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  • From: Lawrence London <lfljvenaura@gmail.com>
  • To: permaculture <permaculture@lists.ibiblio.org>, sustagnet@googlegroups.com
  • Subject: [permaculture] Microorganisms | Free Full-Text | Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction from Symbiotic Microbes | HTML
  • Date: Thu, 23 Jan 2020 12:53:54 -0500

Microorganisms | Free Full-Text | Rhizophagy Cycle: An Oxidative Process in
Plants for Nutrient Extraction from Symbiotic Microbes | HTML
https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM

*Microorganisms* *2018*, *6*(3), 95;
https://doi.org/10.3390/microorganisms6030095
Review
Rhizophagy Cycle: An Oxidative Process in Plants for Nutrient Extraction
from Symbiotic Microbes
by James F. White <https://sciprofiles.com/profile/511307> 1,*
<https://orcid.org/0000-0002-6780-7066>, Kathryn L. Kingsley
<https://sciprofiles.com/profile/author/TDBjQ0Y0S1NCbHBqRkpvdUg0V3UzTmYyVDBlN1lwZHdmaTh6T1dHdG1XWT0=>
1, Satish K. Verma <https://sciprofiles.com/profile/381158> 2 and Kurt P.
Kowalski <https://sciprofiles.com/profile/402251> 3
<https://orcid.org/0000-0002-8424-4701>
1
Department of Plant Biology, Rutgers University, New Brunswick, NJ 08901,
USA
2
Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, UP
221005, India
3
U.S. Geological Survey, Great Lakes Science Center, 1451 Green Road, Ann
Arbor, MI 48105-2807, USA
*
Author to whom correspondence should be addressed.
Received: 22 August 2018 / Accepted: 5 September 2018 / Published: 17
September 2018
Download PDF <https://www.mdpi.com/2076-2607/6/3/95/pdf>
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Abstract*:*
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.
Keywords:
endobiome; endophyte; nutrient transport; reactive oxygen; rhizosphere;
symbiosis
1. Introduction
It is widely known and accepted that most plants obtain nutrients generally
through absorption of dissolved inorganic nutrients from soils [1
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B1-microorganisms-06-00095>].
However, it is also known that some plants engage in nitrogen-transfer
symbioses where plants associate with prokaryotes that fix nitrogen in
association with roots and transfer that nitrogen to plants [2
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B2-microorganisms-06-00095>
,3
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Among these nitrogen-transfer symbioses are actinorhizal symbioses that
occur in three orders of plants (Fagales, Rosales and Cucurbitales) where
roots may become inter-cellularly and intra-cellularly colonized by
diazotrophic actinomycetes of the genus Frankia that inhabit nodules in
roots [2
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B2-microorganisms-06-00095>].
Families of plants where actinorhizal symbioses are common include:
Betulaceae, Elaeagnaceae, Fagaceae, Myricaceae, Rosaceae and so forth [4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B4-microorganisms-06-00095>].
Other nitrogen-transfer symbioses are the rhizobial symbioses where certain
diazotrophic bacteria infect root hairs and move into the root cortex where
they become intracellular and stimulate formation of nodules; bacteria then
situate in the cytoplasm of nodule cells in vesicles and transfer nitrogen
to plants in the form of ammonia [5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B5-microorganisms-06-00095>
,6
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Rhizobial symbioses are limited principally to legumes (family Fabaceae) [5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B5-microorganisms-06-00095>].
In some plants, diazotrophic cyanobacteria form nitrogen transfer
associations with plant tissues where they fix nitrogen and transfer it to
the plant [4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B4-microorganisms-06-00095>].
Among these are species of the genus Gunnera that possess specialized
glands that secrete polysaccharides to attract cyanobacteria, which enter
into tissues of the stem and become intracellular within host cell vesicles
where they fix nitrogen that is subsequently transferred to the host plant [
4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B4-microorganisms-06-00095>
].
In all the previously discussed nitrogen-transfer symbioses, hosts evolved
ways to internalize and engage in prolonged symbiosis with diazotrophic
prokaryotes using specialized plant symbiosis organs or tissues. All of
these associations are restricted to specific families that evolved
specialized symbiosis organs (nodules or glands); however, all species of
plants internalize microbial endophytes into plant tissues that do not
involve specialized organs [7
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B7-microorganisms-06-00095>
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,9
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,15
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,18
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Microbial endophytes have been shown to provide a plurality of benefits to
host plants, including growth promotion, improved biotic and abiotic stress
tolerance and increased disease protection [19
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B19-microorganisms-06-00095>
,20
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,21
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,23
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,29
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One logical means of plant growth promotion by plant endophytes is improved
nutrient acquisition by plants. However, mechanisms for direct nutrient
transfer from endophytic bacteria to plants have been elusive [30
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B30-microorganisms-06-00095>
,31
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In some cases, bacteria that have not been found to be capable of fixing
atmospheric nitrogen are nevertheless found to scavenge nitrogen and other
nutrients from the rhizosphere and transfer them to plants [32
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B32-microorganisms-06-00095>].
In other cases, endophytes have been shown to increase solubilization of
bound phosphates in the rhizosphere, and thus have been hypothesized to
function by increasing plant phosphate supply in the rhizosphere [17
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B17-microorganisms-06-00095>].
In absence of a mechanism for direct transfer of nutrients from microbes to
plants, many scientists attribute growth promotion largely or partially to
effects of microbe-produced phytohormones, disease control, or other
non-nutritive benefits [33
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B33-microorganisms-06-00095>
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].
Evidence for a mechanism for direct transference of nutrients from
symbiotic microbes to plant roots was provided by Paungfoo-Lonhienne et al.
[39
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B39-microorganisms-06-00095>].
Through a series of experiments, these investigators showed that plant
roots (Lycopersicum esculentum and Arabidopsis thaliana) internalized
bacteria and yeasts into root cells where microbes appeared to be degraded
in time. Paungfoo-Lonhienne et al. [40
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B40-microorganisms-06-00095>]
later denominated this microbe internalization and degradation process
‘rhizophagy’ to denote that roots appeared to be ‘eating’ microbes.
Adamczyk et al. [41
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B41-microorganisms-06-00095>]
and Paungfoo-Lonhienne et al. [42
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demonstrated that plants had the capacity to employ secreted proteases in
order to degrade proteins, further supporting the hypothesis that plants
actively degrade microbes and their protein products associated with roots.
White et al. [43
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B43-microorganisms-06-00095>]
documented degradation of bacteria on root surfaces as a result of the
action of root-secreted reactive oxygen and proposed that through the
action of reactive oxygen roots may be scavenging nitrogen from bacteria
that colonize roots. White et al. [44
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B44-microorganisms-06-00095>]
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
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B45-microorganisms-06-00095>
,46
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].
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
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,50
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B50-microorganisms-06-00095>
,51
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B51-microorganisms-06-00095>
,52
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B52-microorganisms-06-00095>
,53
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B53-microorganisms-06-00095>
,54
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B54-microorganisms-06-00095>
,55
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B55-microorganisms-06-00095>].
In this paper, we describe features of the microbivory process and
hypotheses with regard to how the process works. We hypothesize that many
plants, perhaps all plants, acquire some nutrients directly from symbiotic
microbes by a process we term the ‘rhizophagy cycle’ (Figure 1
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f001>).
In the rhizophagy cycle symbiotic microbes (often seed transmitted
bacteria) alternate between an intracellular/endophytic phase and a
free-living soil phase. We hypothesize that microbes acquire soil nutrients
in the free-living soil phase and that those nutrients are extracted from
microbes oxidatively in the intracellular/endophytic phase. We also discuss
proposed mechanisms plants employ to manipulate symbiotic microbes to
transport nutrients from the soil into root cell periplasmic spaces,
extract nutrients through oxidation and deposit surviving microbes
exhausted of their nutrients back into the rhizosphere through the tips of
elongating root hairs (Figure 2
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f002>,
Figure 3
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f003>,
Figure 4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f004>,
Figure 5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f005>,
Figure 6
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f006>,
Figure 7
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f007>,
Figure 8
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f008>,
Figure 9
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f009>,
Figure 10
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f010>,
Figure 11
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f011>,
Figure 12
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f012>,
Figure 13
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f013>,
Figure 14
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f014>,
Figure 15
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f015>,
Figure 16
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f016>,
Figure 17
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f017>
and Figure 18
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f018>
).
[image: Microorganisms 06 00095 g001 550]
*Figure 1.* Diagrammatic representation of the rhizophagy cycle. (*A*)
Diagram of the rhizophagy cycle showing microbes entering root cells at the
root tip meristem and exiting root cells at the tips of elongating root
hairs. Rhizophagy cycle microbes alternate between an intracellular
endophytic phase and a free-living soils phase; soil nutrients are acquired
in the free-living soil phase and extracted oxidatively in the
intracellular endophytic phase; (*B*) Shows bacteria (arrow) in the
periplasmic space of parenchyma cell near root tip meristem of an Agave sp.
seedling (bar = 20 µm; stained with 3,3-diaminobenzidine followed by
aniline blue); (*C*) Bacteria (arrow) emerging from root hair tip of grass
seedling (bar = 20 µm; stained with fluorescent nucleic stain SYTO 9).
[image: Microorganisms 06 00095 g002 550]
*Figure 2.* Tomato seedlings (3 days post germination) with Micrococcus
luteus (black arrows) and without M. luteus (white arrows; stained with
3,3-diaminobenzidine). The endophyte-free seedlings failed to form root
hairs and showed higher presence of reactive oxygen in root tips as is
evidenced by deep brown color.
[image: Microorganisms 06 00095 g003 550]
*Figure 3.* Root parenchyma cells of axenic tomato seedling showing absence
of bacteria in cells (bar = 25 µm; stained with 3,3-diaminobenzidine
followed by aniline blue).
[image: Microorganisms 06 00095 g004 550]
*Figure 4.* Parenchyma cell of tomato seedling inoculated with Micrococcus
luteus showing tetrads of the bacterium (arrows) in periplasmic space of
parenchyma cell (bar = 20 µm; stained with 3,3-diaminobenzidine followed by
aniline blue).
[image: Microorganisms 06 00095 g005 550]
*Figure 5.* Tomato seedling root epidermis showing internal presence of
tetrads (arrows) of Micrococcus luteus (bar = 20 µm; stained with aniline
blue).
[image: Microorganisms 06 00095 g006 550]
*Figure 6.* Rumex crispus seedling root parenchyma cells near root tip
meristem showing internal presence of Micrococcus luteus tetrads (arrows;
bar = 25 µm; stained with 3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g007 550]
*Figure 7.* Root cells of Daucus carota seedling showing cluster of L-forms
of M. luteus (arrow; bar = 20 µm; stained with 3,3-diaminobenzidine
followed by aniline blue).
[image: Microorganisms 06 00095 g008 550]
*Figure 8.* Root hair initial of Rumex crispus seedling showing M. luteus
exiting root hair tip (arrow) and spilling off the sides of the root hair
initial (bar = 10 µm; stained with 3,3-diaminobenzidine followed by aniline
blue).
[image: Microorganisms 06 00095 g009 550]
*Figure 9.* Root hairs of tomato seedling showing emergence of tetrads of M.
luteus (arrows) from hair tips (bar = 20 µm; stained with
3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g010 550]
*Figure 10.* Root hair of Rumex crispus seedling showing tetrads of M.
luteus (arrow) emerging from hair tip (bar = 20 µm; stained with
3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g011 550]
*Figure 11.* Root hair of seedling of grass Cynodon dactylon showing
tetrads of M. luteus (arrow) emerging from ruptured root hair tip (bar = 15
µm; stained with 3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g012 550]
*Figure 12.* L-forms of Bacillus amyloliquefaciens (arrows) in root cap
cells of grass Urochloa ramosa (bar = 15 µm; stained with
3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g013 550]
*Figure 13.* Root hairs of grass Cynodon dactylon seedling showing B.
amyloliquefaciens (arrows) in hair (stained with 3,3-diaminobenzidine
followed by aniline blue). The smaller blue-staining spherical structures
(white arrows) are L-forms with cytoplasmic proteins intact; while larger
spherical structures (black arrows) are oxidized L-forms that are swollen
and lack cytoplasmic proteins, and as a consequence do not stain blue
internally (bar = 20 µm).
[image: Microorganisms 06 00095 g014 550]
*Figure 14.* Tomato seedling root hair tip showing spherical L-forms of
bacteria (arrows; bar = 20 µm; stained with 3,3-diaminobenzidine followed
by aniline blue).
[image: Microorganisms 06 00095 g015 550]
*Figure 15.* Root hairs of Froelichia gracilis seedling showing internal
wall-less cells (mycosomes) of fungus Aureobasidium pullulans (arrows; bar
= 15 µm; stained with 3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g016 550]
*Figure 16.* Root hair tip of Amaranthus viridis seedling showing yeast
cells of Aurobasidium pullulans (arrows) exiting from the tip of the hair
and brown staining walled yeast cells within the hair (bar = 15 µm; stained
with 3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g017 550]
*Figure 17.* Root hair of Froelichia gracilis seedling showing internal
yeast cells (collapsed mycosomes) of Aureobasidium pullulans (arrow; bar =
15 µm; stained with 3,3-diaminobenzidine followed by aniline blue).
[image: Microorganisms 06 00095 g018 550]
*Figure 18.* Root hair of seedling of Froelichia gracilis showing cap
(arrow) composed of compacted yeast cells (bar = 30 µm; stained with
3,3-diaminobenzidine followed by aniline blue).
2. The Symbiotic Bacteria
In our experiments, we employed microbes that were transmitted within or on
the surfaces of seeds of several species of plants [46
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B46-microorganisms-06-00095>
,47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>
,48
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B48-microorganisms-06-00095>
,56
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B56-microorganisms-06-00095>
,57
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B57-microorganisms-06-00095>].
The bacteria that functioned in the rhizophagy cycle in in vitro
experiments include species of genera of Gram-negative bacteria:
Alpha-proteobacteria Bosea, Methylobacterium; Beta-proteobacteria
Achromobacter and Burkholderia; Gamma-proteobacteria Acinetobacter,
Klebsiella,
Pantoea, Pseudomonas and Micrococcus; and Gram-positive Bacilli Bacillus
and Paenibacillus; and Actinobacteria Curtobacterium and Microbacterium.
Bacteria that function in the rhizophagy cycle belong to diverse classes of
bacteria and it seems likely that any bacterium that colonizes roots and
can be induced to enter root cells may be involved in the process [46
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B46-microorganisms-06-00095>
,47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>
,48
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B48-microorganisms-06-00095>
,50
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B50-microorganisms-06-00095>
,55
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B55-microorganisms-06-00095>
].
3. Plant ‘Farming’ of Rhizosphere Microbes
Plants produce a root exudate zone adjacent to and just behind root tip
meristems [58
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B58-microorganisms-06-00095>].
Plants secrete carbohydrates, amino acids, vitamins and organic acids into
this zone [59
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B59-microorganisms-06-00095>].
The literature suggests that plants alter numbers and diversity of microbes
on root surfaces and in the rhizosphere through secretion of exudates [60
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B60-microorganisms-06-00095>].
Plants are known to increase secretion of exudates in nutrient limiting
soils, likely leading to increased microbial activity around roots and
increased ‘microbial mining’ for nutrients [59
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B59-microorganisms-06-00095>].
Root exudates attract microbes that will grow in the root exudates [58
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B58-microorganisms-06-00095>
,61
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B61-microorganisms-06-00095>].
In this sense root exudates act as signal molecules that attract a diverse
community of microbes to the exudate zone and biofilm around the root tip
meristem [61
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B61-microorganisms-06-00095>
,62
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B62-microorganisms-06-00095>
,63
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B63-microorganisms-06-00095>].
Through the continued secretion of root exudates plants are cultivating
microbes and when nutrients are scarce plants increase cultivation of
microbes by producing more exudates [59
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B59-microorganisms-06-00095>].
The response of plants to increase density and diversity of the microbial
community around roots by secreting more root exudates in nutrient limiting
situations is consistent with the hypothesis that the root associated
microbes function in nutrient acquisition. Through the secretion of root
exudates, plants may be considered to be ‘farming’ microbes.
4. Nutrients Transferred to the Host Plant
Some of the bacteria (e.g., Burkholderia and Klebsiella) involved in the
rhizophagy cycle have been frequently found to fix atmospheric nitrogen,
while others are sometimes or rarely reported as nitrogen fixing [64
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B64-microorganisms-06-00095>].
For bacteria involved in the rhizophagy cycle, it is unlikely that any
nitrogen fixation occurs while they are in tissues of plant roots because
bacteria are exposed to high levels of reactive oxygen in roots and
nitrogenases are rapidly degraded by oxygen [43
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B43-microorganisms-06-00095>
,44
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B44-microorganisms-06-00095>
,64
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B64-microorganisms-06-00095>
,65
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B65-microorganisms-06-00095>].
Any nitrogen fixation activities by rhizophagy cycle bacteria would likely
occur in the free-living soil phase where bacteria grow in the rhizosphere
in low oxygen conditions. Consistent with this, Roley et al. [31
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B31-microorganisms-06-00095>]
found that a nitrogen-fixing Burkholderia only showed evidence of active
nitrogen fixation in roots of switchgrass (Panicum virgatum) after root
tissues senesced. On the other hand, it seems logical that bacteria could
deliver nutrients to plants via the rhizophagy cycle without nitrogen
fixation occurring; instead bacteria need only be capable of obtaining
nutrients in the rhizosphere by scavenging of nutrients from soils,
bacteria, fungi or plants. The capacity of some bacteria (including species
of Bacillus) to produce and secrete resistant proteases may enable these
bacteria to scavenge nitrogen from other microbes by degrading and
absorbing their proteins in the rhizosphere [66
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B66-microorganisms-06-00095>].
Irizarry and White [57
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B57-microorganisms-06-00095>]
showed that addition of Bacillus amyloliquefaciens to cotton seedlings
growing in soil resulted in increased growth and an increased expression of
nitrate transporter genes. In isotope tracking experiments using grass
seedlings both with and without bacteria, grown in agarose amended with
15N-labeled proteins, White et al. [55
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B55-microorganisms-06-00095>]
showed that presence of the bacteria on seedlings resulted in acquisition
of approximately 30% more nitrogen by grass seedlings than in seedlings
without bacteria. However, in that experiment, it was not possible to
determine what proportion of the nitrogen was obtained from absorption of
microbe-mineralized nitrogen in media around roots, versus from direct
degradation of microbes within or on surfaces of roots. Hill, Marsden and
Jones [67
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B67-microorganisms-06-00095>]
conducted isotope-tracking experiments to assess the flow of nitrogen into
wheat plants from direct consumption of microbes versus inorganic soluble
nitrogen. These authors concluded that plant consumption of microbes was
occurring but that the rate of movement of nitrogen through rhizophagy was
one to two orders of magnitude slower than soluble inorganic nitrogen.
Hill, Marsden and Jones [67
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B67-microorganisms-06-00095>]
did not examine nutrient transfer to plants other than nitrogen. Thus, no
work has been done to date to identify the particular nutrients that plants
acquire from rhizophagy. It seems probable that plants would not be
internalizing and degrading symbiotic microbes unless critical nutrients
were being obtained from consumption of those microbes.
5. Rhizophagy Microbes as Carriers of Micronutrients
Through the activities of some symbiotic microbes, nutrients (e.g.,
phosphates, organic nitrogen) may be solubilized in the rhizosphere [68
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B68-microorganisms-06-00095>].
Solubilized nutrients may be absorbed by root hairs into roots. However,
bacteria also efficiently scavenge nutrients in the rhizosphere (soil) and
sequester difficult to obtain micronutrients (including boron, cobalt,
copper, iron, manganese, magnesium and zinc) using biogenic ligands with a
high affinity for metals called siderophores [69
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B69-microorganisms-06-00095>].
Root associated bacteria are often motile and capable of moving out away
from the plant root in order to acquire soil nutrients—and of returning to
the plant to acquire additional carbon and other root exudate nutrients.
Bacteria would appear to be ideal carriers of micronutrients that are
required for plant growth and development. Through the process of
rhizophagy, all of the nutrients acquired or produced by bacteria could be
oxidatively extracted from them. Bar-Ness et al. [70
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B70-microorganisms-06-00095>]
showed that a pseudomonad was responsible for transporting iron from soil
to dicot and monocot roots to support plant growth. Bar-Ness et al. [71
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B71-microorganisms-06-00095>]
showed that in cotton (Gossypium sp.) iron was acquired directly from
bacteria at the root tip meristems. In the process of rhizophagy, it is at
the root tip meristems that bacteria enter plant cells and are exposed to
reactive oxygen that likely extracts nutrients from the intracellular
bacteria—inducing electrolyte leakage of bacteria and making nutrients
available for absorption into plant root cells. Further work is needed to
determine precisely which nutrients may be obtained by plants from the
direct consumption/oxidation of microbes.
6. Balance between Microbe-Oxidation Susceptibility and Resistance
Experiments using bacterial endophytes Pseudomonas spp. (from seeds of
grass Phragmites australis) and Micrococcus luteus (from seeds of Lycopersicum
esculentum) that differed in resistance to reactive oxygen degradation due
to their relative capacities to produce antioxidants (carotenoids,
catalases, peroxidases and superoxide dismutase) have suggested that
bacteria that participate in the rhizophagy cycle may be matched to their
particular host plants. More specifically, rhizophagy bacteria must be
degradable by levels of reactive oxygen produced by their hosts. Pseudomonas
spp. that stimulated growth of several grasses [47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>
,49
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B49-microorganisms-06-00095>]
were observed entering root cells and then swelling and losing protein
content as they were degraded. These same bacteria were not observed to
degrade when they were put into the seedlings of dandelion (Taraxacum
officionale) [47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>
,49
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B49-microorganisms-06-00095>].
Micrococcus luteus, a tomato endophyte, was shown to stimulate growth of
seedlings of tomato (Figure 2
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f002>).
However, inoculation of Micrococcus luteus into the seedlings of several
other plant species, including grasses (Festuca arundinaceae and Poa annua),
carrot (Daucus carota), curly dock (Rumex crispus) and Japanese
knotweed (Fallopia
japonica) resulted in internal colonization of root cells and suppression
of root growth. Examination of roots of these species bearing Micrococcus
luteus showed that bacteria colonized the interior of root cells, and
elicited reactive oxygen production, but did not degrade within root cells,
instead copiously replicating in seedling roots (Figure 4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f004>,
Figure 5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f005>,
Figure 6
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f006>,
Figure 7
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f007>,
Figure 8
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f008>,
Figure 9
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f009>,
Figure 10
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f010>
and Figure 11
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f011>)
to exit seedlings and accumulate en masse around roots. This could be
explained by the increased capability of Micrococcus luteus to withstand
reactive oxygen levels in hosts other than tomato. Mohana, Thippeswamy and
Abishek [72
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B72-microorganisms-06-00095>]
showed that carotenoids produced by Micrococcus luteus protect the
bacterium from oxidation. Ohwada et al. [73
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B73-microorganisms-06-00095>]
showed that Micrococcus luteus has 91 times more catalase activity and 20
times more peroxidase activity than Pseudomonas. The results of our
experiments with pseudomonads and Micrococcus seem to indicate that
microbes that establish a symbiosis with plants in the rhizophagy cycle
must be susceptible to degradation by the host in the intracellular phase.
In this study, the pseudomonads were compatible with their grass hosts and
were degraded (or some of them were degraded) within roots. The degradable
pseudomonads may thus provide a source of nutrients to their grass host
plants, resulting in growth stimulation. Micrococcus was resistant to
degradation by several hosts and likely did not provide nutrients. Further,
because Micrococcus luteus was resistant to degradation in the root several
hosts, the numbers of bacteria in cells could not be regulated and likely
overwhelmed the seedlings due to bacterial overload. This emphasizes that
plants and their symbiotic microbes may be adapted optimally to maximize
benefits of the symbiosis. In an optimal rhizophagy cycle relationship,
microbes would enter plant roots and some would be degraded oxidatively,
keeping intracellular microbe numbers in check, while survivors would exit
roots to rejoin soil populations.
7. Mechanisms for Microbe Entry into Roots 7.1. Endocytosis Hypothesis to
Explain Microbe Entry into Root Meristem Cells
Paungfoo-Lonhienne et al. [39
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B39-microorganisms-06-00095>]
proposed that movement of microbes into plant cells is a form of
endocytosis where plant derived cell-wall degrading enzymes play a role in
loosening cell walls to permit entry of microbes into plant root cells.
Experiments using Arabidopsis thaliana and Lycopersicon esculentum
inoculated with Escherichia coli showed that plants expressed higher levels
of cellulases than un-inoculated controls. These authors also found that
bacteria on surfaces of root cells were sometimes covered by a matrix
composed of cellulose fibers as evidenced by immuno-histochemical
experiments. It was proposed that coating microbes in a matrix could be an
early stage of endocytosis into root cells. Further, Paungfoo-Lonhienne et
al. [39
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B39-microorganisms-06-00095>]
reasoned that movements in the root cell cytoskeleton were consistent with
the hypothesized active endocytosis of microbes by root cells. An active
endocytosis mechanism for internalizing microbes into root cells is logical
and cannot be ruled out; however, another mechanism involving manipulation
of microbe virulence is possible based on experiments that we have
conducted.
7.2. Hypothesized Role of Short-Chain Fatty Acids in Induction of Bacteria
to Enter into Root Meristem Cells
Bacteria growing in biofilms on the root surface and in the rhizosphere
anaerobically ferment carbohydrates present in root exudates to form
short-chain fatty acids (SCFAs). Butyric and propionic acids are among the
SCFAs fermented by bacteria associated with roots [74
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B74-microorganisms-06-00095>].
In other research [75
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B75-microorganisms-06-00095>
,76
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B76-microorganisms-06-00095>],
butyric and propionic acids in animal intestines have been shown to act as
signal molecules or inhibitors of some bacteria and yeasts. When SCFAs are
in high concentration in biofilms, bacteria and yeasts (e.g., Salmonella
spp. and Candida spp.) remain in the biofilm phase but when butyric and
propionic acid concentrations fall, virulence genes in microbes are
up-regulated and microbes parasitize epithelial tissues in the walls of the
animal’s gut [75
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B75-microorganisms-06-00095>
,76
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B76-microorganisms-06-00095>].
Butyric acid and its derivatives are now widely being used to suppress gut
parasitism by bacteria in agricultural/industrial animal production [77
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B77-microorganisms-06-00095>
,78
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B78-microorganisms-06-00095>].
In isotope tracking experiments, Tramontano and Scanlon [79
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B79-microorganisms-06-00095>]
showed that root meristem cells absorbed butyric and propionic acids and
transported these compounds to the cell nucleus where the root cell
responded by slowing cell division. Lanzagorta, de la Torre and Aller [80
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B80-microorganisms-06-00095>]
found the 2 mM concentration of butyrate reversibly slowed the cell cycle
of Allium cepa root tip meristem cells. Why plant cell division in the
meristem slows is unknown, but it shows that the plant may respond to
presence of the microbes around the meristem. The active absorption of
these SCFAs by root meristem cells, may stimulate bacteria in the biofilm
around the root meristem to infect the thin-walled meristem cells in a
comparable way microbes in intestines infect intestinal epithelial tissues.
Thus, absorption of SCFAs by the root meristem is a possible ‘rhizophagy
trigger,’ essentially inducing microbes to parasitize the meristem cells.
In this sense, the removal of organic acids from the microbial biofilm
around root meristems may represent part of the symbiotic ‘cross talk’
between plant and microbe, comparable to interactions that occur in
establishment of rhizobial symbioses [5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B5-microorganisms-06-00095>
].
7.3. Propionic Acid and Butyric Acid Experiment to Test SCFA
Removal-Induced Infection of Meristem Cells
To test whether absorption of propionic and butyric acids from the
bacterial biofilm by the root tip meristem is the trigger to initiate entry
of bacteria into root meristem cells, we conducted experiments in which we
grew seedlings of the grass Poa annua (inoculated with Pseudomonas
fluorescens) on agarose (Sigma, Burlington, MA, USA) that contained 0, 2,
4, 6, 8, or 10 mM of butyric or propionic acids (Sigma, Burlington, MA,
USA). After approximately 10 days, seedlings were stained for 15 h in a
solution of 3,3-diaminobenzidine (DAB) (Sigma, Burlington, MA, USA) and
counterstained using aniline blue (0.01%, aqueous; Sigma, Burlington, MA,
USA), then examined microscopically for evidence of intracellular bacteria
using a compound light microscope (Zeiss, Axioskop; Carl Zeiss Microscopy,
Thornwood, NY, USA) [44
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B44-microorganisms-06-00095>].
In these experiments, we found that concentrations of SCFAs from 0–4 mM
gradually reduced entry of bacteria into root cells and at 4 mM no bacteria
could be seen within root cells [46
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B46-microorganisms-06-00095>
,51
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B51-microorganisms-06-00095>
,53
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B53-microorganisms-06-00095>].
These experimental results are consistent with the hypothesis that
absorption of SCFAs from the bacterial biofilm around the root tip meristem
is a trigger for intracellular invasion of bacteria into meristem cells. In
our experiments, at 4 mM/L of SCFAs in the agarose, the root meristem cells
could not remove the SCFAs from the bacterial biofilm due to its constant
replacement by additional SCFAs from the agarose. However, whether a
mechanism of root cell endocytosis, as suggested by Paungfoo-Lonhienne et
al. [39
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B39-microorganisms-06-00095>],
or active infection by microbes triggered by removal of bacterial
fermentation products by the root meristem, a combination of the two
mechanisms, or another mechanism entirely, accounts for internalization of
microbes into root cells will require additional investigation.
8. Loss of Cell Walls by Bacteria on Entry into the Periplasmic Space of
Root Cells
Microscopic examination (Figure 4
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f004>,
Figure 5
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f005>,
Figure 6
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f006>,
Figure 7
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f007>,
Figure 8
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f008>,
Figure 9
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f009>,
Figure 10
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f010>
and Figure 11
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f011>)
of a diverse selection of seedlings of grasses (Cynodon dactylon and Poa
annua) and dicots (Rumex crispus, Daucus carota, Fallopia japonica and
other species) infected by Pseudomonas spp. or Micrococcus luteus shows
that bacteria initially enter root meristem cells as walled
cells—pseudomonads are rod-shaped and Micrococcus luteus cells are
spherical and in tetrads. In the periplasmic space of root cells, bacteria
lose cell walls and form spherical L-forms (Figure 12
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f012>,
Figure 13
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f013>
and Figure 14
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f014>)
[81
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B81-microorganisms-06-00095>].
Likely, it is exposure of bacteria to reactive oxygen, constitutively
produced in the meristematic cells, that triggers bacteria to become
wall-less L-form bacteria [82
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B82-microorganisms-06-00095>].
The reactive oxygen may damage bacterial membrane wall synthesis enzymes
that results in formation of the wall-deficient bacteria. L-forms can also
be induced experimentally in bacteria by exposure to antibiotics that
inhibit cell wall synthesis by bacteria [81
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B81-microorganisms-06-00095>],
or spontaneously in plant and animal tissues [81
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B81-microorganisms-06-00095>].
L-form bacteria have been shown to occur in both animal and plant tissues
and have been associated with symbiosis and disease [83
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B83-microorganisms-06-00095>
,84
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B84-microorganisms-06-00095>
,85
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B85-microorganisms-06-00095>].
In the L-form phase bacteria do not divide regularly or possess defined
cell sizes. Instead, bacteria often form chains of spherical cells that
‘bleb’ or ‘bud’ to smaller and smaller sizes.
9. Intracellular Bacteria Exit Roots to Re-Enter Soil Populations
Our previous observations suggest that bacteria exit root hairs at the
elongating root hair tips (Figure 8
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f008>,
Figure 9
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f009>,
Figure 10
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f010>
and Figure 11
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f011>).
When all bacteria have exited the hair through the tip, hair elongation
stops. This suggests that root hair growth, at least in some cases, is a
function of intracellular bacteria. It also suggests that root hairs may
function as a mechanism to deposit bacteria exhausted of nutrients back out
into the rhizosphere where they can acquire additional nutrients before
returning to the root exudate zone. Confirmation of movement back into the
soil is significant because it completes the cyclic process of
‘rhizophagy’—with the potential that intracellular bacteria may re-enter
soil and eventually return to roots with nutrients that could support plant
growth. A ‘rhizophagy cycle’ where roots continuously extract small amounts
of minerals, vitamins, or other growth factors from endosymbiotic bacteria
could be an important source of nutrients for plants that has been largely
overlooked by plant scientists. The occurrence of a rhizophagy process that
is widespread in plants could explain how some bacteria that are not able
to fix nitrogen themselves nevertheless may show significant enhancements
in plant growth promotion [32
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B32-microorganisms-06-00095>
].
10. Do Fungi Also Function in the Rhizophagy Cycle?
In a recent study, we isolated the fungus Aureobasidium pullulans
(Ascomycota) from seeds and seedlings of the plant Froelichia gracilis
(Amaranthaceae). We also isolated the endophytic yeast Rhodotorula sp.
from Abrus
precatora (Fabaceae). Experiments using A. pullulans and Rhodotorula sp.
demonstrated that these yeasts internally colonized seedling roots of
several plant species, entering into root cells and locating in the
periplasmic spaces of root parenchyma [46
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B46-microorganisms-06-00095>].
Initial colonization appears to occur at the root tip meristem based on
presence of fungal cells in periplasmic spaces of parenchyma cells in outer
cell layers of the root behind the tip meristem and in root hairs at all
stages of development. The fungi also have the capability to form wall-less
protoplasts called ‘mycosomes’ that can bud sequentially to form chains
within plant cells [86
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B86-microorganisms-06-00095>].
In our experiments, we observed both walled fungal cells (Figure 18
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f018>)
and apparent wall-less mycosomes (Figure 15
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f015>
and Figure 17
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f017>)
within seedling root cells. The fungi were also seen to exit root cells at
the tips of elongating root hairs (Figure 16
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f016>),
accumulating around hair tips as masses of yeast cells, often forming caps
on tip of the hairs (Figure 18
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#fig_body_display_microorganisms-06-00095-f018>).
Our experiments using both yeasts show that fungi follow the same path
through plant roots as seen in bacteria involved in the rhizophagy cycle.
These yeasts appear to cycle between an intracellular endophytic phase and
a free-living soil phase. It seems reasonable to hypothesize that nutrients
could be extracted from fungi oxidatively when they are in the protoplast
mycosome phase. Atsatt and Whiteside [86
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B86-microorganisms-06-00095>]
observed mycosome formation in several additional species of fungi in phyla
Ascomycota, Basidiomycota and Zygomycota, suggesting that other fungi may
also possess the capability to become internalized in plant root cells.
Much more work is needed to evaluate the potential benefits of
intracellular fungi to their host plants.
11. Non-Nutritive Functions of Rhizophagy Microbes 11.1. Modulation of
Plant Development
Experiments using seedlings of grasses and other plant species have
demonstrated that some, or perhaps all, microbes that internalize in plant
cells modulate development of the seedlings. Seedlings from rigorously
surface-disinfected seeds using sodium hypochlorite to remove all surface
microbes invariably are diminished developmentally, often showing loss of
root gravitropic response (roots fail to grow downward) and reduced or no
root hair formation. Re-inoculation of the symbiotic bacteria onto axenic
seeds restores normal root growth in seedlings [43
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B43-microorganisms-06-00095>
,48
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B48-microorganisms-06-00095>
,49
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B49-microorganisms-06-00095>
,50
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B50-microorganisms-06-00095>].
Thus, it is evident that plants appear to rely on symbiotic microbes to
modulate development. Modulation of plant development may be considered to
be a basic function of microbes in the rhizophagy cycle. The hypothesized
mechanisms for modulation of plant development may relate to microbial
production, or removal of, plant hormones [36
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B36-microorganisms-06-00095>
,38
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B38-microorganisms-06-00095>
,53
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B53-microorganisms-06-00095>
,87
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B87-microorganisms-06-00095>
,88
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B88-microorganisms-06-00095>
].
11.2. Enhancement in Oxidative Stress Tolerance in Host Plants
Entry of microbes into root cells is generally accompanied by increased
production of defensive reactive oxygen by the root cells [47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>].
Increased production of reactive oxygen may cause the host to increase
production of antioxidants (e.g., superoxide dismutase, peroxidases,
catalases) and oxidative stress-related genes to reduce the negative
effects of reactive oxygen on the host itself. The direct association
between the amount of reactive oxygen secreted by the host and its
resistance to oxidative stress has not been verified but endophytic microbe
colonization of plants frequently provides hosts with increased tolerance
to abiotic stresses (e.g., drought, heavy metals, salinity and high
temperatures) and biotic stresses (e.g., diseases, herbivory) and the
underlying mechanism in many cases has been resistance to oxidative stress [
20
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B20-microorganisms-06-00095>
,21
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B21-microorganisms-06-00095>
,22
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B22-microorganisms-06-00095>
,56
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B56-microorganisms-06-00095>
,57
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B57-microorganisms-06-00095>
,89
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B89-microorganisms-06-00095>
,90
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B90-microorganisms-06-00095>
,91
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B91-microorganisms-06-00095>
,92
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B92-microorganisms-06-00095>
].
11.3. Enhanced Disease Resistance Due to Endophytic Microbes
Some of the microbes that become intracellular in plant roots have been
shown to inhibit pathogenic fungi in the soil or in the plant [25
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B25-microorganisms-06-00095>
,26
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B26-microorganisms-06-00095>
,49
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B49-microorganisms-06-00095>
,50
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B50-microorganisms-06-00095>
,93
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B93-microorganisms-06-00095>
,94
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B94-microorganisms-06-00095>].
Disease protection may be the result of induced systemic resistance (ISR)
where the endophyte causes the plant to up-regulate its disease resistance
genes making plants more resistant to pathogens [26
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B26-microorganisms-06-00095>
,95
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B95-microorganisms-06-00095>].
However, some of these microbes also have direct inhibitory activity on
pathogenic fungi. Soares et al. [27
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B27-microorganisms-06-00095>]
showed that a Bacillus endophyte of English ivy (Hedera helix) produced
antifungal lipopeptides that directly inhibited growth of the pathogenic
fungus Alternaria tenuisima and protected the host from disease.
Pseudomonad endophytes of plants also venture into the soil and colonize
potential fungal pathogens, repressing their growth and reducing virulence [
47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>].
Pseudomonads are known to produce antifungal compounds including
2,4-diacetylphloroglucinol, pyoluteorin, pyrrolnitrin and hydrogen cyanide;
these and/or other compounds may inhibit growth of potential pathogens
and/or alter their behavior in reducing growth and virulence [96
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B96-microorganisms-06-00095>
].
11.4. Endophyte-Mediated Suppression of Competitor Plant Species
Microbes involved in the rhizophagy cycle intimately associate with plant
root tissues and cells, growing around the root tip meristems and passing
through cell walls where they come into direct contact with root cell
plasma membranes. We hypothesize that this intimate association requires
that the microbe must be subject to control by the plant cells. If the
intracellular microbes are resistant to degradation by host-produced
reactive oxygen due to production of antioxidants the microbe may replicate
itself excessively at the expense of the host cell and host growth may be
reduced. If microbes produce metabolites such as hydrogen cyanide or other
compounds that restrict respiration or other functions of the host cell,
plant growth may again be compromised. Thus, it seems reasonable that hosts
and rhizophagy cycle endophytes are adapted to maximize benefits to both
hosts and microbes. Colonization of rhizophagy cycle endophytes into hosts
to which they are not adapted may result in ‘endobiome interference,’ where
endophytes reduce growth and competitiveness of hosts and perhaps interfere
with the growth promotional activities of native endophytes [53
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B53-microorganisms-06-00095>].
In some of our experiments ‘endobiome interference’ may have occurred. For
example, experiments we conducted using seed-transmitted pseudomonads from
the grass Phragmites australis showed that the bacteria stimulated growth
of several grasses but suppressed growth and increased mortality in
seedlings of dandelion (Taraxacum officionale) and curly dock (Rumex crispus)
[47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>].
In other experiments [53
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B53-microorganisms-06-00095>],
we showed that endophytic yeasts Rhodotorula sp. and Aureobasidium pullulans
and bacteria Micrococcus luteus and Paenibacillus sp. from seedlings of
plant species Abrus precatorius, Froelichia gracilis, Lycopersicum
esculentum and Poa annua, respectively, suppressed root growth and
increased mortality of seedlings of dandelion (Taraxacum officionale),
curly dock (Rumex crispus) and clover (Trifolium repens). Here, microbes
that were most inhibitory to seedling growth were those that were resistant
to reactive oxygen due to production of antioxidants—and likely internal
replication of microbes could not be controlled by the inhibited seedlings,
resulting in replication of endophytes at the expense of host growth. We do
not know the mechanisms by which endophytic colonization of non-hosts led
to increased seedling mortality. Endobiome interference could be a factor
that affects competition between plant species in natural plant
communities—with endophytes serving as a means to suppress the growth of
competitor plant species [47
<https://www.mdpi.com/2076-2607/6/3/95/htm?fbclid=IwAR3GswHysSv8HOrHmlEwjhh4tLhxHsVF9h9cWEnrXTvWGK_skeBYGbyVpQM#B47-microorganisms-06-00095>].
Additional experiments are needed to determine whether ‘endobiome
interference’ occurs in natural plant communities.
12. Conclusions
The ‘rhizophagy cycle’ is a process where microbes alternate between an
endophytic phase and a free-living soil phase. Rhizophagy microbes become
intracellular in root cells by infecting cells at the root tip meristem.
Microbes exist primarily as wall-less protoplasts (‘L-forms’ for bacteria
and ‘mycosomes’ for fungi) in close association with host cell plasma
membranes in roots. Root cell plasma membranes secrete reactive oxygen onto
microbes and this may reduce replication of intracellular microbes and
cause leakage of nutrients from microbes. Intracellular microbes trigger
formation of root hairs on roots and they exit cells at the elongating root
tips, reforming cell walls as they exit from root hairs. Plants appear to
manipulate microbes in the rhizophagy cycle by: (1) stimulating bacterial
growth around root tip meristems of seedlings by secretion of root exudates
around the root tip; (2) triggering bacteria to enter into periplasmic
spaces in root cells at the root-tip meristem by absorbing bacterial
fermentation products including butyric acid, causing bacteria to
up-regulate virulence/endoparasitism genes; (3) subjecting bacteria in
periplasmic spaces to superoxide formed on root cell plasma membranes to
extract nutrients from bacteria, and (4) depositing surviving intracellular
bacteria back into the rhizosphere from the tips of elongating root hairs
to maximize new nutrient acquisition by bacteria. Microbes engage in the
rhizophagy symbiosis likely because they also benefit from the nutrients
provided by host plants in terms of root exudates and nutrients that leak
from root cells during the endophytic/intracellular phase. The rhizophagy
symbiosis may be viewed as a mutualism involving an exchange of nutrients
between the plant and microbe participants. Much of our research to date on
the rhizophagy cycle has been done on seedlings, however future research is
needed to confirm that the rhizophagy cycle also occurs at root tips of
more mature plants. While ‘rhizophagy’ has been shown to increase movement
of nitrogen into plants, we hypothesize that the real benefit of the
rhizophagy cycle may be in acquisition of iron and other micronutrients
from symbiotic microbes that sequester these soil nutrients using
siderophores, although this must be proven. The biological implications of
the rhizophagy cycle and microbes that are involved in it in terms of plant
growth promotion and plant-plant interactions via symbiotic microbes are
topics that require much additional research.
Author Contributions
All authors contributed equally in research and writing of this manuscript.
Funding
S.K.V. was supported on a Raman Post-Doctoral fellowship (No.-F 5-11/2016
IC) for the year (2016-17) to conduct research in USA. Funding support was
also provided from USDA-NIFA Multistate Project W3157, the New Jersey
Agricultural Experiment Station, the Rutgers University Turf Science
Center, and from a Cooperative Ecosystems Studies Unit CESU G16AC00433
grant between Rutgers University and the U.S. Geological Survey for control
of invasive Phragmites australis. Any use of trade, product, or firm names
is for descriptive purposes only and does not imply endorsement by the U.S.
Government.
Conflicts of Interest
The authors have no conflict of interest to declare.
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