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The Ecology and Natural History of Foliar Bacteria with a Focus on Tropical Forests and Agroecosystems

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Abstract

Leaves of higher plants comprise perhaps the largest bacterial substrate on earth, yet we know very little about the bacteria that occupy these spaces. In this review, we first examine the ecology and behavior of bacteria that reside on leaf surfaces. Next, we discuss the ecological implications of foliar bacteria that reside in interior portions of leaf tissues. Later, we consider the studies on foliar bacteria in tropical habitats to date. Finally, we examine evidence regarding the potential roles of foliar bacteria in structuring tropical plant communities. Bacteria colonize the phyllosphere via animal vectors or passively from soil, wind, or rain, though there are too few data to determine the relative contributions of these sources to the phyllosphere. Additionally, the degree to which parent plants transmit bacteria to offspring via seed remains unknown. We predict that high temperature, high humidity, low UV radiation, and leaf architecture in the tropical understory enable tropical leaves to support more abundant and diverse bacterial communities compared to temperate leaves. While the extent of competitive interactions among bacteria remains poorly resolved, evidence from agricultural crop species and Arabidopsis thaliana suggests that these interactions cause niche partitioning based on carbon use. The degree to which phyllobacteria and endophytes of tropical plants are pathogenic versus mutualistic or neutral remains unexplored. We hypothesize, however, that the detrimental impact of bacterial pathogens ultimately increases as the abundance of single host tree species increases, which can promote and maintain plant diversity in tropical forests.

Resumen

Las hojas de las plantas superiores constituyen posiblemente el sustrato bacteriológico más extenso en el planeta, sin embargo sabemos muy poco sobre las bacterias que ocupan estos espacios. En este artículo examinamos, en primer lugar, la ecología y el comportamiento de las bacterias que residen en las superficies de las hojas. Luego, discutimos las implicaciones ecológicas de las bacterias foliares que residen en el interior de los tejidos de las hojas. Además, consideramos los estudios sobre bacterias foliares en hábitats tropicales a la fecha. Finalmente examinamos la evidencia que existe sobre el potencial impacto de las bacterias foliares en la estructura de comunidades de plantas tropicales. Las bacterias generalmente colonizan la filosfera a través de vectores animales o pasivamente a través del suelo, el viento o la lluvia, aunque hay poca información para determinar la contribución relativa de estas fuentes a la filosfera. Adicionalmente, no se sabe hasta qué punto ocurre una transmisión bacteriana de progenitor a progenie a través de semillas. Predecimos que las altas temperaturas, la elevada humedad, la baja radiación ultravioleta, y la arquitectura de las hojas en el sotobosque permiten que las hojas tropicales contengan comunidades bacteriológicas más abundantes y diversas en comparación con hojas de clima templado. Aunque el grado de interacciones competitivas entre bacterias aún no ha sido bien entendido, evidencia de especies de interés agronómico y Arabidopsis thaliana sugiere que estas interacciones causan particiones de nicho basadas en el uso de carbono. La naturaleza patógena, mutualista o neutra de las filobacterias y bacterias endófitas de plantas tropicales no se ha explorado hasta el momento. Nuestra hipótesis es, sin embargo, que el impacto negativo de patógenos bacterianos es mayor con el incremento en la abundancia de huéspedes específicos, lo que puede promover y mantener la diversidad de plantas en los bosques tropicales.

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Acknowledgments

We thank Joe Wright, Bert Leigh, Carolin Frank, Shannon Nix, Mike Chips, Sarah Neihaus, Camilo Zalamea, Carolina Sarmiento, the Carson-Pruitt Lab Group, three anonymous reviewers, and in particular Brian Traw and Betsy Arnold for comments on various drafts of this manuscript. We thank Felipe Lacayo for translating the abstract into Spanish. We acknowledge financial support from a National Science Foundation Graduate Research Fellowship, a Smithsonian Tropical Research Institute Predoctoral Fellowship, a Lewis and Clarke Fund for Exploration and Field Research, Sigma Xi Grant-in-Aid of Research, and a CRDF grant from the University of Pittsburgh.

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Table 4 The scientific names associated with common names of plant species used in this manuscript

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Griffin, E.A., Carson, W.P. The Ecology and Natural History of Foliar Bacteria with a Focus on Tropical Forests and Agroecosystems. Bot. Rev. 81, 105–149 (2015). https://doi.org/10.1007/s12229-015-9151-9

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