Re iew
Global Geog aphic Dis ibu ion and Hos Range o
Fusa ium ci cina um, he Causal Agen o Pine
Pi ch Canke
Rein D enkhan 1,*, Beccy Ganley 2, Jo ge Ma ín-Ga cía3,4 , Pe Vahalík5, Kale Adamson 1,
Ka a ína Adamˇcíko á6, Rod igo Ahumada 7, Lio Blank 8, Helena B agança 9,
Paolo Cap e i 10, Michelle Clea y 11 , Ca olina Co nejo 12, Ka e yna Da ydenko 13,14,
Julio J. Diez 3,4 , Ha ice Tu˘gba Do˘gmu¸s Leh ijä i 15, Miloˇn D oˇ ák5, Rasmus Ende le 16 ,
Ge da Fou ie 17, Ma ga i a Geo gie a 18, Luisa Ghela dini 10 , Ja kko Han ula 19,
Renaud Ioos 20 , Eugenia I u i xa 21, Loukas Kane is 22 , Na alia N. Ka pun 23,
And ás Kol ay 24 , Elena Lande as 25, S e lana Ma ko skaja 26, Nebai Mesanza 21,
I an Milenko i´c 27,28 , Dmi y L. Musolin 29 , Kons an inos Nikolaou 30,
Jus yna A. Nowakowska 31 , Nikica Og is 32 , Funda Oskay 33 , Tomasz Oszako 34 ,
I ena Papazo a-Anakie a 35, Ma ius Pa aschi 36, Ma ias Pasquali 37 , F ancesco Peco i 38,
T ond Ra oss 39, K is ina Rai elai y ˙
e26, Rosa Raposo 4,40, Cecile Robin 41 , Ca los A. Rodas 42,
Albe o San ini 38, An onio V. Sanz-Ros 4,43 , And ey V. Selikho kin 29,44, Alejand o Solla 45 ,
Mi kka Soukainen 46, Nikole a Soulio i 47, Emma T. S eenkamp 17, Panaghio is Tsopelas 47,
Aleksanda Vemi´c 27, Anna Ma ia Ve aino 48 , Michael J. Wing ield 17 , S ephen Woodwa d 49,
C is ina Zamo a-Balles e os 50 and Ma in S. Mulle 28,51
1Ins i u e o Fo es y and Ru al Enginee ing, Es onian Uni e si y o Li e Sciences, F . R. K eu zwaldi 5,
51006 Ta u, Es onia; kale [email p o ec ed]
2The New Zealand Ins i u e o Plan and Food Resea ch Limi ed, 412 No.1 Road RD2,
3182 Te Puke, New Zealand; Beccy[email p o ec ed]
3Depa men o Plan P oduc ion and Fo es Resou ces, Uni e si y o Valladolid, A enida de Mad id 44,
34071 Palencia, Spain; [email p o ec ed] (J.M.-G.); jdcase [email p o ec ed] (J.J.D.)
4
Sus ainable Fo es Managemen Resea ch Ins i u e, Uni e si y o Valladolid – INIA, A enida de Mad id 44,
34071 Palencia, Spain; [email p o ec ed] (R.R.); [email p o ec ed] (A.V.S.-R.)
5Facul y o Fo es y and Wood Technology, Mendel Uni e si y in B no, Zemˇedˇelská3,
61300 B no, Czech Republic; pe [email p o ec ed] (P.V.); [email p o ec ed] (M.D.)
6Depa men o Plan Pa hology and Mycology, Ins i u e o Fo es Ecology, Slo ak Academy o Sciences,
Akademická2, 949 01 Ni a, Slo akia; [email p o ec ed]
7Bio o es S.A., Km. 15 S/N, Camino a Co onel, 403 0000 Concepcion, Chile; [email p o ec ed]
8Depa men o Plan Pa hology and Weed Resea ch, Ag icul u al Resea ch O ganiza ion, Volcani Cen e ,
HaMaccabim Rd 68, 7528809 Rishon LeZion, Is ael; [email p o ec ed].il
9Ins i u o Nacional de In es igação Ag á ia e Ve e iná ia, I.P. (INIAV, I.P.) & GREEN-IT Bio esou ces o
Sus ainabili y, ITQB NOVA. A da República, Quin a do Ma quês, 2780-159 Oei as, Po ugal;
helena.b aganca@inia .p
10 Depa men o Ag icul u e, Food, En i onmen and Fo es y, Uni e si àdegli S udi di Fi enze,
Piazzale delle Cascine, 18, 50144 Fi enze, I aly; paolo.cap [email p o ec ed] (P.C.); [email p o ec ed] (L.G.)
11 Sou he n Swedish Fo es Resea ch Cen e, Swedish Uni e si y o Ag icul u al Sciences, Sunds ägen 3,
23053 Alna p, Sweden; [email p o ec ed]
12 WSL Swiss Fede al Resea ch Ins i u e, Zü che s asse 111, 8903 Bi mensdo , Swi ze land;
[email p o ec ed]
13 Depa men o Fo es P o ec ion, G. M. Vyso skiy Uk ainian Resea ch Ins i u e o Fo es y and Fo es
Melio a ion, 61024 Kha ki , Uk aine; [email p o ec ed]
14 Depa men o Fo es Mycology and Plan Pa hology, Swedish Uni e si y o Ag icul u al Sciences, 75007
Uppsala, Sweden
15 Facul y o Fo es y, Ispa a Uni e si y o Applied Sciences, 32260 Ispa a, Tu key;
[email p o ec ed]
Fo es s 2020,11, 724; doi:10.3390/ 11070724 www.mdpi.com/jou nal/ o es s
Fo es s 2020,11, 724 2 o 40
16
Ins i u e o Plan P o ec ion in Ho icul u e and Fo es s, Fede al Resea ch Cen e o Cul i a ed Plan s (JKI),
Messeweg 11/12, 38104 B aunschweig, Ge many; [email p o ec ed]
17 Depa men o Biochemis y, Gene ics and Mic obiology, Fo es y and Ag icul u al Bio echnology
Ins i u e (FABI), Uni e si y o P e o ia, Lynwoond and Uni e si y Roads, 0028 P e o ia, Sou h A ica;
[email p o ec ed] (G.F.); [email p o ec ed] (E.T.S.);
[email p o ec ed] (M.J.W.)
18 Depa men o Fo es En omology, Phy opa hology and Game auna, Fo es Resea ch Ins i u e, Bulga ian
Academy o Sciences, 132 S . Klimen Oh idski Bl d, 1756 So ia, Bulga ia; ma ga i ageo [email p o ec ed]
19 Depa men o Na u al Resou ces, Na u al Resou ces Ins i u e Finland (Luke), La oka anonkaa i 9,
00790 Helsinki, Finland; [email p o ec ed]
20 ANSES Plan Heal h Labo a o y, Uni o Mycology, Domaine de Pixé écou , Bâ . E.,
54220 Malzé ille, F ance; [email p o ec ed]
21 Fo es y Science Depa men , Neike Ins i u e, Campus Ag oalimen a io de A kau e, S/N 01080 A kau e,
Ála a, Spain; ei u i xa@neike .eus (E.I.); nmesanza@neike .eus (N.M.)
22 Depa men o Ag icul u al Sciences, Bio echnology & Food Science, Cyp us Uni e si y o Technology,
A ch. Kyp ianos S . 30, 3603 Limassol, Cyp us; [email p o ec ed]
23 Russian Resea ch Ins i u e o Flo icul u e and Sub opical C ops, J¯
anis Fab iciuss s ., 2/28,
354002 Sochi, Russia; [email p o ec ed]
24
Fo es P o ec ion Depa men , NARIC Fo es Resea ch Ins i u e, Hegyalja u. 18, 3232 M
á
a ü ed, Hunga y;
[email p o ec ed]
25 Labo a o io de Sanidad Vege al, Gobie no del P incipado de As u ias, C/Lucas Rod íguez Pi e, 4-bajo,
33011 O iedo, Spain; [email p o ec ed]g
26 Ins i u e o Bo any, Na u e Resea ch Cen e, Žaliu˛ju˛ eže u˛ 49, 08412 Vilnius, Li huania;
[email p o ec ed] (S.M.); [email p o ec ed] (K.R.)
27 Depa men o Fo es P o ec ion, Facul y o Fo es y, Uni e si y o Belg ade, Kneza Višesla a 1,
11030 Belg ade, Se bia; [email p o ec ed] (I.M.); aleksanda [email p o ec ed] (A.V.)
28 Phy oph ho a Resea ch Cen e, Mendel Uni e si y in B no, Zemˇedˇelská3, 61300 B no, Czech Republic;
[email p o ec ed] o [email p o ec ed]
29 Depa men o Fo es P o ec ion, Wood Science and Game Managemen , Sain Pe e sbu g S a e Fo es
Technical Uni e si y, Ins i u skiy pe ., 5, 194021 Sain Pe e sbu g, Russia; [email p o ec ed] (D.L.M.);
[email p o ec ed] (A.V.S.)
30 Depa men o Fo es s, Minis y o Ag icul u e, Ru al De elopmen and En i onmen , Loukis Ak i as 26,
1414 Nicosia, Cyp us; [email p o ec ed].cy
31
Ins i u e o Biological Sciences, Facul y o Biology and En i onmen al Sciences, Ca dinal S e an Wyszynski
Uni e si y in Wa saw, Wóycickiego 1/3 S ee , 01-938 Wa saw, Poland; [email protected]
32 Depa men o Fo es P o ec ion, Slo enian Fo es y Ins i u e, Veˇcna po 2, 1000 Ljubljana, Slo enia;
[email p o ec ed]
33 Facul y o Fo es y, Çankı ı Ka a ekin Uni e si y, 18200 Çankı ı, Tu key; [email p o ec ed]
34 Depa men o Fo es P o ec ion, Fo es Resea ch Ins i u e in S˛ekocin S a y, B aci Le´snej 3,
05-090 Raszyn, Poland; [email p o ec ed].pl
35 Facul y o Fo es y, Ss. Cy il and Me hodius Uni e si y in Skopje, 16 Makedonska b igada b .1,
1000 Skopje, Republic o No h Macedonia; [email p o ec ed]
36 Depa men o Fo es P o ec ion, Na ional Ins i u e o Resea ch and De elopmen in Fo es y – B as
,o
S a ion, Clos
,ca 13, 500040 B as
,o , Romania; [email p o ec ed]
37 Depa men o Food, En i onmen al and Nu i ional Sciences, Uni e si y o Milan, Via Celo ia 2,
20133 Milano, I aly; [email p o ec ed]
38
Ins i u e o Sus ainable Plan P o ec ion – C.N.R., Via Madonna del Piano, 10, 50019 Ses o Fio en ino, I aly;
[email p o ec ed].i (F.P.); albe o.san ini@cn .i (A.S.)
39
Bio echnology and Plan Heal h Di ision, No wegian Ins i u e o Bioeconomy Resea ch, 1431 Ås, No way;
[email p o ec ed]
40 Cen e o Fo es Resea ch, Na ional Ins i u e o Ag icul u al and Food Resea ch and Technology (INIA),
C. Co una, 28040 Mad id, Spain
41 INRAE, Uni . Bo deaux, BIOGECO, F-33610 Ces as, F ance; cecile. [email p o ec ed]
42
Fo es Heal h P o ec ion P og amme, Smu i Kappa Colombia – Uni e si y o P e o ia, Calle 15 N
◦
18 -109.
Yumbo – Valle Colombia, 760502 Cali, Colombia; Ca los. [email p o ec ed]
Fo es s 2020,11, 724 3 o 40
43 Plan Pa hology Labo a o y, Calabazanos Fo es Heal h Cen e (Regional Go e nmen o Cas illa y León),
Polígono Indus ial de Villamu iel S/N, Villamu iel de Ce a o, 34190 Palencia, Spain
44 Depa men o Biogeog aphy and En i onmen al P o ec ion, Sain Pe e sbu g S a e Uni e si y,
Uni e si e skaya emb., 13B, 199034 Sain Pe e sbu g, Russia
45 Facul y o Fo es y, Uni e si y o Ex emadu a, A enida Vi gen del Pue o 2, 10600 Plasencia, Spain;
[email p o ec ed]
46 Labo a o y and Resea ch Di ision, Plan Analy ics Uni , Finnish Food Au ho i y, Mus ialanka u 3,
00790 Helsinki, Finland; [email p o ec ed]
47 Ins i u e o Medi e anean Fo es Ecosys ems, Te ma Alkmanos, 11528 A hens, G eece;
[email p o ec ed] (N.S.); [email p o ec ed] (P.T.)
48 Depa men o Inno a ion in Biological, Ag o- ood and Fo es Sys ems (DIBAF), Uni e si y o Tuscia,
Via S. Camillo de Lellis, 01100 Vi e bo, I aly; [email p o ec ed]
49 School o Biological Sciences, Uni e si y o Abe deen, C uickshank Building, S . Macha D i e,
Abe deen AB24 3UU, UK; s.woodwa [email p o ec ed]
50
Depa men o Vege al P oduc ion and Fo es y Resou ces, College o Ag icul u al and Fo es y Enginee ing,
Uni e si y o Valladolid, A Mad id 44, 34004 Palencia, Spain; c is inazamo aballes e [email p o ec ed]
51 Fo es Resea ch Fo es Resea ch, Alice Hol Lodge, Su ey, Fa nham GU10 4LH, UK
*Co espondence: [email p o ec ed]
Recei ed: 27 May 2020; Accep ed: 25 June 2020; Published: 1 July 2020


Abs ac :
Fusa ium ci cina um, he causal agen o pine pi ch canke (PPC), is cu en ly one o he
mos impo an h ea s o Pinus spp. globally. This pa hogen is known in many pine-g owing egions,
including na u al and plan ed o es s, and can a ec all li e s ages o ees, om eme ging seedlings
o ma u e ees. Despi e he impo ance o PPC, he global dis ibu ion o F. ci cina um is poo ly
documen ed, and his p oblem is also ue o he hos s wi hin coun ies ha a e a ec ed. The aim o
his s udy was o e iew he global dis ibu ion o F. ci cina um, wi h a pa icula ocus on Eu ope.
We conside ed (1) he cu en and his o ical pa hogen eco ds, bo h posi i e and nega i e, based
on con i med epo s om Eu ope and globally; (2) he gene ic di e si y and popula ion s uc u e
o he pa hogen; (3) he cu en dis ibu ion o PPC in Eu ope, compa ing published models o
p edic ed disease dis ibu ion; and (4) hos suscep ibili y by e iewing li e a u e and gene a ing a
comp ehensi e lis o known hos s o he ungus. These da a we e colla ed om 41 coun ies and
used o compile a specially cons uc ed geo-da abase. A e iew o 6297 obse a ion eco ds showed
ha F. ci cina um and he symp oms i causes on coni e s occu ed in 14 coun ies, including ou in
Eu ope, and is absen in 28 coun ies. Field obse a ions and expe imen al da a om 138 hos species
e ealed 106 suscep ible hos species including 85 Pinus species, 6 non-pine ee species and 15 g ass
and he b species. Ou da a con i m ha suscep ibili y o F. ci cina um a ies be ween di e en hos
species, ee ages and en i onmen al cha ac e is ics. Knowledge on he geog aphic dis ibu ion,
hos ange and he ela i e suscep ibili y o di e en hos s is essen ial o disease managemen ,
mi iga ion and con ainmen s a egies. The indings epo ed in his e iew will suppo coun ies
ha a e cu en ly ee o F. ci cina um in implemen ing e ec i e p ocedu es and es ic ions and
p e en u he sp ead o he pa hogen.
Keywo ds: in asi e pa hogen; clima e change; in e ac i e map o pa hogen; suscep ibili y
1. In oduc ion
Fusa ium ci cina um ( eleomo ph Gibbe ella ci cina a Ni enbe g and O’Donnell [
1
]) is an in asi e
pa hogen ha causes a disease known as pine pi ch canke (PPC). This ungus is a qua an ine o ganism,
included in he EPPO (Eu opean and Medi e anean Plan P o ec ion O ganiza ion) A2 lis and
egula ed in he EU (Eu opean Union) [
2
]. In nu se ies and he wide en i onmen , he pa hogen
Fo es s 2020,11, 724 4 o 40
a ec s pines (Pinus spp.) and Douglas- i (Pseudo suga menziesii) [
3
,
4
]. I has also been isola ed om
asymp oma ic plan s (Poaceae, As e aceae, Lamiaceae, Rosaceae) g owing close o PPC-a ec ed ees
in pine s ands [
5
–
7
]. Addi ionally, a i icial inocula ion ials ha e shown he po en ial o F. ci cina um
o in ec a wide ange o plan gene a, e.g., Abies,La ix,Liboced us,Picea [
3
,
8
–
10
], al hough na u al
in ec ions o species in hese axa ha e no been epo ed.
Fusa ium ci cina um can a ec all s ages o pine de elopmen . Being seed-bo ne [
11
], i can cause
seed and seedling mo ali y (p e- and pos -eme gence damping-o , espec i ely), and ligni ied seedling
decay (la e damping-o ) [
12
]. The pa hogen also causes dieback o b anches and s ems on young and
ma u e ees whe e he main symp oms a e copious esin (‘pi ch’) p oduc ion om canke s, hence he
common name “pine pi ch canke disease” [
13
–
15
]. In ec ion is usually ia wounds h ough which
spo es gain en y in o he plan issue [
16
,
17
]. Howe e , wounds a e no always necessa y o in ec ion
al hough hey a e o disease de elopmen [
18
]. The dispe sal o he in ec i e p opagules occu s
ia agen s such as insec s, wa e , and wind [
19
–
21
]. Howe e , he main a enues o long-dis ance
mo emen o he ungus a e associa ed wi h human ac i i ies, pa icula ly plan ade and mo emen
o con amina ed soil and equipmen [22,23].
Pine pi ch canke was i s desc ibed in he Sou heas USA (No h and Sou h Ca olina) in 1945 [
24
],
whe e ou b eaks ended o occu in poo ly managed s ands o a e se e e d ough e en s [
17
].
Since hen, F. ci cina um has been eco ded in A ica, Asia, Sou h Ame ica, and Sou he n Eu ope,
al hough in o ma ion conce ning i s dis ibu ion in hese egions is o en no easily accessible o
uni o mly p esen ed [
25
–
27
]. Howe e , he pa hogen is now known om mos pine g owing egions,
gene ally wi h high incidence in Medi e anean and sub- opical clima es and some sp ead in o
empe a e egions [
28
]. Because i s sp ead and es ablishmen is s ongly dependen on clima ic
condi ions, p ima ily empe a u e and humidi y [
4
,
28
,
29
], F. ci cina um is unlikely o sp ead o coole ,
no he n la i udes despi e he p esence o suscep ible hos s in hese a eas [
29
,
30
]. Ne e heless,
global ade has exace ba ed he sp ead o many o es pa hogens, and his end seems se o
con inue [
31
,
32
]. In oduc ion o he pa hogen ia an h opogenic ac i i ies in o nu se ies o a eas
wi h sui able mic oclima es could lead o disease sp ead in o wha ha e hi he o been hough o as
gene ally less sui able a eas.
The Eu opean COST Ac ion FP1406 “Pine pi ch canke —s a egies o managemen o Gibbe ella
ci cina a in g eenhouses and o es s (PINESTRENGTH)” b ough oge he scien is s and s akeholde s
om 36 coun ies o es ablish a Eu opean- ocused ne wo k dedica ed o inc easing ou unde s anding
o F. ci cina um and i s e ec s on pine. The main objec i es we e o inc ease knowledge on he
biology, ecology, and sp ead pa hways o F. ci cina um; o e alua e he po en ial o de elop e ec i e
and en i onmen ally iendly p e en ion and mi iga ion s a egies and o deli e hese ou comes o
s akeholde s and policy make s. In his ega d, upda ed in o ma ion on he geog aphic dis ibu ion and
hos ange o he pa hogen, as well as on he ela i e suscep ibili y o di e en hos s, we e conside ed.
These ac o s ep esen impo an elemen s o disease managemen , mi iga ion and con ainmen
s a egies. This would po en ially also allow coun ies cu en ly ee o he pa hogen o implemen
e ec i e p ocedu es and es ic ions o p e en i s in oduc ion.
In his e iew, we conside ed he global dis ibu ion o F. ci cina um, wi h a pa icula ocus
on Eu ope. Mo e speci ically he objec i es we e o (1) de e mine p esen ly a ailable and his o ical
pa hogen eco ds, based on he con i med epo s om Eu ope and globally, (2) e iew he global
popula ions and gene ic di e si y o he pa hogen, (3) compa e he cu en dis ibu ion o PPC in
Eu ope wi h published models o p edic ed disease dis ibu ion; and (4) p o ide a comp ehensi e and
up o da e lis o suscep ible hos s.
2. The Geog aphic Dis ibu ion o F. ci cina um
The occu ence o F. ci cina um is well known o some coun ies, while in o ma ion ega ding
i s dis ibu ion globally o wi hin many coun ies is sca e ed o poo ly documen ed, and in some
cases eco ds a e e oneous. To p esen he cu en dis ibu ion o F. ci cina um, a geo-da abase o he
Fo es s 2020,11, 724 5 o 40
pa hogen was de eloped and used o gene a e an in e ac i e map (see Supplemen a y Ma e ials and
in e ac i e map: h p://bi .do/phy opo al).
The geo-da abase con ains geog aphic coo dina es o 6297 sampling o obse a ion eco ds om
106 di e en hos s in 41 coun ies (including s a es): A ica (1 coun y), No h and Sou h Ame ica
(7 coun ies),
Asia (5 coun ies, including he Asian pa o he Russian Fede a ion and he Asian
pa o Tu key), Eu ope (28 coun ies including he Eu opean pa o he Russian Fede a ion and he
Eu opean pa o Tu key), and Oceania (2 coun ies). The in e ac i e map shows he p esence and i s
epo s o F. ci cina um in 14 coun ies, including ou in Eu ope (Figu e 1; Table 1).
In 12 coun ies (B azil, Chile, Colombia, F ance, I aly, Japan, Mexico, Po ugal, Spain, Sou h A ica,
U uguay, and USA[no alls a es]), hep esence o F. ci cina um was con i medusingmolecula me hods,
and in wo coun ies (Sou h Ko ea and Hai i) he p esence o he pa hogen was e i ied using classical
mo phological app oaches (e.g., ege a i e and ep oduc i e ai s). In F ance and I aly, F. ci cina um
has been ound in nu se ies and a public ga dens, and in bo h o hese Eu opean coun ies he pa hogen
is conside ed o icially e adica ed [
27
] (Figu e 2; Table 1). PPC was conside ed absen in 28 coun ies
(24 Eu opean coun ies, Aus alia, New Zealand, Tu key and Is ael) a e igo ous ield obse a ions
and/o labo a o y es ing (see h p://bi .do/phy opo al). Coun ies o which no da a on p esence o
absence we e a ailable we e no conside ed o be posi i e o nega i e. The da a we e ob ained as
desc ibed in he ins uc ions o he geo-da abase o F. ci cina um dis ibu ion (see Supplemen a y
Ma e ials, Table S1). A summa y o pa hogen dis ibu ion by con inen is p esen ed below.
2.1. Eu ope
In Eu ope, F. ci cina um has been epo ed in ou coun ies: Spain [
33
,
34
], I aly [
35
], F ance [
36
],
and Po ugal [
37
]. The i s eco d o F. ci cina um in Eu ope was in 1995 on nu se y seedlings o
P. adia a and P. halepensis in Galicia, no he n Spain [
33
]. In 1997, he pa hogen was e iden ly ound
in a nu se y in he Basque Coun y, no he n Spain, causing mo ali y o P. adia a seedlings [
38
–
40
],
bu F. ci cian um
p esence was o mally iden i ied in 2004 [
34
]. The disease eappea ed in no he n
Spain, in As u ias, some yea s la e (2003–2004) on nu se y seedlings o P. adia a and P. pinas e [
34
].
In 2004, he pa hogen was epo ed o he i s ime in he o es en i onmen , whe e i caused PPC o
P. adia a in a 20-yea -old o es plan a ion in Can ab ia, no he n Spain [
34
]. Thus, F. ci cina um has
been p esen o o e 20 yea s in Spanish nu se ies and o e 10 yea s in o es s.
In 2006, an e adica ion and con ol p og amme was launched o limi i s sp ead in Spain, and in
2007 he EU adop ed measu es o p e en i s sp ead o o he membe s a es [
2
]. Measu es unde aken
included he elimina ion o in ec ed ma e ial and he es ablishmen o an in ensi e and con inuous
moni o ing p og amme in o es s and o plan ep oduc i e ma e ial om bo h public and p i a e
en i ies. In Cas illa y Le
ó
n, F. ci cina um was ound om 2005 o 2013, bo h in nu se ies and o es s ands,
bu he e ha e been no subsequen epo s o he ungus in ha egion (Fo es Heal h Se ice, di ec
communica ion). Howe e , he pa hogen emains ac i e in se e al coas al a eas despi e e adica ion
a emp s. I F. ci cina um canno be e adica ed om hese egions, i is likely ha new in ec ions will
occu and he pa hogen will con inue o sp ead o inland a eas [41].
In Po ugal, F. ci cina um was i s de ec ed in 2007 om in ec ed seedlings o P. adia a and
P. pinas e in a nu se y loca ed in he cen e o he coun y [
37
]. As a consequence o his i s epo ,
ollowing EU and na ional ules, an ac ion plan was implemen ed by he Fo es Au ho i y o es ablish
ex ao dina y phy osani a y measu es, aiming o e adica e and/o con ol he disease. In bo h Po ugal
and Spain, a e each de ec ion o F. ci cina um, an in es ed zone and a bu e zone (a leas 1 km
wide) we e es ablished a ound he in es ed si e. In Po ugal, he su ey and p og amme esul s
(Figu e 1,h p://bi .do/phy opo al) showed ha un il 2016 all posi i e epo s o F. ci cina um we e
ob ained exclusi ely om nu se ies. In 2016, he ungus was also de ec ed o he i s ime in a
plan a ion o P. adia a in Minho p o ince [
42
] and in he same p o ince on wo P. pinas e ees in
2018 [
42
]. In bo h cases, Pinus plan s in nu se ies and in o es s we e des oyed and he su ounding
a ea in ensi ely su eyed wi h no u he posi i e indings o da e [
27
]. Al hough he lack o new

Fo es s 2020,11, 724 6 o 40
posi i e eco ds sugges s ha he pa hogen has been success ully elimina ed, i is p ema u e o decla e
o icial e adica ion in he whole coun y.
In I aly and F ance, F. ci cina um appea s o ha e been e adica ed success ully. Pine pi ch canke
was epo ed in I aly in 2005 on o namen al plan ings (Foggia, sou he n I aly) o he na i e species
P. pinea and P. halepensis [
35
]. In ec ed plan s we e p omp ly emo ed and des oyed, and no new
eco ds o he disease ha e subsequen ly been epo ed in ga dens, nu se ies o he wide en i onmen .
In F ance, F. ci cina um was eco ded o he i s ime in 2005 in a p i a e ga den (Pe pignany,
Sou h F ance) on a declining Douglas- i ee and a ew declining pine ees [
36
] and was conside ed
o icially e adica ed in 2008 a e in ensi e moni o ing [
43
,
44
]. In 2009, he ungus was ound on
P. adia a seedlings in wo F ench nu se ies: all in ec ed plan s and plan s om he same nu se y beds
we e emo ed and des oyed [
45
]. A e wo yea s o in ensi e su ey in and a ound he nu se ies,
he pa hogen was conside ed e adica ed [27].
The cu en s udy ga he ed 6297 obse a ions om 28 Eu opean coun ies (h p://bi .do/
phy opo al). In 24 o he 28 moni o ed Eu opean coun ies, he e was no e idence o F. ci cina um
p esence (i.e., all su eys and samples we e nega i e) (Figu es 1and 2). Bo h mo phological and
molecula me hods (species-speci ic PCR [
46
] o sequencing) o F. ci cina um de ec ion we e used o
de e mine p esence o absence in 18 coun ies. In nine coun ies, only isual inspec ion o symp oms in
he ield o mo phological diagnosis o cul u es in he labo a o y was used o con i m pa hogen absence
o p esence. Howe e , isual inspec ion alone may no be su icien ly eliable o F. ci cina um de ec ion
and iden i ica ion because he ungus may beha e as an endophy e o la en pa hogen wi h no isible
ex e nal symp oms o i can be mis aken o o he pa hogens ha cause simila symp oms [
7
,
47
,
48
].
I is p e e able, he e o e, o combine isual su eys wi h molecula de ec ion me hods o eliable
and mo e p ecise iden i ica ion [
46
,
49
,
50
]. In he cu en s udy, bo h isual and molecula su eys
we e conside ed.
2.2. No h Ame ica and Sou h Ame ica
Fusa ium ci cina um was i s eco ded on pines in sou heas e n No h Ame ica in 1945 [
24
].
The pa hogen was desc ibed om Pinus i giniana in No h and Sou h Ca olina [
24
]. Pine pi ch canke
has subsequen ly been epo ed om o he s a es including Alabama, A kansas, Cali o nia, Flo ida,
Geo gia, Indiana, Louisiana, Mississippi, Tennessee, Texas, and Vi ginia [
26
,
29
] (see Figu es 1and 2,
Table 1). In Mexico, F. ci cina um was eco ded o he i s ime in 1989 on plan ed P. halepensis and
na u al s ands o P. douglasiana and P. leiophylla [
39
]. Consis en wi h he idea ha F. ci cina um is
na i e o Mexico [
51
,
52
], he pa hogen is widesp ead in his coun y wi h eco ds om a leas nine
s a es (Sinaloa, Naya i , Mexico, Nue o Leon, Puebla, Michoacan, Jalisco, Du ango, and Tamaulipas).
The e we e no published eco ds o he pa hogen in Canada (Tod Rams ield, pe sonal comm.) o in
he USA s a es o Massachuse s and Washing on [27].
The i s epo o PPC in Hai i was in 1953 [
53
], al hough he ea e no new in o ma ion is a ailable
abou he disease in ha coun y. The i s epo o F. ci cina um in Sou h Ame ica was in P. adia a
mo he plan s (hedges) in nu se ies o Chile in 2001 [
54
]. Since hen, he pa hogen has been ound in
U uguay, Colombia, and B azil [
55
–
58
]. In Chile, U uguay, and B azil, he pa hogen has been epo ed
only in nu se ies and i has appa en ly no sp ead o he o es en i onmen . Con e sely, in Colombia,
F. ci cina um was i s de ec ed in 2005, a ec ing seedlings o P. pa ula,P. maximinoi,
and P. ecunumanii
in nu se y, bu was la e also ound in isola ed ees on plan a ions [
56
,
57
]. Mo e ecen ly in 2017, he
pa hogen was epo ed and iden i ied as F. ci cina um causing damages in P. pa ula and high ele a ion
plan a ions o P. ecunumanii (Ca los Rodas, unpublished).
2.3. Asia
In Asia, F. ci cina um is known o be p esen only in Japan and Sou h Ko ea [
59
,
60
]. The e a e no
eco ds o he pa hogen in he Russian Fa Eas , no in wes e n Asia (e.g., Is ael and Tu key, including
he Eu opean pa o Tu key) (see Figu es 1and 2, Table 1). In Japan, PPC was i s eco ded in 1981
Fo es s 2020,11, 724 7 o 40
on na i e P. luchensis ees on Amami
¯
Oshima and Okinawa Islands [
60
]. In Sou h Ko ea, PPC was
epo ed om na u al s ands and plan a ions o P. igida in he mid-1990s whe e i caused ee mo ali y
in Seoul and Kangwon P o inces [59].
2.4. A ica
In A ica, F. ci cina um has been epo ed only om Sou h A ica, whe e i was documen ed o he
i s ime in 1991 [
12
]. The pa hogen was esponsible o an ou b eak o oo and oo colla disease on
P. pa ula seedlings in a single nu se y, and has subsequen ly sp ead o mos pine seedling p oduc ion
nu se ies in he coun y [
4
]. Acco dingly, a ious managemen s a egies ha e been in es iga ed and
de eloped o limi he occu ence and sp ead o F. ci cina um in comme cial o es y, e.g., nu se y
hygiene p ac ices o limi he build-up o inoculum [
61
–
63
] and he use o chemical and biologically
de i ed compounds o boos plan de ence esponses [
64
]. Howe e , F. ci cina um emains a majo
challenge o seedling p oduc ion and plan a ion es ablishmen in Sou h A ica [65,66].
In 2005, PPC was de ec ed o he i s ime ou side he nu se y en i onmen on es ablished
ees in a plan a ion o P. adia a and i is now commonly ound on his species in he Wes e n
Cape P o ince in Sou h A ica [
67
,
68
]. The pa hogen has since been de ec ed also in plan a ions o
P. g eggii in he Eas e n Cape and KwaZulu-Na al P o inces whe e localized ou b eaks o PPC ha e
occu ed [
66
,
68
,
69
]. Addi ionally, in he summe ain all a ea o he coun y, localised ou b eaks o
PPC ha e been eco ded in plan a ions o P. pa ula, which is he mos widely plan ed Pinus species in
Sou h A ica [
70
]; S eenkamp and Wing ield, unpublished]. To limi losses ela ed o PPC, conside able
e o has been dedica ed o de elop and deploy plan ing s ock ha is ole an o mo e esis an o
PPC. These include less suscep ible amilies o P. pa ula [
71
–
73
] and ce ain amilies o P. maximinoi,
P. pseudos obus, low-ele a ion P. ecunumanii, and P. ellio ii a . ellio ii [
65
,
74
]. Va ious hyb ids ha e
also been e alua ed, wi h low-ele a ion P. ecunumanii
×
pa ula,P. ellio ii
×
ca ibaea, and P. pa ula
×
ooca pa showing low le els o suscep ibili y o in ec ion by F. ci cina um [
75
,
76
], and many o hese
hyb ids ha e al eady been deployed comme cially.
2.5. Oceania
Fusa ium ci cina um has no been ound in Oceania. In bo h Aus alia and New Zealand,
su eillance p og ammes egula ly moni o pine and Douglas- i seedlings and ma u e ees o
unwan ed o ganisms including F. ci cina um. Suspec samples a e es ed using mo phological and
molecula me hods and, o da e, all samples es ed ha e p o en nega i e o F. ci cina um (see Figu es 1
and 2). Bo h coun ies ha e s ic bo de biosecu i y egula ions, and a leas one po en ial in oduc ion
o he pa hogen has been p e en ed. In his case, F. ci cina um was de ec ed in 2004 on scions o
Douglas- i om Cali o nia, and he p e-bo de de ec ion equi ed he in ec ed ma e ial o be des oyed
be o e i was impo ed in o New Zealand [77].
Fo es s 2020,11, 724 8 o 40
Figu e 1.
His o ical dispe sal o Fusa ium ci cina um acco ding o he da e he pa hogen was i s
eco ded in he coun y (see Table 1 o de ails). The da a a e based on li e a u e and moni o ing eco ds.
Figu e 2.
Global dis ibu ion o Fusa ium ci cina um showing whe e he pa hogen is p esen , e adica ed,
no ound o da a a e no a ailable. See he in e ac i e map: h p://bi .do/phy opo al o de ailed
loca ions wi hin coun ies.
Fo es s 2020,11, 724 9 o 40
Table 1.
Geog aphic dis ibu ion, by coun y, o Fusa ium ci cina um (FC) including he ype o plan ing, yea ound, hos species a ec ed, and he me hod used o
iden i y he pa hogen.
Con inen /
Coun y/S a e
Yea o Fi s Reco d
o FC in Nu se y
and/o Wide
En i onmen
Hos Species Type o Plan ing/Sampling Si e Iden i ica ion Me hod Re e ences
o Da a Holde
Eu ope
F ance 2005 1, 2 Pseudo suga menziesii, Pinus sp. U ban g eene y species-speci ic PCR, sequence analysis [37]
F ance 2008 2P. menziesii Nu se y species-speci ic PCR, sequence analysis [44]
I aly 2005 1, 2 P. halepensis, P. pinea U ban g eene y species-speci ic PCR [36]
Po ugal 2007 1, 2 Pinus adia a, P. pinas e Nu se y species-speci ic PCR, sequence analysis [38]
Po ugal 2016 2P. adia a Fo es plan a ion species-speci ic PCR, sequence analysis [42]
Spain 1995 1P. adia a, P. halepensis Nu se y, in Galicia isual obse a ion [34]
Spain 1997 P. adia a Nu se ies, in Basque Coun y mycelial mo phology [39]
Spain 2003 P. adia a, P. pinas e Nu se y, in As u ias species-speci ic PCR [35]
Spain 2004 P. adia a Plan a ion, in Can ab ia species-speci ic PCR [35]
Spain 2005 P. syl es is, P. nig a, P. pinas e , P. pinea Nu se ies in Cas illa y León mo phological ai s, species-speci ic PCR Regional Fo es
Heal h Se ice
Spain 2005 P. syl es is, P. nig a, P. pinea, P. adia a Fo es plan a ions, in Cas illa y León mo phological ai s, species-speci ic PCR Regional Fo es
Heal h Se ice
Asia
Japan 1981 1P. luchuensis Fo es , Amamioshima Island (Ryukyu
A chipelago) and he Okinawa island mycelial mo phology [60]
Sou h Ko ea 1995 1P. igida U ban g eene y, o es mycelial mo phology [59]
A ica
Sou h A ica 1991 1P. pa ula Nu se y, Ngodwana Mpumalanga P o ince mycelial mo phology [12]
Sou h A ica 2005 P. adia a Plan a ion, Tokai, Wes e n Cape P o ince species-speci ic PCR, sequence analysis [67]
Sou h A ica 2007 P. g eggii Plan a ion, Ugie, Eas e n Cape P o ince sequence analysis [68,69]
Sou h A ica 2014 P. pa ula
Plan a ion, Louis T icha d , Limpopo P o ince
sequence analysis [70]
No h Ame ica
Hai i 1953 1P. occiden alis Na u al o es mycelial mo phology [53]
Mexico 1989 1P. douglasiana, P. halepensis, P. leiophylla,
P. g eggii, P. pa ula Fo es plan a ion and na u al s and unknown, p obably isual obse a ion [40]
Fo es s 2020,11, 724 16 o 40
Figu e 4.
Eu opean clima ic sui abili y o Fusa ium ci cina um based on he CLIMEX model pa ame e s
o Ganley e al.[
28
]using highe esolu ionclima icda a[
133
]. TheEu opeandis ibu ion o non-nu se y
F. ci cina um indings is shown as ed do s in he main igu e, while he inse displays he da ase used
by Ganley e al. [28] in he o iginal CLIMEX modelling.
Table 2.
Minimum, a e age and maximum alues o clima ic and opog aphical a iables om he
da ase o Hijmans e al. [
134
] and new obse a ions o cu en dis ibu ion o Fusa ium ci cina um om
he geo-da abase p esen ed in he cu en s udy.
Minimum A e age Maximum
Al i ude −3 m a.s.l. 262 m a.s.l. 3619 m a.s.l.
Annual mean empe a u e 6.2 ◦C 13.7◦C 25.4 ◦C
Mean empe a u e o he wa mes mon h 12.4 ◦C 24.7 ◦C 36.5 ◦C
Mean empe a u e o he coldes mon h −14.2 ◦C 4.8 ◦C 16.7 ◦C
Annual p ecipi a ion sum 324 mm 1259 mm 3062 mm
P ecipi a ion sum o he we es mon h 51 mm 154 mm 583 mm
P ecipi a ion sum o he d ies mon h 0 mm 57 mm 151 mm
6. Hos Range
Knowledge o he hos ange o F. ci cina um has been g owing s eadily, and ecen ly epo s o
non-pine hos s ha e inc eased. Fo he pu pose o his e iew, all known hos s o F. ci cina um and
hei suscep ibili y a ings we e compiled and assessed (Tables 3–6). The hos lis and suscep ibili y
a ings we e based on esul s o bo h ield obse a ions and expe imen al inocula ions epo ed in
pee - e iewed and “g ey” li e a u e, as well as om unpublished s udies and he geo-da abase eco ds
compiled in his s udy. Such an ex ensi e and in eg a ed lis has no p e iously been published because
he in o ma ion is sca e ed h oughou nume ous sou ces. We summa ized hese esul s and included
da a o 138 hos s (including 18 Pinus hyb ids) es ed in g ow h chambe , g eenhouse, nu se y and
ield inocula ions o su ey da a om he wide en i onmen .
Taxa om which da a ha e been ga he ed include 96 species in he genus Pinus (including
Pinus hyb ids), 24 o he ee species in 15 gene a (Abies,Ced us,Chamaecypa is, xCup essocypa is,
Cup essus,Eucalyp us,La ix,Liboced us,Picea,Podoca pus,Pseudo suga,Sequoia,Sequoiadend on,Thuja,
and Widd ing onia) and 18 g ass and he b species (see Tables 3–6;h p://bi .do/phy opo al). In o al,

Fo es s 2020,11, 724 17 o 40
F. ci cina um has been epo ed o in ec 106 di e en plan species, including 67 Pinus species and 18
Pinus hyb ids (Tables 3–5), as well as 6 non-pine ee species and 15 g ass and he b species (Table 6).
O e all, le els o suscep ibili y a y wi h he plan ’s age class, om ecen ly eme ged seedlings o
ma u e ees. This a ia ion is p ima ily due o he di e en beha iou o , and ype o disease caused
by, F. ci cina um on plan s o di e en ages. In pine seedlings, o example, F. ci cina um essen ially
causes oo disease (mani es ed as p e- and pos -eme gence, as well as la e, damping-o ), which is
mainly seen in nu se y si ua ions, while he p edominan symp om o in ec ion in olde o es ablished
pine ees a e esinous canke s on he abo e-g ound plan pa s. Many species a ec ed as seedlings in
a nu se y si ua ion ha e no been seen o be a ec ed as ma u e ees in a o es si ua ion (Wing ield,
unpublished). Because he beha iou and disease cycle o F. ci cina um is likely o di e signi ican ly
in hese wo se ings, he suscep ibili y a ings o seedlings and young plan s (Table 3) we e ea ed
sepa a ely om hose o olde o ma u e ees (Table 4). Ne e heless, as nu se y p oduc ion is he
p ima y ou e o F. ci cina um ansmission o he wide en i onmen , a summa y o he suscep ibili y
a ings o bo h seedlings and ma u e ees is gi en below. This ea men allows o an assessmen o
he highes and lowes isk species ha may se e as ‘ca ie s’ o he pa hogen om he nu se y o he
o es and exhibi he disease in bo h se ings.
6.1. Hos Suscep ibili y Ra ings
In his wo k, hos suscep ibili y a ing was based on he ollowing ca ego ies: high, mode a e-high,
mode a e, low-mode a e, low, highly a iable, unknown, and esis an . A hos was conside ed esis an
i no F. ci cina um symp oms we e de ec ed a e inocula ion ials and na u al in ec ion wi h he
ungus does no occu . The highly a iable suscep ibili y ca ego y was assigned o he hos s (seedlings,
young plan s, young o ma u e ees) o which anking a ied in di e en s udies om esis an o
suscep ible. Mo eo e , we did no include in hese a ings endophy ic in ec ions, o asymp oma ic
plan s (plan s in ec ed bu seemingly heal hy), as he e is s ill e y limi ed in o ma ion abou his
pa icula li es yle ai o F. ci cina um.
The p esence o absence o F. ci cina um and se e i y o disease o 96 di e en Pinus axa
(including species, subspecies, a ie ies, and hyb ids), ei he expe imen ally es ed o obse ed,
is epo ed (Tables 3–5). Unambiguous suscep ibili y ankings we e ob ained o 21 Pinus spp.
(i.e., high suscep ibili y— h ee species; mode a e suscep ibili y— ou species; low suscep ibili y—13
species; esis an —one species) and 14 Pinus hyb ids (i.e., mode a e suscep ibili y— h ee hyb ids;
low suscep ibili y—11 hyb ids). Nine een Pinus species and se en Pinus hyb ids we e classi ied
as ha ing a iable suscep ibili y, because di e en s udies placed hem in di e en suscep ibili y
ca ego ies, while o 28 species he suscep ibili y classi ica ion was unknown. No symp oms o disease
we e obse ed on an addi ional 10 Pinus axa (P. cemb a,P. con o a a . la i olia,P. held eichii,P. mugo
subsp. mugo,P. mugo subsp. o unda a,P. nig a subsp. nig a,P. nig a subsp. pallasiana,P. peuce,
P. syl es is a . hama a, and P. wallichiana) which we e moni o ed and sys ema ically inspec ed o
F. ci cina um in he ield (h p://bi .do/phy opo al). Because hese ees we e moni o ed in a eas whe e
he pa hogen has no been epo ed, he suscep ibili y o esis ance s a us emains unknown. I can
he e o e be concluded ha 67 Pinus species and 18 Pinus hyb ids a e known o be suscep ible o
F. ci cina um based on a i icial inocula ion and na u al in ec ion obse a ions (see Tables 3–5).
Suscep ibili y a ings o F. ci cina um we e analysed sepa a ely o di e en age classes o Pinus
and non-Pinus hos s; i.e., seedlings and young plan s ( ecen ly eme ged pine seedling and plan s,
≤10 yea s old)
o ma u e ees (
≥
11 yea s). When only seedlings and plan s o Pinus we e conside ed,
a o al o 18 species we e a ed as highly suscep ible, ou as mode a e-highly suscep ible, 17 as
mode a ely suscep ible, se en as mode a ely-low suscep ible, 22 as low suscep ible, and one as
esis an (P. ko aiensis) o F. ci cina um. Twel e Pinus species known o be hos s o F. ci cina um and
nine o he species ha e unknown suscep ibili y a he seedling s age (Table 3). When ma u e ees
we e conside ed sepa a ely, only a single pine species (P. adia a) was a ed as highly suscep ible, i e
species we e a ed as ha ing low-mode a e suscep ibili y, and ou as ha ing low suscep ibili y o
Fo es s 2020,11, 724 18 o 40
F. ci cina um. Twen y-six ma u e Pinus species known o be hos s o F. ci cina um and 23 o species ha e
unknown suscep ibili y a ing o F. ci cina um (Table 4). Th ee Pinus species in bo h age classes ha e
highly a iable suscep ibili y o F. ci cina um (Tables 3and 4).
Two pine species, P. densi lo a and P. ko aiensis, ha e been eco ded as esis an o F. ci cina um
in 3–4 yea old seedling inocula ion ials conduc ed in g eenhouses [
59
,
135
]. Howe e , F. ci cina um
has been isola ed om P. densi lo a ees in Japan al hough he suscep ibili y o his hos as a ma u e
ee was no a ed [
136
]. The e o e, we conside P. densi lo a o ha e highly a iable suscep ibili y o
F. ci cina um and he only uly esis an Pinus species o be P. ko aiensis.
Non-pine ee species a e gene ally only weakly suscep ible o a e esis an o F. ci cina um.
The suscep ibili y o non-pine hos s o F. ci cina um was es ed o obse ed on 24 ee and 18 he baceous
species (Table 6). Th ee coni e species (La ix kaemp e i,Liboced us decu ens,Pseudo suga menziesii) we e
ca ego ised as ha ing low le el o suscep ibili y. Ano he h ee coni e species (Abies alba,La ix decidua,
Picea abies) we e conside ed as ha ing highly a iable suscep ibili y because ecen ly eme ged seedlings
we e classed as suscep ible o F. ci cina um, whe eas 2-yea -old and olde plan s we e conside ed
esis an [
8
–
10
]. All o he non-pine hos s, 18 non-pine ee species in 10 di e en gene a, as well as
h ee he baceous species, we e classed as esis an o F. ci cina um (Table 6).
Al hough only h ee he baceous plan species a e classi ied as esis an o F. ci cina um (Table 6),
i mus be no ed ha only a e y limi ed numbe o he baceous plan s ha e been es ed in his espec in
pa hogenici y assays. Fi een species o he baceous plan s a e known hos s o F. ci cina um in he wide
en i onmen , bu hei le els o suscep ibili y a e unknown [
5
–
7
,
26
,
137
]. An addi ional conside a ion
is ha in some P. adia a plan a ions in ec ed wi h F. ci cina um, a numbe o he baceous plan s (Table 6)
ha e been epo ed o be in ec ed endophy ically wi h F. ci cina um [
7
]. I is hus clea ha he ull hos
ange o F. ci cina um, and suscep ibili y o each species, has ye o be elucida ed.
Fo es s 2020,11, 724 19 o 40
Table 3. Suscep ibili y lis o Pinus species seedlings and young plan s ( ecen ly eme ged pine seedling and plan s, ≤10 yea s old) o Fusa ium ci cina um.
Suscep ibili y/Hos
Species1Common English Names Subgenus; Sec ion;
Subsec ion2
Type o
In ec ion
G ow h o Tes
Condi ions Seedlings and/o Plan Age3Re e ences
Suscep ibili y high
Pinus b u ia Ten. Tu kish pine, Calab ian pine, Eas
Medi e anean pine, B u ia pine Pinus; Pinus; Halepenses A i icial G ow h chambe 2 yea s J. Ma ín-Ga cía,
unpublished
Pinus cemb oides Zucc. Pinyon pine, Mexican nu pine S obus; Pa ya; Cemb oides A i icial G eenhouse Unknown [138]
Pinus douglasiana Ma ínez Go don’s pine, Douglas pine Pinus; Pinus; Ponde osae;
‘Pseudos obus G oup’ A i icial G eenhouse Unknown [138]
Pinus g eggii Engelm. ex Pa l.
G egg’s pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial Field 2 yea s [76]
Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses A i icial G ow h chambe 2 yea s J. Ma ín-Ga cía,
unpublished
Pinus ha wegii Lindl. Endliche pine Pinus; Pinus; Ponde osae;
‘Mon ezumae G oup’ A i icial G eenhouse Unknown [138]
Pinus he e ae Ma ínez He e a’s pine Pinus; Pinus; Ooca pae;
‘Teoco e G oup’ A i icial G eenhouse 12 weeks [139]
Pinus mon ezumae Lamb. Mon ezuma pine Pinus; Pinus; Ponde osae;
‘Mon ezumae G oup’ A i icial G eenhouse Unknown [138]
Pinus mugo Tu a Moun ain pine, dwa
moun ain pine Pinus; Pinus, Pinus A i icial G ow h chambe Recen ly eme ged [9]
Pinus mugo Tu a subsp.
uncina a (Ramond ex DC.)
Domin. Swiss moun ain pine Pinus; Pinus, Pinus A i icial G ow h chambe Recen ly eme ged [8]
Pinus nig a J.F.A nold Aus ian pine, black pine Pinus; Pinus; Pinus A i icial G ow h chambe Recen ly eme ged, 2 yea s [8], J. Ma ín-Ga cía,
unpublished
Pinus pa ula Schiede ex
Schl dl. & Cham.
Pa ula pine, Jeleco e pine, Mexican
weeping pine,
sp eading-lea ed pine
Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse 7–10 m [71,75,140]
Pinus pinas e Ai on Ma i ime pine Pinus; Pinus; Pinus A i icial G ow h chambe Recen ly eme ged, 2 yea s
[
8
,
141
], J. Ma
í
n-Ga c
í
a,
unpublished
Pinus pseudos obus Lindl. Smoo h-ba k Mexican pine Pinus; Pinus; Ponde osae;
‘Pseudos obus G oup’ A i icial G eenhouse Unknown [138]
Pinus adia a D. Don Mon e ey pine, adia a pine,
insignis pine Pinus; Pinus; A enua ae A i icial G ow h chambe ,
g eenhouse, ield
Recen ly eme ged, 3 mon hs,
1 yea , 2 yea s, 2–3 yea s,
3–4 yea s, unknown [8,76,80,88,139,142,143]
Pinus s obus L.
Eas e n whi e pine, no he n whi e
pine, whi e pine, Weymou h pine
(B i ish), and so pine S obus; S obus;S obi A i icial G ow h chambe Recen ly eme ged [8]
Pinus syl es is L. Sco s/Sco ch pine Pinus; Pinus; Pinus A i icial G ow h chambe ,
g eenhouse Recen ly eme ged, 1.5 yea s,
2 yea s [8,10] J. Ma ín-Ga cía,
unpublished
Pinus aeda L. Loblolly pine Pinus; Pinus; Aus ales A i icial G eenhouse 1 yea [88]
Fo es s 2020,11, 724 20 o 40
Table 3. Con .
Suscep ibili y/Hos
Species1Common English Names Subgenus; Sec ion;
Subsec ion2
Type o
In ec ion
G ow h o Tes
Condi ions Seedlings and/o Plan Age3Re e ences
Suscep ibili y mode a e-high
Pinus leiophylla Schiede ex
Schl dl. & Cham. Chihuahua pine, smoo h-lea pine,
yellow pine Pinus; Pinus; Leiophyllae A i icial Field 5–8 yea s [144]
Pinus pa ula Schiede ex
Schl dl. & Cham.
Pa ula pine, Jeleco e pine, Mexican
weeping pine,
sp eading-lea ed pine
Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse, Field 3 mon hs, 21 weeks, 2 yea s [76,145,146]
Pinus pinas e Ai on Ma i ime pine, clus e pine Pinus; Pinus; Pinus A i icial G eenhouse 6 mon hs, 3 yea s [141,147]
Pinus aeda L. Loblolly pine Pinus; Pinus; Aus ales A i icial G eenhouse, Field 21 weeks, 4 yea s [88,147]
Suscep ibili y mode a e
Pinus banksiana Lamb. Jack pine, sc ub pine Pinus; Pinus; Con o ae A i icial G eenhouse 3.5 yea s [148]
Pinus de oniana Lindl. Michoacán pine Pinus; Pinus; Ponde osae
‘Mon ezumae G oup’ A i icial G eenhouse, ield 12 weeks [97,139]
Pinus echina a Mill. Sho lea pine Pinus; Pinus; Aus ales A i icial G eenhouse 3–4 yea s [135]
Pinus ellio ii Engelm. Slash pine Pinus; Pinus; Aus ales A i icial G eenhouse, ield 7–9 mon hs, 8 yea s [74,75,144]
Pinus g eggii Engelm. ex Pa l.
G egg’s pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse 7 mon hs [75]
Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses A i icial G eenhouse 2 yea s, 3–4 yea s, unknown [138,142,143]
Pinus kesiya Royle ex Go don Khasia pine, Khasi pine,
Bengue pine Pinus; Pinus; Pinus A i icial Field 2 yea s [76]
Pinus leiophylla Schiede ex
Schl dl. & Cham. Chihuahua pine, smoo h-lea pine,
yellow pine Pinus; Pinus; Leiophyllae A i icial G eenhouse Unknown [138]
Pinus mugo Tu a subsp.
uncina a (Ramond ex DC.)
Domin. Swiss moun ain pine Pinus; Pinus, Pinus A i icial G eenhouse 2 yea s [148]
Pinus nig a J.F.A nold Aus ian pine, black pine Pinus; Pinus; Pinus A i icial Field Unknown [8]
Pinus palus is Mill. Longlea pine Pinus; Pinus; Aus ales Na u al Nu se y Recen ly eme ged [149]
Pinus pinas e Ai on Ma i ime pine, clus e pine Pinus; Pinus; Pinus A i icial G eenhouse, ield 2 yea s, Unknown [8,143]
Pinus p inglei Shaw P ingle´s pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse Unknown [138]
Pinus s obus L.
Eas e n whi e pine, no he n whi e
pine, whi e pine, Weymou h pine
(B i ish), and so pine S obus; S obus;S obi A i icial G eenhouse 3.5 yea s [150]
Pinus syl es is L. Sco s/Sco ch pine Pinus; Pinus; Pinus A i icial G eenhouse 2 yea s, 3.5 yea s [143,150]
Pinus ecunumanii
F.Schwe d . ex Eguiluz &
J.P.Pe y
Schwe d ege ’s Pine, Tecun
Uman Pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse
3 mon hs, 12 weeks, 6–8 mon hs
(high ele a ion o igin) [139,145,146]
Pinus i giniana Mill. Vi ginia pine, Je sey pine,
sc ub pine Pinus; Pinus; Con o ae A i icial G eenhouse 3–4 yea s [135]
Fo es s 2020,11, 724 21 o 40
Table 3. Con .
Suscep ibili y/Hos
Species1Common English Names Subgenus; Sec ion;
Subsec ion2
Type o
In ec ion
G ow h o Tes
Condi ions Seedlings and/o Plan Age3Re e ences
Suscep ibili y low-mode a e
Pinus ca ibaea Mo ele Ca ibbean pine Pinus; Pinus; Aus ales A i icial G eenhouse 7 mon hs [75]
Pinus ellio ii Engelm. Slash pine Pinus; Pinus; Aus ales A i icial Field 2 yea s [76]
Pinus mugo Tu a subsp.
uncina a (Ramond ex DC.)
Domin. Swiss moun ain pine Pinus; Pinus, Pinus A i icial Field Unknown [8]
Pinus pinas e Ai on Ma i ime pine, clus e pine Pinus; Pinus; Pinus A i icial G eenhouse 2 yea s [148]
Pinus syl es is L. Sco s/Sco ch pine Pinus; Pinus; Pinus A i icial G ow h chambe ,
g eenhouse Recen ly eme ged, 2 yea s [9,148]
Pinus aeda L. Loblolly pine Pinus; Pinus; Aus ales A i icial G eenhouse 7–9 mon hs, 1 yea [74,151]
Pinus hunbe gii Pa l. black pine, Japanese black pine,
Japanese pine Pinus; Pinus; Pinus A i icial G eenhouse 3–4 yea s [135]
Suscep ibili y low
Pinus ayacahui e Eh enb. ex
Schl dl. Mexican whi e pine,
ayacahui e pine S obus; S obus; S obi A i icial G eenhouse Unknown [138]
Pinus cana iensis C.Sm. Cana y Island pine Pinus; Pinus; Cana ienses A i icial G eenhouse 2–3 yea s, 3–4 yea s [3,142]
Pinus ca ibaea Mo ele Ca ibbean pine Pinus; Pinus; Aus ales A i icial G eenhouse 3 mon hs [139]
Pinus clausa (Chapm. ex
Engelm.) Vasey ex Sa g. Sand pine, Flo ida sp uce pine,
Alabama pine Pinus; Pinus; Con o ae A i icial,
na u al G eenhouse, ield 18 mon hs, 6–8 yea s [82]
Pinus glab a Wal e Sp uce pine Pinus; Pinus; Aus ales A i icial,
na u al G eenhouse, ield 5 mon hs, unknown [152]
Pinus jaliscana Pe ez de la
Rosa Jalisco pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse 3 mon hs [139]
Pinus luchuensis May Luchu/Ryukyu pine Pinus; Pinus; Pinus A i icial G eenhouse 2 yea s [136]
Pinus maximinoi H.E. Moo e Thinlea pine Pinus; Pinus; Ponde osae;
‘Pseudos obus G oup’ A i icial G eenhouse 3 mon hs, 7 mon hs, 8–9
mon hs [56,74,145]
Pinus monophylla To . &
F ém. Singlelea pinyon pine S obus; Pa ya; Cemb oides Na u al Field Unknown [79]
Pinus nig a J.F.A nold Aus ian pine, black pine Pinus; Pinus; Pinus A i icial G eenhouse 2 yea s, 3.5 yea s [143,150,153]
Pinus occiden alis Sw. Wes e n Indian pine Pinus; Pinus; Aus ales Na u al Field Unknown [53]
Pinus ooca pa Schiede ex
Schl dl.
Oco e pine, Egg-cone pine,
hazelnu pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse 3 mon hs, 7 mon hs [75,139,145]
Pinus p inglei Shaw P ingle’s pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse 7 mon hs [75]
Pinus pseudos obus Lindl. syn.
Pinus oaxacana Mi o Smoo h-ba k Mexican pine Pinus; Pinus; Ponde osae;
‘Pseudos obus G oup’ Na u al,
a i icial Field, g eenhouse Unknown, 7 mon hs [74,97]
Pinus pungens Lamb. Table moun ain pine Pinus; Pinus; Aus ales A i icial Unknown Unknown [53]
Pinus esinosa Ai on Red pine, No way pine Pinus; Pinus; Pinus A i icial G eenhouse 3.5 yea s [150]
Pinus igida Mill. Pi ch pine Pinus; Pinus; Aus ales A i icial G eenhouse 3–4 yea s [135]

Fo es s 2020,11, 724 22 o 40
Table 3. Con .
Suscep ibili y/Hos
Species1Common English Names Subgenus; Sec ion;
Subsec ion2
Type o
In ec ion
G ow h o Tes
Condi ions Seedlings and/o Plan Age3Re e ences
Suscep ibili y low-mode a e
Pinus se o ina Michx. Pond pine, ma sh pine,
pocosin pine Pinus; Pinus; Aus ales A i icial G eenhouse 1 yea [53,151]
Pinus syl es is L. Sco s/Sco ch pine Pinus; Pinus; Pinus A i icial Field 2 yea s, Unknown [8]
Pinus aeda L. Loblolly pine Pinus; Pinus; Aus ales A i icial Field 8 yea s [140]
Pinus ecunumanii
F.Schwe d . ex Eguiluz &
J.P.Pe y
Schwe d ege ’s Pine, Tecun
Uman Pine Pinus; Pinus; Ooca pae;
‘Ooca pa G oup’ A i icial G eenhouse, ield 3 mon hs, 12 weeks, 6–8
mon hs, 8 yea s (low-ele a ion
o igin) [56,74,139,144–146]
Pinus hunbe gii Pa l. Black pine, Japanese black pine,
Japanese pine Pinus; Pinus; Pinus A i icial G eenhouse 3–4 yea s [142]
Resis an
Pinus ko aiensis Siebold
and Zucc. Ko ean pine S obus; S obus; Cemb ae A i icial G eenhouse 3 yea s [59]
Highly a iable suscep ibili y
Pinus densi lo a Siebold and
Zucc.
Japanese ed pine, Ko ean ed pine
Pinus; Pinus; Pinus A i icial G eenhouse 3–4 yea s [59,135,136]
Pinus mu ica a D. Don Bishop pine Pinus; Pinus; A enua ae; A i icial G eenhouse Unknown [79]
Pinus pinea L. I alian s one pine, umb ella pine Pinus; Pinus; Pineae A i icial G eenhouse,
g ow h chambe s 6 mon hs, 2 yea s, 3-4 yea s [35,37,143,154], J.
Ma ín-Ga cía,
unpublished
Suscep ible, unknown suscep ibili y a e
Pinus a enua a Lemmon Knobcone pine, Na owcone pine Pinus; Pinus; A enua ae A i icial G eenhouse Unknown [79,154]
Pinus b u ia Ten. a . elda ica
(Medw.) Silba Elda ica pine Pinus; Pinus; Halepenses A i icial G eenhouse Unknown [79]
Pinus cana iensis C.Sm. Cana y Island pine Pinus; Pinus; Cana ienses A i icial G eenhouse Unknown [79]
Pinus con o a Douglas
ex Loudon Sho e pine, lodgepole pine Pinus; Pinus; Con o ae A i icial G eenhouse Unknown [141]
Pinus coul e i D. Don Coul e pine, big-cone pine Pinus; Pinus; Ponde osae;
‘Sabinianae G oup’ A i icial G eenhouse Unknown [79,154]
Pinus halepensis Mill. Aleppo pine Pinus; Pinus; Halepenses A i icial Nu se y 2 yea s [35]
Pinus je eyi A.Mu ay bis Je ey pine Pinus; Pinus; Ponde osae A i icial G eenhouse Unknown [79]
Pinus lambe iana Douglas Suga pine S obus; S obus; S obi A i icial G eenhouse Unknown [79]
Pinus nig a J.F. A nold subsp.
la icio (Poi .) Mai e Co sican pine Pinus; Pinus; Pinus Na u al Nu se y <6 mon hs A.V. Sanz-Ros,
unpublished
Pinus pinas e Ai on Ma i ime pine, clus e pine Pinus; Pinus; Pinus A i icial Nu se y 2 yea s [36]
Pinus ponde osa Douglas
ex Loudon Ponde osa pine, bull pine,
blackjack pine Pinus; Pinus; Ponde osae A i icial G eenhouse Unknown [79]
Pinus sabiniana Douglas
ex D. Don G ay/ oo hill/digge pine Pinus; Pinus; Ponde osae;
‘Sabinianae G oup’ A i icial G eenhouse Unknown [79]
1Hos axonomy is based on Zanoni, Fa jon [155]; 2Subgenus; Sec ion; Subsec ion is based on P ice e al. [156]; 3Seedlings and plan s age: w—week, m—mon h, y—yea .
Fo es s 2020,11, 724 23 o 40
Table 4. Suscep ibili y lis o Pinus species ma u e ees (≥11 yea s) o Fusa ium ci cina um.
Suscep ibili y/Hos Species1Sampling Si e S a us o Hos T ee Age, Yea s Re e ence
Suscep ibili y high
Pinus adia a D. Don Plan a ion, unknown Exo ic, na i e Unknown, 20y [12,34,128,154,157]
Suscep ibili y low-mode a e
Pinus discolo D.K. Bailey & Hawksw. Unknown Na i e Unknown [138]
Pinus douglasiana Ma inéz Unknown Na i e Unknown [138]
Pinus du angensis Ma inéz Unknown Na i e Unknown [138]
Pinus halepensis Mill. Unknown Exo ic Unknown [138]
Pinus leiophylla Schiede ex Schl dl. & Cham. Unknown Na i e Unknown [138]
Suscep ibili y low
Pinus ayacahui e Eh enb. ex Schl dl. Unknown Na i e Unknown [138]
Pinus cana iensis C. Sm. U ban ees Exo ic Unknown [154]
Pinus luchuensis May G eenhouse Na i e 11–19 yea s [136]
Pinus pinas e Ai on Plan a ion Na i e Unknown
Highly a iable suscep ibili y
Pinus densi lo a Siebold and Zucc. Unknown Na i e Unknown [136]
Pinus mu ica a D. Don Unknown, Plan a ion Na i e Unknown, 12-13 yea s [80,153]
Pinus pinea L. Plan a ion, u ban ees Exo ic, na i e Unknown [35,154]
Suscep ible, unknown suscep ibili y a e
Pinus a izonica Engelm. Plan a ion, na u al o es Na i e Unknown [43,97,138]
Pinus a mandii F anch. Na u al o es Na i e Unknown [136]
Pinus a enua a Lemm Unknown Na i e Unknown [154,158]
Pinus cana iensis C. Sm. Unknown Exo ic Unknown [15,80]
Pinus cemb oides Zucc. Unknown Na i e Unknown [138]
Pinus con o a Douglas ex Loudon Unknown Na i e Unknown [154]
Pinus con o a Douglas ex Loudon a . con o a Na u al o es Na i e Unknown [158]
Pinus coul e i D. Don Unknown Na i e Unknown [154]
Pinus ellio ii Engelm. a . densa (Li le and Do man) E. Mu ay Plan a ion Na i e Unknown [17]
Pinus ellio ii Engelm. a . ellio ii Plan a ion, na u al o es Na i e, exo ic Unknown [13,159]
Pinus g eggii Engelm. ex Pa l. Unknown Exo ic Unknown [74,76]
Pinus halepensis Mill. Unknown, u ban ees Exo ic, na i e Unknown [35,80]
Pinus ha wegii Lindl. Plan a ion and na u al o es Na i e Unknown [40,138]
Fo es s 2020,11, 724 24 o 40
Table 4. Con .
Suscep ibili y/Hos Species1Sampling Si e S a us o Hos T ee Age, Yea s Re e ence
Suscep ible, unknown suscep ibili y a e
Pinus kesiya Royle. ex Go don Plan a ion Exo ic Unknown [56]
Pinus leiophylla Schiede ex Schl dl. & Cham. a . leiophylla Na u al o es Na i e Unknown [120]
Pinus mon ezumae Lamb. Unknown Na i e Unknown [138]
Pinus pa ula Schiede ex Schl dl. & Cham. Plan a ion Exo ic Unknown [56]
Pinus ponde osa Douglas ex Lawson Plan a ion Na i e Unknown [154]
Pinus p inglei Shaw Unknown Na i e Unknown [138]
Pinus pseudos obus Lindl. Unknown Na i e Unknown [138]
Pinus pseudos obus Lindl. a . apulcensis (Lindl.) Shaw Plan a ion and na u al o es Na i e Unknown [40,97,138]
Pinus adia a ×a enua a Na u al o es Na i e Unknown [158]
Pinus sabiniana Douglas ex D. Don Unknown Na i e Unknown [154,158]
Pinus aeda L. Unknown, g eenhouse Na i e Unknown, 21 yea s [151,160]
Pinus hunbe gii Pa l. Roadside, gol cou se Na i e Unknown [161]
Pinus o eyana Pa y ex Ca iè e Unknown Na i e Unknown [154,158]
1Hos axonomy is based on Zanoni, Fa jon [155].
Fo es s 2020,11, 724 25 o 40
6.2. Species wi h Va iable Suscep ibili y Ra ings
Suscep ibili y a ings we e a iable o 19 Pinus species and se en Pinus hyb ids due o he ac
ha di e en s udies classi ied hem in di e en suscep ibili y ca ego ies (see Tables 3–5). Va iable
suscep ibili y anging om suscep ible o esis an was ound in wo ma u e pine hos s: P. mu ica a
and P. pinea. The highes disc epancy be ween suscep ible a ings was no ed o species classi ied as
ha ing bo h high and low suscep ibili y: P. nig a,P. pseudos obus, P. syl es is, and P. aeda. Two Pinus
species (P. pinas e and P. mugo subsp. uncina a) we e anked as ha ing bo h high and low-mode a e
suscep ibili y. Sligh di e ences in suscep ibili y a ings, i.e., hose in adjacen anking ca ego ies, we e
eco ded o 11 pine hos s: P. cana iensis,P. ca ibaea,P. ellio ii,P. g eggii,P. halepensis,P. leiophylla,P. pa ula,
P. p inglei,P. s obus,P. ecunumanii, and P. hunbe gii (Tables 3and 4). These mino disc epancies in
suscep ibili y a ings a e mos likely due o expe imen al a ia ion and in e p e a ion o he ca ego ies
by a ious au ho s and a e no discussed u he in his e iew, while he species wi h g ea e
disc epancies in suscep ibili y a ings a e discussed in mo e de ail below.
Among he se en Pinus hyb ids, we ound ambiguous classi ica ions o hose wi h P. ecunumanii
and P. g eggii as one o he pa en al species (Table 5). Seeds o hese wo Pinus species ha e been sou ced
om di e en loca ions in Mexico, and suscep ibili y o F. ci cina um a ies based on seed sou ces [
139
].
Pinus ecunumanii o igina ed om high ele a ions, and P. g eggii om no he n Mexico (i.e., P. g eggii
a . g eggi), a e espec i ely mo e suscep ible o F. ci cina um han low-ele a ion P. ecunumanii
and P. g eggii om sou he n Mexico (i.e., P. g eggii a . aus alis) [
75
,
76
]. Failu e o men ion such
p o enance in o ma ion has acco dingly esul ed in appa en ly inconsis en pa hogenici y da a in
some published s udies.
Ma u e P. pinea was a ed as esis an o F. ci cina um by Go don e al. [
154
], bu in u ban condi ions
in I aly he hos was conside ed suscep ible [
34
]. Fu he mo e, seedlings o P. pinea we e a ed as
ha ing low suscep ibili y [
37
,
142
,
143
,
148
] and unknown suscep ibili y [
35
], bu P. pinea seedlings o
Spanish o igin (6 mon hs, 12–14 cm) we e e y suscep ible and alle seedlings (6 mon hs, >16 cm) o
he same o igin we e esis an (Ma
í
n-Ga c
í
a, unpublished). The e o e, we conside ha P. pinea has
highly a iable suscep ibili y. The esul s o P. mu ica a inocula ion es s by Schmale & Go don [
153
]
indica ed a wide ange o a ia ion in suscep ibili y: 27% o P. mu ica a ees we e conside ed esis an ,
while o he s we e suscep ible o F. ci cina um. In o he s udies, P. mu ica a seedlings and ma u e ees
we e shown o be suscep ible o F. ci cina um [
79
,
80
]. Thus, we conside ed P. mu ica a o be highly
a iable in suscep ibili y o F. ci cina um.
Pinus syl es is seedlings, bo h ecen ly eme ged and 1.5-yea -old seedlings, o Spanish, Czech, and
Sco ish o igin, we e classi ied as highly suscep ible in g ow h chambe and g eenhouse expe imen s
by Ma inez-Al a ez e al. [
8
], Ma
í
n-Ga c
í
a e al. [
10
], and Woodwa d, unpublished. In con as , low
suscep ibili y o P. syl es is seedlings o he Spanish o igin was obse ed in a ield ial [
8
]. No da a
a e a ailable o he suscep ibili y o ma u e P. syl es is ees.
Pinus nig a seedlings o di e en p o enances we e highly suscep ible o F. ci cina um in g ow h
chambe expe imen s [
8
], Ma
í
n-Ga c
í
a, unpublished. In con as , in g eenhouse expe imen s 2-
and 3.5-yea s old seedlings o P. nig a we e ound o ha e low le els o suscep ibili y [
143
,
150
].
This disc epancy could be a esul o di e en en i onmen al condi ions ( empe a u e, humidi y) in he
g ow h chambe and g eenhouse as compa ed o ield condi ions. These kinds o expe imen s should
be done unde he same en i onmen al condi ions. The a ia ion in suscep ibili y o 2-yea -old P. nig a
seedlings o Spanish o igin was qui e high be ween indi iduals, indica ing ha some indi iduals
in his species may be a highe isk o damage om F. ci cina um [
143
]. Less han six- mon hs-old
seedlings o P. nig a subsp. la icio o he Spanish o igin we e ound na u ally (no a i icially inocula ed)
in ec ed in nu se ies (Sanz-Ros, unpublished), and his was conside ed as unknown suscep ibili y.
No da a a e a ailable o he suscep ibili y o ma u e P. nig a.
One-yea -old P. aeda seedlings in Sou h A ica we e ound o be suscep ible o F. ci cina um [
88
],
in con as o o he s udies showing ha P. aeda was highly ole an o F. ci cina um in Sou h
A ica [
76
,
139
]. Se en-mon h-old seedlings o P. pseudos obus we e anked as ha ing low suscep ibili y
Fo es s 2020,11, 724 32 o 40
g eenhouse inocula ions. T ee age clea ly plays an impo an ole in suscep ibili y o F. ci cina um,
and much wo k needs o be done o ully unde s and he in e ac ion be ween hos , en i onmen and
pa hogen and hei in e ac i e in luences on suscep ibili y and se e i y o in ec ion.
Thus, he esul s in his s udy clea ly suppo he need o s anda d p o ocols o be applied
in pa hogenici y es s o compa e da a in di e en condi ions (including labo a o ies) and inc ease
knowledge on he biology and epidemiology o F. ci cina um.
Knowledge o he cen e o o igin and sou ce popula ions o F. ci cina um can aid in sou cing
esis an species o aluable gene ic ma e ial. Combined wi h in o ma ion ega ding in oduc ion
pa hways, i can also help p e en u he in oduc ions by ocusing qua an ine measu es and
moni o ing e o s whe e hey a e mos e ec i e. Gi en he isks posed by he mo emen o he
pa hogen, he e is an u gen need o ou ine su eillance o Pinus and o he species known o be
suscep ible oF. ci cina um, aswellas esea chon heimpo anceo soil,na i einsec s,andasymp oma ic
nu se y plan s o he sp ead o he disease [
166
]. Wi hou main ained le els o su eillance, i is highly
p obable he pa hogen will con inue sp eading o new a eas and ex ending i s hos ange.
Supplemen a y Ma e ials:
The ollowing a e a ailable online a h p://www.mdpi.com/1999-4907/11/7/724/s1,
suppo ing in o ma ion o Geo-da abase, Table S1: Da a ields o he in e na ional Fusa ium ci cina um (FC)
geo-da abase ( o mo e in o ma ion see: h p://bi .do/phy opo al), GIS and map analyses, and s a is ical analyses.
Au ho Con ibu ions:
All au ho s sen moni o ing da a o he pa hogen o geo-da abase and in e ac i e map.
W i ing: R.D., M.S.M., B.G,J.M.G., P.V. Re iew: allau ho s. Edi ing: S.W., K.A. (Ka a
í
na Adamˇc
í
ko
á
). All au ho s
ha e ead and ag eed o he published e sion o he manusc ip .
Funding:
This s udy was inancially suppo ed by COST Ac ion FP1406 (PINESTRENGTH), he Es onian Science
Founda ion g an PSG136, he Fo es y Commission, Uni ed Kingdom, he Phy oph ho a Resea ch Cen e Reg. No.
CZ.02.1.01/0.0/0.0/15_003/0000453, a p ojec co- inanced by he Eu opean Regional De elopmen Fund. ANSES is
suppo ed by a g an managed by he F ench Na ional Resea ch Agency (ANR) as pa o he “In es issemen s
d’A eni ” p og amme (ANR-11-LABX-0002-01, Labo a o y o ExcellenceARBRE). SW was pa ly suppo ed
by BBSRC G an e e ence BB/L012251/1 “P omo ing esilience o UK ee species o no el pes s & pa hogens:
ecological & e olu iona y solu ions (PROTREE)” join ly unded by BBSRC, De a, ESRC, he Fo es y Commission,
NERC and he Sco ish Go e nmen , unde he T ee Heal h and Plan Biosecu i y Ini ia i e. Annual su eys in
Swi ze land we e inancially suppo ed by he Swiss Fede al O ice o he En i onmen FOEN.
Acknowledgmen s:
And ea Kuno a and C is ina Pizza i a e acknowledged o he assis ance in he sampling.
Thanks a e due o Dina Ribei o and Helena Ma ques om ICNF-Po uguese Fo es Au ho i y o p o iding
loca ion coo dina es. We hank h ee anonymous e iwe s o aluable co ec ions and sugges ions.
Con lic s o In e es : The au ho s decla e no con lic o in e es .
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