Nitrogen, carbohydrate and ectomycorrhiza — the classical theories crumble

361

Agriculture, Ecosystems and Environment, 28 (1989) 361-364 Elsevier Science Publishers B.V., Amsterdam Printed in Czechoslovakia

NITROGEN, CARBOHYDRATE AND ECIOMYCORRHIZA - IHE CLASSICAL THEORIES CRUHBLE

Jan-Erik Nylund Department o f Forest Mycology and Pathology, Swedish U n i v e r s i t y o f Agricultural

Sciences, Box 7026, S-750 07 UPPSALA, Sweden

Abstract As e x p l a n a t i o n s of the i n t e r a c t i o n between mineral n u t r i t i o n ,

carbohydrate

s t a t u s and ectomycorrhiza formation, BjOrkman's carbohydrate t h e o r y and S l a n k i s ' hormone t h e o r y are r e s p e c t i v e l y considered i n v a l i d and irrelevant.

Recent r e s u l t s have shown t h a t mycorrhiza may develop on

seedlings w i t h u n l i m i t e d access to mineral n u t r i e n t s , increased a v a i l a b i l i t y

a l s o t h a t the

o f n i t r o g e n w h i l e reducing myeorrhiza, c o n t r a r y to

t h e o r y , increased r o o t and shoot carbohydrate c o n c e n t r a t i o n s . New approaches are needed so as to gain an understanding of the mechanisms r e g u l a t i n g the formation o f mycorrhiza. I n t r o d u c t i o n = the c l a s s i c a l t h e o r i e s In his well-known carbohydrate theory, Bj~rkman (1942) claimed t h a t the a p p l i c a t i o n of increased amounts of n i t r o g e n , by reducing i n t e r n a l c o n c e n t r a t i o n s o f a v a i l a b l e carbohydrates decreased the formation of mycorrhiza. In his experiments, mycorrhiza frequency was more c l o s e l y c o r r e l a t e d w i t h carbohydrate c o n c e n t r a t i o n s than w i t h those o f i n t e r n a l c o n c e n t r a t i o n s or m t r o g e n l e v e l s , and severe carbohydrate reductions attributable

to low l i g h t

intensities

and r i n g - b a r k i n g prevented the

formation of m y c o r r h i z a l a s s o c i a t i o n s . Using BjOrkman's data Richards (1965) found that the occurrence o f mycorrhJza was more c l o s P l y associated with C/N r a t i o s than with carbohydrate alone. A f t e r two decades of c o n f l J c t J n 0 r e s u l t s , Harx e t a ] .

(1977), using improved experimental

designs and a n a l y t i c a l methods, reproduced BjGrkman's data.

362

Heanwhile~ Meyer (1962), i r r e s p e c t i v e

of amounts o f f e r t i l i z e r s ,

obtained

more m y c o r r h i z a when beech and Norway s p r u c e were grown in r i c h m u l l , t h a n in poor mot s o i l s .

In t h i s i n s t a n c e Meyer argued t h a t t h e enhanced

c o n c e n t r a t i o n s o f s u g a r s in t r e e s growing in t h e mull s o i l were t h e r e as a r e s u l t o f m y c o r r h i z a f o r m a t i o n . S i a n k i s (1974) kn;)wing t h a t t h e a p p l i c a t i o n of a u x i n could c a u s e s u g a r s to a c c u m u l a t e i n t h o s e p a r t s of p l a n t s a c t u a l l y t r e a t e d with t h i s p l a n t hormone, f o r m u l a t e d h i s hormone theory, interpreting

eetomycorrhiza formation as being d i r e c t l y

by a u x i n c o n c e n t r a t i o n s r e s u l t i n g

regulated

from t h e p r e s e n c e o f t h e mycobiont. On

t h e b a s i s of p u r e - c u l t u r e e x p e r i m e n t s he a l s o h y p o t h e s i z e d t h a t t h e increased availability

o f n i t r o g e n would d e p r e s s ~he s y n t h e s i s of a u x i n by

mycorrhizai fungi consequently decreasing mycorrhiza formation (Slankis did not i d e n t i f y a r o l e for c a r b o h y d r a t e ) . Slankis' theory was based on the assumption t h a t auxin concentrations would be increased by two to three orders of magnitude. While l i n k s between mycorrhiza formation and the occurrence of auxins have been reported (see Nylund, 1988) the increases (100~-200~) recorded by Subba-Rao & Slankis (1956).are too small to substantrate S l a n k i s ' theory. Recent c o n f l i c t i n 9 e v i d e n c e Dixon e t a l .

(1981) added n i t r o g e n f e r t i l i z e r s

s p r a y s or s o i l a p p l i c a t i o n s .

to oak e i t h e r as f o l i a r

While s o i l a p p l i c a t i o n s ,

as e x p e c t e d ,

decreased mycorrhiza frequency f o l i a r sprays increased t h e i r Like Meyer (1962), Dixon e t a l .

formation.

found t h a t m y c o r r h i z a o c c u r r e n c e was

p o s i t i v e l y a s s o c i a t e d with amounts o f c a r b o h y d r a t e which they t h o u g h t they were a t t r i b u t a b l e

to t h e m y c o r r h i z a t h a t were formed. U n f o r t u n a t e l y no

a n a l y s e s were made of t i s s u e n i t r o g e n . More r e c e n t l y Ingestad et a l .

(1986) found that Scots pine grown in water

c u l t u r e e s t a b l i s h e d strong mycorrhiza with species of S u i l l u s and P i s o l i t h u s in s p i t e of the seedlings being given as much of a balanced m i x t u r e of m i n e r a l s as they could u t i l i z e .

T i s s u e c o n c e n t r a t i o n s of N

exceeded Z%, and were much h i g h e r t h a n c r i t i c a l

c o n c e n t r a t i o n s for

i n h i b i t i n g s y m b i o s i s found by most o t h e r workers. In t h i s i n s t a n c e c a r b o h y d r a t e a n a l y s e s were o m i t t e d , but in comparable c o n d i t i o n s t h e r e was a marked b u i l d - u p of s t a r c h in Sail× f o l i a g e when amounts of n u t r i e n t s

363

were restricted;

similar

experiments

pine

with

observations

have been made in preliminary

in my laboratory.

The observations

made by Rudawska (1986) when studying

ammonia, nitrate

and urea

addition,

regardless

concentrations

of carbohydrates.

my own laboratory directly

to those

With my colleagues in the tissue restricted.

reducing tissue

concentration

limit

and shoots

their

of approximately

1.6% N

is greatly

I

to substrate

bodies

in

were

1989).

formation

corresponds

affected.

than nitrate,

mycorrhiza

that

of mycorrhizal

fungi

with 20, but not 50, ppm N, at which mycorrhiza

was perceptibly

mycorrhizas

her,

(Nylund & Wallander

of 100 or more ppm N. Fruit

extent

roots

above which mycorrhiza

in substrates

formation

before

of

increased ‘1, actually have now been replicated

in both

I have found an internal

This tissue

greater

those

nitrate...

Her results

of sugars

of needles,

concentrations

unlike

- amounts of nitrogen

related

developed

indicated,

of form (ammonia,

the uptake

formation.

has in several

concentrations

Ammonium was taken

and was correspondingly Despite

instances

these

up to a much

more effective

threshold

concentrations

been found developing

of N exceeded

2X (substrate

data

and nitrogen

in

vigorously

content

when

200 ppm).

Conclusions A survey

of published

and N/sugar

ratios

effectively

correlated

frequently,

but sometimes

some instances results

Rudawska suggest

Thus it

that

nitrogen

strongly,

by Ingestad

is likely

et al.

provided

and N/P

was usually

concentrations,

with sugar

ratios

less

concentrations, the best

while

fit.

with N or sugar

in

However,

(1986) and in my laboratory

the correlations

that

basis

earlier

understand ‘effect’

to internal

concentrations

formation

also

the by

concentrations

are

and not causal.

physiological refining

mycorrhiza

N/P and N/sugar

obtained

fortuitous

on sugar

showed that

the traditional

of mycorrhiza

experiments

underlying

has an important

to establish

mycorrhiza

it

mechanisms bearing in forest

theories

formation

concerning

are erroneous.

is now necessary but not without on the practical nursery

practice.

the Instead

of

to seek new approaches accepting

that

explortation

to

nitrogen of methods

364

References B3~RKHAN, [ . : gber die BedJngungcn dec HykorrhJzabiidung bei Klefer und richte. -Symbo]ae Botanicae Upsai|enses V], 1942. DIXON, R.K.,CARR[11, H . [ . , B]XBY, 3.A., COX, G.S. & IOHPSON, 3.C.: Ctowth, ectomycorrhJza| deveJopment,amd root so]ubJe carbohydrates of bJack oak seedJings fertJ]ized by two methods. -forest S~lence 27, 617-6Z~, 1981. ]NG[S1AD, I . , ARVEBY, A. & K~HR, H.: ]he influence or ectomycorrhJza on nitrogen n u t r i t i o n and growth of Pinus sy]vestxis seedlings. -PhysJo|ogia Piantarum 68, 575-582, 1986. HARX., D.H., HA1CH, A.B. & H[NDiC)NO, 3 . r . : High soil f e r t i l i t y decreases sucrose content and susceptJbJ|ity of ]ob]o]]y pine roots to ectomycorrhiza] infection by Pisolithus tJnctorJus. -Canadian 3ournai of Botany 55, 1569-157), 1977.

HEY[R, F.H.: Die Buchen- und rJchtenmykorrhjza Jn verschJedcnen Bodentypen, Jhr Beeinfiussigung dutch HineraidOngung sowie for die Hykorrhizabiidung wlchtige raktoren. -Hittei)ungen dec Bundesforschungsanstait for r o r s t - und Ho]zwissenschaft 5~, 1-7), 1962. H]ICHELL, R.3., CARREl1, H.E., COX, C.S. & AIALAY, A.: Boron and ectom),corrhlzai influences on Jndo]e-)-acetJc ac|d levels and Jndole-)-aeetic acid oxtdase and peroxidase a c t i v i t i e s of Pinus echinata roots. -1fee Physiology 1,1-8, 1986. NYLUND, 3-E. The regulation of mycorrhJza format]on - carbohydrate and hormone theories reviewed. -Scandinavian Oourna] or Forest Research 3:4, 1988.

NYLUND, 0-£. & WALLANDER, H. Effects of ectomycorhiza on host growth and carbon balance Jn a semi-hydroponic c u l t i v a t i o n system. New Phyto]oglst 112 (3). 1989. R ]CHARDS, B.N.: Hycorrhiza development of Job]oily pine seedlings in relation to s?J] reaction and supply of n i t r a t e . -Plant & Soil 22, 187-199, 1965.

RUDAHSKA, H.: Sugar metabolism of ectomycorrhiza] Scots pine seedlings as influenced by d i f f e r e n t nitrogen forms and levels. -PhysJo]ogica) and CenetJca] Aspects of Hycorrhizae. Proe. 1st Eur. Symp. on Hycorrhizae. p.389-39~. ]NRAp Paris, 1986. SLANK]S, V.: So11 factors lnf]ueneJng format]on or mycorrh|za. -Annual Review of Phytopatho]ogy 12, 4}7-457, 1974. SUBBA-RAO, N.S. & SLANK]S, V. ]ndo]e compounds Jn pine mycorrhiza. -Proceedings from the 9th international Botan|cal Congress, vo].2 t p.)86, 1959.

Nylund, i.E., 1989: Nitrogen, c a r b o h y d r a t e and e c t o m y c o r r h i z a - the classical theories crumble. E c o s y s t e m s Environ., 28: 361-364.