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

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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

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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:

F.DiniAndreote@nioo.knaw.nl (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

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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:F.DiniAndreote@nioo.knaw.nlhttps://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