Báo cáo khoa học: " The effects of ectomycorrhizal status on carbon dioxide assimilation capacity, water-use efficiency and response to transplanting in seedlings of Pseudotsuga menziesii (Mirb) Franco"

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Nội dung Text: Báo cáo khoa học: " The effects of ectomycorrhizal status on carbon dioxide assimilation capacity, water-use efficiency and response to transplanting in seedlings of Pseudotsuga menziesii (Mirb) Franco"

Original article The effects of ectomycorrhizal status on carbon dioxide assimilation capacity, water-use efficiency and response to transplanting in seedlings of Pseudotsuga menziesii (Mirb) Franco JM Guehl J Garbaye 1 INRA Centre de Recherches de Nancy, Laboratoire de Bioclimatologie d’Écophysiologie Forestières, 54280 Champenoux; et 2 Centre de Recherches de Nancy, Laboratoire de Microbiologie Forestière, INRA F 54280 France Champenoux, (Received 30 March 1990; accepted 5 December 1990) Summary — One year-old Douglas fir seedlings, mycorrhizal with Laccaria laccata or with Thele- phora terrestris and grown at two levels of phosphorus in the nutrient solution (10 and 40 mg·l P), -1 were compared for water relations and gas exchange before and after transplanting in non-limiting water conditions. The results show that i), L laccata is more efficient than T terrestris in increasing photosynthesis and water use efficiency, ii), phosphorus deficiency reduces photosynthesis and wa- ter use efficiency, iii), the stimulating effect of L laccata on photosynthesis and water use efficiency is, at least partly, due to the improvement of phosphorus nutrition, iv), the photosynthesis reduction resulting from transplanting is due to a non-stomatal mechanism, and v), the recovery of photosyn- thesis involves the regrowth of the external mycelium of mycorrhizas. These results are discussed from the viewpoint of the plant-fungus relationships. ectomycorrhizae / phosphorus nutrition / CO assimilation / water-use efficiency / transplant- 2 ing Résumé — Effets du statut mycorhizien sur la capacité d’assimilation de CO l’efficience , 2 d’utilisation de l’eau et la réponse à la transplantation de semis de Pseudotsuga menziesii (Mirb) Franco. Des semis de 1 an de douglas, mycorhizés par Laccaria laccata ou Thelephora ter- restris ont été élevés durant une saison de croissance à 2 niveaux de phosphore dans la solution nutritive (10 et 40 mg·l et ont été comparés du point de vue des relations hydriques et des -1 P) échanges gazeux avant et après transplantation (à 2 dates différentes, en octobre et en février) en conditions hydriques non limitantes. A faible niveau de phosphore, les plants inoculés par L laccata avaient une surface foliaire plus importante que les plants mycorhizés par T terrestris (tableau 1) et étaient également caractérisés par des taux d’assimilation de CO et d’efficience photosynthétique 2 d’utilisation de l’eau plus élevés (tableau II et fig 1). La carence en phosphore réduit la photosyn- thèse et l’efficience d’utilisation de l’eau (tableau II, fig 1). L’effet stimulant de L laccata sur l’effi- cience de l’eau est dû, au moins en partie, à l’amélioration de la nutrition en phosphore (fig 7 et 9).
La réduction de la photosynthèse consécutiveà la transplantation (fig 2), bien qu’accompagnée par une fermeture stomatique (fig 3), est dûe essentiellement à un mécanisme non stomatique (fig 4) et n’est pas liée à une altération de l’état hydrique et nutritionel (fig 7 et 8) des plants. Le rétablissement de la photosynthèse après transplantation est concomitant à la régénération racinaire (fig 5), mais son déterminisme implique également la reprise d’activité du champignon (fig 6). Ces résultats sont discu- tés du point de vue des relations plante-champignon. ectomycorhize / nutrition phosphatée / assimulation de CO / efficience de l’eau / transplanta- 2 tion MATERIALS AND METHODS INTRODUCTION Plant material Ectomycorrhizal symbiosis is essential for nursery-grown conifer seedlings and is de- Douglas fir (Pseudotsuga menziesii (Mirb) Fran- terminant for plant survival and growth af- co) seedlings were grown in the summer in a ter outplanting (Marx et al, 1977; Le Tacon glasshouse, in 95 ml containers filled with 1/1 (v/ et al, 1988). It is also known that different v) vermiculite-sphagnum peat mix inoculated fungal associates do not provide the same with the ectomycorrhizal fungus Laccaria lacca- ta or non-inoculated. Inoculum was mycelium benefit in this respect, through mecha- aseptically grown for two months in glass jars, in nisms as diverse as improving mineral ab- a vermiculite-peat substrate moistened with nu- sorption and assimilation affecting hormo- trient medium. Twenty per cent (v/v) inoculum nal balance in the plant, enhancing the was mixed with the potting mix before filling the contact between roots and soil, and pro- containers. Each inoculation treatment was wa- tecting roots against disease (Chalot et al, tered with a complete nutrient solution contain- 1988). This paper describes and discuss- ing either 10 or 40 mg·ml phosphorus as -1 Na Each fungus-phosphorus level treat- . 4 PO 2 es the physiological status of one year-old ment involved 120 seedlings. At the end of Sep- Douglas fir seedlings, associated with two tember, when growth stopped and buds were different ectomycorrhizal fungi and grown set up, a random sample of 6 seedlings per phosphorous levels, before they at two treatment was observed for mycorrhizas with a lifted. The behaviour of the same were stereomicroscope after gently washing the root in controlled condi- seedlings transplanted systems. Ectomycorrhizal development was rat- ed according to a four-level scale (0: no mycor- tions was also considered. rare mycorrhizas; 2: several conspicu- rhiza; 1: The results presented here are part of a mycorrhizal clusters and/or mycorrhizas ous project which is aimed at understanding disseminated throughout the root system; 3: my- the role played by the fungal associates corrhizas abundant in all parts of the root sys- tem). Three treatments were chosen for subse- during the transplanting shock suffered by quent measurements and analysis: forest plants when outplanted, even in non-limited water supply conditions (Guehl Tt low phosphorus level, non inoculated, my- - corrhizal with contaminant Thelephora terrestris et al, 1989). Gas exchange parameters (mycorrhizal rating: 1.6); (CO assimilation rate, transpiration rate, 2 water-use efficiency) were used as physio- -TtP: high phosphorus level, non-inoculated, mycorrhizal with T terrestris (rating: 2.4); ] logical criteria for monitoring the behaviour of plants with different ectomycorrhizal LI: low phosphorus level, inoculated with Lac- - caria laccata, predominantly mycorrhizal with L status.
laccata (rating: 2.6) and contaminated Water status and gas exchange slightly with T terrestris. measurements Predawn needle water potential (ψ was deter- ) wp mined on one needle per seedling prior to the Sampling and experimental set-up gas exchange measurements by means of a Scholander pressure bomb specifically devised for measurements on individual conifer needles. The seedlings were kept in a frostless glass- For the November experiment, the plants house during winter, without fertilization, under taken from the climate room to a laborato- conditions such that aerial growth was stopped were ry where gas exchange measurements were from October to March. Two sets of measure- made by means of an open system consisting of ments were performed: in November and in Feb- three assimilation chambers connected in paral- ruary. At each date, 20 plants per treatment lel in which the environmental factors could be were randomly picked among the 50% tallest controlled. Measurements were made at 22.0 ± ones. Before transplanting, 6-8 of these plants 0.5°C air temperature, 10.6 ± 1.0 Pa·kPa leaf- -1 were used for gas exchange measurements and to-air water vapour molar fraction difference, for determining the phosphorus and nitrogen 400 μmol·m photosynthetic photon flux -1 ·s -2 content of the needles. The 12 remaining plants density (400-700 nm) and 350 ± 5 μmol·mol -1 were used for gas exchange measurements and ambient CO concentration (C ). a transplanted as follows: they were immediately 2 lifted, their roots washed, and mycorrhizal devel- For the February experiment, gas exchange opment was quantified. The growing white root measurements were made in the climate room tips were sectioned, and the seedlings were with a portable gas-exchange measurement sys- planted in sphagnum peat in flat (3 cm thick) tem (Li-Cor 6200, Li-Cor, Lincoln, NE, USA). containers with a transparent wall allowing ob- The CO concentration in the climate room was 2 servation of the roots. These containers were kept constant (C = 425 ± 15 μmol·mol ). -1 a placed in a climate chamber under the following assimilation Gas exchange parameters (CO 2 environmental conditions: photoperiod, 16 h; air rate, A; leaf conductance for water vapour, g; in- temperature, 22 ± 0.2°C (d) and 16.0 ± 0.2°C tercellular CO concentration, C were calculat- ) i 2 (night); photosynthetic photon flux density (400- ed with the classical equations (Caemmerer and 700 nm), 400 μmol m provided by fluores- s -2 1 Farquhar, 1981) taking into account simultane- cent tubes; relative air humidity, 60% (day) and ous CO and H diffusion through the stomatal 2 O 2 90% (night); ambient CO concentration (C 2 ), a pores. Intercellular CO concentration (C calcu- ) i 2 420 ± 30 μmol·mol They were watered twice . -1 lations were performed in order to assess a week with the 10 mg·l P nutrient solution in -1 whether differences for A between treatments order to maintain the moisture of the peat near and A changes in response to transplanting field capacity. were due to chloroplastic or to stomatal factors Water status, gas exchange, root regenera- (Jones, 1985). Previous measurements made tion (number of elongated white tips), and re- on conifers (unpublished data) did not show any growth of mycorrhizal extramatical mycelium patch pattern in stomatal closure, so that relia- (quantified according to the same rating scale ble C calculations can be performed from leaf i as above) were assessed 4, 11 and 18 d after gas exchange data. More precisely, CO assimi- 2 transplanting. lation rate was considered in an (A, C graph as ) i being at the intersection of two functions: i), the At the end of each experiment, the seedlings photosynthetic CO demand function (D) which processed for dry weight and leaf area de- 2 were defines the mesophyll photosynthetic capacity termination. Needles were then oven-dried and, ii), the photosynthetic CO supply function 2 (60°C for 48 h) and mineral analyses were per- (Su) defining the diffusional limitation to CO as- 2 formed (February only).
similation. For determining the (D) functions, C RESULTS a varied stepwise and A and C calculat- i were was ed for each step. The Su function is a line with an x-axis intercept approximately equal to C a Plant size and biomass and a negative slope approximately equal to -g (Guehl and Aussenac, 1987). Water-use effi- ciency (WUE) was determined as the A/g ratio. Data relative to the size and biomass of At the end of the experiment, the seedlings the February seedlings (before transplant- were harvested and plant material was separat- ing) are given in table I. Stem height was ed into different compartments (needles, stems highest in the TtP and LI treatments. Root and root systems). Each compartment was collar diameter and total dry weight were oven-dried at 60°C for 48 h and weighed. The significantly higher in TtP than in the other dried needles were kept for mineral analysis. treatments, whereas there was no signifi- needle of the seedlings Projected areas cant difference in the root/shoot ratio be- determined with video camera coupled were a (ΔT area meter; ΔT devic- to an image analyser tween the different treatments. Needle es, Cambridge, UK). area was significantly higher in TtP and LI than in Tt. The seedlings of the different treatments did not exhibit significant differ- ences in their specific leaf dry weight (ratio Mineral analyses of needle dry weight to needle area). The total nitrogen content of the dried and ground needles was determined with a C/N Gas exchange and water-use efficiency analyser (Model 1500; Carlo Erba, Italy). The values obtained with this technique are about 10% higher than those obtained with the Kjel- Table II gives the mean values of CO as- 2 dahl method. The phosphorus concentrations similation rate (A), stomatal conductance were determined after pressure digestion of the (g) and water-use efficiency (WUE A/g)= ground material with 100% HNO at 170°C for , 3 in the different treatments before trans- 6 h (Schramel et al, 1980) with a direct current planting, in the 2 experiments. TtP and LI plasma emission spectrometer (Model Spectro Span 6; Beckman Instruments, USA). exhibited A values significantly higher than
trast, treatment Tt did not exhibit such a those in Tt both in November and in Febru- control of WUE at the individual level since ary. A was higher in TtP than in LI in No- no significant (P < 0.05) correlation be- vember but not in February. In November, tween A and g was observed for this treat- TtP was characterized by g values signifi- cantly higher than those in the other treat- ment. Moreover, the plots of the latter ments, while in February there was no sig- treatment occupied a lower position in the nificant difference for this parameter. (A, g) graphs, thus indicating lower WUE. Water-use efficiency in TtP and LI was Transplanting resulted in a marked de- significantly higher than that in Tt in both of A between day 0 and day 4 in all crease experiments. There was no significant dif- treatments and for the 2 measurement pe- ferences between TtP and LI. For a given riods (fig 2). In February, the decrease of A treatment, the WUE values were identical continued until 18 d after transplanting for for the two experiments. treatment LI, while a slight recovery of A Figure 1 gives an insight into the WUE was observed from d 4 in treatments Tt regulation at the individual level prior to and TtP. Such a recovery was not appar- transplanting. The regression lines were ent in November, when the decrease in A forced through the origin so that their was more pronounced in the TtP seedlings slopes (water-use efficiency) could be than it was in the LI seedlings, since the A compared. In November as well as in Feb- values of these treatments were signifi- ruary, the invididual variability of the plots cantly different at day 0, but were not dif- relative to treatments TtP and LI was or- ferent 18 d after transplanting (fig 2). In dered along the same linear relationship February, a very different pattern was ob- expressing proportionality between A and served with the decrease of A being the g and thus constancy of WUE both for the most pronounced in LI. individual plants and the two dates. In con-
alterations in the photosynthetic demand Transplanting also affected g (fig 3) in a for CO while the supply function (related approximately identical with the ef- 2 manner fects A. However, the decrease of g to stomatal conductance) was affected on less pronounced than that of A, partic- only to a minor extent. was ularly during the first 4 d after transplant- ing. In February, the recovery of g in treat- ments TtP and Tt took place only from d Root and mycorrhizal regeneration 11, and recovery of g was also observed a in treatment LI. Root (fig 5) and mycorrhizal (fig 6) regener- Infigure 4 the gas exchange data of fig- ation of the transplanted seedlings oc- curred fromd 11 after transplanting in No- ures 2 and 3 are presented in A vs C i vember, and from d 4 in February. Root graphs. For both measurement periods regeneration was the highest in treatment and in all treatments the decline of A in re- TtP for both periods and was markedly sponse to transplanting was accompanied lower in the other treatments (fig 5). The by increasing C and was primarily due to , i
seedlings of treatment TtP also had the highest mycorrhizal regeneration in Febru- ary (fig 6), but not in November. Mycorrhi- zal regeneration in the LI treatment was identical to that in TtP and superior to that in Tt in November, but was noticeably low- than that in the other treatments in Feb- er ruary. Before transplanting, needle P concen- Water and nutrient status tration was significantly higher in the TtP seedlings than in the other treatments (fig No significant alteration in ψ was ob- 7). Treatments Tt and LI had identical nee- wp served after transplanting in any of the dle Pconcentrations in November, while in treatments and all treatments had similar February the needle P concentration was values ranging from -0.8 to -0.6 MPa slightly but significantly higher in LI than in wp ψ Tt. In February, transplanting significantly (data not shown).
reduced the needle P content in TtP, while no relationship between these parameters this concentration remained unchanged in and the needle N concentrations. There the other treatments. was a significant correlation between A and needle P concentration only in treat- Needle N concentration in the LI treat- ment Tt (fig 9a), in the other treatments A ment was significantly lower than those of was not related to P. Stomatal conduc- treatments Tt and TtP in November and tance was significantly correlated with P lower than in TtP in February (fig 8). The via a parabolic function (fig 9b), with the seedlings of treatment Tt had higher N minimum of g occurring at about 2000 concentrations in February (fig 8). The -1 μg·g P in the needles. The clearest pic- seedlings of treatment Tt had higher N concentrations in February than in Novem- ture of limiting effect due to P was ob- ber, while no seasonal changes occurred served relative to the WUE data shown in in the other treatments. Transplanting had figure 9c: there was a close linear relation- no significant effect on needle N concen- ship between WUE in treatment Tt, while tration in any of the treatments. the plots relative to treatments LI and TtP occupied the non-limiting P region (P con- Gas exchange parameters of the indi- centration superior to 700 μg·g of the ) -1 vidual plants were examined with respect general relationship. to their needle nutrient status. There was
DISCUSSION -1 l mg· (P) nutrient solution were taller and had a higher biomass that the seedlings associated with T terrestris but supplied The associated with T terrestris with a 10 mg· (P) solution. Seedlings -1 l seedlings mycorrhizal with L laccata and grown un- and with a non-limiting (40 supplied
der P conditions (10 mg· P) -1 l also observed relative to the CO assimila- limiting 2 taller than the seedlings infected with tion characteristics of the seedlings at the were T terrestris and supplied with the same so- end of the first growing season. As com- lution (table I). However, both root collar pared with the Tt seedlings, needle surface diameter and total plant biomass were not area (table I) and CO assimilation rates 2 significantly different between the two lat- (table II) of the LI seedlings were about 42 ter treatments. Harley and Smith (1983) and 48% higher, respectively, thus confer- and Guehl et al (1990) have reported simi- ring to the LI seedlings a whole plant CO2 lar results indicating i), that the extent to assimulation capacity about 2.1 times that which growth was affected by ectomycor- in the Tt seedlings and approximately rhizal infection will depend on the fungal equivalent to that in the TtP seedlings. species and strain used as mycobiont and Several authors (Jones and Hutchinson, ii), that there may be a discrepancy be- 1988; Guehl et al, 1990) have reported tween effects of mycorrhizae on stem el- similar modulations of host plant CO as- 2 ongation on the one hand and on diameter similation capacity due to the nature of the and weight growth on the other. Tyminska mycobiont. CO assimilation rate was 2 et al (1986) observed higher biomass clearly P limited in treatment Tt (fig 9a). Using 31 nuclear magnetic resonance, P growth in Pinus silvestris seedlings infect- ed with L laccata than in seedlings infect- Foyer and Spencer (1986) studied the ef- ed with T terrestris over a wide range of P fects of reduced phosphate supply on in- concentrations in nutrient solution (0.1-31 tracellular orthophosphate (Pi) distribution ). -1 l mg· These authors also observed that and photosynthesis in Hordeum vulgare the difference in biomass between the two leaves. They observed that i), over a wide range of leaf Pi, the cytoplasmic Pi level is treatments was not accompanied by a sig- maintained constant, while the vacuolar Pi nificant difference in needle P concentra- tion, and suggested the stimulating effect is allowed to fluctuate in order to buffer the Pi in the cytoplasm and ii), that an overall of Laccaria laccata - even observed in minimum cytoplasmic Pi concentration of seedlings with a low percentage of mycor- between 5-10 mmol· is required to sus- -1 l rhizal roots - to be related to the capacity tain optimal rates of photosynthesis in the of this fungus to produce growth regulators light. Despite the relatively high P concen- such as indole acetic acid (IAA). They sup- trations found in our study in all the LI and ported this assumption by the work of Ek TtP seedlings, some seedlings of these et al (1983) who found that the same treatments exhibited very low A values (fig strain of L laccata produced large quanti- ties of IAA. In the present study with Pseu- 9a). Thus, other limiting factors are likely to dotsuga menziesii as the host plant, be involved. significant differences in needle P Water-use efficiency was higher and concentrations were found between Tt and less variable in LI than in Tt (table II, fig 1). LI (figs 7 and 9). Furthermore, needle P Guehl et al (1990) observed that Pinus pin- concentration in LI was intermediate be- ea seedlings associated with different ec- tween those in Tt and TtP. That the growth tomycorrhizal fungi were characterized by stimulating effect of Laccaria laccata is higher and less variable WUE values than mediated, at least partially, by a P nutri- non-mycorrhizal plants. This result is of tional effect cannot be precluded here. great importance, since it indicates that ec- tomycorrhizal infection may confer en- In the present study, the superiority of L hanced drought adaptation to the host laccata as compared to T terrestris was
alterations of the mesophyll photosynthetic plant, not only by improving water uptake capacity. Guehl et al (1989) reached the (Druddridge et al, 1980) and plant water same conclusions with transplanted Ce- relations (Boyd et al, 1985), but also drus atlantica seedlings. Our results also through higher WUE. In the present study, indicate that the decline in A cannot be ac- the data of figure 9c suggest that the im- counted for by alterations in plant water provement of WUE in the L laccaria infect- status and in needle nutrient status (N and ed seedlings as compared to the T terres- P). The only significant effect of transplant- tris seedlings is mediated by a nutritional P ing on needle nutrient status was the de- effect involving both effects on A (fig 9a) crease found for P in the TtP seedlings in and g (fig 9b). It is worth noting that there February, in which the recovery of A after was a clear tendancy for g to be increased transplanting was most marked. The na- when total leaf P was lower than 2 000 ture of the factor triggering the decline of A μg·g In Zea mays, Wong et al (1985) . -1 remains unknown. In a previous study observed a dramatic decrease in A without (Guehl et al, 1989) it has been established any effect on WUE (A/g ratio) when P in for transplanted Cedrus atlantica seedlings the nutrient solution was decreased from that the recovery of A, following the initial 41 to 1.2 mg·l However, in Pinus radia- . -1 phase of decline, was concomitant with ta, Conroy et al (1988) found lower WUE in root regeneration. The results obtained P deficient plants (needle P concentration here (figs 2, 5, 6) suggest that the recovery 700-800 μg·g than in non deficient ) -1 of A was related to the recovery of mycor- plants (needle P between 1 000 and 1 500 rhizal activity rather than regeneration of μg·g Thus, their critical value (800 ). -1 elongating non-mycorrhizal white root tips. ug·g was the same as in our experi- ) -1 Two mechanisms could be involved: pro- ments. Harris et al (1983) found that in leaf duction of growth regulators by the grow- discs of Spinacia oleracea, low P led to a i ing fungus, and/or improvement of water loss of stomatal control and wide stomatal and mineral uptake through the re- apertures, while high Pi induced stomatal establishment of mycelial connections be- closure. In the same species, Herold tween the root and the soil. Our results (1978) observed that mannose and deoxy- also show that the ability of the plants to glucose induced wilting by metabolically regenerate mycorrhizae after transplanting sequestering Pi. Feeding Pi deficient Hor- is affected by seasonal parameters as well deum vulgare and Spinacia oleracea cut as their ability to regenerate roots (Ritchie leaves with Pi through the xylem transpira- and Dunlap, 1982). tion flow, Dietz and Foyer (1986) observed a short-term (5 min) increase in CO as- 2 similation and a concurrent decrease in ACKNOWLEDGMENTS transpiration, resulting in a marked in- crease of WUE. This work was supported by a grant from the Of- Transplanting markedly reduced A in all fice National des Forêts. The authors are grate- treatments in both experimental periods ful to R Zimmermann from the University of Bay- (fig 2). Analysing gas exchange data in A reuth (FRG) for mineral analyses. They wish to thank JL Churin, B Clerc, JM Desjeunes, P vs C graphs (fig 4) clearly established that i Gross and F Willm, INRA Nancy, for their techni- this decline of A occurred while the diffu- cal assistance and JL Muller for drawing the fig- sional CO supply to the chloroplasts was 2 ures. They are grateful to Pr B Dell (Murdoch enhanced (C increased), thus indicating i university, Perth, Australia) for reviewing the that the changes in A were primarily due to manuscript.
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