Plant Physiol. (1989) 91, 227-2320032-0889/89/91/0227/06/$01 .00/0

Received for publication February 20, 1989and in revised form Aprl 24, 1989

Root Respiration and Growth in Plantago major as Affectedby Vesicular-Arbuscular Mycorrhizal Infection1

Rob Baas*2, Adrie van der Wert, and Hans LambersInstitute for Ecological Research, P.O. Box 371, 3233 ZG Oostvoorne, The Netherlands (R.B.), and Department ofPlant Ecology, University of Utrecht, Lange Nieuwstraat 106, 3512 PN Utrecht, The Netherlands (A.v.d.W., H.L.)

ABSTRACT

Effects of vesicular-arbuscular mycorrhizal (VAM) infection andP on root respiration and dry matter allocation were studied inPlantago major L. ssp. pleiosperma (Pilger). By applying P, therelative growth rate of non-VAM controls and plants colonized byGlomus fasciculatum (Thaxt. sensu Gerdemann) Gerdemann andTrappe was increased to a similar extent (55-67%). However,leaf area ratio was increased more and net assimilation rate perunit leaf area was increased less by VAM infection than by Paddition. The lower net assimilation rate could be related to a 20to 30% higher root respiration rate per unit leaf area of VAMplants. Root respiration per unit dry matter and specific net uptakerates of N and P were increased more by VAM infection than byP addition. Neither the contribution of the altemative respiratorypath nor the relative growth rate could account for the differencesin root respiration rate between VAM and non-VAM plants. It wasestimated that increased fungal respiration (87%) and ion uptakerate (13%) contributed to the higher respiratory activity of VAMroots of P. major.

photosynthesis or respiration, such as light intensity (3), Pstatus (15), ontogeny of the host plant (24), and/or the pres-ence of other symbionts (2, 4).To sort out confounding nutritional and ontogenetic effects

of VAM infection, both split-root systems (11, 16) and P-fertilized controls with equal dry weight (2, 14, 21, 27) havebeen used. In the latter method, VAM-infection increasedroot respiration rates in Plantago major ssp. pleiospermaplants above those of P-fertilized controls (1). However, VAMplants may have a higher RGR than equal sized non-VAMcontrols because of the shift in C balance during the devel-opment of the symbiosis (14). Therefore, the possibility existsthat higher instantaneous RGRs result in greater rates of rootrespiration of VAM plants. This could also apply to short-term 14C02 labeling studies where only one harvest date wasused to compare VAM and nonVAM treatments (11, 16, 18,22, 27). Hence, the objective of the present study was toanalyze the effect of VAM infection on root respiration anddry matter allocation in VAM and non-VAM P. major plantshaving equal RGR.

Under conditions of low P availability, the increased Puptake and concomitant growth enhancement ofhigher plantsdue to VAM3 infection have been well established (8). One ofthe causes for the increased RGR of VAM plants may beascribed to enhanced photosynthetic rates per unit leaf area

(5), since photosynthesis is dependent on P supply under P-limited conditions (10, 12, 25). Both P addition and VAMinfection may also increase the shoot to root ratio and theLAR (1, 14, 27), which may contribute to an increase inphotosynthesis on a whole plant basis and hence to growth.

Translocation of fixed C to VAM root systems has beenfound to be 4 to 17% higher in leek (27), soybean (14), fababeans (22), Carrizo citrange and sour orange (11, 16) than innon-VAM plants. In leek, this increased translocation was

associated with both increased root respiration and loss oforganic matter (e.g., mycelium) in the soil (27). This increased'below-ground' C sink may offset any increase in whole plantphotosynthesis, so that the RGR may not be affected, or may

even be decreased in VAM plants (2, 7, 17). This C balancewill be determined by a combination offactors affecting either

'Grassland Species Research Group publication No. 160.2 Present address: Research Station for Floriculture, Linnaeuslaan

2A, 1431 JV Aalsmeer, The Netherlands.3Abbreviations: VAM, vesicular-arbuscular mycorrhizal; RGR,

relative growth rate; NAR, net assimilation rate; LAR, leafarea ratio;SNIUR; specific net ion uptake rate.

MATERIALS AND METHODS

Plant Cultivation

A calcareous sandy soil (location Oostvoornse Meer, theNetherlands, pHH2o 8.5, organic matter 0.2%) was y-irradi-ated (2.5 Mrad) and mixed with 1.67 g Ca10(P04)6(OH)2 perkg dry soil, giving 4 gg/g NaHCO3-extractable phosphorus.Inoculum from a pot culture of Glomusfasciculatum (Thaxt.sensu Gerdemann) Gerdemann and Trappe (origin Flevo-polders, the Netherlands) on white clover (Trifolium repensL.) was mixed with the soil (0.83 g per kg soil; M treatment).Sterilized inoculum was added in the control (NM) treatment.

Plastic pots were filled with 600 g soil (dry mass), and twoseedlings of an inbred line of Plantago major L. ssp. pleio-sperma (Pilger) were planted per pot. After 2 weeks, plantswere thinned to one plant per pot. The plants were wateredweekly with 10 mL of a nutrient solution containing thefollowing macronutrients (mM): NO3-, 60; S04-2, 8; K+, 20;Ca+2, 20; Mg+2, 8. Micronutrients in this solution were sup-plied as (,uM): NaFeEDTA, 83; H3BO3, 369; MnCl2.4H20,73; ZnSO4-7H20, 6; CuSO4-5H20, 0.3; Na2MoO4.2H20,0.5. The soil water content during the experiment was keptbetween 10 and 20% (w/w) with demineralized water. Potswere placed in a growth chamber at 20°C and a relativehumidity of 70 to 80%. Photosynthetic photon flux densitywas 220 to 280 MAmol m-2 s-' during the 12-h day and wassupplied by Sylvania Cool White VHO lamps and additional

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Plant Physiol. Vol. 91,1989

60 W incandescent light bulbs at a ratio of 7:1. The plantsremained vegetative during the experiment. At 33 and 43 dafter planting, half of the M and NM treatments received 30,umol KH2PO4/pot (+P treatments). Six plants of each of thefour treatments (M + P, M - P, NM + P and NM - P,respectively) were harvested 40, 43, 47, 50, 54, and 57 d afterplanting. The experiment therefore had a 2 x 2 x 6 factorialdesign, with VAM treatments, P treatments, and times ofharvest as factors.

Analytical Methods

At harvest, soil was washed from the roots, and fresh weightof shoot and roots was determined. Leaf area was measuredwith a leafarea meter (Hayashi Denkoh, Tokyo, Japan). Rootrespiration of whole or half root systems was determinedpolarographically (1) in a 20°C air-saturated nutrient solution,which was 1/16 of the concentration that was used during theexperiment. Assessment of the alternative path to total respi-ration was measured subsequently in a nutrient solution(without Fe) containing 25 mM salicylhydroxamic acid. Thisconcentration has been found to completely inhibit the alter-native respiratory pathway in P. major without having any

effects on the cytochrome pathway (9).Percentages ofVAM infection were assessed by a gridline-

intersect method after staining root samples with chlorazolblack E (6). Entire shoots and roots of individual plants weredried at 70°C (48 h) and subsequently digested in a sulfuricacid-salicylic acid solution. Concentrations oftotal P and totalN were measured spectrophotometrically by the molybde-num-blue and indophenol-blue methods, respectively.

plant. Instantaneous specific net P uptake rate values were

calculated similarly.

Statistical Analyses

Differences in RGR between two treatments were analyzedby two-way ANOVA with time of harvest and P treatment or

VAM-treatment as independent variables, and ln-transformeddry weight data as dependent variable. Significant time xtreatment interactions denote differences in RGR (23). Allother data were analyzed by three-way ANOVA. Tukey'sHSD test was used for comparison of cell means.

RESULTS

During the experimental period, VAM infection levels +SE for the M - P and M + P treatments were not significantlydifferent and were 78 ± 3 and 72 ± 3, respectively.

Exponential growth was constant during the experimentalperiod (Fig. IA). The mean RGR values of the NM + P, M

0-ONM-P A-ANM+P _M-P A-AM+P

0

._

co0

0.6ca

'a

Calculations

The mean RGR of each treatment during the harvestingperiod (40-57 d after planting) was calculated from the slopeof the least squares regression analysis of the ln-transformeddry weight data against time.The RGR (mg g-' (plant) d-') may be partitioned into the

net assimilation rate (g m-2 (leaves) d-') and the leaf area

ratio (m2 (leaves) kg-' (plant)) as follows:

RGR = NAR x LAR.

1.0

0.5

0.0o

-0.5

-1.0

_1 ^

17a3:0

-j(1)

The NAR of each individual plant was calculated from themean RGR per treatment and the LAR of each individualplant. The NAR is the balance of total gross photosynthesisand respiration in the entire plant:

NAR = total gross photosynthesis

- (shoot + root respiration). (2)

Previous data on shoot respiration obtained with P. majorssp. major plants grown under the same environmentalconditions (24) were used to estimate the total grossphotosynthesis.

Total net N uptake was determined by multiplying total Nconcentrations with dry weights of individual plants. Theinstantaneous specific net N uptake rate value (,umol N g-'(root) d-') of each individual plant was calculated from theslope (,umol N ,mol N-' d-') of the least squares regressionanalysis of ln-transformed data of net N uptake against timeand multiplying with (net N uptake)/(root weight) of the

C,.

c0 E.-

4.

h.

o E

141

11[a

1.3

1.1

0.9

0.7

0.5

40 45 50 55

Time, daysFigure 1. Growth (A, natural log scale), leaf area ratio (B), and rootrespiration per unit leaf area (C) in mycorrhizal (M) and nonmycorrhizal(NM) treatments supplied with (+P) or without (-P) additional phos-phate, r2 values for least squares regression analyses of plant weightdata were 0.79, 0.95, 0.89, and 0.95 for the NM - P, NM + P, M -

P and M + P treatments, respectively. Bars indicate ± SE (n = 6).Time indicated as days after planting.

A

B

C

-I/F. r3

- J.0 1/9 I

to,

*0. I

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RESPIRATION AND GROWTH IN VA MYCORRHIZAL PLANTAGO

- P and M + P treatments did not differ significantly butwere higher than in the NM - P treatment. The LAR was

increased both by P and by VAM infection during the exper-iment (Fig. iB); the average increase by 23% in the NM + Ptreatment however was lower than the 49% increase in boththe M - P and M + P treatments (Table I).On average, the NAR was increased by 24% in the NM +

P treatment and by 1% and 4% in the M - P and M + Ptreatments, respectively (Table I). This smaller increase inNAR in theM treatments compared to the NM + P treatmentwas associated with a 20 to 30% higher root respiration rateper unit leaf area in these treatments (Fig. IC; Table I).Compared to the NM - P treatment, estimated total gross

photosynthetic rates per unit leaf area were increased by 11 %,10%, and 3% in the NM + P, M - P, and M + P treatments,respectively (Table I).Root respiration rates per unit root dry weight were on the

average 76 to 79% greater in the M treatments compared tothe NM + P treatment (Fig. 2A); P addition increased rootrespiration in the NM treatment by 38%. The contributionof the alternative respiratory path to total respiration was

hardly affected by phosphate addition and mycorrhizal infec-tion (Fig. 2B). Therefore, when root respiratory energy pro-duction was calculated from the data of the contribution ofthe alternative respiratory path and total root respiration per

unit dry weight (cef 28), marked treatment differences re-mained (Table II).

Concentrations of total P and total N were more increaseddue to VAM infection than by P-addition (Table III). Slopesfor the net uptake rate of N (Fig. 3A) were derived from theln-transformed data of net N uptake as 0.042, 0.060, 0.076,and 0.068 ,umol ,umol-' d-' for the NM - P, NM + P,M - P and M + P treatments, respectively. For the net uptakerate of P (Fig. 3B) these values were 0.019, 0.048, 0.065, and0.066 imol ,umol-' d-', respectively. From these values, spe-cific net uptake rates (ymol g-' (roots) d-') for N and P werecalculated (Table III). The specific net N uptake rate wasincreased in the NM + P and both the M treatments. How-ever, as with the root respiration rate, the increase in specific

net N uptake rate was more pronounced in the M treatments(296 and 31 1% increase compared to the NM - P treatment)than in the NM + P treatment (196% increase). The effect onthe specific net P uptake rate was even more pronounced:increases of 941 and 1108% in the M - P and M + Ptreatments and a 458% increase in the NM + P treatment.

DISCUSSION

Analysis of Growth

VAM and non-VAM treatments with equal RGRs were

produced by applying P (Table I). Compared to the NM - Ptreatment, the RGR was increased both by P addition andVAM infection. To clarify the cause ofincreased growth rates,the RGR was separated into LAR and NAR. VAM infectionincreased the LAR, which agrees with results obtained withleek (27) and soybean (14). Because the 61 to 67% increasein RGR was accompanied by a 49 to 53% increase in LAR,these results show that the increase in RGR by VAM infectionwas mainly associated with an increase in morphology ratherthan an increase in the NAR.Although the RGRs of the M - P, M + P and NM + P

treatments were not significantly different, the VAM treat-ments showed a higher LAR and a lower NAR compared tothe NM + P treatment. These differences in NAR may be a

result of differences in rate of photosynthesis and/or in rateof respiration (cef Eq. 2). By transforming the determined rootrespiration rate (Fig. lC) in similar units as the NAR (TableI), it was shown that, compared to the NM + P treatment,increased root respiration ofVAM plants could partly accountfor the lower NAR ofVAM treatments. The root respirationof the VAM treatments may even have been underestimated,because part of the external mycelium (which would alsocontribute to respiration in the VAM treatments) was presum-ably lost when soil was washed from the roots. The increasedbelow-ground respiration upon VAM infection agrees withresults obtained on faba bean (22) and leek (27) in '4C02labeling experiments.

Table I. Effects of P Addition and VAM Infection on Growth Components of P. major ssp. pleiospermaValues are means from 40 to 57 d ± SE (n = 36). Values within a row followed by the same letter

are not significantly different (P = 0.05).Treatment

ComponentNM-P NM + P M-P M+ P

mg g dry wht-1 d 1

RGR 51 ±5a 78±3b 85±5b 82±4b

m2 kg dry wt-1LAR 9.7 ± 0.3a 12.0 ± 0.3b 14.5 ± 0.3c 14.8 ± 0.4c

g dry wt m-2 d-1NAR 5.4 ± 0.1a 6.7 ± 0.2c 6.0 ± 0.1b 5.6 ± 0.1aRoot respirationa 2.3 ± 0.1b 2.0 ± 0.1a 2.6 ± 0.1c 2.4 ± 0.1cEstimated shoot respirationb 1.5 1.5 1.5 1.5Estimated total gross photosynthesisc 9.2 10.2 10.1 9.5

a Calculated assuming a respiratory quotient of 1.0 and a dry wt/C ratio of 2.5. b Estimated fromdata obtained with Plantago major ssp. major (24). CEstimated using Equation 2: total grossphotosynthesis = NAR + (shoot + root respiration).

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Plant Physiol. Vol. 91, 1989

°-ONM-P A-ANM+P 0-* *-PA-AM+p_a'

*t

O -

4OAm a0-0

0-

L.Ec

a

a

L.

0

a

a

0

CW

50

40

sol

20

10

0

so

68

56

44

*2

20

40 45 50 55

Time, daysFigure 2. Root respiration per unit root weight (A), contribution ofalternative respiratory path (B), and root growth (C, natural log scale)in mycorrhizal (M) and nonmycorrhizal (NM) treatments supplied with(+P) or without (-P) additional phosphate. r2 values for least squaresregression analyses of root weight data were 0.84, 0.95, 0.91 and0.92 for the NM - P, NM + P, M - P, and M + P treatments,respectively. Bars indicate ± SE (n = 6). Time indicated as days afterplanting.

Total gross photosynthetic rates per unit leaf area were

estimated (Table I) from the root respiration data and pre-vious data on shoot respiration of P. major ssp. major (24).The estimated photosynthetic rate per unit leaf area was notincreased to a greater extent in the VAM treatments than inthe NM + P treatment. Hence, considering the higher Pconcentrations in the shoot of the M - P and M + Ptreatments (Table III), photosynthesis in these treatments wasnot likely to have been limited by P supply. Perhaps the lowphoton flux density in the present experiment may explainthis result, because increased photosynthesis per unit leaf areaupon VAM infection has been found (5, 14, 16), althoughnot consistently so (13, 27).

In summary, VAM plants used more daily produced pho-tosynthates for respiration than the NM + P plants. However,dry matter production was not affected by this 'loss' of pho-tosynthates, since no difference in RGR occurred. The lattermay be explained by higher photosynthesis (on a whole plantbasis) of VAM plants, resulting from a greater leaf area perunit plant weight rather than from higher photosynthesis perunit leaf area (Table I).

Analysis of Root Respiration

The increased root respiration rate per unit root dry matterof VAM-infected plants (Fig. 2A; Table II) agrees with pre-

vious results on P. major ssp. pleiosperma (1). Differences inenergy production by root respiration may be obscured bydifferences in the contribution of the alternative respiratorypath, a non-phosphorylating mitochondrial electron transportpathway (20). This alternative pathway in roots of higherplants may be of significance in removing an excess of car-

bohydrates, according to the 'energy overflow model' (19).However, only slight differences in the contribution of thealternative path were apparent (Fig. 2B), so that respiratoryenergy production was significantly different in the VAM andnon-VAM treatments (Table II).The rate ofATP consumption in non-VAM roots depends

on three major energy-requiring processes, i.e. root growth,ion uptake, and the maintenance of root biomass (28, 29).The overall equation can be described as (29):

rATP = MATP + I/YYTP X RGR + 1/UiATP X SNIUR, (3)

Table II. Effects of P Addition and VAM Infection on Contribution of Alternative Respiratory Pathway,Respiratory Energy Production, and Relative Growth Rate of Roots, in P. major ssp. pleiosperma

Values are means from 40 to 57 d ± SE (n = 36). Values within a row followed by the same letterare not significantly different (P = 0.05).

TreatmentComponent

NM-P NM+P M-P M+ P

% of total respirationAlternative path 50 ± 2a 47 ± 2ab 45 ± lab 44 ± lb

mmol ATP g dry wt- d-1

Respiratory energy production' 4.8 ± 0.1a 6.6 ± 0.2b 11.6 ± 0.3c 11.8 ± 0.2c

mg g dry wt-1 d-1

RGRroots 62 ± 5a 90 ± 4b 90 ± 5b 87±4b

a Calculated with an ADP/O ratio of 3 for the cytochrome path and 1 for the alternative path (20).

A

4----L-~~~~~=:-^ - x

elI

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RESPIRATION AND GROWTH IN VA MYCORRHIZAL PLANTAGO

Table Ill. Effects of P Addition and VAM Infection on Concentrations and Specific Net Uptake Rates ofN and P of P. major ssp. pleiosperma

Values are means from 40 to 57 d ± SE (n = 36). Values within a row followed by the same letterare not significantly different (P = 0.05).

TreatmentComponent

NM-P NM + P M-P M+ P

pnol g dry wthIPwx,ot 30 ± la 50 ± 2b 63 ± 2c 71 ± 2dProots 30±la 44±2b 72±3c 75±3cNshoot 2815 ± 28a 3121 ± 63b 3406 ± 46c 3429 ± 57cN,oots 1709 ± 25a 1942 ± 38b 2397 ± 25c 2370 ± 46c

pumol g dry wt-1 d-1Specific net P uptake rate 1.2 ± 0.1a 5.5 ± 0.8b 11.3 ± 0.5c 13.3 ± 0.6dSpecific net N uptake rate 192 ± 7a 377 ± 16b 597 ± 13c 569 ± 21c

O-ONM-P -Atvl+P -4M-Pw-

14..c0

0

0.a

zC

A-AM+P

c 5.0B

4.5-

4440

S.58.0

2.5

40 45 50 55

Time, daysFigure 3. Total uptake (natural log scale) of nitrate (A) and phosphate(B) in mycorrhizal (M) and nonmycorrhizal (NM) treatments suppliedwith (+P) or without (-P) additional phosphate. r2 values for leastsquares regression analyses of nitrate (phosphate) uptake were 0.74(0.34), 0.93 (0.82), 0.87 (0.81), and 0.94 (0.87) for the NM - P,NM + P, M - P, and M + P treatments, respectively. Bars indicate± SE (n = 6). Time indicated as days after planting.

where rATp is the rate of ATP production in root respiration(Table II); mATp is the ATP requirement for maintenance ofroot biomass; I/YrTp is the ATP requirement for the synthesisof cell material; l/UXTp is the ATP requirement for ionuptake; SNIUR is the specific net ion uptake rate. For VAMroots, the extra costs of the VAM symbiosis, designated asfungal respiration, should be added. This component itselfcontains all processes related to the fungal component of thesymbiosis, such as growth (e.g. synthesis of lipids (21), main-

tenance and ion uptake by the fungal tissue. By Equation 3,the contribution of fungal respiration to the total respirationcan be estimated, provided the other components are knownor estimated.

Since the RGR of the roots was not significantly differentin the NM + P, M - P and M + P treatments (Table II), it isassumed that the component of root respiration costs for rootgrowth is equal for VAM and non-VAM roots. It is alsoassumed that the energy required for the maintenance ofelectrochemical gradients across membranes and for turnoverof cellular constituents (mATp) is approximately equal forVAM and non-VAM roots. However, marked differences inspecific uptake rates of N and P were found for VAM andnon-VAM plants (Fig. 3; Table III). An increased specific netP uptake rate due to VAM infection is normally found (e.g.26) and can be ascribed to the increased uptake capacity dueto external mycelium. Increased uptake rates of more mobileions like nitrate, which was the N-source in the nutrientsolution, have not been shown to be consistently increased byVAM infection.Energy costs for the uptake of ions concern mainly anions

(8), of which nitrate is quantitatively the most important. Intwo Carex species, the rate of nitrate uptake amounted to 76to 77% of total anion uptake (28). Total ion uptake required25 to 38% ofthe total root respiratory energy production, andthe mean energy requirement for ion uptake (1/UiATP) wasderived at 4.0 mol ATP mol' ion (28), which agrees withresults obtained on maize (29). Using the latter value inequation 3, together with the rATp data (Table II), and com-paring the M treatments with the NM + P treatment resultsin an estimate for the fungal component of respiration ofapproximately 37%.The estimated respiratory energy requirement for ion up-

take was 20% in both the VAM and non-VAM treatments.Because this value may even be slightly underestimated asother ions besides nitrate have not been included, the resultsconfirm the importance of ion uptake to the total respiratoryenergy requirement (28, 29). However, it is estimated (Eq. 3)that the increase in root respiration due to VAM infectioncan be largely (87%) ascribed to respiratory costs of the VAMsymbiosis, whereas a smaller part (13%) can be ascribed tothe greater ion uptake rates.

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Plant Physiol. Vol. 91,1989

ACKNOWLEDGMENT

We thank Dr. Ries de Visser for comments on the manuscript.

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