Toward Comprehensive Plant Microbiome Research

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ Towa d Comp ehensi e Plan Mic obiome Resea ch © 2020 Saikkonen, Nissinen and Helande . Published e sion Saikkonen, Ka i; Nissinen, Rii a; Helande , Ma jo Saikkonen, K., Nissinen, R., & Helande , M. (2020). Towa d Comp ehensi e Plan Mic obiome Resea ch. F on ie s in Ecology and E olu ion, 8, A icle 61. h ps://doi.o g/10.3389/ e o.2020.00061 2020 PERSPECTIVE published: 13 Ma ch 2020 doi: 10.3389/ e o.2020.00061 F on ie s in Ecology and E olu ion | www. on ie sin.o g 1Ma ch 2020 | Volume 8 | A icle 61 Edi ed by: Anne Duplouy, Lund Uni e si y, Sweden Re iewed by: A ne Weinhold, F eie Uni e si ä Be lin, Ge many Ra ael Soa es Co ea De Souza, Campinas S a e Uni e si y, B azil Desalegn W. E alo, Ne he lands Ins i u e o Ecology (NIOO-KNAW), Ne he lands *Co espondence: Ka i Saikkonen [email p o ec ed] Special y sec ion: This a icle was submi ed o Coe olu ion, a sec ion o he jou nal F on ie s in Ecology and E olu ion Recei ed: 24 No embe 2019 Accep ed: 26 Feb ua y 2020 Published: 13 Ma ch 2020 Ci a ion: Saikkonen K, Nissinen R and Helande M (2020) Towa d Comp ehensi e Plan Mic obiome Resea ch. F on . Ecol. E ol. 8:61. doi: 10.3389/ e o.2020.00061 Towa d Comp ehensi e Plan Mic obiome Resea ch Ka i Saikkonen1*, Rii a Nissinen2and Ma jo Helande 3 1Biodi e si y Uni , Uni e si y o Tu ku, Tu ku, Finland, 2Depa men o Biological and En i onmen al Science, Uni e si y o Jy äskylä, Jy äskylä, Finland, 3Depa men o Biology, Uni e si y o Tu ku, Tu ku, Finland Mic obes ha e d i en eco-e olu iona y adap a ions o ganizing biodi e si y om he o igin o li e. They a e ubiqui ous and abundan , acili a ing he biochemical p ocesses ha make Ea h habi able and shape ecosys em s uc u es, unc ions, and se ices. Recen s udies e eal ha commensalis ic and bene icial mic obes associa ed wi h wild and domes ica ed plan s may aid in es ablishing sus ainable ag icul u e o a changing clima e. Howe e , de eloping mic obe-based bio echnologies and ecosys em se ices equi es a ho ough unde s anding o he di e si y and complexi y o mic obial in e ac ions wi h each o he and wi h highe o ganisms. We discuss he ho and blind spo s in con empo a y esea ch on plan mic obiomes, and how he la es molecula biological echniques and empi ical eco-e olu iona y app oaches could ele a e ou pe cep ion o mic obe–plan in e ac ions h ough mul idisciplina y s udies. Keywo ds: bac e ia, ungi, mic obiome, endophy es, pa hogens, sap obes, ecology, e olu ion UBIQUITOUS MICROBES IN THE SPOTLIGHT Recen ad ances in molecula mic obiology ha e e olu ionized he abili y o he scien i ic communi y o unde s and and s udy he di e si y and unc ions o mic obes associa ed wi h animals and plan s, leading o a ple ho a o ela ed li e a u e. A Web o Science sea ch (Janua y 23, 2020) using “mic obiome” o “mic obiome and plan ” as opic keywo ds p oduced 28,733 e e ences published, wi h 49 and 1,211 o he pape s anked as “ho ” and “highly ci ed.” Mo e han 99% o he pape s we e published a e 2010. These s udies a e la gely based on mass sequencing o axonomic ma ke genes o bac e ia and ungi (communi y sequencing), and o lesse ex en , me agenomes o mic obial communi ies. Cu en ly, s udies elying on molecula me hodologies domina e plan mic obiome li e a u e. Today we know ha mic obes a e ubiqui ous and essen ial associa es o i ually all highe o ganisms. Fo example, he mic obial cells colonizing he human body appea o be mo e abundan as ou soma ic cells and con ain o e whelmingly mo e genes han ou human genome (Gilbe e al., 2018). Simila ly, mic obes ha e been ound in i ually all plan s (Pa ida-Ma inez and Heil, 2011), and a e known o hei immense signi icance e.g., as plan bene icial myco hizae and endophy es. Pa hogens such as co ee us , lea bligh o ubbe , Panama disease o banana, ches nu bligh , Du ch elm disease, and po a o bligh ha e been culp i s o g ea his o ical con ulsions wi h social impac s (Schumann, 1991). His o ically he po a o bligh , he causal agen o he I ish po a o amine causing he dea h by s a a ion o one million people and o e seas emig a ion o a u he wo million people in he mid-1800s (Schumann, 1991), has been pa icula ly in luen ial in he eme gence o ge m heo y and in shaping he concep ual model o disease iangle (Schumann, 1991). Saikkonen e al. Holis ic Phy obiome Resea ch We p opose ha as mic obes associa ed wi h hei sha ed hos plan s comp ise mul ipa i e en i ies, he heo ies o hologenome e olu ion (Saikkonen e al., 2006; Zilbe - Rosenbe g and Rosenbe g, 2008; Mo an and Sloan, 2015; Vandenkoo nhuyse e al., 2015; Theis e al., 2016; Rosenbe g and Zilbe -Rosenbe g, 2018) and he geog aphic mosaic o coe olu ion (Thompson, 2005) p o ide usable amewo ks o unde s and hese mic obial-plan in e ac ions and hei impo ance o ecological, e olu iona y and gene ic p ocesses. Simila ly o human and animal mic obiomes (Gilbe e al., 2018), he majo i y o plan mic obiomes a e acqui ed om he en i onmen o ansmi ed ho izon ally be ween indi iduals. Howe e , in modula o ganisms (Chapman, 1981) cha ac e ized by soma ic emb yogenesis, such as mos seed plan s, many long-las ing mic obe-plan in e ac ions in ol e ei he e ical o pseudo- e ical ansmission om hos plan o i s sexual and/o ege a i e o sp ing (Wilkinson, 1997; Saikkonen e al., 1998; Canka e al., 2005). Thus, plan mic obiomes p o ide a pa icula ly e ile g ound o ecologis s and e olu iona y biologis s in e es ed in all le els o selec ion in co-e olu iona y p ocesses. The use o me agenomic ools allow us o de e mine he di e si y o mic obiomes and he “-omics” app oaches (genomics, p o eomics and me abolomics) can be used o examine how genomic in o ma ion is ansla ed in o s uc u es and unc ions in he in e ac ions among plan and i s mic obial pa ne s (Delmo e e al., 2009; Lundbe g e al., 2012; Sessi sch e al., 2012; Ha doim e al., 2015; Agle e al., 2016; Saikkonen e al., 2016; an de Heijden and Ha mann, 2016). Fu he mo e, i we ake in o accoun ha pheno ypic selec ion may ea he plan and i s associa ed mic obes indi idually o in conce as a pheno ypic and me agenomic uni , he implica ions o concep ions o gene ics, epigene ics (Jaenisch and Bi d, 2003; Zilbe -Rosenbe g and Rosenbe g, 2008; Vannie e al., 2015) and na u al selec ion a e p o ound. The nex s ep owa d a be e unde s anding o he di e se oles o mic obiomes is o combine me agenomic su eys ega ding he composi ion and unc ion o mic obiomes wi h empi ical and heo e ical biological app oaches including ecology, physiology, gene ics and epigene ics, pheno ypic e olu ion, and coe olu ion o in e ac ing species (Saikkonen e al., 2004, 2016; P osse e al., 2007; Vandenkoo nhuyse e al., 2015; Vannie e al., 2015; Rosenbe g and Zilbe -Rosenbe g, 2016; an O e beek and Saikkonen, 2016). This equi es he acknowledgmen and b eaking o ce ain ba ie s and challenges associa ed wi h scien i ic adi ions and managemen o inc easing in o ma ion o e load. WHY INTERDISCIPLINARY COLLABORATION IS NEEDED We con end ha human pe spec i e o en hampe s unde s anding o he complex na u e o mic obe–plan in e ac ions and hei impo ance o ecosys em unc ions and se ices. Con en ional wisdom biased by human pe cep ions migh misdi ec scien i ic p og ess. We ou line h ee cons aining human ac o s, “pi all o scien i ic discipline,” “ he dilemma o classi ica ion,” and “o e ly op imis ic expec a ions,” which will equi e mul idisciplina y esea ch app oaches o be conque ed. Pi all o scien i ic discipline, i.e., dogma ic concep o ma ion in scien i ic discipline, may cons ain one’s op ions. Con en ional li e science disciplines, such as plan physiology, e olu iona y ecology o phy opa hology, ei he la gely igno e mic obes (Holland and Polacco, 1994; Compan e al., 2016; Kauppinen e al., 2016; Saikkonen e al., 2016; an O e beek and Saikkonen, 2016) o examine mic obe–plan in e ac ions om limi ed, p e-de ined pe spec i es, and la gely build on he knowledge and adi ions o hei own discipline. Such s ongly canalized app oaches limi ou abili y o acknowledge he complexi y o biological in e ac ions and di e en le els o egula ion and selec ion (Koskella e al., 2017). Fo example, phy opa hology examines pa hogen–hos plan in e ac ions ocusing on he ecology and e olu ion o pa hogen– hos in e ac ions, and how hese in e ac ions migh be modula ed by mic obial communi y in e ac ions in he pa hobiome (Vayssie -Taussa e al., 2014). Al hough communi y-le el app oaches ha include o he mic obial plan associa es a e inc easingly being adop ed in plan pa hology (San hanam e al., 2015; Syed Ab Rahman e al., 2018), a signi ican p opo ion o phy opa hology esea ch is dedica ed o epidemiology, disease diagnosis, and managemen o mic obial species o economic o en i onmen al impo ance alone. This, combined wi h he long adi ion o one mic obe–one plan app oach in he ield, migh o e emphasize he pa hogenic phase o he mic obe’s li ecycle and di e a en ion om o he ele an aspec s o he same mic obe–plan in e ac ion, and o e look he impac o whole mic obiomes in disease de elopmen o ep ession. Meanwhile, an inc easing numbe o e olu iona y ecology s udies e eal ha he same mic obial species commonly occupy se e al ecological niches. Thus, he na u e o mic obe–plan in e ac ions is labile and con ex -dependen in ecological and e olu iona y ime a he han always bene icial o disad an ageous o he hos (Saikkonen e al., 1998, 2004; Wäli e al., 2013; Rybako a e al., 2016; Selosse e al., 2018). The same mic obial species migh be labeled a pa hogen, pa asi e, o endophy e, and e e ed o by di e en names. Fo example, a mu a ion o a single locus may con e a ungal plan pa hogen o a non-pa hogenic endophy ic symbion (F eeman and Rod iguez, 1993), and he na u e o he in e ac ion wi h he hos plan is condi ioned on en i onmen al ac o s (e.g., he bi o y o a ailable esou ces), li e-his o y cha ac e s, and gene ic combina ions o he hos and he mic obe (Rybako a e al., 2016). Likewise, he bac e ial species Cla ibac e michiganensis is known as a plan pa hogenic species, and C. michiganensis subspecies a e ega ded as qua an ine o ganisms. Howe e , an endophy ic bac e ial s ain, Cla ibac e s En 12, isola ed om subni al alpine plan s and classi ied as C. michiganensis, is shown o inc ease he chilling ole ance o i s hos plan s, and has no been epo ed o be pa hogenic (Ding e al., 2011; Eichenlaub and Ga emann, 2011). Fu he , he e y same mic obial species a e some imes named di e en ly in di e en con ex s. As o he naming o mic obes, a common endophy e o bi ch ees, Fusicladium be ulae, was named Ven u ia di icha by a o es pa hologis . Ven u ia is a eleomo ph ( he sexual ep oduc i e F on ie s in Ecology and E olu ion | www. on ie sin.o g 2Ma ch 2020 | Volume 8 | A icle 61 Saikkonen e al. Holis ic Phy obiome Resea ch s age) and is now i s o mal name, bu he ac is he species is a bio ophic pa hogen and is mo e commonly an asymp oma ic anamo phic (an asexual ep oduc i e s age) endophy e han ob iously pa hogenic (Ahlholm e al., 2002a;Helande e al., 2007). Simila ly, some plan mu ualis ic myco hizal ungi a e epo ed as asymp oma ic endophy es and o ganic ma e deg ading sap o ophs (Weiß e al., 2016; G ele e al., 2017; Smi h e al., 2017; Ma ino e al., 2018; Schneide -Maunou y e al., 2018). The ques ion is whe he we should conside a mic obe sap ophy ic o pa hogenic i i inhabi s i s hos plan asymp oma ically h oughou mos o i s li e cycle—in he case o pe ennial hos s, pe haps o e yea s—and mani es s i sel as pa hogenic o sap ophy ic du ing only a sho pe iod o i s li e. Simila ly o scien i ic disciplines, he dilemma o classi ica ion, i.e., g ouping mic obes ei he based on hei axa o unc ional ole, di ec s and limi s esea che s’ in e es s o di e en pa s o mic obial communi ies. Consequen ly, he ela ed scien i ic heo ies ha e la gely de eloped sepa a ely ( an O e beek and Saikkonen, 2016). Fo example, bac e ia, ungi, and i uses a e usually s udied sepa a ely, al hough hey coexis and likely o en in e ac wi h each o he (Saikkonen e al., 2004; an O e beek and Saikkonen, 2016). Fu he mo e, in ecological and e olu iona y li e a u e mic obe–plan in e ac ions a e gene ally ea ed sepa a ely om he species–species and mul i ophic in e ac ions o highe o ganisms (e.g., plan –he bi o e in e ac ions), al hough all plan and animal in e ac ions una oidably in ol e mic obes. We belie e ha unde s anding any biological in e ac ion equi es aking mic obiomes o highe o ganisms in o accoun , because oge he he o ganism and he di e se assemblages o i s symbio ic mic obes o m a holobion , an ex ended pheno ype and he a ge o pheno ypic selec ion. This concep o holobion should include all plan associa ed mic obes whene e expe imen ally easible. Finally, o e ly op imis ic expec a ions commonly eme ge when a scien is assembles in o ma ion, becomes exci ed by a ac i e disco e ies, concep s and/o economically p o i able applica ion oppo uni ies, and po en ially misses undamen al biological backg ound knowledge. Me agenomic and p o eomic app oaches illumina e he ubiqui y, di e si y, and impo ance o mic obes, and open ou eyes o associa ed po en ial oppo uni ies. E idence shows ha he majo i y o mic oo ganisms de ec ed by me agenomic ools colonize hei hos plan s asymp oma ically (Compan e al., 2016; Gopal and Gup a, 2016; Nissinen e al., 2019). These mic obial associa es o plan s a e commonly de ined as endophy es (Wilson, 1995). Taxonomically, endophy es a e di e se; hey include a chaeal, bac e ial, ungal, and p o is ic mic oo ganisms. Mos a e conside ed plan commensals bu ew, such as he ungal Epichloë species commonly inhabi ing cool-season g asses, a e ega ded as mu ualis ic, especially in high-nu ien ag oecosys ems (Kauppinen e al., 2016; Saikkonen e al., 2016). Plan mu ualis ic bac e ial endophy es a e less documen ed, bu accumula ing genomic and me abolomic in o ma ion on bac e ial genomes and modula ions in plan me abolism s ongly sugges s hey ha e a ole in plan g ow h, de elopmen , and s ess ole ance (Sessi sch e al., 2012; Ha doim e al., 2015; an O e beek and Saikkonen, 2016; Esmaeel e al., 2018). Inspi ed by e idence ha endophy ic mic oo ganisms a e in ol ed in deni i ica ion, ni ogen ixa ion, and g eenhouse gas emissions, and ha hey can a ec plan ole ance o abio ic s ess, and i ually all ypes o plan –plan , plan – he bi o e o plan –pa hogen in e ac ions, an inc easing numbe o scien is s ha e become in e es ed in he po en ial o endophy ic mic oo ganisms in he bioeconomy. He e we p opose ha his de elopmen migh ha e di ec ed he ocus on o e ly ambi ious goals and expec a ions o he ollowing easons. The mo e we look a he basic biology o mic obes, he mo e ob ious i becomes ha al hough we could go e n endophy ic mic obes, we canno ully con ol hem, especially in he ag icul u al ields and na u e. Mic obial in e ac ions a e known o be labile and con ex dependen anging om an agonis ic o mu ualis ic in bo h ecological and e olu iona y ime (Saikkonen e al., 1998, 2004; Lopes e al., 2009; Be g e al., 2016; B ade e al., 2017). Mic obes ha e po en ial o e ol e apidly as esponse o changing selec ion o ces, and he eby a ec na u e o hei in e ac ion wi h he hos as well as associa ed communi y and ecosys em p ocesses (F eeman and Rod iguez, 1993; Saikkonen e al., 2004; e Ho s e al., 2014). Thus, mu ualis ic, commensalis ic and an agonis ic mic obial axa a e insepa able and p esen in i ually all mic obiomes s udied. We should aim o unde s and he mic obiome dynamics, and conside mic obes as pa o he di e se mul i-kingdom communi y ( an Elsas e al., 2012; Koch e al., 2018), pa icula ly when u ilizing plan mu ualis ic endophy es in sus ainable ag icul u e and ood p oduc ion. FUTURE PERSPECTIVES Recen plan mic obiome esea ch is la gely ocused on desc ibing s uc u e and unc ions o mic obial communi ies in di e en plan associa ed niches, and linking speci ic mic obial axa o plan pe o mance. Una guably, hese s udies ha e apidly gi en us solid unde s anding o b oad axonomic ends in plan associa ed mic obio a. In eg a ion o me agenomics o p o eomics, me abolomics and o he omics-app oaches is now enabling associa ing mic obiome s uc u al shi s o plan holobion unc ioning. Howe e , he mass o da a p o ided by hese echniques can easily o e whelm esea che s ha cu en ly o en lack he ools o o ganize and p ocess he da a, esul ing in low o pape s ca aloging plan and/o mic obial unc ions o e en unanno a ed genes. He e, in eg a ion o ecological heo ies in hese s udies (as also esea che aining) would p o ide s uc u ing amewo k, connec ing now la gely sepa a ed mic obiome esea ch o o he ields o plan -mic obe in e ac ions and ecological and e olu iona y biology. Indeed, plan mic obiome esea ch is ansi ioning om desc ip i e su eys o comp ehensi e unde s anding o he plan holobiome in he eco-e olu iona y amewo k. Iden i ica ion o keys one mic obial species and in e connec ed mic obial hubs, as well as hei pu a i e unc ions (Sessi sch e al., 2012; Agle e al., 2016; Saikkonen e al., 2016; an de Heijden and Ha mann, 2016), a e he basic pieces equi ed o sol e F on ie s in Ecology and E olu ion | www. on ie sin.o g 3Ma ch 2020 | Volume 8 | A icle 61 Saikkonen e al. Holis ic Phy obiome Resea ch he eco-e olu iona y puzzle, comp ised o in e ac ing ee-li ing mic obes and holobiome-uni s in ecosys ems. Easy da a acquisi ion has c ea ed he illusion o con ollabili y and he hope o mic obiology-based inno a ions. This has led o he enaissance o mic obial esea ch seeking solu ions o global issues such as diseases, ood secu i y, and sus ainable ag icul u al p ac ices (Duhamel and Vandenkoo nhuyse, 2013; Kauppinen e al., 2016; Busby e al., 2017; Finkel e al., 2017). Howe e , he majo challenge is ha we a e s ill a long way om unde s anding mic obial e sa ili y and how i ela es o he ecology and e olu ion o plan holobion s in e ac ing wi h each o he and hei en i onmen . Mee ing hese challenges equi es combining no el molecula and mic obiological ools wi h empi ical and heo e ical biological app oaches including ecology, gene ics and epigene ics, pheno ypic e olu ion, and coe olu ion o in e ac ing species. O he wise we lack heo e ical insigh s (P osse e al., 2007), and igno e he complexi y and dynamics o mic obe–plan in e ac ions in man-made and na u al ecosys ems. We p opose ha o assemble he plan holobiome puzzle, u u e wo k should ake in o accoun he ollowing p emises and p esump ions. Fi s , he majo i y o plan -mic obe s udies a e ei he plan o mic obe cen e ed. Acco dingly, s udies a e o en designed and in e p e ed wi h ei he he plan as he ac i e membe which ec ui s i s mic obes (Geh ing and Whi ham, 1994) o he hos plan as a backg ound a iable (e.g., “plan geno ype”) o a habi a . Ins ead, bo h he plan and associa ed mic obes should be aken in o accoun as ac i e membe s o he in e ac ion (Saikkonen e al., 1999; Bulga elli e al., 2012; Dini-And eo e and Raaijmake s, 2018). This equi es de eloping ue dialogue, ecip ocal unde s anding, and mu ual collabo a ion be ween esea che s om di e en li e science ields. Second, we con end ha mic obe–plan in e ac ions ollow simila e olu iona y and ecological p ocesses as hos –pa hogen o hos –pa asi e in e ac ions, and he e o e need no o be ea ed di e en ly (Saikkonen e al., 2004; Co do ez e al., 2019). The p e ailing insigh is ha like o he species in e ac ions, e en obliga e mic obe-plan mu ualism is based on mu ual exploi a ion a he han ecip ocal al uism and bene i s o he pa ne s a e only a ely symme ic (Thompson, 1994; Mayna d Smi h and Sza hma y, 1995; Doebeli and Knowl on, 1998; Saikkonen e al., 2004). Symbioses be ween mic obes and hei hos plan s may also in ol e ecip ocal manipula ion o pheno ypes, including mo phology and physiology, and li ecycle o pa ne s (Saikkonen e al., 2016). Thus, con lic ing selec ion o ces a e likely o des abilize hem, and he ou come o in e ac ions can change in ime and space p ojec ing he ecological su ace o a dynamic i ness landscape wi h adap i e peaks and alleys (Thompson, 1994, 2005; Saikkonen e al., 2004). Fo example, mu ualis ic myco hizae and Epichloë endophy es can become pa asi ic in he p esence o he bi o es o hemipa asi ic plan s especially in esou ce-limi ed en i onmen s (Ahlholm e al., 2002b; Leh onen e al., 2005; Saikkonen e al., 2010a; Wäli e al., 2013). Thi d, co-occu ing plan -associa ed mic obes, i espec i e o axa, a e likely o in e ac wi h each o he . Mic obes compe e, in e ac chemically, and/o media e he hos quali y o each o he . Chemical in e play may include signaling and chemical c oss- alk among mic obes and hei hos plan cells (Hamil on e al., 2012; Compan e al., 2016; an O e beek and Saikkonen, 2016) bu can also ex end o co e o he o ganisms eeding on he sha ed hos plan as well as associa ed ood webs (Leh onen e al., 2006; Saikkonen e al., 2006; Saa i e al., 2010; Li e al., 2014). I is no ewo hy ha ce ain pa hways egula ing plan esponses o he e o ophic o ganisms, such as salicylic acid and jasmonic acid pa hways, ha e been shown o coun e ac (Balla é, 2011; Thale e al., 2012; Pineda e al., 2013). Fo ins ance, chemical c oss alk be ween mu ualis ic mic obes, bio ophic and nec o ophic pa hogens (Bas ias e al., 2018), and he bi o es may cons ain he hos plan om eaching op imal pa hogen- o he bi o e-speci ic esis ance (Ahlholm e al., 2002a), bu is likely o be bene icial o o e all i ness o he holobion . Simila ly, communi y-le el app oaches o bac e ial and ungal in e ac ions a e needed o unde s and he impo ance o he s uc u e and unc ions o mic obial communi y associa ed wi h plan s on plan pe o mance as well as on ecosys em unc ions and se ices (Dini-And eo e and Raaijmake s, 2018). Mo e knowledge abou mul ispecies coe olu ion is necessa y o ully unde s and any pa icula bipa i e mic obe–plan in e ac ions and how hey modula e cascading in e ac ions ac oss ophic laye s. Fou h, he pe o mance o plan -associa ed o ganisms such as mu ualis ic, commensalis ic, and an agonis ic mic obes, as well as he bi o es, may also be a esponse o gene ically o epigene ically de e mined plan ai s a he han in e connec ed associa ions among hem. The ole o epigene ics is s ill poo ly unde s ood. In con as , empi ical e idence sugges s ha o example gene ic compa ibili y can de e mine endophy ic mic obe-plan combina ions ha can be mu ualis ic o commensalis ic depending on en i onmen al condi ions (Saikkonen e al., 2010b). Fu he mo e gene ically de e mined plan ai s can de e mine plan quali y o he e o ophic o ganisms such as mic obes and/o he bi o es (F i z and Simms, 1992) and gene ic co ela ions be ween plan esis ance o pa hogens and he bi o es ha e been sugges ed o cons ain plan s om eaching op imal species-speci ic esis ance (Ahlholm e al., 2002a). Fi h, mic obes a e highly di e se and e sa ile, and he ecological ole o mic obes is o en complex and liable o change. Mic obes can occupy se e al ecological niches ha may o e lap, and he na u e o mic obe–plan associa ion is con ex dependen . The same ecological unc ion can be p o ided by se e al di e en mic obes, and indi idual mic obes can be—a leas pa ially—subs i u able by o he s. This calls impo ance o s udies on he mic obial media ed key unc ions in di e en en i onmen s. The spec um, complexi y, and dynamics o mic obe–plan in e ac ions demons a e ha plan mic obiomes p o ide a e ile g ound o unde s anding uni o selec ion, mul i ophic in e ac ions, e olu ion o li e his o ies, and co-e olu iona y p ocesses, and how mic obiomes should be aken in o accoun when de eloping mic obe-based bio echnologies and ecosys em se ices. Two unanswe ed ques ions emain: (1) How plan s and hei associa ed mic obes indi idually and/o in conce as a pheno ypic uni espond o p e ailing selec ion p essu es? F on ie s in Ecology and E olu ion | www. on ie sin.o g 4Ma ch 2020 | Volume 8 | A icle 61 Saikkonen e al. Holis ic Phy obiome Resea ch (2) Wha p opo ion o ecological ou come is de e mined by gene ics, epigene ics, and pheno ypic plas ici y in he ecologically ele an ai s, and hus in he adap i e adia ion o holobion s? P esen ba ie s mus be disman led in o de o dissemina e cu en knowledge o plan mic obiomes and c ea e a mo e concep ual amewo k wi h empi ical and heo e ical examples, and p edic able hypo heses ( an O e beek and Saikkonen, 2016; F ank e al., 2017). This knowledge is u gen ly needed o ackle he o emos global challenges o ou imes: he biodi e si y loss, clima e change and he inc easing demand o ood p oduc ion o mee wo ld’s popula ion g ow h (Sp ingmann e al., 2018; Tolle son, 2019). Fo example, in he deba e on biodi e si y loss and endange ed species, pa icula a en ion should be paid o he impo ance o abundan keys one species main aining c ucial ecosys em unc ions ha a e i al o h i ing ecosys ems o species ha may h ea en o he species by dis up ing ecosys em unc ions. Mic obes a e la gely igno ed in his con ex al hough hey a e essen ial o p ocesses ha make Ea h habi able o p ima y p oduce s and o he o ganisms subsis ing on hem. Simila ly mic obes should be aken in o accoun in isk analyses and solu ions o aim mi iga ing clima e change as well as in sus ainable ood p oduc ion (Duhamel and Vandenkoo nhuyse, 2013; Gundel e al., 2013; Kauppinen e al., 2016). Fo example, ecen e idence sugges s ha mic obes can inc ease ca bon sink in e es ial ecosys ems by enhancing ca bon up ake in o soils and in o plan s by p omo ing plan g ow h (e.g., myco hizae, hizobia and endophy es) o al e he lux o g eenhouse gases om he soil o he a mosphe e (Clemmensen e al., 2013; Iqbal e al., 2013; A e ill e al., 2014). Bene icial mic obial plan symbion s ha e been sugges ed o ha e g ea po en ial in sus ainable ag icul u al and ho icul u al p ac ices, and o en i onmen al imp o emen as well (Duhamel and Vandenkoo nhuyse, 2013; Gundel e al., 2013; Kauppinen e al., 2016). These goals migh pa ly be o e ly ambi ious because mic obe-plan in e ac ions a e complex, labile and con ex dependen , and hus, we ne e can ully con ol plan associa ed mic obiomes in na u e. Howe e , some o hese ambi ious goals can be a ained i we in es esou ces in mul idisciplina y collabo a ion ac oss a ious ields o expe ise, as unde s anding he plan - mic obiome dynamics and ac o s impac ing holobion ecology and e olu ion can enable us o u ilize he plan mic obiomes o sus ainable u u e. AUTHOR CONTRIBUTIONS KS, RN, and MH ha e con ibu ed equally in ini ializing, inno a ing, and w i ing he pape . FUNDING This wo k was suppo ed by he Academy o Finland, G an Nos. 295976 and 326226 and Finnish Cul u al Founda ion. REFERENCES Agle , M. T., Ruhe, J., K oll, S., Mo henn, C., Kim, S. T., Weigel, D., e al. (2016). Mic obial hub axa link hos and abio ic ac o s o plan mic obiome a ia ion. PLoS Biol. 14:e1002352. doi: 10.1371/jou nal.pbio.10 02352 Ahlholm, J. 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F on ie s in Ecology and E olu ion | www. on ie sin.o g 7Ma ch 2020 | Volume 8 | A icle 61