1
The phyllosphe e mic obiome and i s applica ions in
sus ainable ag icul u e
Ka en Uchida1
1Depa men o Plan Sciences, Uni e si y o Camb idge, UK
Summa y
Plan s in e ac wi h di e se mic oo ganisms ha collec i ely o m a mic obiome. These mic obial
communi ies play an impo an ole in main aining plan heal h and o e p omising al e na i es
o syn he ic e ilise s and pes icides which ha m he en i onmen . The phyllosphe e e e s o
abo e-g ound po ion o a plan . This e iew p o ides an o e iew o he cu en esea ch on
he phyllosphe e mic obiome in majo ood c ops and discusses i s po en ial applica ions in
ag icul u e. Fu he s udies a e needed o expand ou knowledge o mic obiome unc ions and
link hem o plan gene ics. This could unlock no el mic obiome-based app oaches ha suppo
sus ainable ood p oduc ion o he g owing global popula ion.
In oduc ion
Cu en ag icul u al p ac ices a e de imen al o he en i onmen wi h he ex ensi e use o
e ilise s and pes icides dis up ing he global biogeochemical cycles and leading o he loss o
na u al biodi e si y (Campbell e al., 2017). Wi h he global popula ion p ojec ed o each 9.7
billion by 2050, ood demand is expec ed o ise by up o 60% be ween 2010 and 2050 (UN,
2017; an Dijk e al., 2021). Hence i is essen ial o shi owa ds sus ainable ag icul u al
p ac ices ha maximise ood p oduc ion while minimising en i onmen al impac s (Ga ne e al.,
2013; Richa dson e al., 2023). Ha nessing plan -associa ed mic obes is p oposed as a
p omising al e na i e o syn he ic chemicals o enable sus ainable ood p oduc ion (Hu, Chen
and He, 2022).
Plan s in e ac wi h di e se mic oo ganisms including bac e ia, ungi, a chaea, p o is s and
i uses ha o m he plan mic obio a (Be g e al., 2020; Zilbe -Rosenbe g & Rosenbe g, 2008).
The e m mic obiome, i s in oduced by Whipps and his eam in 1988, desc ibes a collec ion o
genomes, me aboli es and unc ions o he mic obio a and hei in e ac ions wi h i s hos plan
and he su ounding en i onmen (Ma chesi and Ra el, 2015). Dis inc mic obiomes can be
ound ac oss di e en pa s o a plan including he phyllosphe e, which encompasses all abo e-
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g ound pa s including lea es, s ems (caulosphe e), lowe s (ca poshe e) and ui s
(an hosphe e) (Figu e 1A, B) (Lindow and B andl, 2003).
Lea es a e among he la ges mic ohabi a s on Ea h wi h hei o al su ace es ima ed o be
wice he size o all land a ea and inhabi ed by up o 1026 bac e ia (Vo hol , 2012). They a e
colonised by epiphy es on he su ace and endophy es wi hin he in e nal issues (Figu e 1C)
(Soh abi e al., 2023). Mic obial species a e he e ogeneously dis ibu ed ac oss he lea su ace
(Figu e 1D) (Kuss a sche e al., 2020; Remus-Emse mann e al., 2014; Saa enpää e al.,
2024). Fo example, some bac e ial species inhabi glandula ichomes on oma o lea es whe e
Figu e 1: Plan s in e ac wi h di e se mic oo ganisms ha collec i ely o m he
mic obiome. (A) Dis inc mic obial communi ies a e associa ed wi h di e en plan
compa men s. (Bpd) Mic obiomes consis o a complex ne wo k o in e ac ions wi hin and
be ween mic obial species. (C) Epiphy es colonise he lea su ace while endophy es inhabi
he in e nal lea issues. (D) Bac e ia colonising lea ichomes. Mic oo ganisms occupy
dis inc spa ial niches ac oss he plan su ace.
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plan me aboli es accumula e (Kuss a sche e al., 2020). Despi e he impo ance o spa ial
dis ibu ion o mic obial in e ac ions wi h plan s and o he mic obes, i is o en o e looked in
s udies ha ely solely on bioin o ma ic app oaches.
The phyllosphe e mic obiome is a complex ne wo k o plan -mic obe and mic obe-mic obe
in e ac ions (Figu e 1B) (Chaudh y e al., 2021). Wi hin his ne wo k, mic oo ganisms ha a e
consis en ly ound ac oss samples om a speci ic habi a o a plan a e known as he co e
mic obiomes (Shade and Handelsman, 2012). Compu a ional analyses o mic obial ne wo ks
a e used o iden i y he “hub” o “keys one” species, which in e ac wi h mul iple species and
play a cen al ole in shaping he mic obiome (Agle e al., 2016). These key species a e a ge s
o manipula ing he mic obiome as changing hei abundance can signi ican ly al e he o e all
mic obiome composi ion and s uc u e (Toju e al., 2018).
Mos plan mic obiome esea ch has ocused on below-g ound mic obiomes which accoun ed
o o e 80% o s udies in ce eal c ops (Michl, Be g and Ce na a, 2023). Ne e heless, he
phyllosphe e mic obiome is gaining a en ion o i s ole in p omo ing g ow h and disease
esis ance (De Mandal and Jeon, 2023). This e iew will p o ide an o e iew o he cu en
s a e o phyllosphe e mic obiome esea ch wi h a ocus on ag icul u ally impo an ood c ops
and discuss hei po en ial applica ions in sus ainable ag icul u e.
Main
Cu en phyllosphe e mic obiome esea ch
To gain an o e iew o he cu en s a e o he phyllosphe e mic obiome esea ch, a li e a u e
sea ch was conduc ed on he Web o Science by using he keywo ds “Plan ,” “Phyllosphe e”
and “Mic obiome.” This esul ed in 584 p ima y esea ch a icles and 89 e iews as o 1s Ma ch
2025. Wi hin he esea ch a icles, en ies ha we e misca ego ised, such as e iews, book
chap e s o s udies ocused exclusi ely on he hizosphe e we e excluded, esul ing in a lis o
503 publica ions. While phyllosphe e mic obiome esea ch began in he ea ly 2000s as e iden
by key e iews including Lindow and B andl (2003) and Vo hol (2012), he ea lies a icles om
his sea ch was om 2013 (Figu e 2A). This could be due o changes in e minology o e ime,
highligh ing he limi a ion o his sea ch me hod. Ne e heless, he lis was used o u he
analysis o gain an insigh in o he ends in phyllosphe e mic obiome esea ch o e he pas
decade.
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The g owing in e es in phyllosphe e mic obiome esea ch was e iden in he inc easing numbe
o publica ions (Figu e 2A). O e all, 57.5% o he a icles ocused on ood c ops such as
ce eals, ege ables and ui s o cash c ops including apeseed, cacao and co on, while 39.1%
co e ed non-ag icul u al plan s including wild ees, g asses and sh ubs. The emphasis on
ag icul u ally ele an c ops is p omising as his could d i e p og ess owa ds ha nessing
mic obiomes in ag icul u e.
Figu e 2: O e iew o cu en phyllosphe e mic obiome esea ch. (A) Numbe o
esea ch a icles published pe yea . A icles we e ca ego ised as ag icul u e ( ood c ops o
cash c ops) o ecology (non-ag icul u al plan species) based on he plan species s udied.
(B) Di e si y o ood c ops s udied wi h he numbe o a icles indica ed o each c op. (C)
P opo ion o s udies using amplicon o me agenomic sequencing. (D) Types o
mic oo ganisms s udied using amplicon sequencing.
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Al hough he phyllosphe e mic obiome has been s udied in o e 70 di e en ood c ops, he
esea ch p ima ily ocused on globally impo an s aple c ops such as ice, whea and maize
(Figu e 2B). Toma oes and le uce we e among he mos ex ensi ely s udied ege ables.
G ape ines we e widely esea ched in Eu ope due o hei economic alue o ui and wine
p oduc ion (Awad e al., 2023). Highly s udied c ops such as ice had ex ensi e esou ces,
including high-quali y sequencing da ase s ha can be used o u he s udies (Masuda e al.,
2024; Su e al., 2022). Resea ch ocused on speci ic c ops can help build obus model sys ems
o ad ance ou unde s anding o mic obiomes and apply hem o o he plan s.
A key s ep in mic obiome esea ch is using sequencing o cha ac e ise he composi ion,
abundance, di e si y, and s uc u e o a gi en mic obiome. Two commonly used sequencing
echniques a e amplicon o me agenomic sequencing (Liu e al., 2021). Amplicon sequencing
in ol es he ampli ica ion o a a iable gene ic egion (Regalado e al., 2020). Fo p oka yo es
and a chaea, his locus is in he 16S ibosomal RNA ( RNA), while in euka yo es, he in e nal
ansc ibed space (ITS) egion o he 18S RNA is used (Schoch e al., 2012). In con as ,
me agenomic app oaches use sho gun o long- ead sequencing o cha ac e ise he en i e
gene ic con en o a sample, including plasmids and i uses (Handelsman e al., 1998; Masuda
e al., 2024; Po ik, B own & Pie ce-Wa d, 2022). While some s udies ca ego ise amplicon
sequencing as ‘me agenomics,’ i is impo an o dis inguish hese e minologies as
ampli ica ion-based me hods do no cha ac e ise he en i e genome (Aguia -Pulido e al., 2016;
Quince e al., 2017). In his e iew, he e m 'me agenomics' speci ically e e s o whole-genome
sequencing.
O e 80% o s udies elied on amplicon sequencing (Figu e 2C). Al hough i is high- h oughpu
and cos -e ec i e, majo d awbacks include low axonomic-le el esolu ion and p ime bias
which can hinde he de ec ion o ce ain axa (Liu e al., 2021). Ne e heless, amplicon da a a e
o en used in co ela ion-based ne wo k analyses o p edic mic obial in e ac ions and iden i y
key axa (Faus and Raes, 2012; Sapko a, Jø gensen and Nicolaisen, 2017). Me agenomics
can o e come hese limi a ions by p o iding species-le el classi ica ion, enabling ad anced
unc ional cha ac e isa ion (Su e al., 2022). In eg a ing sequencing wi h mul i-omics
app oaches, such as ansc ip omics and me abolomics can expand ou unde s anding o
mic obiome unc ions (Wu e al., 2024). Howe e , i is impo an o no e ha hese bulk analysis
me hods ail o cap u e he spa ial dis ibu ion o mic obe-mic obe in e ac ions which in luence
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hei unc ions (Remus-Emse mann and Schlech e , 2018). The e o e, addi ional expe imen s
a e needed o alida e he in e ed obse a ions.
Despi e being e med ‘mic obiome’, mos s udies ha e p ima ily ocused on bac e ia and ungi,
lea ing a signi ican knowledge gap ega ding he di e si y and unc ions o phyllosphe e
a chaea, p o is s and i uses (Figu e 2D). This is due o he widesp ead use o bac e ial and
ungal-speci ic amplicon sequencing and he lowe abundance o a chaea and p o is s in he
phyllosphe e compa ed o bac e ia and ungi, which makes hem di icul o de ec (Ta ne e
al., 2019). Ne e heless, a chaea and p o is s ha e key oles in plan nu ien cycling and
pa hogen con ol (Sun e al., 2021; Ta ne e al., 2019). This unde sco es he need o di e si y
esea ch me hods o gain a mo e comple e unde s anding o he mic obiome.
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Box 1: Ho spo s o phyllosphe e mic obiome esea ch
To in es iga e he global dis ibu ion o phyllosphe e mic obiome esea ch, he s udy
loca ions p o ided in he me hods sec ion we e mapped (Figu e 3). This e ealed ha
esea ch on ood c ops was concen a ed in China, he Uni ed S a es and India. The
dis ibu ion mi o ed ends obse ed in a me a-analysis o o e 300,000 plan science
publica ions, which highligh ed he geog aphic dispa i ies in cu en esea ch (Ma ks e al.,
2023). The s udy also poin ed ou he bias owa ds s udying a limi ed numbe o plan
species, p ima ily model sys ems and majo c ops, which was also obse ed in phyllosphe e
mic obiome esea ch.
Mic obial p oduc s a e o en p oposed as p omising ools o sus ainable ag icul u e as pa
o achie ing global goals such as he Uni ed Na ions Sus ainable De elopmen Goal Ze o
Hunge (Hu, Chen and He, 2022). Howe e , ha nessing mic obes would equi e expanding
esea ch o di e se geog aphic loca ions and plan species, including o phan c ops and wild
a ie ies o comme cial c ops (Ce na a, 2024; Yin e al., 2023). This would acili a e he
de elopmen o mic obiome-based s a egies ailo ed o di e en egions (Ayeni e al., 2024).
Figu e 3: Geog aphic dis ibu ion o phyllosphe e mic obiome esea ch. G een ci cles
ep esen ing include s udies on majo ood and cash c ops.
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Nume ous s udies ha e in es iga ed he e ec o bio ic, abio ic and an h opogenic ac o s on
he composi ion o he phyllosphe e mic obiome as e iewed by Bashi e al. (2022). Building on
hese indings, he emainde o his e iew will ocus on hei po en ial applica ions in
sus ainable ag icul u e. Th ee main s a egies o ha nessing he phyllosphe e mic obiome
include: (1) enginee ing mic obial communi ies o enhance bene icial ai s, (2) manipula ing
hos plan gene ics o na u ally ec ui a ou able mic obiomes and (3) adap ing ag icul u al
p ac ices o p omo e he o ma ion o bene icial phyllosphe e mic obiome.
Enginee ing he phyllosphe e mic obiome
The knowledge o phyllosphe e mic obiome di e si y and composi ion can be applied o design
mic obial communi ies wi h desi ed unc ions using mic obiome enginee ing (Figu e 4).
(Lawson e al., 2019). This include bo om-up app oaches whe e he indi idual mic oo ganisms
a e isola ed and cha ac e ised (Ke, Wang and Yoshikuni, 2021). Mic obial s ains wi h bene icial
ai s can be used o build syn he ic communi ies (SynComs) o hei me aboli es can be applied
as p obio ics o ec ui bene icial mic obiomes (Figu e 4A, B). In con as , op-down app oaches
u ilise exis ing mic obiomes, ei he by di ec ansplan a ion o modi ying hem h ough selec i e
passaging o i us-media ed enginee ing o en ich bene icial ai s (Figu e 4C-E). This sec ion
will discuss key indings in phyllosphe e mic obiome esea ch on ood c ops unde he
amewo k o mic obiome enginee ing.
9
Designe mic obiomes as p obio ics
A syn he ic communi y (SynCom) is an assembly o unc ionally cha ac e ised mic oo ganisms
(Vo hol e al., 2017). I is commonly used as a simpli ied model o a complex mic obial
communi y o in es iga e ac o s ha in luence he mic obiome assembly (Niu e al., 2017).
Beyond undamen al s udies, SynComs can be assembled om bene icial mic oo ganisms o
p oduce p obio ics ha enhance plan heal h by p omo ing g ow h and p o iding p o ec ion
agains diseases (Vassile a e al., 2020).
Combining se e al s ains in a SynCom p oduces an addi i e e ec ha enhances he bene icial
ai s o indi idual s ains. Fo example, di e en combina ions o Pseudomonas s ains, isola ed
om po a oes in ec ed wi h he la e bligh oomyce es Phy oph ho a in es ans, we e es ed using
a lea disk assay (De V ieze e al., 2018). This iden i ied combina ions o wo s ains ha
exhibi ed highe p o ec ion agains P. in es ans han when applied indi idually (De V ieze e al.,
2018). Likewise, in A abidopsis haliana, bac e ial s ains ha supp ess Pseudomonas sy ingae
Figu e 4: Mic obiome enginee ing consis s o bo om-up and op-down s a egies.
Bo om-up app oaches include (A) syn he ic communi ies (SynComs) and (B) he use o
me aboli es as p ebio ics. Top-down app oaches include (C) mic obiome ansplan , (D)
successi e passaging and (E) i us-media ed enginee ing.
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ha educed use o pes icides and he bicides could help p ese e bene icial mic obial
communi ies on c op su aces.
Addi ionally, no- ill a ming sys ems demons a ed a highe eco e y o ungal ne wo ks
ollowing ungicide applica ion, wi h 61% o co e mic obiome eco e ed compa ed o 34% in
con en ional sys ems (Noel e al., 2022). This was likely due o ae ial spo e dispe sal by yeas s
pe sis ing in esidual c ops om he p e ious season in no- ill ields (Noel e al., 2022). Al hough
he unde lying molecula mechanisms emain unclea , hese indings sugges ha p inciples o
egene a i e ag icul u e, such as minimal chemical inpu and no- ill managemen may suppo
he esilience and heal h o he phyllosphe e mic obiome (Khangu a e al., 2023).
While he use o li es ock manu e as e ilise s enhances mic obiome ichness in o ganic
a ming, i is also associa ed wi h inc eased abundance o phyllosphe e bac e ia ca ying
an ibio ic esis ance genes (ARGs), aising conce ns abou he sp ead o an ibio ic esis ance
(Chen e al., 2018, 2020). This was seen in le uce and bok choy and he p oposed mechanisms
o ARG ansmission o he lea included soil- o- oo and oo - o-lea ans e o ae ial dispe sal
(Li e al., 2025; Zhang e al., 2019). Biocha , o cha coal, could se e as an al e na i e o
manu e o enhancing mic obiome ichness wi hou con ibu ing o he sp ead o ARGs (Li e al.,
2025).
Va ious s a egies o manipula ing he mic obiome can be in eg a ed in o exis ing a ming
p ac ices. This was demons a ed in a s udy ha es ed a combina ion o syn he ic e ilise s and
a SynCom, consis ing o h ee yeas s ains wi h g ow h-p omo ing ai s isola ed om ice
(Mu huk ishanan e al., 2024). G eenhouse and ield ials showed ha combining he SynCom
wi h 75% o he ecommended e ilise dosage mos e ec i ely inc eased he g ow h and yield
o ice compa ed o using e ilise s o SynComs alone. Such in eg a ed esea ch me hods help
iden i y ways o apidly inco po a e new indings in o cu en a ming p ac ices. These can help
educe he use o chemicals while complemen ing cu en limi a ions o mic obiome-based
me hods, p omo ing he ansi ion owa ds sus ainable ag icul u al p ac ices.
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Conclusion
Phyllosphe e mic obiome esea ch is s ill i s ea ly s ages wi h mos s udies ocusing on
cha ac e ising he composi ion and di e si y o mic obial communi ies wi h a bias owa ds
bac e ia and ungi. Combining sequencing wi h mul i-omics app oaches is key o add ess he
cu en knowledge gaps in he gene ic and molecula basis o mic obiome ai s, including
enhanced plan heal h and esilience agains disease. Recen ad ances in iden i ying plan
genes linked o bene icial mic obiomes p esen a p omising s a egy o inco po a ion in o
b eeding p og ams compa ed o mic obiome enginee ing app oaches, which pose signi ican
challenges in scalabili y. Fu he s udies a e equi ed o alida e hese indings unde ield
condi ions. Mo ing o wa d, mos widely s udied c ops, such as ice and oma oes, could se e
Figu e 5: S a egies o ha nessing phyllosphe e mic obiome in sus ainable
ag icul u e. Based on p e ious indings ha demons a ed e ec s o bio ic, abio ic and
an h opogenic ac o s in shaping he phyllosphe e mic obiome, h ee majo s a egies o
ha nessing he mic obiome in sus ainable ag icul u e we e discussed in his e iew.
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as model sys ems o demons a ing p oo -o -concep o mic obiome-based s a egies.
Ul ima ely, in eg a ed esea ch me hods ha inco po a e cu en indings in o exis ing a ming
p ac ices will be key o p omo e ansi ion owa ds sus ainable ag icul u e o mee he g owing
global ood demand.
Acknowledgemen s
I would like o hank P o esso Sebas ian E es- an den Akke o his guidance du ing he ini ial
discussion. I would also like o exp ess my g a i ude o D Albin Teule , D Da ius Kosmü zky
and D Alex Guyon om he Scho nack g oup o hei aluable ad ice on he d a o his essay.
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