Available online at www.sciencedirect.
com
ScienceDirect
The unseen rhizosphere root–soil–microbe interactions
for crop production
Ruifu Zhang1,2, Jorge M Vivanco3 and Qirong Shen1
The underground root–soil–microbe interactions are extremely
complex, but vitally important for aboveground plant growth,
health and fitness. The pressure to reduce our reliance on
agrochemicals, and sustainable efforts to develop agriculture
makes rhizosphere interactions’ research a hotspot. Recent
advances provide new insights about the signals, pathways,
functions and mechanisms of these interactions. In this review,
we provide an overview about recent progress in rhizosphere
interaction networks in crops. We also discuss a holistic view of
the root–soil–rhizomicrobiome interactions achieved through
the advances of omics and bioinformatics technologies, and
the potential strategies to manage the complex rhizosphere
interactions for enhancing crop production.
Addresses
1
Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National
Engineering Research Center for Organic-based Fertilizers, Jiangsu
Collaborative Innovation Center for Solid Organic Waste Resource
Utilization, Nanjing Agricultural University, Nanjing, 210095, PR China
2
Key Laboratory of Microbial Resources Collection and Preservation,
Ministry of Agriculture, Institute of Agricultural Resources and Regional
Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, PR
China
3
Department of Horticulture and Landscape Architecture and Center for
Rhizosphere Biology, Colorado State University, Fort Collins, CO 80523,
United States
Corresponding author: Shen, Qirong (shenqirong@njau.edu.cn)
Current Opinion in Microbiology 2017, 37:8–14
This review comes from a themed issue on Environmental
microbiology
Edited by Marcio C Silva and Jorge Vivanco
For a complete overview see the Issue and the Editorial
Available online 21st April 2017
http://dx.doi.org/10.1016/j.mib.2017.03.008
1369-5274/ã 2017 Elsevier Ltd. All rights reserved.
Introduction
Increasing word population needs more crop production,
and this has so far been achieved by the input of chemical
fertilizers and pesticides. As the gateway for plants to
uptake water and nutrients, and to interact with the soil,
the plant rhizosphere can potentially be managed to
increase crop yields while decreasing agrochemicals’
input. The rhizosphere, which is considered as the second
genome of plants, is a hotspot for root–soil–microbe
Current Opinion in Microbiology 2017, 37:8–14
interactions [1]. Roots secrete large amounts of fixed
carbon as secretions, and they also deposit root cap border
cells and polysaccharide mucilage [2–4]. Thus, the rhizo-
sphere is a very attractive, nutrient-rich environment for
microbes.
In the rhizosphere, plant roots take up water and nutrients
from soil and exert their effects on the adjacent soil
through rhizodeposits. Rhizosphere microbes are actively
involved in root–soil interactions, while the microbe–
microbe and soil–microbe interactions in rhizosphere
are also mediated by the roots [1]. More important, the
direct root–microbe interactions play vital roles for plant
growth, health and fitness. The intricate interactions in
the rhizosphere indicate that all the partners (plant roots,
soil and microbes) of the tripartite interactions can be
manipulated or engineered to shift the direction in favor
of plants for sustainable agricultural gains [5–7]. Rhizo-
sphere engineering may ultimately reduce our reliance on
agrochemicals by replacing their functions with beneficial
microbes, but this strategy is largely based on the in-
depth understanding of rhizosphere root–soil–microbe
interactions. Many insights have emerged from the model
plant Arabidopsis [8], however, in recent years, rhizo-
sphere studies have paid more attention to crops due to
the urgent need to develop agriculture in a sustainable
way.
This review will introduce the recent progresses in rhi-
zosphere of root–soil–microbe interactions (Figure 1),
particularly of crops. Our discussion is mainly targeted
to the plant beneficial microbes, while the soil borne
pathogens are not the focus of this review.
Soil microbes are actively participating in the
root–soil interactions
The root–soil interface is a critical gateway for plants to
take up water and nutrients from soils and exert their
effects on soils through rhizodeposits. Under natural
conditions, root–soil interactions are very complex with
a multitude of microbes are actively participating in the
association. Arbuscular mycorrhizal fungi (AMF) colonize
more than 80% of terrestrial plants, and they help plant
roots to uptake soil phosphorus. Some other rhizosphere
microbes can fix nitrogen, release plant available phos-
phorus, potassium and other micronutrients, and assist
the root in the efficient uptake of these nutrients [9]. The
interaction between plants and soil, a belowground pro-
cess termed as plant–soil feedback (PSF), is recognized as
a major driver of plant community dynamics and nutrient
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 Rhizosphere root–soil–microbe interactions Zhang, Vivanco and Shen 9
Figure 1
Soil 1 3
2 4
Soil
Current Opinion in Microbiology
Schematic representation of rhizosphere root–soil–microbe
interactions. Soil microbes are actively involved in the root–soil
interactions; Root mediate microbe–microbe and soil–microbe
interactions in the rhizosphere; Direct root–microbe interactions
involve extensive signal communications; Holistic view of the root–
soil–rhizomicrobiome interactions.
cycling. A change in the composition of a plant commu-
nity leads to a change in litter quality, which alters the
local nutrient cycling process and soil conditions; the
changed soil conditions may in turn drive a further change
in plant community composition [10]. However, the
plant-mediated PFS often neglects the roles of root-
associated microbes, which determines the decomposi-
tion rate of plant litter and directly or indirectly affect the
plants. Recent studies have challenged the plant-cen-
tered view of PSF, suggesting mechanisms of microbial-
mediated PSF, and proposed the term plant–microbe–soil
feedback (PMSF) [11,12].
The rhizosphere soil differs chemically and physically
from bulk soil due to the effect of root exudates and other
root deposits. However, it is argued that the direct influ-
ence of root exudates is limited, because the root exu-
dates are rapidly assimilated by root-associated microbes,
and are modified before released into the rhizosphere soil
by the microbes themselves [13]. Indeed, recent studies
with stable isotope-labeled root exudates demonstrate
the fast assimilation and response of rhizosphere microbes
to root exudates [14,15]. The assimilation of root depos-
its by rhizosphere microbes may improve soil quality, for
example, it is reported that root polysaccharides induced
the biofilm matrix production of plant-beneficial Bacillus
subtilis, which resulted in the enhanced root colonization
and plant beneficial effects [16], and the biofilm matrix in
the rhizosphere may also help maintain the soil moisture
and facilitate the formation of soil aggregation.
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Plant roots mediate microbe–microbe and
soil–microbe interactions in the rhizosphere
for their benefits
At the scale of meters or kilometers, environmental
parameters have relatively large effect on the soil micro-
bial communities, but in the microscale environments
like the rhizosphere, microbial communities are likely to
be dominated by the microbial interactions [17]. It has
been reported that interactions of root-associated
microbes are more complex than those of microbes in
bulk soil probably due to the density and diversity of
microbial cells in rhizosphere, and predominant interac-
tions are positive (>80%), indicating that the rhizosphere
has a greater potential for mutualistic associations [18].
Plant roots also mediate indirect interactions of plant
beneficial and pathogenic microbes through the root
secreted signals, which are usually for the benefits of
plants themselves. Studies show that the attack of crops
by soil borne pathogens is proceeded by the recruitment
and stimulation of antagonistic bacteria by roots, which is
a potential plant defense strategy against pathogen attack
[1]. For example, in a split root system, the infection by
the wilt disease pathogen Fusarium oxysporum f. sp. cucu-
merinum (FOC) increased the cucumber root secretion of
citric acid and fumaric acid, which helped to recruit plant
beneficial B. amyloliquefaciens SQR9 and enhanced its root
colonization [19]. Infection of Pythium ultimum on one side
of barley roots induced the expression of the 2,4-diace-
tylphloroglucinol (DAPG) biosynthesis gene phlA of the
biocontrol bacterium Pseudomonas fluorescens CHA0 in
another side of the roots. This induction was through
increased secretion of vanillic acid, fumaric acid and p-
coumaric acid, which could induce DAPG production of
CHA0 in vitro at very low concentrations [20].
Plant roots have been shown to secrete components that
interfere with quorum sensing (QS) [21,22], a cell–cell
signaling mechanism in bacteria that is very important in
group coordinated processes [23,24]. Many root-associ-
ated bacteria require QS for colonization of the rhizo-
sphere and regulate a wide range of phenotypes including
rhizosphere competence, virulence, conjugation, secre-
tion of hydrolytic enzymes, and the production of sec-
ondary metabolites [25]. The rhizosphere is potentially
favorable for QS signaling due to the high bacterial
density and diversity [26]. Plant roots can produce QS-
signal mimics or QS-interfering molecules and result in
the quorum quenching (QQ) [27]. Some crops, including
rice, soybean and tomato, were found to secrete com-
pounds having AHL-mimicking activities [21,28,29].
AHL signal-mimicking compounds seem to be important
in determining the outcome of interactions between
plants and a diverse range of pathogenic microbes. QQ
has been proposed as a novel biocontrol strategy against
plant pathogens [27]. However, it is possible that QQ
strategies may also prevent QS-regulated functions in
plant beneficial bacteria [30].
Current Opinion in Microbiology 2017, 37:8–14
10 Environmental microbiology
Microorganisms play critical roles in soil formation from
rocks and minerals, and together plant roots and soil
microorganisms synergistically enhance rock weathering
and soil maturation [31,32]. Recently, a new concept
‘mineralosphere’ was coined to describe the interface
of the rocks (or mineral surfaces) and the surrounding
soil with the associated microbial communities [33]. Plant
roots exert strong effects on microbial-driven soil nutrient
cycling. Nitrification and denitrification are pivotal micro-
bial-driven soil processes related to the N loss from
terrestrial ecosystems through NO3 leaching and gas-
eous N2 emission. The loss of ammonium fertilizer is
mainly caused by nitrification and consequent denitrifi-
cation, and these soil processes are critical for increasing
the N-use efficiency (NUE) of crops [34]. Plant roots
mediate these soil-microbe interaction processes through
the secretion of biological nitrification inhibitors (BNIs)
and biological denitrification inhibitors (BDIs) [35].
Recently, an efficient novel BNI, 1,9-decanediol, was
identified in rice root exudates with the potential to be
used in agriculture to improve NUE [36]. BNIs and
BDIs can be exploited by breeding programs to develop
crop cultivars with improved crop NUE and reduce N loss
from the field, benefiting both the agricultural production
and the environment.
Another effect of roots on microbe–soil interactions is the
rhizosphere priming effect (RPE). Labile organic sub-
stances released from roots accelerate the decomposition
of soil organic matter (SOM) and stimulate the dissolution
of insoluble minerals by rhizosphere microbes [4]. Studies
in plant growth chambers and greenhouses indicate that
the RPE varies widely, ranging from 17% to 380%
enhancement of SOM turnover [37], and a recent
meta-analysis showed that root-accelerated mineraliza-
tion and priming could account for up to one-third of
the total C and N mineralized in temperature forest soils,
and these effects could be induced by relatively modest
fluxes of the root-derived C [38]. The RPE can be
significantly influenced by both plant traits and rhizo-
sphere properties [39]. Although the quality and quantity
of root exudates are thought to be key plant traits con-
trolling RPE [40], however, the actual traits responsible
for the large observed differences in RPE are virtually not
clear [39]. A recent study indicated root biomass and
length played a minor role in the plant species variation
in RPE, while rhizosphere acidification caused by root
exudates was shown to be an important factor affecting
the magnitude and direction of RPE [41].
Direct root–microbe interactions involve
extensive signal communications
Rhizosphere is not only a battlefield of roots and soilborne
pathogens, but also a playground for roots and beneficial
microbes [42]. Due to the chemoattractant and signaling
of root exudates and the biotic surface of the rhizoplane
for attachment, roots are colonized or associated with
Current Opinion in Microbiology 2017, 37:8–14
various microbes. These associations can be beneficial,
harmful or neutral, and can significantly influence plant
growth, health and fitness. Root secreted flavonoids,
strigolactones, cutin monomers, phenolic acids, organic
acids and volatiles have been recognized as signals to
regulate root–microbe interactions and microbial gene
expression [43]. It is very likely that many more chemical
signals secreted by the root will be identified and poten-
tially used to enhance the root colonization of beneficial
microbes for crop production. A recent study, for exam-
ple, showed that root secreted methyl salicylate could
induce root colonization of beneficial Bacillus subtilis
strain [44]. Rhizosphere beneficial microbes actively
respond to root exudates by adjusting their transcriptional
program toward traits involved in chemotaxis, mobility,
biofilm formation, detoxification, transportation, polysac-
charide degradation and secondary metabolism [45,46].
Once rhizosphere beneficial bacteria are established on
the root, root exudates components may function as
environmental cues to promote biofilm formation on
the root surface [16]. Many excellent reviews have
elegantly reviewed the mechanisms of root–microbe
interactions, including their functions and the communi-
cation signals [8,47–50]. A recent study demonstrated
interesting synergy of roots and associated bacterium
for plant growth promotion; the plant beneficial Bacillus
amyloliquefaciens SQR9 stimulated the secretion of tryp-
tophan from roots, and then used tryptophan to produce
the phytohormone auxin in the rhizosphere to promote
plant growth [51].
Rhizosphere microorganisms do not only perceive plant
root secreted signals, they also release diverse signaling
molecules to influence their plant hosts for enhancing
biotic and abiotic stress resistance or tolerance, root
development and plant growth. Some PGPR strains
release various molecules that serve as elicitors of plant
induced systemic resistance (ISR), and these molecules
include AHL-type QS molecules, diffusible signal factor
diketopiperazines (DKPs), rhizosphere pseudomonads-
produced antibiotics (such as DAPG, pyocyanin), rhizo-
sphere bacilli-produced lipopeptides and polyketides,
siderophores, biosurfactants, and volatile organic chemi-
cals (VOCs) (such as 2,3-butanediol and indole) [52–54].
Beneficial Bacillus subtilis GB03 emitted volatile 2,3-
butanediol, which was demonstrated to trigger induced
systemic tolerance (IST) in plants through regulating the
transcription of the high-affinity K+ transporter 1 (HKT1)
in plant shoots and roots [55,56]. Rhizosphere microbes
also release chemical molecules to affect plant root devel-
opment. High concentration of these molecules inhibit
primary root elongation and promote lateral root and root
hair formation, indicating that these effects are through
modulation of the endogenous root development pro-
grams. Some rhizosphere bacteria or fungi produce auxin,
which directly interfere with root auxin signaling [57].
But, indole derivatives produced by root endophyte
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 Rhizosphere root–soil–microbe interactions Zhang, Vivanco and Shen 11
Piriformospora indica are not involved in root develop-
ment and growth of barley, instead, they are required for
biotrophic colonization of barley roots [58,59]. Other
signals secreted by rhizosphere bacteria or fungi included
AHLs [60–62], DKPs [63], the volatile compounds of
indole [64] and dimethyl disulfide [65], the antibiotics
DAPG [66] and pyocyanin [67]. These molecules inter-
fered with the root auxin signaling pathways to modulate
plant root architecture systems. The detailed regulating
mechanism of endogenous root development pathways is
not the scope of this review, and some excellent reviews
are referred [68–70].
Holistic view of the root–soil–rhizomicrobiome
interactions
It is widely recognized that most of (>99%) the soil
microorganisms are not yet cultured, but they may play
important roles for plant productivity. With the develop-
ment of culture-independent ‘omics’ and bioinformatics
approaches, deeper insights into the structures and func-
tions of crop rhizomicrobiomes provided holistic view of
the root–soil–rhizomicrobiome interactions. The key
questions are how is the rhizomicrobiome assembled
and what factors shape its structure? Besides the model
plant Arabidopsis [71–74], rhizomicrobiomes of many
crops are also characterized, including rice [75], maize
[76], wheat [77], barley [78] and soybean [79]. These
studies confirmed that the rhizomicrobiome consist of a
subset of the bulk soil microbiome. Soil type is identified
as a major factor shaping the composition of the rhizo-
microbiome. However, under identical environmental
conditions and soils, the plant genotype is the main factor
affecting the structure and function of the rhizomicro-
biome, indicating that the plant acts as a filter for its own
rhizomicrobiome. In natural ecosystems with long-term
co-evolution of root and rhizomicrobiome, the effect of
plant genotype is thought to be higher [80]. The plant
genotype-mediated effects on rhizomicrobiome can have
large effects on host growth and health [81].
Based on these well characterized rhizomicrobiomes of
Arabidopsis and several crops, a two-step selection model
[82] and later a three step enrichment model have been
proposed to unveil the assembly process of the micro-
biome from bulk soil to the rhizosphere [83]. In both
models, the bulk soil provides a microbial seed bank, the
physical–chemical properties, the biogeography and cli-
mate conditions. In turn, the rhizosphere provides the
rhizodeposits and other root factors such as oxygen and
pH [84], the plant genotype and developmental stage,
and plant defense-related hormones [85]. Specific micro-
bial traits like biofilm formation and surface adhesion may
also determine who can colonize these root compart-
ments. Therefore, the structure of the rhizomicrobiome
is the result of complex root–soil–microbe interactions.
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Concluding remarks
Despite great advances in understanding the complex
networks in the rhizosphere, our understanding is still in
its infancy, and most of our insights are derived from
model plants with the study for major crops just starting.
The complexity of rhizosphere continues to present a
multitude of ‘black boxes’ to our understanding of fun-
damental issues concerning signals, recognition and path-
ways, cost and balance, function and management of
root–soil–microbe interactions. With more restrictive reg-
ulations for the use of agrochemicals being implemented
and the demand for more food to feed the ever-increasing
world population, comprehensive studies of the rhizo-
sphere interactions to support crop production are even
more urgent.
The close interactions between crops and rhizosphere
microbes (and other plant microbiomes) have catalyzed
the view of plants as a superorganism-the holobiont [86].
Any modification of a component of the holobiont may
affect other modules; thus application of beneficial
microbes or any agricultural practice to enhance the
rhizosphere microbial activity should take into account
the other components. For rhizosphere management, all
the components (plant roots, soil and microbes) can be
manipulated or engineered to favor crop growth and
health. The current practices, such as the application
of biofertilizers and biocontrol agents, or soil amendments
with organic materials, are mainly targeting the microbes
and soils, while the crops as hosts are usually neglected.
Enhancing root-beneficial microbe associations through
crop breeding should be undertaken [87]. Unfortunately,
the domestication and the breeding of modern crop
cultivars have affected the associated microbiome; for
instance, mycorrhizal colonization of modern crop culti-
vars is lower than that of ancestral lines or wild-type
plants, possibly due to the highly fertile soil conditions
needed by modern cultivars [87]. Discovery of novel
rhizosphere signaling compounds, elucidation of the
mechanisms involved in the perception of the molecular
dialog between plant roots and the rhizomicrobiome,
identification of crop key genes controlling beneficial
microbes’ root colonization are important issues for crop
breeding to take into account.
Acknowledgements
We acknowledge the journal of Current Opinion in Microbiology for inviting us
to write this review. The authors also thank Dr. Yunpeng Liu for help with
the figure. R. Z. and Q. S. are supported by the National Key Basic
Research Program of China (973 program, 2015CB150505), National
Natural Science Foundation of China (31330069, 31572214) and the
111 Project (B12009).
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
 of special interest
 of outstanding interest
Current Opinion in Microbiology 2017, 37:8–14
12 Environmental microbiology
1. Berendsen RL, Pieterse CM, Bakker PA: The rhizosphere
microbiome and plant health. Trends Plant Sci. 2012, 17:478-
486.
2. Badri DV, Vivanco JM: Regulation and function of root
exudates. Plant Cell Environ. 2009, 32:666-681.
3. van Dam NM, Bouwmeester HJ: Metabolomics in the
rhizosphere: tapping into belowground chemical
communication. Trends Plant Sci. 2016, 21:256-265.
4. Jones DL, Hodge A, Kuzyakov Y: Plant and mycorrhizal
regulation of rhizodeposition. New Phytol. 2004, 163:459-480.
5. Dessaux Y, Grandclément C, Faure D: Engineering the
rhizosphere. Trends Plant Sci. 2016, 21:266-278.
6. Zhang Y, Ruyter-Spira C, Bouwmeester HJ: Engineering the
plant rhizosphere. Curr. Opin. Biotechnol. 2015, 32:136-142.
7. Ryan PR, Dessaux Y, Thomashow LS, Weller DM: Rhizosphere
engineering and management for sustainable agriculture.
Plant Soil 2009, 321:363-383.
8. Bednarek P, Kwon C, Schulze-Lefert P: Not a peripheral issue:
secretion in plant–microbe interactions. Curr. Opin. Plant Biol.
2010, 13:378-387.
9. Lambers H, Mougel C, Jaillard B, Hinsinger P: Plant–microbe–soil
interactions in the rhizosphere: an evolutionary perspective.
Plant Soil 2009, 321:83-115.
10. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM: Plant–soil
feedbacks: a meta-analytical review. Ecol. Lett. 2008, 11:980-
992.
11. Miki T, Ushio M, Fukui S, Kondoh M: Functional diversity of
microbial decomposers facilitates plant coexistence in a
plant–microbe–soil feedback model. Proc. Natl. Acad. Sci. U. S.
A. 2010, 107:14251-14256.
12. Ke PJ, Miki T, Ding TS: The soil microbial community predicts
 the importance of plant traits in plant–soil feedback. New
Phytol. 2015, 206:329-341.
This research proposed that litter decomposition is dependent on the
composition of root-associated microbes; thus providing new perspec-
tives of plant–soil feedback.
13. Dennis PG, Miller AJ, Hirsch PR: Are root exudates more
important than other sources of rhizodeposits in structuring
rhizosphere bacterial communities? FEMS Microbiol. Ecol.
2010, 72:313-327.
14. Hernández M, Dumont MG, Yuan Q, Conrad R: Different bacterial
 populations associated with the roots and rhizosphere of rice
incorporate plant-derived carbon. Appl. Environ. Microbiol.
2015, 81:2244-2253.
Using stable isotope probing (SIP) approach, the roots, root exudates and
rhizosphere microorganisms of the major crop rice in fields were identi-
fied. The labeled OTUs in the root compartment corresponded to a
greater proportion of the 16S rRNA sequences (20%) than did those
in the rhizosphere (4%), indicating that a proportion of the active
microbial community on the roots is greater than that in the rhizosphere.
15. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA, Houtekamer MJ,
Boschker HT, Bodelier PL, Whiteley AS, van Veen JA et al.:
Shifting carbon flow from roots into associated microbial
communities in response to elevated atmospheric CO2. Proc.
Natl. Acad. Sci. U. S. A. 2010, 107:10938-10942.
16. Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R: Bacillus
subtilis biofilm induction by plant polysaccharides. Proc. Natl.
Acad. Sci. U. S. A. 2013, 110:E1621-E1630.
17. Cordero OX, Datta MS: Microbial interactions and community
assembly at microscales. Curr. Opin. Microbiol. 2016, 31:227-
234.
18. Shi S, Nuccio EE, Shi ZJ, He Z, Zhou J, Firestone MK: The
 interconnected rhizosphere: high network complexity
dominates rhizosphere assemblages. Ecol. Lett. 2016, 19:926-
936.
With well organized replicated experiments for two seasons, oat rhizo-
sphere bacterial networks were substantially more complex than those in
surrounding soils, network complexity increased as plants grew. Most
Current Opinion in Microbiology 2017, 37:8–14
interactions were positive, suggesting that extensive mutualistic interac-
tions may occur among rhizosphere bacteria.
19. Liu Y, Zhang N, Qiu M, Feng H, Vivanco JM, Shen Q, Zhang R:
Enhanced rhizosphere colonization of beneficial Bacillus
amyloliquefaciens SQR9 by pathogen infection. FEMS
Microbiol. Lett. 2014, 353:49-56.
20. Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S:
Plants respond to pathogen infection by enhancing the
antifungal gene expression of root-associated bacteria. Mol.
Plant Microbe Interact. 2011, 24:352-358.
21. Teplitski M, Robinson JB, Bauer WD: Plants secrete compounds
that mimic bacterial N-acyl homoserine lactone signal
activities and affect population density-dependent behaviours
in associated bacteria. Mol. Plant Microbe Interact. 2000,
13:637-648.
22. Gao MS, Teplitski M, Robinson JB, Bauer WD: Production of
substances by Medicago truncatula that affect bacterial
quorum sensing. Mol. Plant Microbe Interact. 2003, 16:827-834.
23. von Bodman SB, Bauer WD, Coplin DL: Quorum sensing in plant-
pathogenic bacteria. Annu. Rev. Phytopathol. 2003, 41:455-482.
24. Waters CM, Bassler BL: Quorum sensing: communication in
bacteria. Annu. Rev. Cell Dev. Biol. 2005, 21:319-346.
25. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP:
Quorum-sensing in Gram-negative bacteria. FEMS Microbiol.
Rev. 2001, 25:365-404.
26. D’Angelo-Picard C, Faure D, Penot I, Dessaux Y: Diversity of N-
acyl homoserine lactone-producing and -degrading bacteria
in soil and tobacco rhizosphere. Environ. Microbiol. 2005,
7:1796-1808.
27. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH:
Quenching quorum-sensing-dependent bacterial infection by
an N-acyl homoserine lactonase. Nature 2001, 411:813-817.
28. Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK,
Christensen KB, Jensen PO, Andersen JB, Koch B, Larsen TO,
Hentzer M et al.: Identity and effects of quorum-sensing
inhibitors produced by Penicillium species. Microbiology 2005,
151:1325-1340.
29. McDougald D, Rice SA, Kjelleberg S: Bacterial quorum sensing
and interference by naturally occurring biomimics. Anal.
Bioanal. Chem. 2007, 387:445-453.
30. Molina L, Constantinescu F, Michel L, Reimmann C, Duffy B,
Défago G: Degradation of pathogen quorum-sensing
molecules by soil bacteria: a preventive and curative bilogical
control mechanism. FEMS Microbiol. Ecol. 2003, 1522:1-11.
31. Sun L, Gao J, Huang T, Kendall JR, Shen Q, Zhang R: Parental
material and cultivation determine soil bacterial community
structure and fertility. FEMS Microbiol. Ecol. 2015, 91:1-10.
32. Sun L, Xun W, Huang T, Zhang G, Gao J, Ran W, Li D, Shen Q,
Zhang R: Alteration of the soil bacterial community during the
parent materials maturation driven by different fertilizations.
Soil. Biol. Biochem. 2016, 96:207-215.
33. Uroz S, Kelly LC, Turpault MP, Lepleux C, Frey-Klett P: The
mineralosphere concept: mineralogical control of the
distribution and function of mineral-associated bacterial
communities. Trends Microbiol. 2015, 23:751-762.
34. Subbarao GV, Sahrawat KL, Nakahara K, Rao IM, Ishitani M,
Hash CT, Kishii M, Bonnett DG, Berry WL, Lata JC: A paradigm
shift towards low-nitrifying production systems: the role of
biological nitrification inhibition (BNI). Ann. Bot. 2013, 112:297-
316.
35. Bardon C, Piola F, Bellvert F, Haichar FZ, Comte G, Meiffren G,
Pommier T, Puijalon S, Tsafack N, Poly F: Evidence for biological
denitrification inhibition (BDI) by plant secondary metabolites.
New Phytol. 2014, 204:620-630.
36. Sun L, Lu Y, Yu F, Kronzucker HJ, Shi W: Biological nitrification
 inhibition by rice root exudates and its relationship with
nitrogen-use efficiency. New Phytol. 2016, 212:646-656.
This study searched among 19 rice varieties for root secreted potential
biological nitrification inhibitors (BNIs); a new nitrification inhibitor, 1,9-
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 Rhizosphere root–soil–microbe interactions Zhang, Vivanco and Shen 13
decanediol, was identified. Plant N-use efficiency (NUE) using15N-label-
ing method showed both BNI abilities and 1,9-decanediol amounts of root
exudates were positively correlated with plant ammonium-use efficiency.
This manuscript provided important new insights into the plant–bacterial
interactions involved in the soil N cycle, and improved our understanding
of the BNI capacity of rice in the context of NUE.
37. Zhu B, Cheng WX: Rhizosphere priming effect increases the
temperature sensitivity of soil organic matter decomposition.
Glob. Change Biol. 2011, 17:2172-2183.
38. Finzi AC, Abramoff RZ, Spiller KS, Brzostek ER, Darby BA,
Kramer MA, Phillips RP: Rhizosphere processes are
quantitatively important components of terrestrial carbon and
nutrient cycles. Glob. Change Biol. 2015, 21:2082-2094.
39. Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S,
McNickle GG, Brzostek E, Jastrow JD: Synthesis and modeling
perspectives of rhizosphere priming. New Phytol. 2014, 201:31-
44.
40. Kuzyakov Y: Priming effects: interactions between living and
dead organic matter. Soil. Biol. Biochem. 2010, 42:1363-1371.
41. Wang X, Tang C, Severi J, Butterly CR, Baldock JA: Rhizosphere
 priming effect on soil organic carbon decomposition under
plant species differing in soil acidification and root exudation.
New Phytol. 2016, 211:864-873.
This study indicated that root biomass and length played a minor role in
the plant species variation in the rhizosphere priming effect (RPE). The
rhizosphere acidification caused by root exudates was shown to be an
important factor affecting the magnitude and direction of RPE.
42. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-
Loccoz Y: The rhizosphere: a playground and battlefield for
soilborne pathogens and beneficial microorganisms. Plant Soil
2009, 321:341-361.
43. Venturi V, Keel C: Signaling in the rhizosphere. Trends Plant Sci.
2016, 21:187-198.
44. Kobayashi K: Plant methyl salicylate induces defense
 responses in the rhizobacterium Bacillus subtilis. Environ.
Microbiol. 2015, 17:1365-1376.
This research showed that the root defense signal methyl salicylate can
induce colonization of beneficial Bacillus subtilis strain.
45. Zhang N, Yang D, Wang D, Miao Y, Shao J, Zhou X, Xu Z, Li Q,
Feng H, Li S et al.: Whole transcriptomic analysis of the plant
beneficial rhizobacterium Bacillus amyloliquefaciens SQR9
during enhanced biofilm formation regulated by maize root
exudates. BMC Genomics 2015, 16:685.
46. Balsanelli E, Tadra-Sfeir MZ, Faoro H, Pankievicz VC, de Baura VA,
Pedrosa FO, de Souza EM, Dixon R, Monteiro RA: Molecular
adaptations of Herbaspirillum seropedicae during
colonization of the maize rhizosphere. Environ. Microbiol. 2016,
18:2343-2356.
47. Rasmann S, Turlings TC: Root signals that mediate mutualistic
interactions in the rhizosphere. Curr. Opin. Plant Biol. 2016,
32:62-68.
48. Rosier A, Bishnoi U, Lakshmanan V, Sherrier DJ, Bais HP: A
perspective on inter-kingdom signaling in plant-beneficial
microbe interactions. Plant Mol. Biol. 2016, 90:537-548.
49. Huang XF, Chaparro JM, Reardon KF, Zhang R, Shen Q,
Vivanco JM: Rhizosphere interactions: root exudates,
microbes, and microbial communities. Botany 2014, 92:267-
275.
50. Haichar FZ, Santaella C, Heulin T, Achouak W: Root exudates
mediated interactions belowground. Soil. Biol. Biochem. 2014,
77:69-80.
51. Liu Y, Chen L, Zhang N, Li Z, Zhang G, Xu Y, Shen Q, Zhang R:
 Plant-microbe communication enhances auxin biosynthesis
by a root-associated plant beneficial bacterium Bacillus
amyloliquefaciens SQR9. Mol. Plant Microbe Interact. 2016,
29:324-330.
This study revealed interesting synergy of roots and associated bacterium
for plant growth promotion; the plant beneficial Bacillus amyloliquefa-
ciens SQR9 stimulated the secretion of tryptophan from roots, and then
used tryptophan to produce the phytohormone auxin in the rhizosphere to
promote plant growth.
www.sciencedirect.com
52. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van
Wees SC, Bakker PA: Induced systemic resistance by
beneficial microbes. Annu. Rev. Phytopathol. 2014, 52:347-375.
53. Schenk ST, Hernández-Reyes C, Samans B, Stein E, Neumann C,
Schikora M, Reichelt M, Mithöfer A, Becker A, Kogel KH et al.: N-
Acyl-homoserine lactone primes plants for cell wall
reinforcement and induces resistance to bacterial pathogens
via the salicylic acid/oxylipin pathway. Plant Cell 2014, 26:2708-
2723.
54. Sieper T, Forczek S, Matucha M, Krämer P, Hartmann A,
Schröder P: N-acyl-homoserine lactone uptake and systemic
transport in barley rest upon active parts of the plant. New
Phytol. 2014, 201:545-555.
55. Yang J, Kloepper JW, Ryu C: Rhizosphere bacteria help plants
tolerate abiotic stress. Trends Plant Sci. 2009, 14:1-4.
56. Zhang H, Kim M, Sun Y, Dowd SE, Shi H, Paré PW: Soil bacteria
confer plant salt tolerance by tissue-specific regulation of the
sodium transporter HKT1. Mol. Plant Microbe Interact. 2008,
21:737-744.
57. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J:
Phenotypical and molecular responses of Arabidopsis
thaliana roots as a result of inoculation with the auxin-
producing bacterium Azospirillum brasilense. New Phytol.
2014, 201:850-861.
58. Lee YC, Johnson JM, Chien CT, Sun C, Cai D, Lou B, Oelmüller R,
Yeh KW: Growth promotion of Chinese cabbage and
Arabidopsis by Piriformospora indica is not stimulated by
mycelium-synthesized auxin. Mol. Plant Microbe Interact. 2011,
24:421-431.
59. Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A:
Indole derivative production by the root endophyte
Piriformospora indica is not required for growth promotion but
for biotrophic colonization of barley roots. New Phytol. 2012,
196:520-534.
60. Ortı́z-Castro R, Martı́nez-Trujillo M, López-Bucio J: N-Acyl-L-
homoserine lactones: a class of bacterial quorum-sensing
signals alter post-embryonic root development in Arabidopsis
thaliana. Plant Cell Environ. 2008, 31:1497-1509.
61. Liu F, Bian Z, Jia Z, Zhao Q, Song S: The GCR1 and GPA1
participate in promotion of Arabidopsis primary root
elongation induced by N-acyl-homo-serine lactones, the
bacterial quorum-sensing signals. Mol. Plant Microbe Interact.
2012, 25:677-683.
62. Zhao Q, Zhang C, Jia Z, Huang Y, Li H, Song S: Involvement of
calmodulin in regulation of primary root elongation by N-3-
oxo-hexanoyl homoserine lactone in Arabidopsis thaliana.
Front. Plant Sci. 2015, 5:807.
63. Ortiz-Castro R, Dı́az-Pérez C, Martı́nez-Trujillo M, del Rı́o RE,
Campos-Garcı́a J, López-Bucio J: Transkingdom signaling
based on bacterial cyclodipeptides with auxin activity in
plants. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7253-7258.
64. Bailly A, Groenhagen U, Schulz S, Geisler M, Eberl L, Weisskopf L:
The inter-kingdom volatile signal indole promotes root
development by interfering with auxin signalling. Plant J. 2014,
80:758-771.
65. Meldau DG, Meldau S, Hoang LH, Underberg S, Wünsche H,
Baldwin IT: Dimethyl disulfide produced by the naturally
associated bacterium Bacillus sp B55 promotes Nicotiana
attenuata growth by enhancing sulfur nutrition. Plant Cell 2013,
25:2731-2747.
66. Brazelton JN, Pfeufer EE, Sweat TA, Gardener BB, Coenen C: 2,4-
diacetylphloroglucinol alters plant root development. Mol.
Plant Microbe Interact. 2008, 21:1349-1358.
67. Ortiz-Castro R, Pelagio-Flores R, Méndez-Bravo A, Ruiz-
Herrera LF, Campos-Garcı́a J, López-Bucio J: Pyocyanin, a
virulence factor produced by Pseudomonas aeruginosa, alters
root development through reactive oxygen species and
ethylene signaling in Arabidopsis. Mol. Plant Microbe Interact.
2014, 27:364-378.
Current Opinion in Microbiology 2017, 37:8–14
14 Environmental microbiology
68. Verbon EH, Liberman LM: Beneficial microbes affect
endogenous mechanisms controlling root development.
Trends Plant Sci. 2016, 21:218-229.
69. Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C,
Lopez-Bucio J: Trichoderma virens, a plant beneficial fungus,
enhances biomass production and promotes lateral root
growth through an auxin-dependent mechanism in
Arabidopsis. Plant Physiol. 2009, 149:1579-1592.
70. Zamioudis C, Mastranesti P, Dhonukshe P, Blilou I, Pieterse CMJ:
Unraveling root developmental programs initiated by
beneficial Pseudomonas spp. bacteria. Plant Physiol. 2013,
162:304-318.
71. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J,
Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG et al.:
Defining the core Arabidopsis thaliana root microbiome.
Nature 2012, 488:86-90.
72. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E,
Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R,
Schmelzer E et al.: Revealing structure and assembly cues for
Arabidopsis root-inhabiting bacterial microbiota. Nature 2012,
488:91-95.
73. Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E,
Schulze-Lefert P: Quantitative divergence of the bacterial root
microbiota in Arabidopsis thaliana relatives. Proc. Natl. Acad.
Sci. U. S. A. 2014, 111:585-592.
74. Bai Y, Müller DB, Srinivas G, Garrido-Oter R, Potthoff E, Rott M,
Dombrowski N, Münch PC, Spaepen S, Remus-Emsermann M
et al.: Functional overlap of the Arabidopsis leaf and root
microbiota. Nature 2015, 528:364-369.
75. Edwards J, Johnson C, Santos-Medellı́n C, Lurie E, Podishetty NK,
 Bhatnagar S, Eisen JA, Sundaresan V: Structure, variation, and
assembly of the root-associated microbiomes of rice. Proc.
Natl. Acad. Sci. U. S. A. 2015, 112:E911-E920.
A very detailed characterization of the root-associated microbiomes of
the major crop by deep sequencing, using rice plants grown under
controlled conditions as well as field cultivation at multiple sites.
76. Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES,
Ley RE: Diversity and heritability of the maize rhizosphere
microbiome under field conditions. Proc. Natl. Acad. Sci. U. S.
A. 2013, 110:6548-6553.
77. Ofek-Lalzar M, Sela N, Goldman-Voronov M, Green SJ, Hadar Y,
Minz D: Niche and host-associated functional signatures of the
root surface microbiome. Nat. Commun. 2014, 5:4950.
Current Opinion in Microbiology 2017, 37:8–14
78. Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J,
Pan Y, McHardy AC, Schulze-Lefert P: Structure and function of
the bacterial root microbiota in wild and domesticated barley.
Cell Host Microbe 2015, 17:392-403.
79. Mendes LW, Kuramae EE, Navarrete AA, van Veen JA, Tsai SM:
Taxonomical and functional microbial community selection in
soybean rhizosphere. ISME J. 2014, 8:1577-1587.
80. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH:
Going back to the roots: the microbial ecology of the
rhizosphere. Nat. Rev. Microbiol. 2013, 11:789-799.
81. Haney CH, Samuel BS, Bush J, Ausubel FM: Associations with
 rhizosphere bacteria can confer an adaptive advantage to
plants. Nat. Plants 2015, 1:15051.
This study demonstrated that the small plant genotype-mediated effects
on rhizomicrobiome can have large effects on host growth and health.
82. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E,
Schulze-Lefert P: Structure and functions of the bacterial
microbiota of plants. Annu. Rev. Plant Biol. 2013, 64:807-838.
83. Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T:
Roots shaping their microbiome: global hotspots for microbial
activity. Annu. Rev. Phytopathol. 2015, 53:403-424.
84. Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM:
Application of natural blends of phytochemicals derived from
the root exudates of Arabidopsis to the soil reveal that
phenolic related compounds predominantly modulate the soil
microbiome. J. Biol. Chem. 2013, 288:4502-4512.
85. Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J,
 McDonald M, Malfatti S, Glavina del Rio T, Jones CD, Tringe SG
et al.: Salicylic acid modulates colonization of the root
microbiome by specific bacterial taxa. Science 2015, 349:860-
864.
This study demonstrated that plant immune signal, salicylic acid, mod-
ulates colonization of the root by specific bacterial families, and drove the
selection from the available microbial communities to sculpt the root
microbiome.
86. Pieterse CM, de Jonge R, Berendsen RL: The soil-borne
supremacy. Trends Plant Sci. 2016, 21:171-173.
87. Germida JJ, Siciliano SD: Taxonomic diversity of bacteria
associated with the roots of modern, recent and ancient wheat
cultivars. Biol. Fertil. Soils 2001, 33:410-415.
www.sciencedirect.com