Evidence for Widespread Microbivory of Endophytic Bacteria in Roots of Vascular Plants Through Oxidative Degradation in Root Cell Periplasmic Spaces

White, James F.; Torres, Mónica S.; Verma, Satish; Elmore, Matthew T.; Kowalski, Kurt P.; Kingsley, Kathryn L.

doi:10.1016/b978-0-12-815879-1.00009-4

Cited by 15 publications

(28 citation statements)

References 79 publications

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“…However, it may be that acquisition of difficult to obtain micronutrients ( e.g ., iron, copper, zinc) is a key function of the rhizophagy cycle. Microbes possess siderophores and other mechanisms that sequester micronutrients efficiently and many are motile and move around in soils acquiring nutrients . Metals also adhere to the cell walls of microbes because microbe cell walls have a net negative charge, while metals have a positive charge .…”

Section: Nutritional Functions Of Endophytesmentioning

confidence: 99%

“…Microbes possess siderophores and other mechanisms that sequester micronutrients efficiently and many are motile and move around in soils acquiring nutrients . Metals also adhere to the cell walls of microbes because microbe cell walls have a net negative charge, while metals have a positive charge . Unlike nodule‐forming symbioses, the rhizophagy cycle appears to occur in most vascular plants and likely represents an important mechanism for nutrient acquisition by plants …”

Section: Nutritional Functions Of Endophytesmentioning

confidence: 99%

“…27 Unlike nodule-forming symbioses, the rhizophagy cycle appears to occur in most vascular plants and likely represents an important mechanism for nutrient acquisition by plants. 27…”

Section: Rhizophagy Cycle and Nutrient Acquisitionmentioning

confidence: 99%

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Review: Endophytic microbes and their potential applications in crop management

White

Kingsley

Zhang

et al. 2019

Pest Management Science

293

200

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Endophytes are microbes (mostly bacteria and fungi) present asymptomatically in plants. Endophytic microbes are often functional in that they may carry nutrients from the soil into plants, modulate plant development, increase stress tolerance of plants, suppress virulence in pathogens, increase disease resistance in plants, and suppress development of competitor plant species. Endophytic microbes have been shown to: (i) obtain nutrients in soils and transfer nutrients to plants in the rhizophagy cycle and other nutrient‐transfer symbioses; (ii) increase plant growth and development; (iii) reduce oxidative stress of hosts; (iv) protect plants from disease; (v) deter feeding by herbivores; and (vi) suppress growth of competitor plant species. Because of the effective functions of endophytic microbes, we suggest that endophytic microbes may significantly reduce use of agrochemicals (fertilizers, fungicides, insecticides, and herbicides) in the cultivation of crop plants. The loss of endophytic microbes from crop plants during domestication and long‐term cultivation could be remedied by transfer of endophytes from wild relatives of crops to crop species. Increasing atmospheric carbon dioxide levels could reduce the efficiency of the rhizophagy cycle due to repression of reactive oxygen used to extract nutrients from microbes in roots. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

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Section: Nutritional Functions Of Endophytesmentioning

confidence: 99%

Section: Nutritional Functions Of Endophytesmentioning

confidence: 99%

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Review: Endophytic microbes and their potential applications in crop management

White

Kingsley

Zhang

et al. 2019

Pest Management Science

293

200

View full text Add to dashboard Cite

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“…White et al [ 44 ] later documented internalization of bacteria into periplasmic spaces of root cells and their oxidative degradation within cells through use of a reactive oxygen staining technique. Collectively, these observations have suggested that plants are engaging in a process of microbivory in order to extract nutrients from microbes that colonize roots [ 45 , 46 ].…”

Section: Introductionmentioning

confidence: 99%

“…Over the past several years, we have conducted experiments using various host species and endophytic bacteria to elucidate how the plant microbivory process works in plant roots [ 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 ]. In this paper, we describe features of the microbivory process and hypotheses with regard to how the process works.…”

Section: Introductionmentioning

confidence: 99%

Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction from Symbiotic Microbes

et al. 2018

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In this paper, we describe a mechanism for the transfer of nutrients from symbiotic microbes (bacteria and fungi) to host plant roots that we term the ‘rhizophagy cycle.’ In the rhizophagy cycle, microbes alternate between a root intracellular endophytic phase and a free-living soil phase. Microbes acquire soil nutrients in the free-living soil phase; nutrients are extracted through exposure to host-produced reactive oxygen in the intracellular endophytic phase. We conducted experiments on several seed-vectored microbes in several host species. We found that initially the symbiotic microbes grow on the rhizoplane in the exudate zone adjacent the root meristem. Microbes enter root tip meristem cells—locating within the periplasmic spaces between cell wall and plasma membrane. In the periplasmic spaces of root cells, microbes convert to wall-less protoplast forms. As root cells mature, microbes continue to be subjected to reactive oxygen (superoxide) produced by NADPH oxidases (NOX) on the root cell plasma membranes. Reactive oxygen degrades some of the intracellular microbes, also likely inducing electrolyte leakage from microbes—effectively extracting nutrients from microbes. Surviving bacteria in root epidermal cells trigger root hair elongation and as hairs elongate bacteria exit at the hair tips, reforming cell walls and cell shapes as microbes emerge into the rhizosphere where they may obtain additional nutrients. Precisely what nutrients are transferred through rhizophagy or how important this process is for nutrient acquisition is still unknown.

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