Acta Sil va e et Ligni 120 (2019), 1–12 1 Pregledni znanstveni članek / Review article VPLIV SUŠE NA DROBNE KORENINE DREVES IN EKTOMIKORIZO V GOZDNIH EKOSISTEMIH EFFECTS OF DROUGHT ON TREE FINE ROOTS AND ECTOMYCORRHIZA IN FOREST ECOSYSTEMS Tanja MRAK 1 , Hojka KRAIGHER 2 (1) Gozdarski inštitut Slovenije, tanja.mrak@gozdis.si (2) Gozdarski inštitut Slovenije, hojka.kraigher@gozdis.si IZVLEČEK Sušni stres sproži tako pri drobnih koreninah dreves kot pri ektomikoriznih glivah številne spremembe na različnih nivojih. Drevesa se branijo pred sušo z mehanizmi izogibanja in tolerance. Suša lahko vpliva na kolonizacijo z ektomikoriznimi glivami in na strukturo ektomikorizne združbe. Pomembno vlogo pri preživetju mladja ob suši imajo skupne micelijske mreže. Ob zmerni suši je kolonizacija z ektomikoriznimi glivami večja kot ob ekstremni suši, kar ima za drevo številne pozitivne učinke. V sušnih razmerah se pogosto še posebej poveča pogostnost ektomikorizne vrste Cenococcum geophilum Fr., ki omogoča, da drobne korenine ostanejo funkcionalne in takoj po končanem sušnem obdobju pričnejo z absorpcijo vode. V sušnih razmerah se poveča tvorba težko razgradljivih molekul v koreninah (lignin), prav tako pa se težko razgradljive molekule (melanin) tvori- jo tudi pri ektomikorizni vrsti C. geophilum, kar prispeva h kopičenju težko razgradljivih organskih snovi v tleh. Ključne besede: globalne spremembe, drobne korenine, mikorizne glive, prilagoditve, organska snov v tleh ABSTRACT Drought stress elicits many changes in tree fine roots and ectomycorrhizal fungi. Trees cope with drought through avoidance mechanisms or tolerance. Drought can result in changes in colonization by ectomycorrhizal fungi and in the structure of ecto- mycorrhizal communities. Survival of tree seedlings is supported through common mycelium networks. In moderate drought, there is greater colonization by ectomycorrhizal fungi compared to severe drought, resulting in several beneficial effects to the tree. Under drought, the frequency of ectomycorrhizal fungus Cenococcum geophilum Fr. often increases. C. geophilum sustains tree fine roots function and therefore roots are able to absorb water as soon as the drought period is over. Under drought, syn- thesis of recalcitrant organic compounds in roots, e.g. lignine, is increased. Recalcitrant compounds such as melanine are also found in C. geophilum, contributing to the accumulation of recalcitrant soil organic matter. Key words: global changes, fine roots, mycorrhizal fungi, adaptation, soil organic matter GDK 164.3:181.31(045)163.6=111 Prispelo / Received: 22. 7. 2019 DOI 10.20315/ASetL.120.1 Sprejeto / Accepted: 29. 8. 2019 1 UVOD 1 INTRODUCTION V zadnjih desetletjih v nekaterih delih Evrope bele- žijo vse pogostejša sušna obdobja kot posledico nara- ščajočih temperatur (Briffa in sod., 2009; Hanel in sod., 2018). Pričakovati je, da se bo trend naraščanja tempe- ratur in pogostosti ter intenzivnosti vročinskih valov v prihodnosti nadaljeval (Kirtman in sod., 2013; Vogel in sod., 2017), kar bo poleg neposrednega negativnega vpliva na vlažnost tal okrepilo negativne učinke more- bitne manjše količine padavin. V prihodnosti naj bi se poleti povprečna količina padavin v Mediteranu in sre- dnji Evropi zmanjšala, padavine pa naj bi se pogosteje pojavljale v obliki padavinskih ekstremov (Rajczak in Schär, 2017). Vlažnost površinskega sloja tal naj bi v južni Evropi upadala prek celega leta, poleti in jeseni pa tudi v osrednji in zahodni Evropi, medtem ko naj bi pogostnost zelo nizkih vrednosti talne vlage naraščala (Ruosteenoja in sod., 2018). Povratna zanka med vla- žnostjo tal in temperaturo zraka dodatno krepi tempe- raturne ekstreme (Vogel in sod., 2017). Nizka vlažnost tal zmanjšuje evapotranspiracijo ter tako povečuje to- plotni tok, z njim pa pojavljanje višjih temperatur zraka, medtem ko visoke temperature zraka povečujejo defi- cit vlage v zraku, s čimer se evapotranspiracija nada- ljuje kljub upadajoči vlažnosti tal (Ruosteenoja in sod., 2018). Navedene spremembe bodo imele močan vpliv na obstoječe gozdne ekosisteme in biogeokemijsko kroženje v njih. Naraščajoča pogostost ekstremnih vre- menskih dogodkov bo prispevala k odmiranju gozdov in povzročila spremembe gozdnih združb zaradi večje občutljivosti drevesnega mladja na ekstremne vremen- ske dogodke (največji delež umrljivosti je pri mladju) ter zaradi povečanih obstoječih pritiskov na gozdove 2 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih Slika 1: Shema povezav med drevesi prek skupnih micelij- skih mrež. Večje oblike so starejša in večja drevesa. Starejša drevesa imajo vlogo vozlišč. Prilagojeno po Simard (2018). Fig. 1: Connections between trees via common mycelial net- works. Larger shapes represent older and larger trees. Older trees act as hubs. Adapted from Simard (2018). v marginalnih okoljih (Pickles in Simard, 2017). Poleg same suše v toplejših in sušnejših razmerah gozdovom grozijo tudi pogostejši požari in napadi žuželk (Seidl in sod., 2017). Medtem ko je bilo opravljenih razmeroma veliko raziskav o vplivu globalnih sprememb na nadze- mne dele najpogostejših evropskih drevesnih vrst, je vpliv na drevesne korenine in mikorizne glive, ki živi- jo v tesnem sožitju z drobnimi koreninami gozdnega drevja, precej neraziskan. Drobne korenine gozdnega drevja, ki jih običajno definiramo kot korenine, tanjše od 2 mm, dosegajo manj kot 2 % drevesne biomase v zmernih in borealnih gozdovih, vendar pa so nadvse aktiven del gozda, saj prek njih poteka absorpcija vode in hranil, s svojim hitrim obratom (angl. turnover rate) pa znatno prispevajo h kroženju ogljika v tleh (Brun- ner in Godbold, 2007). Mikorizne glive so med ključnimi talnimi organizmi za delovanje gozdnih ekosistemov. V evropskih gozdo- vih zmernega pasu je večina sestojnih drevesnih vrst ektomikoriznih (Kraigher in sod., 2013). Pri ektomi- korizi glivni plašč ovija drobne korenine, hife pa pro- dirajo med koreninskimi celicami v obliki mreže, ki jo imenujemo Hartigova mreža. Z izvenmatričnim mice- lijem, ki ga sestavljajo posamezne hife, ter rizomorfi, snopi hif, ki lahko vsebujejo specializirane strukture za transport vode in topljencev, ektomikorizna gliva sega tudi v okoliški substrat (Agerer, 2001) ter ustvarja ve- like skupne micelijske mreže (angl. common mycelial networks), ki povezujejo koreninske sisteme sosednjih ter tudi bolj oddaljenih dreves (Simard in Durall, 2004; Simard in sod., 2012). Skupne micelijske mreže pove- zujejo več dreves iste vrste ali več različnih drevesnih in glivnih vrst. Velikost skupnih micelijskih mrež meri- mo v desetinah metrov, lahko pa ena sama gliva zajema območje velikosti več sto hektarov gozda. Velika stara drevesa, t.i. materinska drevesa, v skupnih micelijskih mrežah delujejo kot vozlišča (slika 1). Skupne micelij- ske mreže vplivajo na vzpostavitev drevesnega mladja, njihovo preživetje, rast, fiziologijo, zdravstveno stanje in kompeticijske sposobnosti. Prek skupnih micelijskih mrež poteka izmenjava virov (ogljik, voda, dušik, fos- for, mikronutrienti), stresnih molekul, alelokemikalij, s pomočjo skupnih micelijskih mrež pa se z ektomikori- znimi glivami kolonizira tudi mladje. Izmenjava virov poteka po principu gradienta vir-ponor. Stresni signali lahko po skupnih micelijskih mrežah potujejo zelo hi- tro, v roku nekaj ur (Gorzelak in sod., 2015). Morfolo- ško lahko ektomikorizne glive glede na izhajajoče hife in rizomorfe razporedimo v različne eksploracijske tipe (npr. kontaktni eksploracijski tip, eksploracijski tip na kratke, srednje ali dolge razdalje, itd.), ki naj bi imeli v tleh različno funkcijo, razlikujejo pa se v tem, kako daleč v okoliški substrat segajo hife oz. rizomorfi (Agerer, 2001). Tako npr. lahko kontaktni eksploracij- ski tip, ki nima izhajajočih hif ter rizomorfov, privze- ma snovi samo prek plašča, ki je v neposrednem stiku z okoliškim substratom, medtem ko eksploracijski tip na dolge razdalje lahko privzema snovi iz okoliškega substrata tudi več decimetrov stran od koreninskega vršička, saj rizomorfi segajo tako daleč (Agerer, 2001). Ektomikorizne glive zagotavljajo v gozdnih ekosi- stemih številne usluge s pomočjo morfoloških, fizio- Acta Sil va e et Ligni 120 (2019), 1–12 3 loških in ekoloških mehanizmov, kot so: kolonizacija večjega volumna tal, kolonizacija manjših por v tleh za- radi manjšega premera glivnih hif v primerjavi z drob- nimi koreninami, povečana površina za absorpcijo hra- nil, sproščanje slabo dostopnih makrohranil, izločanje eksudatov, ki omogočajo večjo dostopnost mikrohranil, spreminjanje pH v mikorizosferi, prerazporejanje vode in hranil v prostoru in času ter vzpostavljanje povezav med viri in ponori ogljika (Kraigher in sod., 2013). Če želimo z večjo natančnostjo predvideti odziv gozdnih ekosistemov na okoljske spremembe v prihodnosti, moramo poznati tudi odziv drobnih korenin v povezavi z mikoriznimi glivami (Staddon in sod., 2003). 2 VPLIV SUŠE NA DROBNE KORENINE DREVES 2 EFFECTS OF DROUGHT ON TREE FINE ROOTS Rastlinam dostop do omejenih virov v tleh omo- gočajo različne strategije, ki jih lahko razdelimo v pet skupin: arhitekturne (razraščanje koreninskega siste- ma, globina koreninjenja), morfološke (premer kore- nin, specifična dolžina korenin), fiziološke (kinetika privzema hranil, respiracija, izločanje eksudatov) in biotske (interakcije s simbiontskimi in drugimi orga- nizmi) (Bardgett in sod., 2014). Variabilnost v značil- nostih koreninskega sistema (angl. root traits) je velika tako med vrstami kot tudi med genotipi, poleg tega pa je koreninski sistem izredno plastičen, kar omogoča, da se rastlina prilagaja spremenljivim razmeram v okolju, še posebej kar se tiče dostopa do hranil in vode (Bardgett in sod., 2014). Posamezni deli koreninskega sistema se pojavljajo v slojih oz. delih tal z različno vla- žnostjo, pri čemer prihaja do pasivnega gibanja vode prek korenin iz vlažnejših proti sušnim delom tal, kar imenujemo hidravlična distribucija (slika 2). Ko se li- stne reže zaprejo in je transpiracija majhna, se vodni potencial rastline poskuša izenačiti z vodnim potenci- Slika 2: Shema hidravlične redistribucije vode v tleh s po- močjo drevesnih korenin (rumene puščice) ter povzetek pri- lagoditev korenin na sušo (pripravila D. Finžgar in T . Mrak). Fig. 2: Hydraulic redistribution of soil water by tree roots (yellow arrows) and summary of adaptation of roots to drought (prepared by D. Finžgar & T . Mrak). 4 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih alom tal, v katerih je najaktivnejši del korenin, zato se tla navlažijo. Najbolj poznan tip hidravlične redistri- bucije je hidravlični dvig, do katerega pride, kadar so globlji deli tal vlažnejši kot površinski (Prieto in sod., 2012). Hidravlični dvig je možen le pri rastlinah, ki so sposobne tvorbe globokega koreninskega sistema, vendar pa imajo od njega lahko koristi tudi sosednje rastline s plitvejšim koreninskim sistemom, npr. kom- binacija gradna (Quercus petraea (Matt.) Liebl.) in bu- kve (Fagus sylvatica L.) (Pretzsch in sod., 2013), bodisi neposredno s privzemom vode, ki jo rastlina z globo- kim koreninskim sistemom sprošča v okolico, bodisi posredno prek mikoriznih gliv (Prieto in sod., 2012). V mešanih sestojih lahko prihaja v sušnih razme- rah do kompeticije med drobnimi koreninami. V me- šanih sestojih bukve in navadne smreke (Picea abies (L.) Karst) so drobne korenine smreke še bliže površju tal kot v čistih sestojih smreke, kjer so potencialno bolj izpostavljene poletni suši, poleg tega pa so manj razve- jene ter imajo manjši delež simbioze z eksploracijski- mi tipi ektomikoriznih gliv na dolge razdalje. Vendar pa je učinek prisotnosti bukve na dostopnost vode za smreko po drugi strani v času spomladanske suše pozi- tiven, saj je v mešanih sestojih bukve in smreke zaradi listopadnosti bukve kompeticija za vodo manjša kot v čistih sestojih smreke. Kompeticiji so izpostavljene samo smreke, ki so v neposredni soseščini bukve, kar pomeni, da je v mešanem gozdu z vidika suše pojavlja- nje smrek v skupinah bolj ugodno od pojavljanja posa- meznih smrek (Goisser in sod., 2016). Tako kot nadzemni deli, se tudi korenine odzivajo na stresne razmere suše po načelu dveh strategij - iz- ogibanja in tolerance. Pri izogibanju suši gre za uskla- jevanje vodnega statusa nadzemnega in podzemnega dela, lovljenje ravnotežja med izgubo vode in njenim privzemom. Kratkoročno se drevo izogiba pretirani izgubi vode z zapiranjem listnih rež, dolgoročno pa z zmanjšano rastjo nadzemnega dela, ki vodi v poveča- nje razmerja med koreninami in nadzemnim delom. Privzem vode v korenine se lahko izboljša s tvorbo ve- čjega števila drobnih korenin ter tvorbo globokih kore- nin, ki iščejo vire vode (Brunner in sod., 2015). Mehanizmi tolerance omogočajo neprekinjen tran- sport vode, izmenjavo plinov in preživetje celic pri majhnih vodnih potencialih, kar drevo doseže s prila- goditvijo ozmotskega potenciala v koreninah s kopi- čenjem topljencev, s povečanjem odpornosti na kavi- tacijo z učvrstitvijo celičnih sten prevodnih tkiv ter z zmanjšanjem premera ksilemskih prevodnih elemen- tov, ter s sposobnostjo celic, še posebej meristemskih, da ostanejo žive (Vilagrosa in sod., 2012; Brunner in sod., 2015). Korenine so bolj občutljive za kavitacijo kot deblo, tako pri listavcih kot pri iglavcih, še posebej pa so kavitaciji izpostavljene tanjše korenine. Drevesa iste vrste, ki rastejo v sušnejših razmerah, so bolj od- porna proti kavitaciji kot drevesa, ki rastejo v razme- rah, kjer je vlage ves čas dovolj. V ekstremnih sušnih razmerah naj bi bila popolna kavitacija v tanjših kore- ninah zaščitni mehanizem, ki drevo hidravlično izolira od vedno bolj suhih okoliških tal. Dokler ostajajo listne reže zaprte, se tako prepreči, da bi v deblu nastal tako nizek tlak, da bi prišlo v njem do popolne kavitacije. Po končanem obdobju suše se vzpostavi nova rast ko- renin, tako da se hidravlična prevodnost zopet pove- ča, kavitirane prevodne poti pa se zapolnijo (Sperry in Ikeda, 1997). Pod vplivom suše se zmanjša pojavljanje lenticel v olesenelih drobnih koreninah, medtem ko je njen vpliv na pojavljanje branik v olesenelih drobnih koreninah različen med vrstami. Pri črničevju (Quercus ilex L.) se je pojavljanje branik v olesenelih drobnih ko- reninah debeline 2 mm zmanjšalo, pri dobu (Quercus robur L.) pa povečalo (Mrak in sod., 2019). V drobnih koreninah sadik različnih provenienc bu- kve je suša povzročila upad količine ogljika, medtem ko je pri nekaterih proveniencah povzročila povečanje ko- ličine dušika, pri drugih pa ni bilo sprememb. Posledič- no se je pri vseh proveniencah zmanjšalo razmerje med C in N v drobnih koreninah (Dounavi in sod., 2016). Življenjska doba drobnih korenin se v sušnih raz- merah skrajša, razen takrat, kadar prihaja do hidra- vlične redistribucije vlage iz delov tal z večjo vlažno- stjo v dele tal z manjšo vlažnostjo (McCormack in Guo, 2014). Poleg tega se zmanjša biomasa drobnih korenin, njihova dolžina ter frekvenca koreninskih vršičkov, na nekatere druge parametre, kot je specifična dolžina ko- renin, gostota koreninskega tkiva ter indeks korenin- ske površine, pa naj suša ne bi imela vpliva. Vendar na te rezultate vpliva odločitev, katere debelinske razrede vključiti v definicijo drobnih korenin. Raziskovalci, ki so mejo postavili pri 0,5 mm, namesto pri 2 mm, so v primeru suše ugotovili povečano biomaso drobnih korenin, njihova specifična dolžina je bila povečana, prav tako tudi gostota koreninskega tkiva, povprečni premer ter vsebnost dušika pa sta se zmanjšala (Brun- ner in sod., 2015). V sadikah doba (Q. robur) se je delež najtanjših korenin (debelinski razred 0,0–0,1 mm) pod vplivom suše značilno povečal, medtem ko se je delež debelejših drobnih korenin zmanjšal. Pri isti vrsti se je povprečna debelina drobnih korenin zmanjšala za 8,49 % (Mrak in sod., 2019). Pri črničevju (Q. ilex) so drobne korenine, ki zrastejo v suhem mediteranskem poletju, tanjše (Montagnoli in sod., 2019). V sušnih razmerah se v koreninah sproži sinteza po- večanih količin suberina in lignina. Suberin je v endo- Acta Sil va e et Ligni 120 (2019), 1–12 5 dermu in eksodermu korenin ter v peridermu sekun- darno odebeljenih korenin. Suberinizacija zmanjšuje izgubo vode iz korenin, še posebej v sušnih razmerah, in izboljšuje učinkovitost izrabe vode. Z lignifikacijo celičnih sten se poveča njihova mehanska odpornost ter zmanjša izguba vode iz celic ter njihova dehidracija. Zaradi povečanih količin suberina in lignina v koreni- nah pride ob suši do sprememb v količini in razgradnji odmrle organske snovi v tleh ter s tem do sprememb v hitrosti obrata organske snovi v tleh. Zaradi suberi- na organska snov v tleh postane hidrofobna, lignin pa so sposobni razgrajevati le nekateri mikroorganizmi v tleh – glive rjave trohnobe in aktinobakterije, kjer pa lahko pride do vpliva suše na (encimsko) aktivnost teh mikroorganizmov. Poleg tega je za razgradnjo lignina v tleh ključno tudi razmerje med količino lignina in duši- ka (Brunner in sod., 2015). 3 VPLIV SUŠE NA SIMBIOZO Z EKTOMIKORI- ZNIMI GLIVAMI 3 EFFECTS OF DROUGHT ON SYMBIOSIS WITH ECTOMYCORRHIZAL FUNGI S pomočjo ekstramatričnega micelija se lahko voda prenaša od rastlin z dostopom do vira vode v globljih plasteh tal do rastlin, ki jim vode primanjkuje (Eger- ton-Warburton in sod., 2007). Ta način oskrbe z vodo je zelo pomemben za preživetje drevesnega mladja (Lehto in Zwiazek, 2011). V sušnih gozdovih je do- stop do micelijskih mrež materinskih dreves ključen za vzpostavitev mladja. Mladje, ki raste znotraj mice- lijskih mrež materinskih dreves, je večje in bolj učin- kovito pri izrabi vode. Združba ektomikoriznih gliv pri mladju je zelo podobna kot pri sosednjih odraslih drevesih. Povezava v micelijske mreže odraslih dreves mora nastopiti še pred pričetkom sušnega obdobja, zato imajo tu prednost lokalne, suši prilagojene prove- nience, ki kalijo zgodaj in se hitro povežejo v micelij- ske mreže odraslih dreves (Pickles in Simard, 2017). Izbira provenience ter način ravnanja s sadikami je v razmerah, kjer pričakujemo hude suše, bolj pomemb- na kot zanašanje na podporo skupnih micelijskih mrež. Sadike iste provenience, vzgojene v drevesnicah, imajo v takih razmerah prednost pred naravno rege- neracijo iz semen (Bingham in Simard, 2013). Micelij, ki ima dostop do vira vode, lahko preživi v zelo suhih tleh (do -2,5 MPa vodnega potenciala tal ali celo manj). Hife so funkcionalno aktivne celo po 68–77 dneh suše in sposobne rasti po 70–80 dneh suše. Pri transportu vode na daljše razdalje igrajo glavno vlogo rizomorfi, ki omogočajo transport vode po simplastu (Querejeta in sod., 2003). Rizomorfe tvorijo glive s hidrofobnimi celičnimi stenami, glive s hidrofilnimi stenami pa tran- sportirajo vodo po apoplastu. Zelo malo je znanega o tem, ali obstaja kakšna povezava med lastnostmi celič- nih sten mikoriznih gliv ter njihovo odpornostjo proti suši (Lehto in Zwiazek, 2011). Ko so primerjali eksplo- racijske tipe ektomikoriznih gliv v sestoju obmorskega bora (Pinus pinaster Aiton) v vlažnejših in bolj sušnih razmerah, so ugotovili, da so eksploracijski tipi na dol- ge in kratke razdalje značilno bolj pogosti v sušnih tleh, kontaktni eksploracijski tipi pa v vlažnejših razmerah. Pogostnost eksploracijskih tipov na srednje razdalje je bila približno enaka (Bakker in sod., 2006). Pickles in Simard (2017) navajata, da ob suši pri mladju posta- nejo pogostejši tipi na srednje (Amphinema, Boletus, Cortinarius, Tomentella, Tricholoma) in dolge razdalje (Rhizopogon, Suillus). Ugotovitve o vplivih suše na kolonizacijo z ektomi- koriznimi glivami ter strukturo glivne združbe so zelo različne, kar lahko pripišemo razlikam v poskusnih razmerah (npr. trajanje suše in njena intenziteta) ter razlikam v izbranih ektomikoriznih inokulih v primeru uporabe inokuliranih sadik. Globalno naj bi bila koloni- zacija z ektomikoriznimi glivami manjša v okoljih, kjer zasledimo veliko sezonskost padavin (Soudzilovskaia in sod., 2015). V naravnih razmerah naj bi kolonizacija z ektomikoriznimi glivami sledila hipotezi zmernega stresa gostiteljske rastline, z večjo stopnjo kolonizaci- je v razmerah zmernega stresa ter manjše v razmerah kroničnega stresa. Manjša kolonizacija z ektomikori- znimi glivami v razmerah hude suše, ko je stopnja foto- sinteze majhna, pomaga pri ohranjanju omejenih zalog ogljika, ki bi jih rastlina sicer namenila glivi v zameno za hranila, za preživetje rastline (Swaty in sod., 2004). V sestojih hrasta vrste Quercus agrifolia Née, ki jih je prizadela večletna suša, je bila kolonizacija z ektomi- koriznimi glivami zmanjšana (Querejeta in sod., 2003). Primerjava sestojev bora vrste Pinus muricata D. Don v razmerah 7-odstotne in 13-odstotne talne vlage je po- kazala, da je kolonizacija večja v razmerah 13-odstotne talne vlage (Kennedy in Peay, 2007). Po drugi strani pa zmerna suša ni vplivala na kolonizacijo pri sadikah bu- kve (Fagus sylvatica L.) z naravno obstoječo mikorizo (Shi in sod., 2002) ter pri sadikah bukve, inokuliranih s petimi vrstami mikoriznih gliv (Pena in Polle, 2014). Kolonizacija se tudi ni spremenila v sušnem poskusu na sadikah hrasta, prav tako ni bilo značilnega vpliva na vrstno pestrost (Mrak in sod., 2019). Po drugi strani pa lahko na vrstno pestrost vpliva genotip rastline. Vr- stna pestrost pri genotipu bora (Pinus edulis Engelm.), odpornega proti suši, je bila dvakrat večja kot pri geno- tipu, občutljivem za sušo. V primeru, ko sta bila oba ge- notipa izpostavljena sušnim razmeram, se je struktura ektomikorizne glivne združbe pri genotipu, občutlji- 6 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih vem za sušo, spremenila, pri genotipu, odpornem proti suši, pa ne (Patterson in sod., 2019). Pogosto ob suši pride do sprememb v pogostnosti nekaterih vrst ektomikoriznih gliv (Shi in sod., 2002; Swaty in sod., 2004; Herzog in sod., 2013; Pena in Pol- le, 2014; Mrak in sod., 2019), npr. pogostnost ektomi- koriznih gliv iz rodu Tomentella je ob suši upadla pri genotipu bora, občutljivega za sušo (Patterson in sod., 2019), prav tako pa je njihova pogostnost upadla pri sadikah hrastov, izpostavljenih suši, narasla pa je pogo- stnost vrste Sphaerosporella brunnea (Alb. & Schwein.) Svrcek & Kubicka ter vrste iz rodu Thelephora (Mrak in sod., 2019). Sprememba strukture glivne združbe proti na sušo odpornim ektomikoriznim glivam (oz. glivam, ki se zadovoljijo z zelo omejenim dotokom ogljika) bi bila za gostiteljsko rastlino ugodna/koristna, saj bi gli- va rastlini potencialno še naprej zagotavljala različne usluge. V stresnih razmerah je privzem makrohranil (N in P) v rastlino moten, ektomikorizne glive pa lahko to omejitev vsaj v določeni meri odstranijo. V laboratorijskih razmerah so ugotovili, da se miko- rizna vrsta Cenococcum geophilum Fr. (slika 3) na sušni stres odziva v manjši meri kot druge mikorizne glive (Jany in sod., 2003; di Pietro in sod., 2007). Ta vrsta zagotavlja, da mikorizirane drobne korenine ostajajo funkcionalne, kar omogoča takojšen odziv na vir vode po končanem sušnem obdobju (Jany in sod., 2003). Povečano kolonizacijo z vrsto C. geophilum so pogo- sto zasledili v različnih stresnih razmerah, vključno s sušo (Bakker in sod., 2006; Grebenc in Kraigher, 2007; Kraigher in sod., 2007; Kraigher in sod., 2011). Pod vplivom suše se regulacija dveh tipov akvaporinov pri tej vrsti glive v ektomikorizi spremeni, vendar pa raz- iskovalcem za zdaj značilne pozitivne povezave med fiziološkimi parametri drevesne vrste in mikorizacije z glivo C. geophillum še ni uspelo dokazati (Peter in sod., 2016). Pogostnost te vrste naj bi se povečala tudi v raz- merah povišanih temperatur zraka in naj bi bila v po- zitivni korelaciji z rastjo nadzemnega dela (Herzog in sod., 2013). Ker so hife vrste C. geophilum melanizira- ne, so po odmrtju zelo odporne proti razgradnji v tleh, saj je melanin kompleksen polimer. Kopičenje melani- ziranih ostankov v tleh zaradi nezmožnosti razgradnje prispeva k povečanju količine organske snovi v tleh (SOM). Na zmožnost razgradnje melaniziranih ostan- kov močno vpliva tudi razmerje med količino melanina in dušika, podobno kot v primeru korenin med količino lignina in dušika (Fernandez in Koide, 2014). Encimska aktivnost ektomikorize, ki je povezana s sproščanjem C, N in P iz kompleksnih organskih mo- lekul v tleh, je večja kot pri nemikoriznih koreninah, in ostane povečana kljub omejenemu dostopu do vode. Zelo je odvisna od vrste ektomikorizne glive in upada po naslednjem vrstnem redu: Suillus granulatus (L.) Roussel > Rhizopogon roseolus (Corda) Th. Fr. > Paxil- lus involutus (Batsch) Fr. > C. geophilum (Kipfer in sod., 2012). Oskrba z N v obliki NH 4 + , ki jo vrsta C. geophilum zagotavlja v razmerah suše, je zelo majhna v primerjavi z drugimi ektomikoriznimi vrstami. Sposobnost za pri- vzem N iz suhih tal naj bi bila povezana tudi z drugimi okoljskimi parametri (npr. osončenost) (Pena in Polle, 2014). Za vrsto C. geophilum so ugotovili tudi, da se en- Slika 3: Ektomikorizna gliva Cenococcum geophilum Fr. Fig. 3: Ectomycorrhizal fungus Cenococcum geophilum Fr. Acta Sil va e et Ligni 120 (2019), 1–12 7 cimska aktivnost poveča le v kombinaciji suše s poviša- nimi temperaturami, zelo pa naj bi bila odvisna tudi od vrste gostiteljske rastline (Herzog in sod., 2013). Z vidika rastline imajo ektomikorizne glive v sušnih razmerah veliko pozitivnih učinkov. Izboljša se vodni potencial rastline, ohranja se hidravlična prevodnost, fotosinteza je večja kot pri nemikoriznih sadikah, zmanjšani so negativni učinki suše na rast podzemnih in nadzemnih delov, struktura lesa je manj prizadeta, smrt koreninskih vršičkov zakasnjena, vsebnost P v listih manj zmanjšana ter oksidativni stres manjši (Or- tega in sod., 2004; Walker in sod., 2004; Alvarez in sod., 2009a; Alvarez in sod., 2009b; Kipfer in sod., 2010; Be- niwal in sod., 2010; Danielsen in Polle, 2014). V sušnih razmerah se lahko poveča ozmotski potencial miko- riznih vršičkov zaradi kopičenja topnih sladkorjev in sladkornih alkoholov – poliolov (produkti gliv) z na- menom ohranjanja privzema vode (Shi in sod., 2002). 4 SKLEPI 4 CONCLUSIONS Drevesa imajo zelo plastičen koreninski sistem, kar omogoča različne prilagoditve na sušne razmere. Prilagoditve se kažejo na področju rasti in razvoja ko- renin, morfologije, anatomskih in biokemijskih lastno- stih ter biotskih interakcij (slika 2). Kljub temu, da so glavni mehanizmi prilagoditev poznani, ostaja na tem področju še veliko neznank, sploh na področju biotskih in abiotskih interakcij, kar onemogoča takojšnji prenos teoretičnih znanj v načrtovanje gojenja gozdov. Zara- di klimatskih sprememb v smeri toplejših in sušnejših razmer bo najbolj na udaru drevesno mladje, ki še nima razvitega obsežnega koreninskega sistema. Čeprav lah- ko odrasla drevesa prek skupnih micelijskih mrež pod- pirajo obstoj mladja, bo v primeru pričakovanih hudih suš zelo pomembna izbira ustreznih provenienc sadik. 5 ZAHVALA 5 ACKNOWLEDGEMENTS Prispevek je nastal v okviru infrastrukturnega pro- jekta FP7 Euforinno, ki ga je financirala Evropska unija, ter raziskovalnega programa št. P4-0107, ki ga sofinan- cira Javna agencija za raziskovalno dejavnost Republi- ke Slovenije iz državnega proračuna. 6 VIRI 6 REFERENCES Agerer R. 2001. Exploration types of ectomycorrhizae. Mycorrhiza, 11, 2: 107–114. Alvarez M., Huygens D., Fernandez C., Gacitúa Y., Olivares E. in sod. 2009a. Effect of ectomycorrhizal colonization and drought on re- active oxygen species metabolism of Nothofagus dombeyi roots. Tree Physiology, 29, 8: 1047–1057. Alvarez M., Huygens D., Olivares E., Saavedra I., Alberdi M. in sod. 2009b. Ectomycorrhizal fungi enhance nitrogen and phospho- rus nutrition of Nothofagus dombeyi under drought conditions by regulating assimilative enzyme activities. Physiologia Planta- rum, 136, 4: 426–436. Bakker M.R., Augusto L., Achat D.L. 2006. Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites. Plant and Soil, 286, 1–2: 37–51. Bardgett R.D., Mommer L., De Vries F.T . 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution, 29, 12: 692–699. Beniwal R.S., Langenfeld-Heyser R., Polle A. 2010. Ectomycorrhi- za and hydrogel protect hybrid poplar from water deficit and unravel plastic responses of xylem anatomy. Environmental and Experimental Botany, 69, 2: 189–197. Bingham M.A., Simard S.W. 2013. Seedling genetics and life histo- ry outweigh mycorrhizal network potential to improve conifer regeneration under drought. Forest Ecology and Management, 287: 132–139. Briffa K.R., van der Schrier G., Jones P .D. 2009. Wet and dry summers in Europe since 1750: evidence of increasing drought. Internati- onal Journal of Climatology, 29, 13: 1894–1905. Brunner I., Godbold D.L. 2007. Tree roots in a changing world. Jour- nal of Forest Research, 12, 2: 78–82. Brunner I., Herzog C., Dawes M., Arend M., Sperisen C. 2015. How tree roots respond to drought. Frontiers in Plant Science, 6: 1–16. Danielsen L., Polle A. 2014. Poplar nutrition under drought as affec- ted by ectomycorrhizal colonization. Environmental and Experi- mental Botany, 108: 89–98. di Pietro M., Churin J.L., Garbaye J. 2007. Differential ability of ecto- mycorrhizas to survive drying. Mycorrhiza, 17, 6: 547–550. Dounavi A., Netzer F., Čelepirović N., Ivanković M., Burger J. in sod. 2016. Genetic and physiological differences of European beech provenances (F. sylvatica L.) exposed to drought stress. Forest Ecology and Management, 361: 226–236. Egerton-Warburton L.M., Querejeta J.I., Allen M.F. 2007. Common mycorrhizal networks provide a potential pathway for the trans- fer of hydraulically lifted water between plants. Journal of Expe- rimental Botany, 58, 6: 1473–1483. Fernandez C.W., Koide R.T . 2014. Initial melanin and nitrogen con- centrations control the decomposition of ectomycorrhizal fun- gal litter. Soil Biology and Biochemistry, 77, 150–157. Goisser M., Geppert U., Rötzer T ., Paya A., Huber A. in sod. 2016. Does belowground interaction with Fagus sylvatica increase drought susceptibility of photosynthesis and stem growth in Picea abies? Forest Ecology and Management, 375: 268–278. Gorzelak M.A., Asay A.K., Pickles B.J., Simard S.W. 2015. Inter-plant communication through mycorrhizal networks mediates com- plex adaptive behaviour in plant communities. AoB PLANTS, 7: plv050. Grebenc T ., Kraigher H. 2007. Changes in the community of ecto- mycorrhizal fungi and increased fine root number under adult beech trees chronically fumigated with double ambient ozone concentration. Plant Biology, 9, 2: 279–287. Hanel M., Rakovec O., Markonis Y., Máca P ., Samaniego L. in sod. 2018. Revisiting the recent European droughts from a long-term per- spective. Scientific Reports, 8, 1: 9499. Herzog C., Peter M., Pritsch K., Günthardt-Goerg M.S., Egli S. 2013. Drought and air warming affects abundance and exoenzyme profiles of Cenococcum geophilum associated with Quercus ro- bur, Q. petraea and Q. pubescens. Plant Biology, 15, 230–237. Jany J.L., Martin F., Garbaye J. 2003. Respiration activity of ectomy- corrhizas from Cenococcum geophilum and Lactarius sp. in rela- tion to soil water potential in five beech forests. Plant and Soil, 255, 2: 487–494. 8 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih Kennedy P ., Peay K. 2007. Different soil moisture conditions chan- ge the outcome of the ectomycorrhizal symbiosis between Rhi- zopogon species and Pinus muricata. Plant and Soil, 291, 1–2: 155–165. Kipfer T ., Egli S., Ghazoul J., Moser B., Wohlgemuth T . 2010. Suscep- tibility of ectomycorrhizal fungi to soil heating. Fungal Biology, 114, 5–6: 467–472. Kipfer T ., Wohlgemuth T ., van der Heijden M.G.A., Ghazoul J., Egli S. 2012. Growth response of drought-stressed Pinus sylvestris see- dlings to single- and multi-species inoculation with ectomycorr- hizal fungi. PLoS ONE, 7, 4: e35275. Kirtman B., Power S.B., Adedoyin J.A., Boer G.J., Bojariu R. in sod. 2013. Near-term climate change: Projections and predictability. V: Climate Change 2013: The Physical Science Basis. Contribu- tion of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker T .F., Qin D., Plattner G.-K., Tignor M., Allen S.K., Boschung J., Nauels A., Xia Y., Bex V., Midgley P .M. (ur.). Cambridge, United Kingdom and New York, NY, USA, Cambridge University Press: 953–1028. Kraigher H., Al Sayegh-Petkovšek S. 2011. Mycobioindication of stress in forest ecosystems. V: Rai M., Varma A. (ur.). Diversity and biotechnology of ectomycorrhizae. Soil biology, vol. 25. Hei- delberg, New York, Springer: 301–322. Kraigher H., Al Sayegh-Petkovšek S., Grebenc T ., Simončič P . 2007. Types of ectomycorrhiza as pollution stress indicators: case studies in Slovenia. Environmental monitoring and Assessment 128, 1: 31–45. Kraigher H., Bajc M., Grebenc T . 2013. Chapter 8 - Mycorrhizosphere Complexity. V: Developments in Environmental Science. Matys- sek R., Clarke N., Cudlin P ., Mikkelsen T .N., Tuovinen J.P ., Wieser G., Paoletti E. (ur.). Developments in Environmental Science, El- sevier: 151–177. Lehto T ., Zwiazek J.J. 2011. Ectomycorrhizas and water relations of trees: a review. Mycorrhiza, 21, 2: 71–90. McCormack M.L., Guo D. 2014. Impacts of environmental factors on fine root lifespan. Frontiers in Plant Science, 5: 1–11. Montagnoli A, Dumroese R.K., Terzaghi M., Onelli E., Scippa G.S., Chi- atante D. 2019. Seasonality of fine root dynamics and activity of root and shoot vascular cambium in a Quercus ilex L. forest (Italy). Forest Ecology and Management, 431: 26–34. Mrak T ., Štraus I., Grebenc T ., Gričar J., Hoshika Y., Carriero G., Paoletti E., Kraigher H. 2019. Different belowground responses to eleva- ted ozone and soil water deficit in three European oak species (Quercus ilex, Q. pubescens and Q. robur). Science of the Total En- vironment, 651: 1310–1320. Ortega U., Duñabeitia M., Menendez S., Gonzalez-Murua C., Majada J. 2004. Effectiveness of mycorrhizal inoculation in the nursery on growth and water relations of Pinus radiata in different water regimes. Tree Physiology, 24, 1: 65–73. Patterson A., Flores-Rentería L., Whipple A., Whitham, T ., Gehring C. 2019. Common garden experiments disentangle plant gene- tic and environmental contributions to ectomycorrhizal fungal community structure. New Phytologist, 221: 493–502. Pena R., Polle A. 2014. Attributing functions to ectomycorrhizal fungal identities in assemblages for nitrogen acquisition under stress. Isme Journal, 8, 2: 321–330. Peter M., Kohler A., Ohm R.A., Kuo A., Krützmann J. in sod. 2016. Ecto- mycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nature Communicati- ons, 7: 12662. Pickles B.J., Simard S.W. 2017. Chapter 18 - Mycorrhizal networks and forest resilience to drought. V: Mycorrhizal mediation of soil. Johnson N.C., Gehring C., Jansa J. (ur.). Elsevier: 319–339. Pretzsch H., Schütze G., Uhl E. 2013. Resistance of European tree species to drought stress in mixed versus pure forests: evidence of stress release by inter-specific facilitation. Plant Biology, 15: 483–495. Prieto I., Armas C. Pugnaire F.I. 2012. Water release through plant roots: new insights into its consequences at the plant and ecosy- stem level. New Phytologist, 193, 4: 830–841. Querejeta J., Egerton-Warburton L., Allen M. 2003. Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying. Oecologia, 134, 1: 55–64. Rajczak J., Schär C. 2017. Projections of future precipitation extre- mes over Europe: A multimodel assessment of climate simula- tions. Journal of Geophysical Research: Atmospheres, 122, 20: 10773–10800. Ruosteenoja K., Markkanen T ., Venäläinen A., Räisänen P ., Peltola H. 2018. Seasonal soil moisture and drought occurrence in Europe in CMIP5 projections for the 21st century. Climate Dynamics, 50, 3: 1177–1192. Seidl R., Thom D., Kautz M., Martin-Benito D., Peltoniemi M. in sod. 2017. Forest disturbances under climate change. Nature Climate Change, 7: 395. Shi L.B., Guttenberger M., Kottke I., Hampp R. 2002. The effect of drought on mycorrhizas of beech (Fagus sylvatica L.): changes in community structure, and the content of carbohydrates and nitrogen storage bodies of the fungi. Mycorrhiza, 12, 6: 303–311. Simard S.W. 2018. Mycorrhizal networks facilitate tree communica- tion, learning, and memory. V: Memory and learning in plants. Signaling and communication in plants. Baluska F., Gagliano M., Witzany G. (ur.). Cham, Springer: 191–213. Simard S.W., Beiler K.J., Bingham M.A., Deslippe J.R., Philip L.J. in sod. 2012. Mycorrhizal networks: Mechanisms, ecology and model- ling. Fungal Biology Reviews, 26, 1: 39–60. Simard S.W., Durall D.M. 2004. Mycorrhizal networks: a review of their extent, function, and importance. Canadian Journal of Bo- tany, 82, 8: 1140–1165. Soudzilovskaia N.A., Douma J.C., Akhmetzhanova A.A., Bodegom P .M., Cornwell W.K. in sod. 2015. Global patterns of plant root mycor- rhizal colonization intensity. Global Ecology and Biogeography, 24: 371–382. Sperry J.S., Ikeda T . 1997. Xylem cavitation in roots and stems of Dou- glas-fir and white fir. Tree Physiology, 17: 275–280. Staddon P .L., Thompson K., Jakobsen I., Grime J.P ., Askew A.P . in sod. 2003. Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Global Change Biology, 9, 2: 186–194. Swaty R.L., Deckert R.J., Whitham T .G., Gehring C.A. 2004. Ectomy- corrhizal abundance and community composition shifts with drought: Predictions from tree rings. Ecology, 85, 4: 1072–1084. Vilagrosa A., Chirino E., Peguero-Pina J.J., Barigah T .S., Cochard H. in sod. 2012. Xylem cavitation and embolism in plants living in water-limited ecosystems. V: Plant Responses to Drought Stress. Aroca R. (ur.). Berlin, Heidelberg, Springer: 63–109. Vogel M.M., Orth R., Cheruy F., Hagemann S., Lorenz R. in sod. 2017. Regional amplification of projected changes in extreme tempe- ratures strongly controlled by soil moisture-temperature feed- backs. Geophysical Research Letters, 44, 3: 1511–1519. Walker R.F., McLaughlin S.B., West D.C. 2004. Establishment of sweet birch on surface mine spoil as influenced by mycorrhizal inocu- lation and fertility. Restoration Ecology, 12, 1: 8–19. Acta Sil va e et Ligni 120 (2019), 1–12 9 1 INTRODUCTION The frequency of summer drought events in some parts of Europe has increased as a consequence of in- creasing temperatures (Briffa et al., 2009; Hanel et al., 2018). It is expected that temperatures and the fre- quency and intensity of heat waves will continue to increase in the future (Kirtman et al., 2013; Vogel et al., 2017), directly affecting soil moisture and exacer- bating the effects of a potential reduction in precipita- tion. In the future mean summer precipitation in the Mediterranean and Central Europe is predicted to dec- rease, and extreme events are expected to occur more frequently (Rajczak and Schär, 2017). Moisture in sur- face soil layers is predicted to decrease over the whole year in Southern Europe, and over summer and autumn in Central and Western Europe. Periods of very low soil moisture levels are expected to increase in frequen- cy (Ruosteenoja et al., 2017). Feedback between soil moisture and air temperature additionally enhances temperature extremes (Vogel et al., 2017). Low soil hu- midity reduces evapotranspiration and increases heat flux, thus promoting the occurence of higher air tem- peratures. On the other hand, higher air temperatures increase water vapour deficit, which contributes to the persistence of evapotranspiration despite decreasing soil moisture (Ruosteenoja et al., 2017). These chan- ges will result in substantial negative effects on forest ecosystems and their biogeochemical cycling. The in- creasing frequency of extreme weather events will con- tribute to forest mortality and changes in forest com- munities due to greater sensitivity of tree seedlings to extreme weather events (tree seedlings experience the highest mortality rates) and increasing pressures on forests in marginal environments (Pickles and Simard, 2017). Apart from drought, forests under warmer and drier conditions will be prone to more frequent forest fires and insect attacks (Seidl et al., 2017). While there are a great deal of research data available on the effects of drought on the aboveground parts of common Euro- pean tree species, tree roots and ectomycorrhizal fungi living in symbiosis with tree fine roots still remain rela- tively unexplored. Tree fine roots, which are usually de- fined as roots thinner than 2 mm in diameter, amount to less than 2 % of tree biomass in boreal and temper- ate forests. Nevertheless, they are an extremely active part of the forest ecosystem, as they absorb water and nutrients and contribute to carbon cycling because of their quick turnover rate (Brunner and Godbold, 2007). Mycorrhizal fungi are among the key soil organisms for the functioning of forest ecosystems. In European temperate forests, the majority of stand forming tree species are ectomycorrhizal (Kraigher et al., 2013). In ectomycorrhiza the fungal mantle ensheaths the tree fine root, and the hyphae penetrate between the cells of the root cortex and form a Hartig net. Via extramatrical mycelium comprised of hyphae and/or rhizomorphs (i.e. bundles of hyphae that may contain specialized structures for transport of water and solutes), ectomyc- orrhizal fungi grow in the surrounding substrate (Ager- er, 2001) and create huge common mycelial networks connecting the tree root systems of neighbouring and even more distant trees (Simard and Durall, 2004; Si- mard et al., 2012). Common mycelial networks (CMN) connect trees of the same species or different tree and fungal species. CMN extend over tens of meters, and in some cases a single fungus can extend across hundreds of hectares of forest. In CMN large old trees, i.e. “moth- er trees”, act as hubs (Figure 1). CMN affect the estab- lishment of tree seedlings and their survival, growth, physiology, health status and competitive ability. Via CMN, exchange of resources (carbon, water, nitrogen, phosphorus, micronutrients), stress molecules and al- lelochemicals occurs. Tree seedlings are colonized with ectomycorrhizal fungi via this pathway. Resource ex- change follows the source-sink gradient. Stress signals can travel through CMN very quickly, in a time span of a few hours (Gorzelak et al., 2015). Ectomycorrhizal hyphae or rhizomorphs grow to different extents into surrounding substrate, thus forming morphologically distinct exploration types of ectomycorrhizae (e.g. con- tact exploration type and short, medium and long dis- tance exploration types), with some evidence of their different functional roles (Agerer, 2001). For example, the contact exploration type, which is characterized by a smooth mantle and only a few emanating hyphae, takes up substances mainly via the mantle, which is in close contact with the surrounding substrate, while the long distance exploration type exploits substrate which is several decimetres away through extensive rhizo- morphs (Agerer, 2001). Ectomycorrhizal fungi, with their morphological, physiological and ecological mechanisms, provide nu- merous benefits to forest ecosystems, such as coloni- zation of larger soil volumes, colonization of tiny soil pores due to the smaller diameter of fungal hyphae compared to fine roots, increased nutrient absorption surface, release of poorly available macronutrients, se- cretion of exudates that improve availability of micro- nutrients, changes in soil pH in the mycorhizosphere, redistribution of water and nutrients in time and space, and the establishment of connections between sources and sinks of carbon (Kraigher et al., 2013). To be able to predict the response of forest ecosystems to future en- vironmental changes with greater accuracy, it is neces- 10 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih sary to understand the response of fine roots in connec- tion with ectomycorrhizal fungi (Staddon et al., 2003). 2 EFFECTS OF DROUGHT ON TREE FINE ROOTS To assure access to limited resources belowground, plants have developed different strategies for their belo- wground parts. These can be classified into five groups: architectural (e.g. ramification of root system, depth of rooting), morphological (e.g. root diameter, specific root length) and physiological (e.g. nutrient uptake ki- netics, respiration, exudation) (Bardgett et al., 2014). Root trait variability among species and genotypes is huge, and above all, the root system is extremely pla- stic. The plasticity of the root system enables plants to adapt to variable environmental conditions, particular- ly with respect to water and nutrient access (Bardgett et al., 2014). Separate parts of the root system are loca- ted in soil layers or areas with different moisture levels, whereby water is passively distributed from moist to dry soil areas via tree roots. This process is called hy- draulic distribution (Figure 2). When leaf stomata clo- se and transpiration is minimal, plant water potential tends to equal soil water potential in areas where the most active roots are located, thereby wetting the dry soil in the surroundings. The most known type of hy- draulic distribution is hydraulic lift, which occurs when deeper soil layers contain higher moisture levels than the surface soil (Prieto et al., 2012). Hydraulic lift can occur only in trees that form a deep root system, but also benefits neighbouring plants with shallower roots, e.g. combination of sessile oak (Quercus petraea (Matt.) Liebl.) and common beech (Fagus sylvatica L.) (Pretz- sch et al., 2013), either directly via uptake of water that the tree with the deep root system releases into soil or indirectly via mycorrhizal fungi (Prieto et al., 2012). In mixed stands competition among fine roots of different species can occur. In comparison to pure Norway spruce (Picea abies (L.) Karst) stands, the fine roots of Norway spruce in stands mixed with common beech are pushed towards the soil surface where they are potentially more prone to summer drought. In ad- dition, spruce roots in mixed stands are less ramified and less colonized by long distance exploration types of ectomycorrhizal fungi. On the other hand, during spring drought, the presence of beech is beneficial for spruce, as there is less competition for water in mixed stands compared to pure spruce stands due to the de- ciduous nature of beech. Competition occurs only in spruce that are in the immediate vicinity of beech, whi- ch means that from the viewpoint of drought mitiga- tion, spruce groups are more favourable compared to single spruce trees (Goisser et al., 2016). Similar to the aboveground parts, tree roots re- spond to drought by using either avoidance or tole- rance strategies. In drought avoidance water status between the belowground and aboveground parts is adjusted, balancing between water uptake and loss. In the short term, the tree avoids water loss by closing the leaf stomata, and in the longer term by reducing the growth of aboveground parts, leading to an increased root to shoot ratio. Water uptake can improve with the formation of a larger number of fine roots and deep roots seeking sources of water (Brunner et al., 2015). Mechanisms of tolerance maintain continuous wa- ter transport, gas exchange and cell survival even at low water potentials, which is achieved through the adjust- ment of osmotic potential in roots with solute accumu- lation, increased resistance to cavitation through the strengthening of cell walls and reduction of xylem ves- sel diameter, and the ability of cells, particularly meris- tematic cells, to stay alive (Vilagrosa et al., 2012; Brun- ner et al., 2015). Roots, and fine roots in particular, are more prone to cavitation compared to the stem, both in broadleaves and conifers. Trees that grow in drier conditions are more resistant to cavitation compared to trees of the same species that grow under conditions of constant adequate moisture. Under extreme drought, cavitation of thinner roots protects the tree through hy- draulic isolation from the surrounding drying soil. As long as leaf stomata remain closed, hydraulic isolation by cavitation in thinner roots prevents complete cavi- tation in the stem. When the drought is over, new root growth is established, hydraulic conductivity increases and cavitations fill up (Sperry and Ikeda, 1997). Drou- ght reduces the occurrence of lenticels in woody fine roots, but its effect on the occurrence of growth rings in woody fine roots can vary between species of the same genus; in holm oak (Quercus ilex L.) drought reduced the occurrence of growth rings in woody fine roots, while in common oak (Q. robur L.) the occurrence of growth rings increased due to drought (Mrak et al., 2019). In fine roots of common beech provenance seedlin- gs, drought induced a decrease in carbon content, an increase in nitrogen content in some provenances and no change in nitrogen in others. Consequently, C to N ra- tio decreased in all provenances (Dounavi et al., 2016). Fine root life span decreases in drought, except when there is hydraulic redistribution of moisture from areas with higher soil water content to areas with lower soil water content (McCormack and Guo, 2014). In additi- on, the biomass, length and root tip density of fine roots decreases in drought, while specific root length, root tis- sue density and root surface area index are not affected. However, these results are affected by how fine roots are Acta Sil va e et Ligni 120 (2019), 1–12 11 classified. When the diameter limit for fine roots was set at 0.5 mm instead of 2 mm, fine root biomass, specific root length and root tissue density increased due to drought, while fine root diameter and nitrogen content decreased (Brunner et al., 2015). In seedlings of com- mon oak, the percentage of the finest roots (0.0–0.1 mm diameter) significantly increased, while the percentage of thicker fine roots decreased. In the same species, the mean diameter of fine roots decreased by 8.49 % (Mrak et al., 2019). In holm oak fine roots formed during the dry Mediterranean summer are thinner compared to those formed in other seasons (Montagnoli et al., 2019). In drought conditions synthesis of suberin and li- gnin is increased. Suberin is located in the endodermis and exodermis of roots and in the periderm of roots that have undergone secondary growth. Suberinisati- on decreases water loss from the roots and improves water use efficiency. Cell wall lignification improves the mechanical resistance of cell walls and decreases water loss from the cells and dehydration. Due to increased levels of suberin and lignin in roots, the quantity and decomposition of soil organic matter changes, thereby affecting soil organic matter turnover. Only a limited number of organisms are capable of lignin degradation (brown rot fungi and actinobacteria). Drought may af- fect the (enzymatic) activity of these microorganisms. For lignin degradation in soil, the lignin to nitrogen ra- tio is crucial. Due to suberin, soil organic matter beco- mes more hydrophobic (Brunner et al., 2015). 3 EFFECTS OF DROUGHT ON SYMBIOSIS WITH ECTOMYCORRHIZAL FUNGI Via extramatrical mycelium, water can be transfer- red from plants with access to the water supply in dee- per soil layers to plants experiencing water shortage (Egerton-Warburton et al., 2007). This type of water supply is very important for the survival of tree see- dlings (Lehto and Zwiazek, 2011). In drought prone fo- rests, access to the CMN of mother trees is crucial for seedling establishment. Seedlings growing within the CMN of mother trees are larger and have better water use efficiency. The community of ectomycorrhizal fungi in seedlings is very similar to that in neighbouring adult trees. Connection to the CMN of adult trees must esta- blish before the onset of the drought period; therefore, local drought adapted provenances with early germina- tion and establishment of mycorrhizal connections are advantageous (Pickles and Simard, 2017). When severe droughts are expected, appropriate provenance selecti- on and seedling life history are more important than the support of CMN. Seedlings of the same provenance esta- blished in tree nurseries are advantageous compared to natural regeneration from seeds of the same provenan- ce (Bingham and Simard, 2013). Mycelium with access to a water supply is able to survive in very dry soil (up to -2.5 MPa water potential or less). Hyphae are functio- nally active even after 68–77 days of drought and able to grow after 70–80 days of drought. Long distance water transport occurs via rhizomorphs in the symplast (Que- rejeta et al., 2003). Rhizomorphs are formed by fungi with hydrophobic cell walls, while water transport in hydrophilic fungi occurs via the apoplast. Knowledge on the relationship between the cell walls of mycorrhizal fungi and their resistance to drought is scarce (Lehto and Zwiazek, 2011). When exploration types of ecto- mycorrhizal fungi were compared in humid and drier Pinus pinaster Ait. stands, it was shown that long and short distance exploration types are significantly more abundant in drier conditions, while contact explorati- on types are more abundant in humid conditions. The abundance of medium distance exploration types was similar in both stands (Bakker et al., 2006). Pickles and Simard (2017) indicate that medium (Amphinema, Bo- letus, Cortinarius, Tomentella, Tricholoma) and long di- stance (Rhizopogon, Suillus) exploration types become dominant in seedlings under drought. Findings on the effects of drought on ectomycorrhi- zal fungal colonization and structure of fungal commu- nities vary widely, which can be ascribed to differences in experimental conditions (e.g. drought stress durati- on and intensity) and differences in selected ectomy- corrhizal inoculi when inoculated seedlings were used. Globally, ectomycorrhizal colonization is lower in envi- ronments with large precipitation seasonality (Soudzi- lovskaia et al., 2015). In natural conditions, colonization by ectomycorrhizal fungi follows the moderate stress hypothesis, with greater colonization in conditions of moderate host plant stress and lower colonization in conditions of chronic stress. The lower colonization of ectomycorrhizal fungi in severe drought, when photo- synthesis levels are low, helps to preserve the limited carbon supply, which would otherwise be spent to su- pport fungi in exchange for nutrients, for plant survival (Swaty et al., 2004). In stands of Quercus agrifolia Née affected by multi-year drought, colonization with ecto- mycorrhizal fungi decreased (Querejeta et al., 2003). Comparison of Pinus muricata D. Don stands with 7 % and 13 % soil humidity showed that ectomycorrhizal colonization was greater in conditions of 13 % soil hu- midity (Kennedy and Peay, 2007). On the other hand, moderate drought did not affect colonization in beech seedlings (Fagus sylvatica L.) with natural present my- corrhiza (Shi et al., 2002) and beech seedlings inocula- ted with five species of ectomycorrhizal fungi (Pena and 12 Mr ak T ., Kr aigher H.: V pli v suše na dr obne k or enine dr e v es in ekt omik or iz o v go z dnih ek osist emih Polle, 2014). In addition, ectomycorrhizal colonization rate did not change in a drought experiment with oak seedlings, and there was no significant effect on species richness (Mrak et al., 2019). However, species richness can be affected by plant genotype. Species richness in a drought resistant genotype of Pinus edulis Engelm. was two times higher than that in a drought sensitive geno- type. When both genotypes were exposed to drought conditions, the structure of the ectomycorrhizal fungal community in the drought sensitive genotype changed, while no changes were recorded in the drought resis- tant genotype (Patterson et al., 2019). Drought often results in changes in the abundance of certain ectomycorrhizal fungi (Shi et al., 2002; Swaty et al., 2004; Herzog et al., 2013; Pena and Polle, 2014; Mrak et al., 2019), e.g. the abundance of ectomycorrhizal fungi from the Tomentella genus decreased in a drought sen- sitive pine genotype (Patterson et al., 2019). A similar response was detected in oak seedlings exposed to dro- ught, while the abundance of Sphaerosporella brunnea (Alb. & Schwein.) Svrcek & Kubicka and Thelephora sp. increased (Mrak et al., 2019). Changes in fungal commu- nity structure towards drought resistant ectomycorrhi- zal fungi (or fungi that can cope with very limited carbon supply) would be beneficial for the host plant, as the fun- gi would potentially still provide several services to the plant. In stress conditions the uptake of macronutrients (N and P) into the plant is disturbed, and ectomycorrhi- zal fungi could reduce this deficiency to a certain extent. In laboratory conditions it was found that ectomy- corrhizal species Cenococcum geophilum Fr. (Figure 3) response to drought stress is lower compared to other ectomycorrhizal fungi (Jany et al., 2003; di Pietro et al., 2007). This species sustains the functionality of ecto- mycorrhizal fine roots, enabling immediate response to available water after the end of the drought period (Jany et al., 2003). Increased colonization rate of C. geophilum is common in stress conditions, including drought (Bakker et al., 2006; Grebenc & Kraigher, 2007, Kraigher in sod. 2007, Kraigher in sod. 2011). Under drought, the regulation of two types of aquaporins in this fungal species changes, but no significant positive correlation between physiological parameters of trees and mycorrhization with C. geophillum was discovered (Peter et al., 2016). The abundance of this species is also greater under elevated air temperatures and cor- relates positively with the growth of the aboveground part (Herzog et al., 2013). As the hyphae of C. geophilum are melanized, they are very resistant to decomposition after death. Accumulation of melanized remnants in the soil contributes to increased soil organic matter (SOM). Decomposition of melanized remnants is strongly in- fluenced by the melanin to N ratio, similar to the lignin to N ratio in fine roots (Fernandez and Koide, 2014). The enzymatic activity of ectomycorrhiza, which is related to the release of C, N and P from complex orga- nic matter in the soil, is higher compared to non-mycor- rhizal roots and remains elevated despite limited water access. It is dependent on the species of ectomycorrhi- zal fungus and decreases in the following order: Suillus granulatus (L.) Roussel > Rhizopogon roseolus (Cor- da) Th. Fr. > Paxillus involutus (Batsch) Fr. > C. geophi- lum (Kipfer et al., 2012). Nitrogen supply in the form of NH 4 + from C. geophilum during drought is very low compared to other ectomycorrhizal fungi. The capacity for N uptake from dry soil is also related to other en- vironmental parameters, e.g. sun exposure (Pena and Polle, 2014). In C. geophilum enzymatic activity incre- ases only in drought combined with high temperatures and depends on host plant species (Herzog et al., 2013). From the point of view of the plant, the presence of ectomycorrhizal fungi in drought conditions has many positive effects. It improves plant water potential, pre- serves hydraulic conductivity, increases the rate of photosynthesis compared to non-mycorrhizal seedlin- gs, diminishes the negative effects of drought to above- ground and belowground parts, reduces effects on the structure of wood, delays the death of root tips, mitiga- tes the reduction in leaf P content and reduces oxidative stress (Ortega et al., 2004; Walker et al., 2004; Alvarez et al., 2009a; Alvarez et al., 2009b; Beniwal et al., 2010; Kipfer et al., 2010; Danielsen and Polle, 2014). In dro- ught conditions ectomycorrhizal root tips may increase their osmotic potential with accumulation of soluble sugars and sugar alcohols or polyols (fungal products) to sustain the uptake of water (Shi et al., 2002). 4 CONCLUSIONS The root system of trees is very plastic, enabling a multitude of adaptations to drought conditions. Adap- tations occur in the growth and development of tree roots, morphology, anatomical and biochemical pro- perties and biological interactions (Figure 2). Altho- ugh the main mechanisms of adaptations are known, there are still many unknowns in this field of study, particularly with respect to biotic and abiotic interac- tions, which make it impossible to immediately trans- fer theoretical knowledge into forest planning. Climate change towards warmer and drier conditions will most affect tree seedlings due to their underdeveloped root system. Although adult trees may support seedlings via common mycelial networks, in cases where severe droughts are expected, proper selection of tree see- dling provenances will be of great importance.