pls-08-00883 May 23, 2017 Time: 16:8 # 1
ORIGINAL RESEARCH
published: 26 May 2017
doi: 10.3389/ pls.2017.00883
Edi ed by:
Essaid Ai Ba ka,
Uni e si y o Reims
Champagne-A denne, F ance
Re iewed by:
Au elio Ciancio,
Consiglio Nazionale Delle Rice che
(CNR), I aly
Madhaiyan Munusamy,
Temasek Li e Sciences Labo a o y,
Singapo e
*Co espondence:
Riikka Linnakoski
[email p o ec ed]
Special y sec ion:
This a icle was submi ed o
Plan Mic obe In e ac ions,
a sec ion o he jou nal
F on ie s in Plan Science
Recei ed: 13 Decembe 2016
Accep ed: 11 May 2017
Published: 26 May 2017
Ci a ion:
Linnakoski R, Fo bes KM,
Wing ield MJ, Pulkkinen P and
Asiegbu FO (2017) Tes ing P ojec ed
Clima e Change Condi ions on
he Endoconidiopho a polonica /
No way sp uce Pa hosys em Shows
Fungal S ain Speci ic E ec s.
F on . Plan Sci. 8:883.
doi: 10.3389/ pls.2017.00883
Tes ing P ojec ed Clima e Change
Condi ions on he Endoconidiopho a
polonica /No way sp uce
Pa hosys em Shows Fungal S ain
Speci ic E ec s
Riikka Linnakoski1,2*, K is ian M. Fo bes3, Michael J. Wing ield2, Pe i Pulkkinen4and
F ed O. Asiegbu1
1Depa men o Fo es Sciences, Uni e si y o Helsinki, Helsinki, Finland, 2Depa men o Mic obiology and Plan Pa hology,
Fo es y and Ag icul u al Bio echnology Ins i u e, Uni e si y o P e o ia, P e o ia, Sou h A ica, 3Depa men o Vi ology,
Uni e si y o Helsinki, Helsinki, Finland, 4Na u al Resou ces Ins i u e Finland, Läyliäinen, Finland
Clima e changes, exempli ied by inc eased empe a u es and CO2concen a ion, pose
a global h ea o o es heal h. O pa icula conce n a e pes s and pa hogens, wi h a
wa ming clima e al e ing hei dis ibu ions and e olu iona y capaci y, while impai ing
he abili y o some plan s o espond o in ec ions. P og ess in unde s anding and
mi iga ing such e ec s is cu en ly hinde ed by a lack o empi ical esea ch. No way
sp uce (Picea abies) is one o he mos economically impo an ee species in no he n
Eu ope, and is conside ed highly ulne able o changes in clima e. I is commonly
in ec ed by he ungus Endoconidiopho a polonica, and we hypo hesized ha damage
caused o ees will inc ease unde u u e clima e change p edic ions. To es his
hypo hesis an in i o g eenhouse expe imen was conduc ed o e alua e he e ec s
o a changed g owing en i onmen on E. polonica in ec ed No way sp uce seedlings,
compa ing ambien condi ions o p edic ed empe a u es and CO2le els in Finland o
he yea s 2030 and 2100. In o al, 450 seedlings we e andomized amongs he h ee
ea men s, wi h 25 seedlings om each alloca ed o inocula ion wi h one o i e di e en
ungal s ains o mock-inocula ion. Seedlings we e moni o ed h oughou he he mal
g owing season o mo ali y, and lesion leng h and dep h indices we e measu ed a he
expe imen conclusion. Disease se e i y (mo ali y and lesions) was consis en ly g ea e
in ungal-inocula ed han mock-inocula ed seedlings. Howe e , subs an ial di e ences
we e obse ed among ungal s ains in esponse o clima e scena ios. Fo example,
al hough o e all seedling mo ali y was highes unde he mos dis an (and se e e)
clima e change expec a ions, o he wo ungal s ains wi h he highes mo ali y coun s
( e e ed o as F4 and F5), one p oduced g ea e mo ali y unde he 2030 and 2100
scena ios han ambien condi ions, whe eas clima e scena io had no e ec on he o he .
This s udy con ibu es o a limi ed body o empi ical esea ch on he e ec s o p ojec ed
clima e changes on o es y pa hosys ems, and is he i s o in es iga e in e ac ions
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Linnakoski e al. Fungus-T ee Pa hosys em and Clima e Change
be ween No way sp uce and E. polonica. The esul s indica e he po en ial o u u e
clima e changes o al e he impac o o es pa hogens wi h implica ions o p oduc i i y,
while highligh ing he need o a s ain-speci ic le el o unde s anding o he disease
agen s.
Keywo ds: blue s ain ungi, ca bon dioxide, clima e change, Endoconidiopho a polonica, o es pa hogen, in i o,
pa hogenici y, Picea abies
INTRODUCTION
Human- ela ed dis u bances including clima e change and
globaliza ion pose no el h ea s o global o es heal h (Gau hie
e al., 2015;T umbo e e al., 2015;Wing ield e al., 2015;
Ghela dini e al., 2016). Al hough o es s can adap o ole a e and
eco e om some le el o dis u bance, adap a ion p ocesses a e
cu en ly unde mined by he a e o clima e change (Julkunen-
Tii o e al., 2015;T umbo e e al., 2015). Pa hogens and pes s
ep esen some o he mos impo an h ea s o o es heal h
whe e clima e change is occu ing (Ay es and Lomba de o, 2000;
Allen e al., 2010;Wing ield e al., 2015;Ghela dini e al., 2016).
These ac o s a e ecognized as an inc easing conce n wo ldwide,
bu an unde s anding o how sys ems will espond o clima e
change, and he associa ed need o enac mi iga ion s a egies, is
hinde ed by a lack o empi ical esea ch.
Wa me empe a u es, ele a ed CO2le els and longe
g owing seasons a o many pa hogens h ough enhanced
g ow h a e, ep oduc ion, su i al and accele a ed e olu ion
(Chak abo y and Da a, 2003;Roy e al., 2004;Chak abo y,
2013). Clima e change can also in luence plan esis ance and
ole ance o pes s and pa hogens (Jamiesen e al., 2012). Fo
ins ance, esea ch add essing he e ec s o d ough s ess on
o es ecosys ems has indica ed he po en ial o exace ba ed
epidemics unde clima e change (Allen e al., 2010;Jac el e al.,
2012). Damage caused by pes s and pa hogens is gene ally
expec ed o inc ease unde u u e clima e change scena ios
(Coakley e al., 1999;Ay es and Lomba de o, 2000;Allen
e al., 2010;Bjö kman and Niemelä, 2015), and is suppo ed
by model-based simula ions (B asie , 1996;Jönsson e al., 2009;
Ma ini e al., 2012) and some expe imen al esea ch (Ka nosky
e al., 2002;Pe cy e al., 2002;Chak abo y and Da a, 2003;
Mi chell e al., 2003;Roy e al., 2004;Vá y e al., 2015). O he
s udies ha e iden i ied educed o no e ec o clima e change
on plan diseases (Chak abo y e al., 1998;Coakley e al., 1999;
Roy e al., 2004). These e ec s a y geog aphically and a e o en
species and s ain speci ic (Coakley e al., 1999;Sallé e al., 2005;
Ga e e al., 2006), highligh ing he need o sys ems-based
esea ch.
Bo eal o es s in No he n Eu ope a e pa icula ly ulne able,
whe e p edic ions o u u e clima e changes a e amongs he
mos se e e (Jylhä e al., 2004;Field e al., 2014). O e all,
ele a ed empe a u es and a mosphe ic CO2concen a ions a e
expec ed o a o ee g ow h and inc ease o es y p oduc i i y
(Be gh e al., 2003;Kellomäki e al., 2008). Howe e , some ee
species a e sensi i e o wa ming empe a u es and d ough s ess,
which could lead o majo shi s in ee species dis ibu ions
(Bonan, 2008;Hanewinkel e al., 2011;Lé esque e al., 2013;
Field e al., 2014). An iconic example is he No way sp uce
(Picea abies), which is one o he mos economically impo an
o es y ee species in Eu ope. This species is conside ed
pa icula ly ulne able o clima e change, as i appea s o
ha e a limi ed capaci y o adjus o wa ming-induced d ough
condi ions (Kellomäki e al., 2008;Lé esque e al., 2013) and
inc eased CO2le els (Sallas e al., 2003;K one and Way, 2016).
P edic ed clima e changes a e likely o dec ease i s sou he n
ange abundance, wi h consequen nega i e impac s on economic
po en ial in some egions (Kellomäki e al., 2008;Lé esque e al.,
2013).
One o he mos impo an pes s o No way sp uce in
Eu ope is he Eu asian sp uce ba k bee le (Ips ypog aphus).
Like many insec species, he ba k bee le is highly esponsi e
o changes in empe a u e (Bjö kman and Niemelä, 2015), and
a wa ming clima e has al eady had obse able e ec s on i s
de elopmen and ol inism (Jönsson e al., 2009;Økland e al.,
2015). The bee le has a symbio ic associa ion wi h se e al ungi
o which i se es as a ec o (Wing ield e al., 1993;Sei e
e al., 2013). The mos pa hogenic ungus associa ed wi h he
Eu asian sp uce ba k bee le is Endoconidiopho a polonica, which
is capable o killing ma u e No way sp uce ees (Ch is iansen
and Ho n ed , 1983;Solheim, 1988;K okene and Solheim, 1998;
Ki isi s and O en hale , 2002). I is no known how p ojec ed
clima e changes will in luence he e ec s o E. polonica on
ee heal h o i s abili y o acili a e coloniza ion by he ba k
bee le.
The aim o his s udy was o expe imen ally es in i o
he e ec s o a changed g owing en i onmen on E. polonica
in ec ed No way sp uce seedlings, compa ing cu en ambien
condi ions ( o he yea 2015) o p ojec ed empe a u e
and CO2le els o he yea s 2030 and 2100 in Finland
(Jylhä e al., 2004, 2009). P e ious esea ch has demons a ed
ha seedlings p o ide an e ec i e model o la ge ee
heal h wi hin his sys em (K okene and Solheim, 1998;Repe
e al., 2015). Due o he gene al inabili y o his ee
species o adjus o en i onmen al changes, we hypo hesized
ha disease se e i y on seedlings would be g ea e unde
p edic ed u u e clima e change scena ios han cu en ambien
condi ions.
MATERIALS AND METHODS
Plan Ma e ial
A o al o 450 (2-yea -old) No way sp uce seedlings (Fin Fo elia
Oy, Nu mijä i) o igina ing om Ima a, Sou he n Finland
(61◦090N, 28◦0480E) we e used. A e age seedling heigh
a he beginning o he expe imen was 40 cm. Seedlings
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we e po ed in o plas ic ays o 36 cells (Plan ek 36 F), each
64 mm ×64 mm ×90 mm (dep h), illed wi h e ilized pea
(Vapo pea o o es ees). Plan densi y in he ays was
240 plan s/m2. All seedlings we e main ained in a g eenhouse
(mean empe a u e 14.8◦C) o 1 week and hen ans e ed o
ea men condi ions (see below), whe e hey we e acclima ized
o ∼4 weeks p io o ungal inocula ions.
Expe imen Design
The expe imen was conduc ed du ing he 2015 he mal
g owing season (be ween 9 June and 28 Oc obe ) a he
Haapas ensy jä ield s a ion o he Na u al Resou ces Ins i u e
Finland (Luke) in sou he n Finland. This a ea is cha ac e ized
by a semi-con inen al clima e. Du ing he expe imen al pe iod,
he mean daily empe a u e anged om 4 o 15◦C, consis en
wi h long- e m a e ages. The excep ion occu ed in Augus –
Sep embe , which was app oxima ely 1.5◦C wa me han he
long- e m mean (Finnish Me eo ological Ins i u e, 2016). The
a e age ambien CO2le el was 402 ppm (a he SMEAR
II s a ion (61◦510N, 24◦170E, 4.2 m a.s.l.) (Junninen e al.,
2009). The ield s a ion is equipped wi h a comme cial clima e
con ol sys em LCC-1200 linked o LCC-1240 using Supe Link
.3.5 so wa e (DGT-Volma ic, Odense, Denma k) o moni o
and/o con ol, e.g., he empe a u es and CO2le els ou side
and inside he g eenhouse compa men s a in e als o
1 min.
Fo he expe imen , he 450 sp uce seedlings we e block
andomized (in ays) amongs h ee ea men s: (1) ou side
empe a u e +1◦C+ele a ed CO2, (2) ou side empe a u e
+4◦C+ele a ed CO2, and (3) ou side/ambien empe a u e and
CO2condi ions. One hund ed and i y seedlings we e alloca ed
o each ea men . These empe a u es a e based on clima e
p edic ions o sou he n Finland o he yea s 2030 (+1◦C) and
2100 (+4◦C) (Jylhä e al., 2004, 2009). CO2le els we e se a
550 ppm, consis en wi h low ange p edic ions.
The wo empe a u e-con olled seedling g oups we e
main ained in sepa a e compa men s o a la ge g eenhouse,
whe e he DGT-Volma ic sys em moni o ed ou side
empe a u es and inc eased he g eenhouse oom empe a u es
acco dingly. The con ol seedlings we e main ained alongside
he g eenhouse, and we e hus subjec o e y simila condi ions
o hose in he clima e scena io ea men g oups (including
na u al day leng h, wi h empe a u e and CO2le els he
no able excep ions). Howe e , we canno exclude he possibili y
ha o he po en ial di e ences, such as ligh in ensi y and
quali y (Balla é, 2014), in luenced seedling esis ance o he
ungal in ec ions. Each seedling was inocula ed wi h one
o i e E. polonica s ains (Supplemen a y Table S1), o
mock-inocula ed (25 seedlings pe ungal s ain/ ea men ).
The inocula ion expe imen s a ed a he beginning o
July and was concluded 12 weeks la e , in Oc obe 2015,
o encompass he he mal g owing season in he egion.
Du ing he expe imen , seedlings we e wa e ed as equi ed
o main ain mois soil (usually h ee imes a week). No
addi ional e iliza ion was gi en. The ays we e o a ed
e e y 3 weeks o minimize po en ial e ec s due o hei
posi ioning.
Fungal Inocula ions
Endoconidiopho a polonica s ains we e isola ed om adul
Eu opean sp uce ba k bee les (I. ypog aphus) and hei
pho e ic mi es collec ed om ou b eak egions o Finland and
neighbo ing Russia (Linnakoski, 2011;Linnakoski e al., 2016).
Fo he pu poses o his s udy, ungal s ains a e designa ed
F1 – F5, and u he desc ibed in Supplemen a y Table S1. S ains
we e pla ed on 2% Mal Ex ac Aga (MEA; 20 g Bac oTM Mal
ex ac and 20 g Di co Bac oTM aga om Bec on, Dickinson and
Company, Spa ks, MD, Uni ed S a es, and 1000 ml o MQ-wa e )
in 9 cm Pe i dishes. Cul u es we e g own in an incuba o a 25◦C
o 1 week p io o being used o he inocula ions.
Seedling inocula ions we e made app oxima ely hal way
up he s ems (on he 1s -yea shoo ) by cu ing a ba k lap
(3 ×4 mm) wi h a s e ile scalpel (Figu e 1A). An inoculum o
app oxima ely he same size was cu om he ac i ely g owing
ou e zone o he cul u e pla e, and placed on o he wound wi h
he mycelial su ace acing he exposed sapwood egion. The
inoculum si e was hen co e ed wi h he ba k lap and sealed
wi h Pa a ilm o p e en con amina ion and desicca ion. The
Pa a ilm was emo ed 2 weeks la e . Mock-inocula ions we e
made in he same way, bu using s e ile 2% MEA as inoculum. All
inocula ions we e pe o med by he same pe son (RL) o inc ease
uni o mi y.
Da a Collec ion
Seedling heigh was measu ed a he beginning and end o
he expe imen ( o he nea es 0.5 cm) and seedlings we e
moni o ed o mo ali y a mon hly in e als ( ou moni o ing
occasions h oughou he expe imen ). Mo ali y was de ined
as discolo a ion o all needles abo e he inocula ion poin ,
consis en wi h p e ious s udies (K okene and Solheim, 1998;
Jankowiak, 2006). A he conclusion o he expe imen , he ull
leng h o he nec o ic lesion on he ou e ba k (Figu e 1B) was
measu ed wi h an elec onic calipe ( o he nea es 0.01 mm),
and he ba k was peeled back o expose he sapwood (xylem).
The ull leng h o he nec o ic lesion along he sapwood su ace
(Figu e 1C) was measu ed in he same way. The s em was
hen cu in hal a he uppe edge o he inocula ion si e,
and he s em diame e and lesion dep h (Figu e 1D) we e
measu ed.
To e i y in ec ions, e-isola ions we e made om 25
andomly selec ed inocula ed seedlings om each ea men
(in o al 75 seedlings) a he conclusion o he expe imen by
cu ing small sapwood samples om a ound he inocula ion si es.
These samples we e pla ed on 2% MEA, incuba ed a 25◦C, and
inspec ed o ungal g ow h o up o 2 weeks.
S a is ical Analyses
Gene al linea mixed models (GLMM) we e cons uc ed o
e alua e he e ec s o he clima e change scena ios on ba k
and sapwood lesion leng hs and dep h a he expe imen
conclusion. Due o inhe en imp ecision in measu ing lesion
leng h/dep h in dead wood, seedlings ha died h oughou he
expe imen (53 seedlings) we e excluded om he analyses.
Signi ican ou lie s we e emo ed (G ubb’s es , P<0.05) and
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FIGURE 1 | Lesion indices on he seedling s em in ela ion o he inocula ion: (A) inocula ion poin (B) nec o ic lesion on he ou e ba k (ba k lesion), (C)
nec o ic lesion along he sapwood su ace (sapwood lesion), and (D) lesion dep h.
da a we e na u al log ans o med (lesion leng hs) o app oxima e
no mali y. Ini ial explana o y a iables o he ba k and sapwood
lesion leng h models we e seedling heigh a he onse o
he expe imen (con inuous a iable), clima e change scena io,
ungal inocula ion s ain (bo h ca ego ical a iables), and all
in e ac ions. Seedling ay numbe (ca ego ical), posi ion in he
ay ( h ee ca ego ies; ows/columns anging om he ou side o
he in e io ) and he in e cep we e se as andom ac o s. The
same model was conduc ed o lesion dep h, wi h seedling heigh
eplaced by s em diame e . Since he lesions o mock-inocula ed
seedlings e y a ely ex ended inwa d om he inocula ion poin
(only wo e y mino cases we e iden i ied), hese da a we e
emo ed om he analyses. All models we e sequen ially educed,
whe eby non-signi ican in e ac ion e ms we e emo ed i hei
emo al did no inc ease AIC by >2 uni s (Li ell e al., 2006).
Model compa isons we e made using he maximum likelihood
(ML) me hod and inal alues we e ob ained using es ic ed
maximum likelihood (REML). Model assump ions we e isually
checked om he esidual dis ibu ion.
To acili a e in e p e a ion o a h ee-way in e ac ion be ween
seedling heigh a he onse o he expe imen , ungal s ain and
clima e change scena io in he sapwood lesion leng h model
(Fclima e scena io × ungal s ain ×beg_heigh 10,357 =1.81, P=0.057),
a mixed model was cons uc ed wi h sapwood lesion leng h
explained by heigh a he onse o he expe imen . T ay numbe ,
posi ion in he ay and he in e cep we e again se as andom
ac o s. The esiduals o his model we e hen used as he esponse
a iable in a linea mixed model in which sapwood lesion leng h
was explained by ungal s ain, clima e change scena io and hei
in e ac ion, as pe he me hods desc ibed abo e.
Due o he low o e all p opo ion o seedling dea hs, he
in e ac i e e ec s o clima e change scena io and ungal s ain
on mo ali y le els could no be e alua ed using a linea model
app oach. Ins ead chi-squa ed es s we e used o pai -wise
compa isons o mo ali y coun s be ween he h ee clima e
change scena ios (summing all ungal s ains). Gene alized linea
mixed models, wi h a bina y dis ibu ion and logi link unc ion,
we e cons uc ed o sepa a ely e alua e he e ec s o clima e
change scena io on mo ali y a he end o he expe imen
(dicho omous ou come; ali e o dead) o seedlings inocula ed
wi h he wo ungal s ains ha p oduced he g ea es numbe
o dead seedlings (F4 and F5). Again seedling ay numbe ,
posi ion in he ay and he in e cep we e included as andom
ac o s. Chi-squa ed es s we e used o compa e wi hin-s ain
mo ali y coun s be ween clima e change scena ios o he
o he ungal s ains, excluding mock-inocula ions, which had no
mo ali y.
Pea son co ela ion es s we e used o assess he ela ionship
be ween ou e ba k and xylem sapwood lesion leng h, lesion
dep h and seedling mo ali y. Fo hese compa isons, he
es ima ed ma ginal means o ba k and sapwood lesion leng h
( om he seedling heigh adjus ed model) and lesion dep h o
each clima e change scena io/s ain combina ion we e compa ed
agains each o he and he espec i e g oup seedling mo ali y
coun s. S a is ical analyses we e conduc ed using SAS e sion 9.3
(SAS Ins i u e Inc., Ca y, NC, Uni ed S a es).
RESULTS
To al seedling mo ali y du ing he expe imen was 12%
(53/450), and anged om 0% in he mock-inocula ed g oup
o 25% o seedlings inocula ed wi h ungal s ains F4 and F5
(Figu es 2A,B). Nine y- wo pe cen age o seedling mo ali y
occu ed du ing he ini ial 2 mon hs o he expe imen .
Mo e seedling dea hs occu ed unde he 2100 clima e change
scena io han unde ambien condi ions (26 e sus 9 dea hs; χ2
alue =9.35, P=0.002; Figu e 2A). No signi ican di e ence
was de ec ed be ween he 2030 and 2100 clima e change scena ios
(χ2 alue =1.70, P=0.192).
Fo seedlings inocula ed wi h ungal s ain F5, mo ali y
a ied based on he clima e change scena io (Table 1 and
Figu e 2B). Mo e dea hs occu ed in seedlings assigned o he
2100 (pai -wise di e ence P=0.011) and 2030 (P=0.050)
clima e change scena ios han ambien condi ions. No di e ence
was de ec ed be ween 2030 and 2100 clima e change scena ios.
Con e sely, no a ia ion in seedling mo ali y occu ed unde
clima e change scena ios using he F4 ungal s ain (Table 1
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FIGURE 2 | Seedling mo ali y coun s a he expe imen conclusion: (A) all ungal s ains combined, and (B) di e ences be ween ungal s ain as iden i ied in
gene alized linea models (s ains F4 and F5) and chi-squa ed es s (s ains F1, F2, and F3). Di e en le e s abo e coun s ep esen s a is ically signi ican (P<0.05)
di e ences among clima e change scena ios.
TABLE 1 | Mos pa simonious models o explain esponse a iables (gene al and gene alized linea mixed models).
Response Sou ce o a ia ion Num. d. Den. d. F P
Mo ali y – s ain F5 Clima e scena io 2 66 3.40 0.039
Mo ali y – s ain F4 Clima e scena io 2 66 0.08 0.923
Ba k lesion leng h Onse heigh 1 358 0.00 0.946
Clima e scena io 2 374 1.74 0.177
Fungi s ain 5 374 44.29 <0.001
Scena io ×s ain 10 373 3.82 <0.001
Sapwood lesion leng h Clima e scena io 2 375 8.36 <0.001
Fungi s ain 5 375 142.62 <0.001
Scena io ×s ain 10 375 4.82 <0.001
Lesion dep h S em wid h 1 299 77.09 <0.001
Clima e scena io 2 299 0.31 0.732
Fungi s ain 4 299 28.15 <0.001
Scena io ×s ain 8 299 3.36 0.001
Ini ial lesion models included all in e ac ions be ween he sou ces o a ia ions. Sapwood lesion leng h is adjus ed by heigh a he expe imen onse (see Ma e ials and
Me hods). Highes o de in e ac ions o e ec s a e bolded.
and Figu e 2B). Fo s ain F1, mo ali y was g ea e in he 2100
clima e change scena io han ambien condi ions (Fishe ’s exac
es , wo-sided P=0.022), bu did no a y be ween 2030 and
2100 o be ween ambien condi ions and he 2030 clima e change
scena io. No mo ali y di e ences we e de ec ed be ween clima e
change scena ios o seedlings inocula ed wi h s ains F2 o F3
(Figu e 2B).
Ba k lesion leng h (Table 1 and Figu e 3A), sapwood lesion
leng h (Figu e 3B) and lesion dep h (Figu e 3C) all a ied
based on he in e ac ion be ween clima e change scena io and
he ungal s ain. A sui e o wi hin-s ain di e ences in lesion
leng h and dep h due o clima e change scena ios we e iden i ied,
which a e indica ed in he igu es. Lesion dep h inc eased
wi h seedling diame e (Table 1). Ba k and sapwood lesion
leng hs we e g ea e ac oss all ungal s ains han wi h mock-
inocula ions (s a is ical compa ison was no possible o lesion
dep h, as lesions om mock-inocula ions a ely ex ended in o
he sapwood). Mean sapwood lesion leng h (35.60 mm, ange
4.9 – 139.4 mm) was longe han he mean ba k lesion leng h
(13.7 mm, ange 4.5 – 36.0 mm).
Bo h ba k ( =0.54, P=0.022) and sapwood ( =0.60,
P=0.009; Figu e 4) lesion leng hs we e posi i ely co ela ed
wi h seedling mo ali y coun s, while lesion dep h was no . Ba k
and sapwood lesion leng h we e no co ela ed wi h each o he
(Pea son co ela ion coe icien 0.92, P<0.001). The dep h and
ba k o sapwood lesion leng hs we e no co ela ed.
Minimal seedling g ow h occu ed du ing he expe imen al
pe iod wi h no g ow h eco ded o 243 o 450 seedlings (g ow h
ange 0 o 2 cm). E. polonica was success ully e-isola ed om 74
o he 75 es ed seedlings a he expe imen conclusion.
DISCUSSION
Resul s o his s udy show ha ou comes o ungal in ec ions
may a y be ween cu en en i onmen al condi ions and u u e
clima e change p edic ions in he No way sp uce – E. polonica
pa hosys em. While he mos dis an and se e e p ojec ions
we e he mos de imen al o ee heal h o e all, his end
masked subs an ial be ween-s ain a ia ion in esponses o
he p ojec ed clima e scena ios. This is he i s expe imen al
e alua ion o clima e change e ec s on his pa hosys em, and
indica es po en ial implica ions o u u e o es y p oduc i i y
in no he n Eu ope.
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FIGURE 3 | Es ima ed ma ginal means (e o ba s depic 95% con idence in e als) o seedling lesions a he expe imen conclusion in ela ion o
clima e scena ios and ungal s ain: (A) ba k lesion leng h, (B) sapwood lesion leng h (adjus ed by seedling heigh a he onse o he expe imen and he e o e
an index ela i e o each o he ; see Ma e ials and Me hods), and (C) lesion dep h. Di e en le e s abo e e o ba s ep esen s a is ically signi ican (P<0.05)
wi hin-s ain di e ences.
FIGURE 4 | Rela ionship be ween sapwood lesion leng h index
(es ima ed ma ginal means) and seedling mo ali y coun s (o e all
co ela ion = 0.60, P= 0.009). Each poin ep esen s he mo ali y
coun /mean sapwood lesion leng h o each s ain/ ea men g oup
combina ion. No e ha sapwood lesion leng h is an index adjus ed by
seedling heigh a he beginning o he expe imen .
All o he ungal s ains used in his s udy we e pa hogenic,
and able o induce g ea e seedling damage han he
mock-inocula ions. Mos ungal s ains we e om he same
locali y (Linnakoski e al., 2016), and he among-s ains
di e ences in esponse o clima e change scena ios (e.g., he
mo ali y di e ences be ween s ains F4 and F5; Figu e 2B),
a e hus consis en wi h p e ious obse a ions ha E. polonica
popula ions can include s ains o a ying agg essi eness
(K okene and Solheim, 1998;Lieu ie e al., 2003;Sallé e al.,
2005). The ba k bee le ec o is able o dispe se o e long
dis ances (Nilssen, 1984;Fo sse and Solb eck, 1985), and he eby
accumula e ungal assemblages om di e se geog aphical a eas.
Howe e , his inding highligh s p oblems associa ed wi h
gene alizing esul s ac oss and wi hin pa hogen and hos species,
and hus he need o a ge ed sys em-based esea ch.
Al hough po en ial new pheno ypic and gene ic ma ke s
ha e been de eloped, me hods o accu a ely measu e ee
esis ance/suscep ibili y and ungal pa hogenici y emain
challenging (Ko alchuk e al., 2013;K okene e al., 2013).
P esen ly, measu emen s o nec osis leng h a e he mos
commonly used ma ke s (Ch is iansen and Ho n ed , 1983;
Ho n ed e al., 1983;Solheim, 1988;K okene and Solheim,
1998;Ki isi s and O en hale , 2002). In his s udy, he lesion
leng h indices we e e ec i e gene al p edic o s o seedling
mo ali y, wi h sapwood lesion leng h he mos accu a e. By also
e alua ing mo ali y, which was acili a ed by he high seedling
numbe s, we unco e ed subs an ial wi hin-s ain disco dance
be ween he lesion indices and mo ali y coun s. Fo example,
he mo ali y coun was g ea e unde he 2100 clima e scena io
han ambien condi ions o seedlings in ec ed wi h ungi F5,
bu none o he lesion indices di e ed be ween he wo clima e
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Linnakoski e al. Fungus-T ee Pa hosys em and Clima e Change
scena ios. These esul s hus indica e a need o cau ion when
ex apola ing lesion indices as mo e gene al ou comes o plan
heal h. F om a p ac ical poin o iew, mo ali y occu ed in 25%
o seedlings inocula ed wi h ungal s ain F5 (compa ed o 0%
wi hou ungal in ec ion). Twen y- i e pe cen age o s and loss
alone will ha e se e e economic implica ions, and we ound ha
mo ali y le els app oached 50% unde he 2100 clima e scena io
(Figu e 2B).
P e ious esea ch showing he inabili y o No way sp uce o
espond o en i onmen al changes (Sallas e al., 2003;Kellomäki
e al., 2008;Lé esque e al., 2013;K one and Way, 2016) sugges s
ha seedling esis ance ( a he han ungal agg essi eness)
p ima ily media e he obse ed e ec s o clima e scena ios on
seedling heal h. Howe e , his hypo hesis calls o u u e a ge ed
esea ch add essing indices o plan immuni y. Al hough coni e s
ha e highly e ol ed de ense mechanisms agains he bi o es
and pa hogens (K okene e al., 2013), se e al clima e change
ac o s a e likely o con ibu e o plan s ess and he eby
impai hei de enses (Julkunen-Tii o e al., 2015). P e ious
s udies ha e in es iga ed he po en ial impac o ele a ed
empe a u e and CO2le els on he ca bon based (phenolics and
e penoids) de ense chemis y o No way sp uce (Sallas e al.,
2003;Julkunen-Tii o e al., 2015), indica ing ha clima ic ac o s
a e likely o induce changes in he phenolic and mono e pene
concen a ions.
No way sp uce geno ypes (clones) a y in hei esis ance o
ungal in ec ions (Swedjema k and S enlid, 1997;Ke iö e al.,
2015;Lundén e al., 2015). Ou b ed seedlings we e used o he
p esen s udy, ep esen ing he na u al gene ic di e si y ha is
cu en ly employed in bo eal o es y p ac ices. Monocul u es
o esis an clones would p o ide a possible solu ion o comba
speci ic in ec ion isk. Howe e , he subsequen lack o gene ic
di e si y would also in oduce o he isks o ee heal h,
speci ically he abili y o espond o unan icipa ed en i onmen al
pe u ba ions such as d ough s and o he in ec ions (Wing ield
e al., 2015).
Fo es y is a majo economic indus y in no he n Eu ope.
Much esea ch has add essed he e ec s o p ojec ed clima e
changes on ee species dis ibu ions and hei p oduc i i y
(Kellomäki e al., 2008;Lé esque e al., 2013), while he po en ial
impac s o pes s and pa hogens ha e ecei ed a less a en ion.
Ou esul s highligh he need o inco po a e disease e ec s in o
u u e o es y planning. They sugges ha p edic ed clima e
changes ha e he po en ial o al e he damage caused o No way
sp uce by he ungus E. polonica, bu ha such e ec s can
a y ma kedly among ungal s ains. Howe e , we acknowledge
he mul i ace ed e ec s o clima e change on plan -pa hogen
in e ac ions. Fac o s such as ola ile o ganic compounds (VOCs),
gaseous emissions and adia ion may ha e impo an in luences
(Niineme s e al., 2013), and we encou age u he empi ical
esea ch on his opic.
AUTHOR CONTRIBUTIONS
RL, MW, PP, and FA designed he expe imen . RL collec ed he
da a. KF con ibu ed o pa s o he da a collec ion and conduc ed
he s a is ical analyses. MW, PP, and FA con ibu ed eagen s,
ma e ials and analysis ools. RL and KF d a ed he manusc ip ;
MW, PP, and FA we e in ol ed in he esul s in e p e a ion
and inaliza ion o he manusc ip . All au ho s lis ed ha e made
subs an ial, di ec and in ellec ual con ibu ion o he wo k, and
app o ed i o publica ion.
FUNDING
This s udy was inancially suppo ed by he Uni e si y o Helsinki
(RL), he T ee P o ec ion Co-ope a i e P og amme (TPCP) and
he THRIP ini ia i e o he Depa men o T ade and Indus y
(RL, MW), Sou h A ica. KF is inancially suppo ed by he
Finnish Cul u al Founda ion.
ACKNOWLEDGMENT
We hank he echnical s a a he Haapas ensy jä ield s a ion o
he Na u al Resou ces Ins i u e Finland (Luke) o hei assis ance
in main aining he seedlings.
SUPPLEMENTARY MATERIAL
The Supplemen a y Ma e ial o his a icle can be ound online
a : h p://jou nal. on ie sin.o g/a icle/10.3389/ pls.2017.00883/
ull#supplemen a y-ma e ial
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