Spotlight
Embracing CommunityEcology in PlantMicrobiome ResearchFrancisco
Dini-Andreote1,*,@ andJos M. Raaijmakers1
Community assembly is mediatedby selection, dispersal, drift,
andspeciation. Environmental selec-tion is mostly used to date
toexplain patterns in plant micro-biome assembly, whereas
theinfluence of the other processesremains largely elusive.
Recentstudies highlight that adoptingcommunity ecology concepts
pro-vides a mechanistic framework forplant microbiome research.
Community Ecology as aFramework for Plant MicrobiomeResearchThe
discipline of community ecologyoffers a mechanistic framework to
unravelhow eco-evolutionary processes operateat the fine scales
from individuals to pop-ulations, modulating the distribution
ofspecies in space and time. In a recentconceptual synthesis,
Vellend [1] advo-cates that any given community is modu-lated by
the interplay of four high-levelprocesses, namely selection,
dispersal,drift, and speciation. Selection is definedas the result
of biotic and abiotic effects,in combination with interactions
ensuingfitness differences across individuals orspecies. This
process has traditionallybeen adopted to explain patterns in
plantmicrobiome assembly, for instance thoseassociated with
differences in micro-biome composition owing to soil type,plant
genotype, exudate profiles, and/oragricultural practices [2]. To
date, how-ever, the importance of the other pro-cesses in plant
microbiome assemblyhas been largely ignored.
Dispersal is defined as the movement ofspecies from one location
to another, andaccounts for the introduction of specieswithin a
local community. The conse-quences of dispersal are dependent onthe
diversity, abundance, and composi-tion of the donor and recipient
communi-ties. The theme of dispersal has oftenbeen explored in
studies of invasion ecol-ogy and in investigations of
ecologicalresilience and resistance of microbialcommunities in the
face of disturbances.In addition, dispersal timing and fre-quency
are crucial but often overlookedfactors that structure plant
microbiomes(see below). The effect of drift – in otherwords random
changes in populationsizes via stochastic birth and deathevents –
on the community is pronouncedfor low-abundant species because
theyare more prone to occasionally becomeextinct. Nemergut et al.
[3] further con-ceptualized that, in a community context,drift is
expected to be important whenselection is weak and when the
overallpopulation size and diversity status islow. These conditions
are commonlyobserved in the initial establishment ofmicrobial
communities in host-associatedenvironments. Speciation (or
‘diversifica-tion’ sensu Nemergut [3]) is the evolution-ary process
by which, through growthrates, mutation, recombination, and
hori-zontal gene transfer, microbes diversifyand adapt to changing
environmentalconditions. Of crucial importance is
thatdiversification leads to the generation ofnovel microbial
genotypes and, at a largescale, contributes to variations in
commu-nity composition. This process hasgreater importance for
spatially separatedsystems by shifting the strength and/ormechanism
by which selection operates.
The appreciation of community ecologyas a framework unfolds a
sweeping per-spective on plant microbiome research. Itallows a
pragmatic change from focusingon questions such as ‘who is there’
and
‘what they are doing’ towards a morefundamental understanding of
the build-ing blocks that underpin any given com-munity assembly
and spatiotemporaldynamics. That is, studies across distinctsoil
types, plant genotypes, and scalesare likely to result in
idiosyncratic out-comes of factors that determine thestructure of
plant microbiomes. However,community ecology enables for a
con-ceptual and mechanistic unification by(i) quantifying the
degree to which thesefour high-level processes operate
acrossdistinct systems, and (ii) identifying themechanisms (biotic
and/or abiotic) thatregulate their relative influences acrosstime
and space [4].
How Can Community EcologyHelp in Engineering
PlantMicrobiomes?The ongoing revolution in plant micro-biome
research has unequivocally shownthat microbes impact on plant
growth,nutrition, and tolerance to (a)bioticstresses. To date,
however, these micro-biome-associated phenotypes (MAPs) [5]have
been primarily qualitative and taxon-omy-driven rather than
quantitative andtrait-based. Hence, translating funda-mental
knowledge into effective strate-gies to manipulate and engineer
plantmicrobiomes remains a major challenge.This is evidenced by the
numerous failedattempts to effectively manipulate andengineer
single microbial strains as bio-fertilizers and/or biocontrols that
consis-tently perform at large temporal scalesand across different
geographic loca-tions. Within this context, Oysermanet al. [5]
recently introduced the conceptof the ‘modular microbiome’ –
microbialconsortia that are engineered in concertwith the plant
genotype to confer differentbut mutually compatible MAPs to a
singlehost or host population.
We propose here that future directions inplant microbiome
research would benefit
Trends in Plant Science, June 2018, Vol. 23, No. 6 467
by incorporating community ecology the-ory. In particular,
community ecology canprovide a foundation upon which pro-spective
experimental designs can bedeveloped and ecological theories canbe
tested. For instance, understandinghow community assembly
processesinterplay in structuring plant microbiomesover the course
of plant development iscrucial (Figure 1). A quantitative
frame-work for the relative importance andquantitative influences
of communityassembly processes and the mechanisticunderpinning has
been previouslyreported [1,6] and successfully appliedacross
divergent systems (e.g., [6,7]).This effort can enhance our
predictability
of the factors that determine the success-ful establishment of
introduced microbialstrains or modular microbiomes in thecontext of
the recipient (‘indigenous’)plant-associated microbiome. In a
recentstudy, Niu et al. [8] reported the develop-ment of a greatly
simplified ‘modular’ bac-terial community in a gnotobiotic
maizemodel system. By narrowing down thecomplexity of the
root-associated micro-biome, these authors reported an effec-tive
consortium (or ‘module’) consisting ofonly seven strains
(Enterobacter cloacae,Stenotrophomonas maltophilia, Ochro-bactrum
pituitosum, Herbaspirillum frisin-gense, Pseudomonas
putida,Curtobacterium pusillum, and
Chryseobacterium indologenes). Theyelegantly showed that the
removal ofone strain (E. cloacae) led to collapse ofthe
root-associated community and theconcomitant loss of protection of
the hostplant against the fungal pathogen Fusar-ium
verticillioides. Their findings constitutea classic example of how
the order inwhich microbes disperse towards and/or colonize
plant-roots, in other wordspriority effects, impact on
microbiomeassembly (through coexistence dynam-ics) and on
microbiome functionality.The studies by Vannette and Fukami [9]and
Toju et al. [10] provide additionalenlightening examples of the
role of dis-persal and priority effects on the
*Priority effects
*
*Priority effeccttsority effeffecfffforityiiti
****
*P*P irioP iioo
Selec�on . bio�c/abio�c interac�ons resul�ng in fitness
differences
Dri� . random changes in popula�on sizes owing to stochas�c
birth and deathDispersal . the movement of organisms across
space
DispersalDri�
Selec�onPredicted changes in the rela�ve influences of community
assembly processes (%)
Figure 1. Conceptual Figure Depicting the Relative Influences of
Community Assembly Processes ThatMediate the Establishment and
Dynamics ofPlant-Associated Microbiomes. The seed and emerging root
system are more prone to priority effects because they are
initially exposed to primary colonization.Priority effects are also
hypothesized to be important duringmicrobiome assembly of emerging
flowers and leaves. The external surfaces of aboveground sections
of theplant (leaves, shoots) are more prone to microbial dispersal
(e.g., via air, insects) and drift, given their exposure to abiotic
(UV radiation, temperature) and biotic (plantpathogen, insets)
stressors. Drift is also expected to be intensified in communities
with low densities and richness that are regularly exposed to
dispersal [12].Belowground, the rhizobiome is hypothesized to be
influenced by a complex interplay of selection, dispersal, and
drift, with a gradual change in selection as the plantages.
Themechanismsmediating the balance among these community assembly
processes across distinct plant sections vary according to plant
genotype/phenology(exudation profile), soil type (physicochemical
properties including pH, organic matter content, and moisture),
biotic/abiotic stressors, and agricultural managementpractices. The
process of speciation (or ‘diversification’) is only expected to be
pronounced among sets of communities that do not exchange
individuals throughdispersal [1,3,6]. The relative influence of
this particular process is not depicted in the conceptual
figure.
468 Trends in Plant Science, June 2018, Vol. 23, No. 6
functional properties of plant micro-biomes that colonize floral
nectar. Theyfound not only that priority effects gener-ate
variability in species colonization andcommunity divergences [9],
but also thatsuch divergence can persist for anextended period
within and across floralgenerations [10]. Based on the
availableliterature it is difficult to grasp to whatextent priority
effects influence rhizo-biome assembly in natural settings, andthe
degree to which this effect may persistacross plant generations.
Such investiga-tions will provide insight into how manip-ulation of
plant microbiomes should takeinto account how orderly species
arrive inthe system, and how their interactionsmodify the local
environment and leadto coexistence through communityassembly. In
synthesis, by recognizingthat microbiomes are modular
entitiesdynamically influenced by well-definedeco-evolutionary
processes, fundamen-tals of community ecology provide apromising
path towards engineering plantmicrobiome systems.
PerspectivesTransforming our broader fundamentalunderstanding of
microbe–plant interac-tions into practical management strate-gies
requires the integration ofcommunity ecology theory into
plantmicrobiome research. We see new ave-nues for experimental
designs in plantmicrobiome research that can profit fromthis
quantitative framework. For instance,to what extent do plant seeds
and seed-lings treated with synthetic microbialcommunities develop
distinct and stablemicrobiome assemblages? (e.g., [11]).What is the
relative influence of priorityeffects in determining the success of
seedendophytes through plant generationsand across distinct plant
genotypes?How do distinct microbiomes and theexpression of
plant-beneficial traitschange over the course of plant
develop-ment? Further, to what extent do abiotic(e.g., heat,
drought) and biotic (e.g.,
pathogen, insect) stressors affect the rel-ative importance of
the four high-levelprocesses (selection, dispersal, drift,and
speciation) in plant microbiomeassembly and functioning?
Our perspective is that community ecol-ogy offers the tools and
concepts todevelop a more holistic and mechanisticsynthesis in
plant microbiome research. Itis likely that more studies will
progres-sively appear in the literature that contex-tualize the
interplay of communityprocesses in plant microbiome assembly.In
this sense, this article anticipates a callfor action highlighting
recent studies thatprovide a valuable guideline to assistthese
future research directions. In doingso, we foresee that adopting an
ecologi-cal perspective and systems approach inplant microbiome
research enables apath forward towards enhancing theeffectiveness
and practical implementa-tion of modular microbiomes for the
sus-tainable production of food, feed, andfiber.
AcknowledgmentsWe thank Lucas W. Mendes for critical reading of
the
manuscript [76_TD$DIFF][74_TD$DIFF]. Publication number 6513 of
the
Netherlands Institute of Ecology, NIOO-KNAW.
1Department of Microbial Ecology, Netherlands Institute
of Ecology (NIOO-KNAW), 6708 PB Wageningen, The
Netherlands@Twitter: @FDiniAndreote
*Correspondence:
[email protected] (F. Dini-Andreote).
https://doi.org/10.1016/j.tplants.2018.03.013
References1. Vellend, M. (2016) The Theory of Ecological
Communities,
Princeton University Press
2. Busby, P.E. et al. (2017) Research priorities for
harnessingplant microbiomes in sustainable agriculture. PLoS
Biol.15, e2001793
3. Nemergut, D.R. et al. (2013) Patterns and processes
ofmicrobial community assembly. Microbiol. Mol. Biol. Rev.77,
342–356
4. Dini-Andreote, F. et al. (2015) Disentangling mechanismsthat
mediate the balance between stochastic and deter-ministic processes
in microbial succession. Proc. Natl.Acad. Sci. U. S. A. 112,
E1326–E1332
5. Oyserman, B.O. et al. (2018) Road MAPs to engineer
hostmicrobiomes. Curr. Opin. Microbiol. 43, 46–54
6. Stegen, J.C. et al. (2013) Quantifying community
assemblyprocesses and identifying features that impose them. ISMEJ.
7, 2069–2079
7. Wang, J. et al. (2013) Phylogenetic beta diversity in
bac-terial assemblages across ecosystems: deterministicversus
stochastic processes. ISME J. 7, 1310–1321
8. Niu, B. et al. (2017) Simplified and representative
bacterialcommunity of maize roots. Proc. Natl. Acad. Sci. U. S.
A.114, E2450–E2459
9. Vannette, R.L. and Fukami, T. (2017) Dispersal enhancesbeta
diversity in nectar microbes. Ecol. Lett. 20, 901–910
10. Toju, H. et al. (2017) Priority effects can persist across
floralgenerations in nectar microbial metacommunities. Oikos127,
345–352
11. Mitter, B. et al. (2017) A new approach to modify
plantmicrobiomes and traits by introducing beneficial bacteria
atflowering into progeny seeds. Front. Microbiol. 8, 11
12. Evans, S. et al. (2017) Effects of dispersal and selection
onstochastic assembly in microbial communities. ISME J.
11,176–185
SpotlightNPR1 in JazzSet with[35_TD$DIFF]Pathogen EffectorsYali
Sun,1 ThomasWard Detchemendy,1 KarolinaMarta Pajerowska-Mukhtar,1
andM. Shahid Mukhtar1,2,*,@
NON-EXPRESSOR OF PATHO-GENESIS-RELATED GENES 1(NPR1) is a master
regulator of sal-icylic acid (SA)-mediated systemicacquired
resistance (SAR), a broad-spectrumdisease resistancemech-anism in
plants. NPR1 controlsapproximately 90% of SA-depen-dent
transcriptome in Arabidopsis.Here, we discuss how pathogeneffectors
manipulate NPR1 func-tions in different cellular compart-ments to
establish disease.
Up [37_TD$DIFF]first: Regulation of NPR1 indiverse cellular
statesPlants detect molecular components ofthe invading pathogens
including micro-bial-associated molecular patterns(MAMPs) and
pathogen effectors, rewirethe flow of biological information,
and
Trends in Plant Science, June 2018, Vol. 23, No. 6 469
https://twitter.com/@FDiniAndreotemailto:[email protected]://doi.org/10.1016/j.tplants.2018.03.013http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0005http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0005http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0010http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0010http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0010http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0015http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0015http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0015http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0020http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0020http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0020http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0020http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0025http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0025http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0030http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0030http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0030http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0035http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0035http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0035http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0040http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0040http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0040http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0045http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0045http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0050http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0050http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0050http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0055http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0055http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0055http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0060http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0060http://refhub.elsevier.com/S1360-1385(18)30081-5/sbref0060
Embracing Community Ecology in Plant Microbiome
ResearchCommunity Ecology as a Framework for Plant Microbiome
ResearchHow Can Community Ecology Help in Engineering Plant
Microbiomes?PerspectivesAcknowledgmentsReferences
NPR1 in JazzSet with Pathogen EffectorsUp first: Regulation of
NPR1 in diverse cellular statesWhat's good with: NPR1 and pathogen
effectorsRough translation: AvrPtoB-mediated ubiquitination of
NPR1Bullseye: Outlook of NPR1 as a target of pathogen
effectorsAcknowledgmentsReferences
The Plant Target of Rapamycin Kinase: A connecTOR between Sulfur
and GrowthWhat Is TOR?Sulfur Metabolism in PlantsHow Does TOR Sense
Sulfur Availability?Another TOR Connection with
SulfurAcknowledgmentsReferences
The Dual Face of Cyclin B1Concluding Remarks - A Word of
CautionAcknowledgmentsReferences