Báo cáo khoa học: "Sensitivity of seedlings from different oak species to waterlogging: effects on root growth and mineral nutrition"

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Original article Sensitivity of seedlings from different oak species to waterlogging: effects on root growth and mineral nutrition P Biron E M Dreyer Colin-Belgrand 1 d’Étude des Sols et de la Nutrition, INRA Nancy, Champenoux, 54280 Seichamps; Laboratoire 2 Laboratoire de Bioclimatologie et d’Ecophysiologie Forestière, INRA Nancy, France 54280 Seichamps, Champenoux, (Received 16 August 1990; accepted 30 November 1990) Summary — The tolerance of oak seedlings from 3 species (Quercus robur, Q rubra, Q palustris) to a 7-wk period of waterlogging was tested under greenhouse conditions. The seedlings had comple- ted their height growth when treatments were applied. A permanent water table was maintained at 6 cm below the soil surface. Shoot growth, root growth and mineral content of xylem sap (P, K, Ca, Mg) and leaf tissues (N, P, K, Ca, Mg, S, Mn) were monitored weekly. Waterlogging had strong consequences on root development; flooded roots decayed, while hypertrophied lenticels and sub- sequently adventitious roots appeared on the taproot. Although the mineral nutrient content in xylem sap displayed significant differences between species, no effect of waterlogging could be detected. But the combination of constant concentration and reduced transpiration in waterlogged seedlings probably resulted in a reduced nutrient flux to the leaves. Leaf nutrient contents decreased marked- ly, in particular for total N, and to a lesser extent for S and K; but in all cases they remained well above deficiency levels. No phytotoxic accumulation of Mn could be detected. Important interspecific differences appeared. The development of root adaptations was much greater for Q robur than for both Q palustris and Q rubra, probably indicating a higher tolerance to flooding in the former spe- cies. Surprisingly, N and S concentrations decreased more in Q roburthan in both other species, but this could be due to the fact that only Q robur continued leaf growth, leading to a dilution of N in leaf tissues. Quercus palustris / Quercus rubra / Quercus robur / xylem sap hypoxia / Résumé — Sensibilité à l’ennoyage de semis de plusieurs espèces de chêne : effets sur la croissance racinaire et le statut nutritionnel. La toléranceà l’hypoxie racinaire a été testée sur des semis de 3 espèces de chênes (Quercus robur, Q rubra, Q palustris) au cours d’une période d’ennoyage contrôlé de 7 semaines. La nappe d’eau permanente était maintenue à 6 cm de la sur- face du sol, et ce traitement a été appliqué à la fin de la période de croissance active en hauteur. La croissance aérienne, racinaire, et les teneurs en éléments minéraux de la sève brute (P, K, Ca, Mg) et des tissus foliaires (N, P, K, Ca, Mg, S, Mn) ont été mesurées hebdomadairement. L’ennoyage a provoqué de fortes perturbations de la croissance racinaire; les racines ennoyées ont rapidement dépéri, alors que des lenticelles hypertrophiées, puis des racines adventives sont progressivement * Correspondence and reprints
au collet du pivot racinaire. Les teneurs en éléments minéraux de la sève ont présenté des apparues différences interspécifiques significatives, mais aucune modification induite par la contrainte n’a pu être détectée. Étant donnée la réduction observée de la transpiration, cette constance des concentra- tions s’est cependant probablement traduite par une forte réduction du flux total d’éléments minéraux vers les feuilles. Les teneurs foliaires en éléments minéraux ont sensiblement diminué au cours de l’ennoyage, en particulier en ce qui concerne N, et dans une moindre mesure S; mais dans tous les cas, les concentrations foliaires sont restées largement au-dessus des seuils de carence décrits pour les chênes. L’ennoyage ne s’est pas traduit par une accumulation toxique de Mn. D’importantes diffé- rences interspécifiques dans les réactions à la contrainte sont apparues. La néoformation racinaire a été beaucoup plus importante chez Q robur que chez Q palustris et Q rubra, ce qui semble indiquer une meilleure tolérance à l’ennoyage chez la première espèce. Les concentrations foliaires de N et S ont plus fortement diminué chez Q robur que dans les 2 autres espèces, mais cette différence est probablement due au maintien d’une certaine croissance chez Q robur, entraînant une dilution de l’azote initialement présent et non renouvelé du fait de l’ennoyage. Quercus robur / Quercus rubra / sève sylémique palustris / hypoxie racinaire / Quercus exhibit different behaviours when planted INTRODUCTION in temporarily waterlogged soils in North- eastern France. The former species seems Forest trees display a broad spectrum of to present a better tolerance to soil hypox- tolerances to waterlogging. Their degree ia at the seedling stage, as shown by of tolerance is often estimated from either growth experiments with different depths of duration of survival or measured growth water tables (Lévy et al, 1986). But the lat- and productivity in forest stands or young ter displays a better productivity on tempo- plantations submitted to root hypoxia due rary flooded soils in forest stands and to flooding under natural conditions. Survi- shows much larger increases of growth fol- val time may vary from a few wk for the lowing mechanical soil drainage (Becker most sensitive species, to several (2-3) yr and Lévy, 1986). At the seedling stage, a for the most tolerant ones (Kozlowski, rating of decreasing flood tolerance 1982). Large differences in tolerance showed that Q robur behaved better than sometimes appear in closely related spe- Q petraea, and Q rubra had the poorest cies, and the underlying physiological growth (Belgrand, 1983). mechanisms are seldom clearly analysed. tolerance Differences in waterlogging greatly in their sensi- Oak species vary petraea and Q robur between Q rubra, Q tivity to waterlogging. Some oak species differ- appeared strongly correlated with a are common in bottomlands and flood- ability to develop root adaptations entiated plains and seem very flood-tolerant. For in- (Belgrand, 1983). In fact, the most fre- stance, survival under inundation was 2-3 quently reported reaction of trees to soil yr for Quercus nigra, Q nuttali and Q phel- hypoxia is the induction of morphological lis (Hall et al, 1946; in Kozlowski, 1982). and anatomical changes in the root sys- Q palustris did not show altered water rela- tems of flood-tolerant species (Justin and tions after 2 yr of continuous flooding in Armstrong, 1987). Formation of hypertro- the central Mississipi valley, although it phied lenticels followed by the differentia- displayed premature leaf yellowing and ab- tion of adventitious and flood-adapted scission (Black, 1984). Q robur is thought roots has been commonly described for a to tolerate up to 97 d of flooding every broad range of species (Coutts and Arm- year (Dister, 1983). Q robur and Q petraea
of water table level. precise control Seedlings strong, 1976; Coutts, 1982; Harrington, grown in glasshouse Nancy; day near were a 1987; McKevlin et al, 1987). temperatures were maintained between 20- induces important perturba- Flooding 30 °C, with a night temperature of 16 °C main- tions in mineral nutrient assimilation. Leaf tained through heating, and humidity ≈ 60%. No N content of Picea abies was strongly re- additional light was supplied. Height growth was monitored weekly from germination on. duced by flooding (Lévy, 1981).For most elements (N, K, Fe, Mn and to a lesser ex- tent Mg and Ca) leaf content was reduced Waterlogging in different Pinus species after 30 d of root hypoxia in nutrient solutions (Topa and McLeod, 1986). But these effects were Plants were flooded with tap water on June mainly observed with trees still growing 15th. The upper level of the water table was ad- during the waterlogging period. No infor- justed daily to 6 cm below the soil surface, and maintained for 7 wk. Pots were then drained and mation on mineral nutrients circulating in seedlings allowed to grow for 2 more wk. Sixty the xylem sap of waterlogged seedlings is plants were used for each species, with 30 ran- currently available. domly selected as controls and 30 treated. The In this study, we compared 3 species experimental design consisted of 3 blocks (1 per species), in which treatments were randomly known to differ in their waterlogging toler- distributed. Destructive measurements (bio- (Q robur, Q rubra and Q palustris) ance mass, water status, nutrient content and xylem and tested their ability to produce adventi- sap composition) were made weekly on 2 ran- tious roots in response to a 7-wk flooding. domly selected waterlogged and 2 control We tried to assess the consequences of plants. Roots were rinsed with tap water. The these differences on the transport of miner- structure of the root system was observed; in particular, the presence of lenticels and the de- al nutrients to shoots, and on the leaf min- gree of root senescence were assessed visual- eral content. In a forthcoming paper ly. Root systems were divided thereafter into old (Dreyer et al, 1991) the consequences of roots, white tips and neoformed roots, and were the observed perturbation in root growth oven-dried (65 °C for 24 h). Leaves and stems on shoot physiology will be assessed. were used for mineral content analysis. MATERIALS AND METHODS Water status and xylem sap extraction Plant material Shoots of selected plants (2 control and 2 treat- ed saplings per species) were cut off once weekly after being submitted to at least 12 h Acorns were collected during autumn 1987, un- darkness, and predawn leaf water potential der individuals of Q robur L (Amance Forest, (ψ was measured with a pressure chamber. ) wb near Nancy, France), Q rubra L (Fénétrange After attaining the balancing pressure, the bark Forest, Moselle, France) and Q palustris was removed from the cut end, the pressure Muenchh (Pujo Forest, Tarbes, Hautes Pyré- was slowly increased to 2.5 MPa, and main- nées, France). Acorns were stored at -1 °C and tained for 5 min. Extruding sap was collected sown during the following February in special in- with a micropipette and frozen immediately in dividual 5-I, 25-cm deep pots, containing a 50/ liquid nitrogen before being stored at -18 °C. 50 v/v mixture of peat/sandy loam. The main Roots were rinsed with tap water and xylem sap features of this substrate are shown in table I. was extracted by the same technique as for the An external transparent vertical tubing was con- nected to the bottom of these pots, allowing a shoots.
RESULTS Effects of flooding shoot on and root growth Flooding was imposed after complete growth cessation in Q rubra and Q shoot palustris as shown by growth dynamics (fig 1).Two growth flushes had been complet- ed on Q rubra and Q palustris; while a 3rd flush was beginning on Q robur. In this lat- ter case, flooding slightly reduced height growth, while in the former 2 species, it Mineral analyses Concentrations of P, K, Mg and Ca in the xylem sap were measured directly with an inductively coupled plasma spectrometer (ICP, Jobin Yvon). Nutrient concentrations were measured together on the leaves of 2 seedlings, and the results were therefore mean concentrations of both seedlings. Total leaf nitrogen was deter- mined by Kjeldahl mineralization and a colori- metric procedure (Technicon Autoanalyser), while leaf P, Ca, Mg, K, S and Mn concentra- tions determined after wet mineralization were ICP quantitation. (HClO + H and 42 ) O Statistical analysis Results were analysed using an ANOVA and testing for differences between collection dates, species and treatments. As soon as no signifi- cant change could be detected over a longer period of time, data were gathered for the main waterlogging period (ie, from wk 1-7) and com- pared directly with corresponding controls using a Student t-test; n 14 for root and shoot xylem = 7 for leaf mineral content. sap, and n =
had no effect no shoot growth; an apparent decrease in height for Q rubra was only due to recurrent sampling and consequent reduction of plant number. No resumption of growth occurred after drainage. Leaf characteristics were very different between species but were not dramatically affected by waterlogging (table II). Q rubra had the largest leaf area per plant despite limited height, and the largest leaf specific weight, while Q robur showed only 2/3 of this area, and Q palustris had lower area and specif- ic leaf weights. Flooding had no significant effect on these parameters; specific leaf weight increased slightly but this increase was only significant for Q robur. No leaf necrosis was detected during the entire pe- riod. Root growth dynamics were much more affected by flooding. Some morphological features were common to all species: flooding induced a rapid decay of preexist- ing roots, with senescence and disappear- ance of white tips, and necrosis of tap root and flooded lateral roots. Hypertrophied lenticels appeared by the end of the 3rd week at the root collar and on non flooded roots and developed mark- edly. Finally, adventitious roots were formed from the 4th week on, in the soil
above the water table. These new roots Effects of flooding nutrient transport on poorly ramified, had a larger diame- in the xylem sap and on shoot nutrient were ter, and were not suberized even after 4 status wk (fig 4). These reactions occurred in all species, Table III shows the measured concentra- but with very different intensities. Q robur tions of mineral nutrients in the xylem sap seedlings developed abundant hypertro- extracted from roots and shoots. As no sig- phied lenticels by the end of the 3rd wk, nificant change could be detected in con- and numerous adventitious roots ap- trol or in flooded plants after wk 1, we com- peared after 4 wk of waterlogging. Q rubra pared all the data collected till the end of seedlings showed a remarkable hypertro- the waterlogging period directly. As a gen- phy of stem and lenticels but only very few eral rule, nutrient concentrations were adventitious roots, which appeared only af- about twice as high in the sap extracted ter 6 wk of flooding. Q palustris displayed from roots than in the sap from shoots. only few adventitious roots, and almost no Significant differences related to species lenticels or stem hypertrophy. were found for all the tested elements, with As shown in fig 3a, total root biomass the exception of Ca. Q robur showed the (including senescing roots) was slightly de- highest concentrations of Mg and K, while creased in flooded Q rubra and Q palustris Q rubra had the highest concentrations of after 4 wk of waterlogging but increased in P. Only seldom were the effects of flooding Q robur as compared to the control. A statistically significant. Significant reduc- strong decrease in the biomass of white tions only appeared for K and Ca in Q pa- tips, eg growing root apices, appeared at lustris and in Q rubra. Large variations be- the same time (fig 3b) in response to flood- tween individual plants did not allow closer ing in all species. The total weight of ad- comparisons. ventitious roots was very variable: Q robur developed the largest amount, while Q ru- Leaf nutrient contents showed large dif- bra and Q palustris formed only very few ferences between species. Total N was such roots. In Q robur, they achieved a significantly higher in Q robur, while Ca substantial biomass (fig 3b). was more concentrated in Q rubra (table IV). The total mass of nutrients present in the leaves was much higher in Q rubra due to a larger leaf area than in Q robur and Q palustris (table IV). Flooding induced a highly significant reduction in total leaf N, and significant reductions in S contents. The reduction in leaf nitrogen appeared very rapidly in Q robur, for which it was highly significant; it was less marked and slower but still significant in Q rubra and Q palustris (fig 4). Reductions in S and K also appeared in Q robur, and were non significant for both the other species. No phytotoxic increase in Mn could be ob- served.
DISCUSSION Root adaptations very strong in all 3 Root reactions were Shoot growth of the flooded fraction of species. Decay the root systems occurred during the first The experiment was designed to assess few weeks, with apparently the same inten- the waterlogging effects on well developed sity for all seedlings. The appearance of seedlings which had already completed hypertrophied lenticels and adventitious their annual growth. Effects on shoot roots in the soil layers above the water ta- growth were therefore only detected in Q ble was also noted in all seedlings, al- robur which was the only species still dis- though with different intensities. These root playing growth. The limited increases in reactions are a common feature of water- specific leaf weight and the lack of necro- logging effects on tree seedlings; they sis showed that waterlogging had no dele- have been observed on a wide range of terious effects on the leaves. However, this species including Quercus macrocarpa result cannot be generalised, as growing (Tang and Kozlowski, 1982), Fraxinus leaves probably would have reacted differ- pennsylvanica (Gomes and Kozlowski, 1980), Alnus rubra and Populus trichocar- ently.
(Harrington, 1987), Actinidia chinensis improve oxygen diffusion through hyper- to pa (Savé and Serrano, 1986), Gmelina arbor- trophied lenticels and gas transport to non aerated roots (Hook et al, 1971; Keeley, ea (Osonubi and Osundina, 1987), Crypto- 1979; Drew, 1983). They may also be as- meria japonica (Yamamoto and Kozlowski, sociated with resistance to iron or manga- 1987), Picea sitchensis (Coutts, 1981), Pi- (Green and Etherington, nus contorta (Coutts and Philipson, 1978) nese toxicity and many others. 1977). Flood-induced roots are white, thick, more succulent and poorly ramified, and Mineral nutrition lack root hairs; they display both larger cells and aerenchyma (Keeley, 1979; An- The reliability of our xylem sap extraction geles et al, 1986; Justin and Armstrong, technique with relatively high pressure (2.5 1987). These modifications are supposed
logging, particularly for P, Mg and K. Could these differences be related to different growth habits ? Q robur, displaying the highest K and Mg, had the greatest height growth, while Q rubra, with higher P, built up the largest leaf area. But concentrations are not necessarily correlated with the total nutrient fluxes from roots to shoots. In fact, transpiration was lower in Q rubra despite its larger leaves (Dreyer et al, 1991) and total nutrient fluxes therefore lower. Q pa- lustris had the lowest concentrations and transpiration rates among the 3 species, and therefore probably the lowest nutrient transport to the leaves. Waterlogging had only very limited ef- fects on the xylem sap concentrations; sig- nificant reductions only appeared for K. We do not know of any other attempt to analyse flooding effects on xylem sap con- tents. Effects of water stress on xylem sap composition have sometimes been as- sessed; Scuiller (1990) observed only limit- ed increases in osmotic potential and ion concentrations with decreasing predawn leaf water potential. It may be concluded that the stability of xylem sap concentra- tions, associated with a reduced transpira- tion flux (Dreyer et al, 1991), probably re- sulted in a reduction of the total flux of mineral nutrients to shoots in waterlogged seedlings. Leaf mineral contents of our seedlings for all species and treatments well were above the deficiency levels for oaks (Bon- MPa) may be questioned. The fact that neau, 1986). Large interspecies differenc- concentrations were about twice as high in es were observed for N and Ca. Despite sap extracted from roots than from shoots the fact that Q rubra is a well known calci- may be partly explained by the differences fuge species, it concentrated ≈ 2/3 more in ion mobilisation in pressurized roots vs Ca in its leaves than the other 2 species. shoots. Concentrations of K, Mg and Ca measured by Scuiller (1990) in seedlings But Q robur displayed much higher N con- tents, which may be correlated with the of different Quercus species growing on higher rates of photosynthesis observed in the same substrate were very similar to this species (Dreyer et al, 1991).Q rubra ours. Despite a large interindividual vari- mobilized the largest total amount of nutri- ability, significant differences appeared be- ents due to its high leaf area. The effects tween species independently from water-
of on leaf nutrient contents waterlogging of waterlogging tolerance Comparison limited and showed a great variability among species were between species and measured elements. Observed decreases in total N, which ap- The 3 oak species tested are thought to peared in Q robur seedlings and to a less- display wide differences in waterlogging er extent in the other species, were in ac- tolerance. Q robur is supposed to tolerate cordance with earlier observations by Lévy root hypoxia (Lévy et al, 1986), Q rubra is (1981) with Picea abies, or Meyer et al well known for its marked intolerance, (1986) with Gossypium hirsutum. In fact, while Q palustris is supposed to be more decreases in N contents are often the ear- liest response to flooding (Drew and Sis- tolerant (Abbott and Dawson, 1983). The intensity of the root reactions observed 1979; Meyer et al, 1986; Harrington, woro, 1987). These decreases may either be was in agreement with these observations due to nitrate reduction and accelerated for Q robur and Q rubra and confirmed ear- denitrification (Lévy, 1981),or to the inabil- lier findings (Belgrand, 1983). The weak ity of the roots to take up enough N even reactions of Q palustris roots were surpris- before the onset of strong denitrification ing and may have been caused by our par- (Drew and Sisworo, 1979; Meyer et al, ticular growth conditions. Root reactions of 1987). Decreases in other elements in Q actively growing seedlings may be very dif- robur were not statistically significant. In ferent from those observed here. both the other species, apart from de- Differences in root reaction were not fol- creases in N, no difference could be de- lowed by strong differences in mineral nu- tected. In this respect, our results differ trition. The greatest reductions appeared in from earlier reports, which showed signifi- Q robur, which showed the largest root ad- cant decreases in almost all the tested ele- aptations. This could be explained by a di- ments (N, P, K in 3 different Pinus spe- lution of elements, particularly N, in the still cies; Topa and McLeod, 1986; K, Mg in growing tissues of Q robur associated with Alnus rubra and Populus trichocarpa; Har- a decrease in absorption. In both the other rington, 1987). In fact, improving soil fertili- species, the cessation of growth, which ty often limits the effects of waterlogging was not related to waterlogging, allowed a on tree growth (De Bell et al, 1984), but in relative stability of nutrient contents. In these cases, flooding was imposed on ac- fact, the mineral richness of the culture tively growing plants, while our seedlings medium which resulted in mean leaf con- had almost stopped shoot and leaf growth. tents largely above deficiency levels and Only Q robur maintained to some extent even above optimal levels (Bonneau, growth and also displayed the most signifi- 1986) probably explained this stability. cant reductions in leaf mineral contents. The most important difference in water- Further data are needed to clarify mineral logging tolerance that we observed was re- budgets of saplings submitted to waterlog- lated to the ability of Q robur to develop ging and flooding. root adaptations in flooded plants. It is still Mn toxicity, which has been associated difficult to develop an analysis of flooding with waterlogging by some authors tolerance between species in the absence (Sonneveld and Voogt, 1975) was not de- of a general model of hypoxic stress ef- tected here; Mn contents decreased or re- fects at the whole sapling level. There is mained at the same levels as in controls, still need for further research to improve as was also observed by Topa and McLe- our knowledge in this area. od (1986) and Harrington (1987).
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