The Influence of Flower Anatomy and Apple Cultivar on the Apple Flower Phytobiome

Steven, Blaire; Huntley, Regan B.; Zeng, Quan

doi:10.1094/pbiomes-03-18-0015-r

Cited by 73 publications

(50 citation statements)

References 37 publications

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“…The stigma is particularly nutrient rich and harbors a larger microbial biomass than other flower parts (5, 6). Previous research has documented a relatively low diversity of the stigma microbiome, although certain lineages predominantly within the families Enterobacteriaceae and Pseudomonadaceae tend to be dominant (7).…”

Section: Introductionmentioning

confidence: 99%

Temporal and spatial dynamics in the apple flower microbiome in the presence of the phytopathogenErwinia amylovora

Cui

Huntley

Zeng

et al. 2020

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17Plant microbiomes have important roles in plant health and productivity. However, 18 despite flowers being directly linked to reproductive outcomes, little is known about the 19 microbiomes of flowers and their potential interaction with pathogen infection. Here, we 20 investigated the temporal dynamics and spatial traits of the apple stigma microbiome 21 when challenged with a phytopathogen Erwinia amylovora, the causal agent of fire blight 22 disease. We profiled the microbiome from the stigmas of a single flower, greatly 23 increasing the resolution at which we can characterize shifts in the composition of the 24 microbiome. Individual flowers harbored unique microbiomes at the OTU level. 25However, taxonomic analysis of community succession showed a population gradually 26 dominated by bacteria within the families Enterobacteriaceae and Pseudomonadaceae. 27 Flowers inoculated E. amylovora established large populations of the phytopathogen, 28 with pathogen specific gene counts of >3.0 x 10 7 in 90% of the flowers. Yet, only 42% of 29 inoculated flowers later developed fire blight symptoms. This reveals pathogen amount 30 on the stigma is not sufficient to predict disease outcome. Our data demonstrate that 31 apple flowers represent an excellent model in which to characterize how plant 32 microbiomes establish, develop, and interact with biological processes such as disease 33 progression in an experimentally tractable plant organ.34 35 36 37 38 39 40 Flowers, the reproductive organs of angiosperms, play a critical role in the plant's 41 lifecycle. The most important function of flowers is to provide a mechanism for 42 pollination, the union of sperm contained within pollen, to the ovules contained in the 43 ovary. The fertilized ovules produce seeds that will later germinate to become the next 44 generation of plants. Yet, unlike other vegetative organs such as the roots, stems, and 45 leaves that are present through a large part of the plant's lifecycle, flowers develop on 46 mature plants and are typically present for the limited period during bloom. As such, 47 research characterizing the microbiome of the flower is generally less developed than for 48 other plant organs. 49 Flowers of apple (Malus domestica) have been subject to considerable research 50 attention as they are the direct precursors of apple fruits, one of the most consumed fruits 51 worldwide (1). The ephemeral nature of apple flowers, with mature flowers from petal 52 open to petal fall only lasting for 5-10 days in spring, offers a unique environment in 53 which to study community succession (1, 2). During bloom, petals open up in a relatively 54 short period of time, typically within one day, which exposes the internal flower parts to 55 the environment and microorganisms. Several of these internal flower parts exude various 56 types of nutrient-rich secretions including nectar, stigmatic exudate, and pollen exudate, 57 for the purpose of attracting pollinators, and inducing the germination of pollen grains (1, 58 3). These secretio...

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Section: Introductionmentioning

confidence: 99%

Temporal and spatial dynamics in the apple flower microbiome in the presence of the phytopathogenErwinia amylovora

Cui

Huntley

Zeng

et al. 2020

Preprint

Self Cite

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“…, Steven et al. ). Indeed, different flower organs (e.g., corolla, pistil, stamens, and nectary) can possess distinct microbial communities (Aleklett et al.…”

Section: Introductionmentioning

confidence: 99%

“…, Junker and Keller , Steven et al. ; M. Rebolleda‐Gómez and T.‐L. Ashman, unpublished manuscript ), but it is not known whether this is due to differences in dispersal mediated via interactions with pollinators or differences in the strength of floral organs as environmental filters (Allard et al.…”

Section: Introductionmentioning

confidence: 99%

“…The dispersal of floral microbes has been considered nearly exclusively in the context of pollinators visiting flowers for nectar (Brysch-Herzberg 2004, Herrera et al 2008, Hausmann et al 2017. Yet flowers are complex structures composed of multiple organs that differ in morphology, function, and suitability as habitats for floral microbes (Aleklett et al 2014, Steven et al 2018. Indeed, different flower organs (e.g., corolla, pistil, stamens, and nectary) can possess distinct microbial communities (Aleklett et al 2014, Junker and Keller 2015, Steven et al 2018; M. Rebolleda-G omez and T.-L. Ashman, unpublished manuscript), but it is not known whether this is due to differences in dispersal mediated via interactions with pollinators or differences in the strength of floral organs as environmental filters (Allard et al 2018; M. Rebolleda-G omez and T.-L. Ashman, unpublished manuscript).…”

Section: Introductionmentioning

confidence: 99%

“…Yet flowers are complex structures composed of multiple organs that differ in morphology, function, and suitability as habitats for floral microbes (Aleklett et al 2014, Steven et al 2018. Indeed, different flower organs (e.g., corolla, pistil, stamens, and nectary) can possess distinct microbial communities (Aleklett et al 2014, Junker and Keller 2015, Steven et al 2018; M. Rebolleda-G omez and T.-L. Ashman, unpublished manuscript), but it is not known whether this is due to differences in dispersal mediated via interactions with pollinators or differences in the strength of floral organs as environmental filters (Allard et al 2018; M. Rebolleda-G omez and T.-L. Ashman, unpublished manuscript). Pollinators physically interact with different floral organs to varying degrees (Laverty 1980), which should mediate patterns of microbial dispersal among floral organs, and, subsequently, microbial community assembly.…”

Section: Introductionmentioning

confidence: 99%

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Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

et al. 2019

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Dispersal is central to the ecology and evolution of spatially structured communities. While flower microbial communities are spatially structured among floral organs, how dispersal vectors distribute microbes among floral organs is unknown. Pollinators are recognized as key microbial vectors, but effects of their different foraging behaviors on transfer dynamics among flowers or different floral organs are not known. We asked how foraging behaviors of a model pollinator (Bombus impatiens) affect acquisition and dispersal of microbes among flower organs. We used monkeyflowers (Mimulus guttatus) to examine dispersal within a natural context and artificial flowers to test how common bee foraging behaviors (nectaring, buzzing, or scrabbling) shaped dispersal of a green fluorescent protein‐labeled bacteria, Pseudomonas fluorescens. Bees acquired 1% of a flower's microbes and dispersed 31% of acquired microbes to the next flower. All bees acquired microbes, and 85% and 76% of bees dispersed microbes to live and artificial flowers, respectively. Microbes acquired from the corolla were mainly deposited on the corolla, followed by the stamens, and least on the nectary/pistil. Bee foraging behavior affected acquisition, with scrabbling for pollen resulting in 23% more microbes acquired than nectaring, and with buzzing for pollen resulting in a 79% slower rate of microbial acquisition relative to scrabbling. Bee foraging behavior also affected deposition but depended on the floral organ: Scrabbling and buzzing for pollen led to greater deposition than nectaring for corolla and stamen but not nectary. Our results have implications for transmission of beneficial and pathogenic microbes among plants and pollinators, and thus the ecology and evolution of floral microbial communities.

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Spatially explicit depiction of a floral epiphytic bacterial community reveals role for environmental filtering within petals

et al. 2021

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The microbiome of flowers (anthosphere) is an understudied compartment of the plant microbiome. Within the flower, petals represent a heterogeneous environment for microbes in terms of resources and environmental stress. Yet, little is known of drivers of structure and function of the epiphytic microbial community at the within‐petal scale. We characterized the petal microbiome in two co‐flowering plants that differ in the pattern of ultraviolet (UV) absorption along their petals. Bacterial communities were similar between plant hosts, with only rare phylogenetically distant species contributing to differences. The epiphyte community was highly culturable (75% of families) lending confidence in the spatially explicit isolation and characterization of bacteria. In one host, petals were heterogeneous in UV absorption along their length, and in these, there was a negative relationship between growth rate and position on the petal, as well as lower UV tolerance in strains isolated from the UV‐absorbing base than from UV reflecting tip. A similar pattern was not seen in microbes isolated from a second host whose petals had uniform patterning along their length. Across strains, the variation in carbon usage and chemical tolerance followed common phylogenetic patterns. This work highlights the value of petals for spatially explicit explorations of bacteria of the anthosphere.

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The Influence of Flower Anatomy and Apple Cultivar on the Apple Flower Phytobiome

Cited by 73 publications

References 37 publications

Temporal and spatial dynamics in the apple flower microbiome in the presence of the phytopathogenErwinia amylovora

Temporal and spatial dynamics in the apple flower microbiome in the presence of the phytopathogenErwinia amylovora

Movers and shakers: Bumble bee foraging behavior shapes the dispersal of microbes among and within flowers

Spatially explicit depiction of a floral epiphytic bacterial community reveals role for environmental filtering within petals

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