentration of IAA had a positive effect on root development. In coinoculation experiments on radish roots, strain 1290 was only partially able to alleviate the inhibitory effect of bacteria that in culture overproduce IAA. Our findings imply a biological role for strain 1290 as a sink or recycler of IAA in its association with plants and plant-associated bacteria.One intriguing type of interorganismal interaction is the manipulation by some microbes of their host's hormone system. A good example is given by bacteria of the genus Wolbachia, which convert male woodlice into females, supposedly by suppressing a gland that produces a masculinizing hormone (37). Another striking example is the microbial production of plant hormones such as auxin, cytokinin, and gibberellin, which allows certain bacteria and fungi to direct a plant's physiology toward their own advantage (5,7,14,20).Indole-3-acetic acid (IAA) is the main auxin in plants, controlling many important physiological processes including cell enlargement and division, tissue differentiation, and responses to light and gravity (45). Bacterial IAA producers (BIPs) have the potential to interfere with any of these processes by input of IAA into the plant's auxin pool. The consequence for the plant is usually a function of (i) the amount of IAA that is produced and (ii) the sensitivity of the plant tissue to changes in IAA concentration. A root, for instance, is one of the plant's organs that is most sensitive to fluctuations in IAA, and its response to increasing amounts of exogenous IAA extends from elongation of the primary root, formation of lateral and adventitious roots, to growth cessation (8).The existence of BIPs was recognized very early in the research on auxin, and plant-associated BIPs have long been considered a source of contamination in measurements of IAA present in plant tissues (24, 51, 52). Later, BIPs were identified as the cause of symptoms associated with severe plant disease...

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Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290

Leveau

Lindow

2005

Appl Environ Microbiol

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269

146

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“…In contrast to the production of biosurfactants and syringomycin, which appears to be restricted to Pseudomonas species, the biosynthesis of the plant growth regulator indole-3-acetic acid (IAA) is widespread among bacterial colonizers of the phyllosphere (14,27,32,71). Although bacterial production of auxin is a major pathogenicity determinant in many bacteria inducing hyperplasia on plants (122), its role in other pathogenic and nonpathogenic plant-associated bacteria has not been determined.…”

Section: Microbial Modification Of the Leaf Habitatmentioning

confidence: 99%

Microbiology of the Phyllosphere

Lindow

Brandl

2003

Appl Environ Microbiol

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1,796

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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“…Bacteria that produce plant hormones may also alter leaf and fruit habitats. For example, strains of E. herbicola that produce indoleacetic acid cause russetting of pear fruit (194). Habitat modification by pathogenic and ice nucleation-active P. syringae will be discussed further in subsequent sections.…”

Section: The Playersmentioning

confidence: 99%

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

Hirano

Upper

2000

Microbiol Mol Biol Rev

826

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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Occurrence of Indole-3-Acetic Acid-Producing Bacteria on Pear Trees and Their Association with Fruit Russet

Cited by 76 publications

References 33 publications

Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290

Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290

Microbiology of the Phyllosphere

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

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