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Nội dung Text: Báo cáo khoa học: "Compared sensitivity of seedlings from 3 woody species (Quercus robur L, Quercus rubra L and Fagus silvatica L) to water-logging and associated root hypoxia: effects on water relations and photosynthesis"

article Original Compared sensitivity of seedlings from 3 woody species (Quercus robur L, Quercus rubra L and Fagus silvatica L) to water-logging and associated root hypoxia: effects on water relations and photosynthesis E Dreyer Écophysiologie, Unité d’Écophysiologie Forestière, INRA-Nancy, Bioclimatologie et F 54280 France Champenoux, 1993; accepted 25 October 1993) 7 June (Received Summary - Seedlings of Quercus robur, Q rubra and Fagus silvatica were submitted to a period of partial (water table at 6 cm below ground) or total water-logging for 4 weeks. Important disorders were induced by the latter treatment in growth (root decay, partial leaf wilting), water relations (decreased predawn water potential) and photosynthesis (stomatal closure, reduced net assimilation rates, lowered O evolution under saturating CO and irradiance, and limited 2 2 photochemical efficiency of PS II). It has been concluded that the observed stomatal closure was accompanied by strong disorders at chloroplast level, which happened without visible water- logging-induced deficiencies in mineral nutrient supply. Reactions to partial water-logging were much more limited. F silvatica displayed the strongest disorders in response to both treatments, Q robur showed only slight stress effects in response to partial water-logging and Q rubra had intermediate behaviour. These observations are in agreement with the reported differences in to water-logging of adult trees in the stand. The precise chain of events leading to these sensitivity disorders in the shoots of water-logged seedlings remains to be elucidated. stomatal conductance / conductance / mineral nutrition / / hydraulic photochemistry photosystem II Abbreviations. ψ and ψ midday and predawn leaf water potential (MPa); PFD: photon flux density (μmol : wα wm -2 -1 m s A: net CO assimilation rate (μmol m s g leaf conductance to water vapour (mmol m s c -2 -1 w -2 -1 i );: 2 ); ); : intercellular concentration of CO (μmol mol Δw: leaf to air difference in vapour mole fraction; g specific 2 ); -1 : L hydraulic conductance from soil to leaves (mmol m s MPa Fo, Fm and Fo’, Fm’: basal and maximal -2 -1 -1); fluorescence after dark adaptation and 10 min at 220 μmol s respectively; Fv/Fm: photochemical efficiency of -2 -1 , PS II in dark-adapted leaves: ΔF/Fm’ and Fv’/Fm’: photochemical efficiency of PS II and of open PS II centres after 10 min at a given irradiance (220 or 800 μmol m s qp: photochemical quenching of fluorescence; A -2 -1 ); : max maximal rate of photosynthetic O evolution under 5% CO and 800 μmol mol irradiance (μmol O m s C: -1 2 -2 -1), 2 2 control treatment; PF: partially water-logged treatment; F: completely water-logged treatment.
Résumé - Sensibilité de jeunes plants de chêne pédonculé (Quercus robur L), de chêne rouge d’Amérique (Q rubra L) et de hêtre (Fagus silvatica L) à l’ennoyage et l’hypoxie racinaire : effets sur la photosynthèse et les relations hydriques. De jeunes plants de chêne pédonculé (Quercus robur L), de chêne rouge d’Amérique (Q rubra L) et de hêtre (Fagus silvatica L) ont été soumis à un ennoyage total (nappe affleurant en permanence à la surface des pots) ou partiel (nappe à 6 cm sous le niveau du sol) pendant 4 sem. Le premier traitement a fortement perturbé la croissance des plants en provoquant une importante mortalité racinaire. Des dysfonctionnements majeurs ont aussi été constatés sur les parties aériennes : diminution du potentiel hydrique de base, fermeture des stomates, limitation de l’assimilation nette de CO et de 2 la capacité photosynthétique (mesurée par le dégagement d’O en conditions de CO et 2 2 d’éclairement saturants), réductions irréversibles de l’efficience photochimique du phostosystème II. Le second a provoqué des réactions plus limitées. D’importantes différences interspécifiques ont été constatées ; F silvatica a présenté la plus grande sensibilité, avec des nécroses foliaires très étendues, et des réductions massives de la capacité photosynthétique dans les 2 traitements, alors que Q robur n’a que peu réagi à l’ennoyage partiel. Ces résultats sont en accord avec les observations sur les exigences écologiques de ces espèces en peuplement. Enfin, elles démontrent que les désordres imposés à la photosynthèse par l’ennoyage sont dus à la conjonction d’une fermeture des stomates et d’importants dysfonctionnements au niveau cellulaire, qui n’ont pas été induits par une dégradation de la disponibilité en éléments minéraux, les concentrations totales en N, P, K, Ca, Mg, S mesurées au niveau foliaire n’ayant que peu changé au cours des traitements. hydraulique / nutrition minérale / photochimie / conductance stomatique / conductance photosystème II INTRODUCTION water-logging intolerant than even more both the indigenous species (Belgrand, 1983). Fagus silvatica is known to be Temporary water-logging is a very common strongly intolerant, and never occurs on soils occurrence in the plain forests of north-east- in which temporary water tables occur. ern France. Oak stands in particular fre- The effects of water-logging woody on quently grow on soils with temporary high species have frequently been analysed water tables, which produce gleyic or (Kozlowski, 1982). Water-logging induces pseudo-gleyic accumulation layers in the soil hypoxia and decreases redox-potential soil profile (Becker and Levy, 1986). Water- (Gambrell et al, 1991) which may impair logging has both direct (poor growth) and root metabolism (Konings and Lambers, indirect consequences (shallow rooting pre- 1991),decrease nitrogen availability through disposing trees to summer water stress) for denitrification (Drew, 1983), and promote tree growth and productivity (Becker and the accumulation of toxic species such as Levy, 1986). Oak species present different reduced manganese or iron cations (Gam- sensitivities to this constraint: Quercus robur brell et al, 1991).Root dysfunctions in turn is known to exhibit a lower sensitivity than induce marked stress effects on shoots. Q petraea to direct effects of soil hypoxia, Reduced root hydraulic conductance but also to display some difficulties in coping (Andersen et al, 1984; Harrington, 1987; with periods of drought following water-log- Smit and Stachowiak; 1988) has sometimes ging (Becker and Levy, 1986; Levy et al, been reported to promote decreases in leaf 1986). Q rubra, which is now widely afforested in France, is suspected to be water potential (Zaerr, 1983; Osonubi and
photosynthesis during water-log- tions of Osundina, 1987). Stomatal closure and stress has still to be identified. ging associated decreases in net CO assimila- 2 tion are now considered as general In the present work, we analyse photo- responses to root anoxia (see, for instance synthetic functions of potted seedlings from Dreyer et al, 1991; Pezeshki, 1991; Reece the 3 cited tree species during periods of and Riha, 1991; Topa and Cheeseman, water-logging using gas exchange mea- 1992). Reductions in growth, appearance surements to assess stomatal conductance of leaf necroses and decreases in leaf nutri- and net CO assimilation rates, photosyn- 2 ent contents have also been frequently thetic oxygen evolution under high CO con- 2 described (Colin-Belgrand et al, 1991; Drew, centrations, saturating irradiance to esti- mate maximal photosynthesis, and finally 1991. ) chlorophyll-a fluorescence to monitor photo- mechanisms leading The physiological chemical efficiency of PS II. to these disorders in shoot behaviour are poorly understood. It is now widely accepted that the decreases in leaf water potential MATERIAL AND METHODS due to reduced hydraulic conductance do not form the trigger mechanism leading to stomatal closure during water-logging, and Plant material that hormonal signals must be involved. Root issues abscisic acid (ABA) is thought Acorns of Q robur L and Q rubra L were collected to be this signal during water-logging (Brad- under selected individual trees in the Forêt Doma- ford, 1983; Jackson and Hall, 1987; Zhang niale de Manoncourt en Woëvre (Meurthe et and Davies, 1987). Large amounts of ethy- Moselle, eastern France) and in the Forest of lene are issued during root hypoxia and Schopperten (Moselle, eastern France) during seem to induce some of the growth reac- Autumn 1989 and kept over-winter in a cold tions like the appearance of root chamber at -1°C. Sixty seedlings of each species aerenchyma (Jackson, 1985; Voesenek et were grown in a sandy loam in 5 L, 25-cm-deep pots from spring 1990 onwards in a glasshouse at al, 1992), but an involvement in stomatal INRA Champenoux, under natural illumination behaviour and photosynthesis regulation (irradiance≈ 70% of external; minimal tempera- remains to be demonstrated. There are still ture over winter 10°C, maximal temperature dur- many open questions about how leaf pho- ing summer 30°C; manual watering; fertilisation tosynthesis is impaired. Water-logging- with 30 g slow release fertiliser per plant on June 12, 1990, Nutricote 100, N/P/K 13/13/13 + oligo induced decreases of net CO assimilation 2 elements). Sixty F silvatica L saplings (1-year- rates (A) have been reported to occur at old saplings from Office National des Forêts, Clair- constant or even increasing values of inter- lieu nursery near Nancy, seed collected in the cellular CO concentrations (c (Pezeshki ) i 2 Forêt Domaniale de Haye) were planted into sim- and Sundstrom, 1988; Smith and Ager, ilar pots during February 1990 and grown under 1988; Dreyer et al, 1991; Vu and Yelen- the same conditions. At the end of 1990, mean heights and stem diameters were: 473 ± 7.3 and ovski, 1991),which would mean that pho- 7.58 ± 0.24 mm, 331 ± 7.1 and 6.48 ± 0.23 mm, tosynthetic processes other than the diffu- 356 ± 4.05 and 6.67 ± 0.38 mm for Q robur, Q sion of CO through stomata are impaired. 2 rubra and F silvatica, respectively. Calculation of c in stressed leaves may lead i to artefacts due to potential non-uniform stomatal closure (Terashima et al, 1988), Experimental design and the above results need therefore to be confirmed by independent methods of anal- An external transparent tubing was connected to ysis. Moreover, the site of primary limita- the bottom of the pots, allowing a precise con-
trol of the water table. Forty-eight seedlings were of CO c μmol mol and presented as A/c ), -1 ,, 2i i selected in each species, and randomly dis- relationships (Guehl and Aussenac, 1987). We tributed into 3 treatments: control (C); partially computed the specific (ie related to leaf area) flooded to 6 cm below soil surface (PF); and com- hydraulic conductance from soil to leaves as: g L = pletely flooded (F). Water-logging was initiated g Δ (ψ ψ according to Reich and w w wd wm - ), • on May 25 1991 with tap water; the level of the Hinckley (1989). water table was controlled every day. Under such conditions, O partial pressure is expected to 2 drop in a few days to well below the critical oxy- Chlorophyll fluorescence gen pressure for root tip growth (around 20 kPa) and oxygen evolution or even for older root maintenance (5 kPa) (Saglio et al, 1984; Drew, 1991) and soil redox potential to decrease to -100 to -200 mV (Gambrell et Chlorophyll-a fluorescence from photosystem II al, 1991).The characteristic smell for methane (PS II) was recorded at wavelengths around 690 production was detected in our pots after approx- nm at ambient temperature with a pulse ampli- imately 8-10 d of water-logging. Sapling tude modulated fluorometer (PAM 101, Walz, responses to these conditions were tested every Germany), using the procedure described by week on 3 randomly selected individuals in each Epron and Dreyer (1992). Leaf disks (20 mm species x treatment. Midday leaf water-potential diameter) were punched from seedlings kept in (ψ was measured in the greenhouse on the ) wm darkness overnight, and inserted into a temper- selected individuals, which were thereafter trans- ature-controlled leaf-disk holder (22°C). Initial ported into a growth chamber with following cli- fluorescence (Fo) was determined with a pulsed mate: temperature 22/16°C; 16/8 h day/night; light-emitting diode (< 10 mW m at a frequency ) -2 irradiance around 300 μmol m s Chlorophyll- -2 -1. of 1.6 kHz; maximal fluorescence (Fm) was a fluorescence and oxygen evolution at 5% CO 2 obtained with an oversaturating flash of white were measured the following morning, and gas light (0.7 s; 4 000 μmol m s Schott KL 1 500N -2 -1 ; exchange monitored on 2 leaves per plant in the FRG). The optimal photochemical efficiency of afternoon, after at least 4 h of illumination. PS II, eg after complete relaxation in the dark Predawn leaf water potential (ψ was mea- (Krause and Weis, 1984; Genty et al, 1987), was ) wm sured during next morning and all saplings were estimated from the ratio Fv/Fm (Fm - Fo)/ Fm. = harvested for biomass, chlorophyll content, and After 10 min exposure to actinic white light (Schott KL1500, FRG, 220 μmol m s an additional -2 -1 ), nutrient composition determination.The whole white light flash allowed computation of the photo- procedure was repeated every week from week 1 chemical efficiency of PS II according to Genty to 4 after beginning of water-logging. Twelve et al (1989) from ΔF/Fm’ were ΔF = Fm’-F (F: saplings had been analysed per species and level of steady-state fluorescence, and Fm, fluo- treatment at the end of the experiment. rescence during a saturation). Basic fluorescence (F0) was recorded immediately after switching off actinic illumination, and used to compute the Photosynthesis and water relations photochemical efficiency of open PS II reaction centres as: Fv’/Fm’ = (Fm’-Fo’)/Fm’. Photo- chemical quenching, ie the fraction of open PS ψ and ψ were measured on 2 leaves per wm wd II reaction centres, was computed according to individual with a pressure chamber. Gas Genty et al (1989) as: qp (Fv’/Fm’) / (ΔF/Fm’). A exchange was monitored with a portable photo- = second period of induction was imposed imme- synthesis chamber Li Cor 6200 on 2 leaves per diately thereafter (10 min, 800 μmol m s and -2 -1 ), plant. Mean values ± confidence intervals of the parameters recorded. microclimate during measurements were as fol- same lows: PFD: 310 ± 2 μmol m s leaf tempera- -2 -1 ; Maximal photosynthetic O evolution rate 2 ture: 26.1 ± 0.2°C; CO concentration in air: 422 2 (A μmol O m s was measured on a sec- 2 -2 -1 ) , max ± 2 μmol mol leaf to air difference in water ; -1 ond leaf disk with an oxygen electrode assembly vapour (Δw): 20.0 ± 0.4 Pa kPa Leaf area was . -1 (LD2 MK2, Hansatech, UK, 22°C, N + O + CO 222 : determined with a ΔT planimeter. Results were 80/15/5%). A period of 20 min induction under computed as in Ball (1987) (net assimilation rate, an irradiance of 800 μmol m s (Light Unit LS2, - 2 -1 A, μmol m s leaf conductance to water vapour -2 -1 : Hansatech, UK) was provided before the mea- g mmol m s and intercellular concentration -2 -1 ; , w surements.
(brown spots at leaf margins); these week Specific leaf weight (g dm oven-dried at , -2 85°C for 24 h) and total chlorophyll content (3 ml together with brown spots along necroses, DMSO, incubation at 60°C during 90 min, opti- vascular bundles, progressively spread over cal densities measured at 663 and 645 nm, the whole leaf laminae in the following according to Hiscox and Israeltam, 1979) were weeks. Surprisingly, after 3 weeks, new determined on the same disks. growth was initiated, and short shoots with tiny, vitreous leaves were formed, while the primary foliage decayed progressively. No Leaf nutrient content epinasty was observed. Root systems dis- played a strong decay with no lenticels and Saplings were separated into leaf, stem and root no new root formation. PF induced analo- compartments, and oven-dried at 85°C for dry- gous symptoms with less severity and a determination. Total mineral content was weight week’s delay; roots survived in the upper, measured as follows. Samples were crushed unflooded soil layer but no additional root (Tecator-Cyclotrec 1093 Sample Mill) and total growth occurred there. New leaf formation nitrogen was measured with an autoanalyzer Technicon after mineralization with H and 4 SO 2 was slightly more intense than in F. H and all other elements (S, P, Mn, Mg, Ca, K) , O 2 Oaks displayed very different symptoms. were quantitated with an ICP (Jobin Yvon JY 438 F saplings never showed leaf necrosis, but Plus) after a mineralization with HClO and H 4 . O 2 sometimes very strong epinasty after 2 weeks. On a few individuals, epinastic leaves dried out very rapidly during days with high Statistical analysis of results VPD and temperature (around 30°C). Root systems of Q robur and Q rubra behaved Due to the rapidity of reactions to water-logging, differently. While F induced almost the same many parameters were strongly modified during intensity of root decay, with no appreciable week 1, but showed no significant evolution from growth, no lenticels and no adaptive feature week 1 to week 4. We therefore pooled the data to water-logging, PF allowed growth of new together, and analysed them as a factorial design ( 3 species x 3 treatments x 12 individuals). roots in the non-flooded soil layer on Q robur Results are presented as means ± standard error alone, and none at all on Q rubra. Newly of the mean. grown roots were thick, non-ramified and white along their whole length. Their forma- tion began from the third week on wards. RESULTS This observation is in agreement with that made earlier by Colin-Belgrand et al (1991) on the same species. Growth and external signs Figure 1 displays the total biomass of the of water-logging stress saplings. Reductions in root biomass were very significant due root decay in the F treat- Flooding was imposed during a period of ments. Shoot biomass was less affected, growth in all species. The height active and only a fraction of the leaves completely growth of F silvatica was slow (due to strong dried out. ramification and sympodial growth in this species). Growth was completely stopped on all species by the total (F) and partial Water relationships (PF) water-logging treatments. Visual symp- toms induced by water-logging were very Water relationships were strongly affected different among species. In F silvatica, F by the water-logging (table I). Significant induced visible signs of leaf necrosis after 1
decreases in predawn (ψ and midday ) wd General effects of water-logging (ψ leaf water potentials were recorded ) wm photosynthesis on in F in Q robur and Q rubra, while PF pro- moted only limited effects. Because of reduc- The effects of water-logging on A is shown tions in leaf area, the estimated specific soil through A vs c relationships in figure 2. i to leaf hydraulic conductance (g showed ) L Important interspecific differences appeared. no significant decrease in PF, and F even Q roburdisplayed both highest values of A induced a slight increase of g Q robur. L in in controls and very limited decreases in Srong leaf decay in F silvatica in F impaired the water relationship measurements.
response to PF. Q rubra was characterised and lowest values for maximal fluo- (Fo), by low A and c in controls, and by a stronger (Fm), and for photochemical effi- rescence i decline in PF, and finally, F silvatica dis- ciencies of dark-adapted PS II (Fv/Fm), PS played low A in controls and the steepest II (ΔF/Fm’), and open reaction centres (Fv’/Fm’) at 800 μmol m s PFD. On dark- -2 -1 decrease in PF. All 3 species responded to F by large reductions in A which reached leaves, basic fluorescence Fo was adapted values below 1 μmol m s Declines in A -2 -1 . constant with water-logging, displaying slight increases only in Q robur. Maximal fluores- were accompanied by increases in c sug- , i cence Fm decreased only slightly in F treat- gesting that stomatal closure was not the ments for Q roburand Q rubra. In contrast, only cause of these decreases in photo- F silvatica reacted very strongly, present- synthetic activity. ing steep declines in both treatments. The O evolution rates at saturating CO 2 2 photochemical efficiency of PS II in dark- (A and total chlorophyll content ) max adapted leaves (Fv/Fm) declined signifi- decreased in response to PF and F as com- cantly in the F treatment, F silvatica dis- pared to controls (fig 3) with the exception of playing the sharpest decline and Q robur Q rubra, where controls displayed very low the most limited. The relationship between A Total chlorophyll contents in the leaf . max weekly A and Fv/Fm (fig 4) was very differ- disks were highest in Q robur, lowest in F sil- ent among species: in both oaks Fv/Fm vatica. A was highest in control Q robur, max remained above 0.7 even while A had and very low and close to A in all other decreased to almost zero, while in F silvat- species and treatments. ica Fv/Fm was low even in controls and decreased at higher A. After 10 min induc- tion at 800 μmol m s the photochemical -2 -1 , Photochemical efficiency of PS II of PS II(ΔF/Fm’) of control plants efficiency was lowest in F silvatica, and highest in Q Important species-related differences appeared in some of the fluorescence parameters (table II). In particular, F silvat- ica displayed the highest basic fluorescence
robur. This is in agreement with the other observations on the photosynthetic activity of the 3 species. Flooding induced reduc- tions in ΔF/Fm’ were steepest for Fsilvatica and only moderate in Q robur. Finally, we analysed the relationship between ΔF/Fm’ and the photochemical effi- ciency of open PS II centres (Fv’/Fm’) and the photochemical quenching of fluores- cence (qp) measured at both 220 and 800 μmol m s irradiance (fig 5). All species -2 -1 and irradiance levels aligned on the same curves, which showed that the decline in ΔF/Fm’ was always accompanied by simul- taneous decreases in qp, indicating a decrease in the fraction of open PS II reac- tion centres, and in Fv/Fm’, indicating an increase in thermal deexcitation of PS II. Fig 5. Relationship between photochemical effi- ciency of PS II (ΔF/Fm’) of leaves of Q robur, (•,&cir;), Q rubra (&squf;,&squ;) and F silvatica (&utrif;,&utri;) after Nutrient contents in the leaves 10 min induction at 220 (black symbols) or 800 (open symbols) μmol m s and photo-chemical -2 -1 quenching (qp) and photochemical efficiency of Results of the mineral nutrient quantifica- open reaction centres(Fv’/Fm’) under different tions are shown in table III. Strong species- intensities of water-logging. Duration of water- related differences appeared in the leaves, logging: 1-4 weeks, n 12. Means ± standard = F silvatica displaying lowest contents in N, P error.
review). The observed decay was severe and K per leaf area and Q roburthe highest a in the in N, P, Mg. Significant disorders occurred in completely water-logged (F) treat- ment. None of the expected specialised root- response to water-logging in the former adaptation criteria, such as aerenchyma species, with increases in almost all ele- ments for the F treatment, probably due to development and adventitious root growth, detected. The occurrence of some internal recycling after leaf wilting. These were adventitious roots in Q robur after 3 weeks increases were much lower in PF. In both oak species, the effects of water-logging in the partially water-logged (PF) treatment were much more limited, and only few showed that the intensity of the hypoxia changes could be observed. No clear Mn induced by F rather than the limited dura- accumulation was detected in leaves or tion of the experiment were responsible for this lack of appearance of adventitious roots. roots. The ranking of sensitivity among the tested species as inferred from the intensity of dis- DISCUSSION AND CONCLUSION orders in growth was in agreement with the generally known sensitivities to water-log- ging. F silvatica is known to be strongly flood- Effects of water-logging on growth sensitive, while Q robur is expected to be and nutrient concentrations rather insensitive (Belgrand, 1983; Lévy et al, 1986). Root decay and leaf necroses were the worse in the former species. of root sys- Water-logging-induced decay Drew (1991) hypothesised that one of tems is feature among woody a common major effects of root hypoxia on shoot the Colin-Belgrand et al, 1991, for species (see
physiology could be mediated by decreased leaf area due to leaf decay, or by artefacts nutrient assimilation and translocation, in due to the use of predawn water potential as particular N, K and P. For instance Drew an estimate of soil water potential. Direct and Sisworo (1979) observed reductions of measurements of root hydraulic conductiv- N content in barley to 2/3 of the initial con- ity would be needed to solve this question. centrations. Colin-Belgrand et al (1991) obtained significant decreases in the N con- tent and no effect on any other element in Photosynthesis under oak saplings. In the present study we water-logging stress observed declines for a few elements in PF, but not in F. Accumulation of toxic reduced stomatal closure occurred in all Important cations like Fe or Mn is sometimes sus- 2+ 2+ species in response to treatments and pected to be another deleterious conse- water-logging. This observation has been quence of hypoxia (Gambrell et al, 1991). widely reported for many species and inten- We observed a slight accumulation of total sities of root hypoxia (see, for instance, Mn in oak roots, but it is unlikely that such Childers and White, 1942; Lewty, 1990; low concentrations can be really toxic. In Dreyer et al, 1991).Such stomatal closure general, all nutrient contents measured in strongly limits CO influx into the mesophyll 2 our saplings were largely above generally and therefore net assimilation rates (A) of accepted deficiency thresholds. water-logged plants. However the observed decreases occurred at increasing values of intercellular CO mole fraction (c as pre- 2 ), i Water relations of water-logged saplings viously reported by Dreyer et al (1991),Vu and Yelenosky (1991) and Pezeshki (1991). In addition, photosynthetic O evolution 2 The fact that PF induced only limited measured at 5% CO and under saturating 2 changes in predawn leaf water potential light (A and photochemical efficiency ), max (ψ has previously been shown for oak ) wd of PS II were all depressed. This latter seedlings (Dreyer et al, 1991).Complete observation opposes many results obtained water-logging induced a very strong decline with drought stress, where photosynthesis in ψ as reported earlier by Zaerr (1983) , wd decreases occur at constant A and max and Osonubi and Osundina (1987). Such a photochemical efficiency (see review by decline may be considered as an additional Chaves, 1991, and Epron and Dreyer, 1993, index for extensive root decay in the F for an example with oaks). We may con- seedlings. Soil hypoxia is known to cause clude that in the case of water-logging, rapid decreases in root hydraulic conduc- important dysfunctions are induced at tivity (Everard and Drew, 1987; Harrington, chloroplast level. This supports earlier obser- 1987; Smit and Stachowiak, 1988). Sur- vations (Bradford, 1983). prisingly, despite the observed root decay, our estimates of the overall soil-to-leaf spe- hypotheses are generally put for- Two cific hydraulic conductance(g did not ) L explain reductions in photosynthetic ward to decrease in PF, and even increased slightly performance during water-logging: (1) in F. The g values we calculated with con- reduced mineral supply to leaves in partic- L trol and PF seedlings were in agreement ular N and P (Drew, 1991);and (2) toxic with those generally reported for oaks (see compounds produced by anaerobic Dreyer et al, 1993, for a review). However metabolism in the roots. The decrease in the maintenance of g F may only be content observed here in chlorophyll Lin explained by the decline in the transpiring response to water-logging in all species was
analogous to the reported chlorosis occur- in addition to the limitation of CO diffusion 2 ring in many cereals (Drew, 1991).The due to stomatal closure. They nevertheless absence of really significant decreases in do not provide any clear evidence of these total nitrogen or phosphate levels in the disorders. Direct effects at PS II level may be suspected, but are not confirmed by an leaves opposes the hypothesis that nutri- increase in Fo. A limitation of the photo- of the reduced ent imbalance the was cause synthetic reduction cycle resulting in turn in photosynthetic performance. Disorders in a down-regulation of photochemistry could mineral nutrition probably act during long- also be suggested. Solving this point and term and partial water-logging in forest detecting potential toxic spieces issued by stands. roots under hypoxia clearly needs further The observed decreases in PS II effi- experiments. ciency of dark-adapted leaves (Fv/Fm) were due to decreases in maximal fluorescence (Fm) at almost constant basic fluorescence ACKNOWLEDGMENTS (Fo). Reversible decreases in photochemi- cal efficiency are a common feature in oaks The author thanks JM Gioria and JM Desjeunes under natural irradiance, but they vanish for having performed many of the measurements, after a few hours of darkness (Epron et al, A Lallement for the nutrient analyses, D Epron 1992). Irreversible decreases were still for fruitful discussions on chlorophyll a fluo- apparent after a night of recovery and were rescence and JM Guehl for comments on an ear- accompanied by increases in F which were o lier draft. The technical skill in mineral analyses of the Laboratory for Soil Science and Tree Nutrition, until now, only observed on seedlings sub- INRA Nancy (M Colin-Belgrand and C Bréchet) is mitted to drought during several days, on gratefully acknowledged. which net assimilation rates were already zero (Epron et al, 1993). The same applied in our case to Q robur and Q rubra, with REFERENCES the exception that Fo remained constant. In F silvatica, morning values of photo- Andersen PC, Lombard PB, Westwood MN (1984) Effect chemical efficiency decreased before photo- of root anaerobiosis on the water relations of seve- synthesis was completely impaired. Photo- ral Pyrus species. Physiol Plant 62, 245252 chemical efficiency of PS II after a 10 min Baker NR (1991) A possible role for photosystem II in activation (ΔF/Fm’) was also decreased by environmental perturbations of photosynthesis. Phy- siol Plant 81, 563-570 water-logging. This decline was due to Ball JT (1987) Calculations related to gas exchange. In: simultaneous reductions of the efficiency of Stomatal Function (E Zeiger, G.D Farquhar, IR open PS II centres (Fv’/Fm’) and the frac- Cowan eds) Stanford University Press, pp 445-477 tion of open centres as estimated by the Becker M, Levy G (1986) Croissance radiale comparée photochemical quenching qp (Genty et al, de chênes adultes (Quercus robur L et Q petraea (Matt) Liebl) sur sol hydromorphe acide : effet du 1989; Baker, 1991). Interestingly, the same drainage. Acta Oecologica Oecol Plant 4, 299-317 balance between ΔF/Fm’, Fv’/Fm’ and qp M (1983) Comportement de jeunes plants Belgrand was detected on all species: a given stress- feuillus (chêne pédonculé, chêne sessile, hêtre) sur induced reduction of PS II activity (ΔF/Fm’) substrat ennoyé. Adaptations racinaires. Applica- was obtained by an analogous down-regu- tion à la mise en valeur forestière sur pseudogley. These Doct Ing, INA Paris-Grignon lation of the efficiency of open PS IIcentres Bradford KJ Involvement of plant growth sub- (1983) and a decrease of the fraction of open cen- stances in the alteration of leaf gas exchange of tres. These observations clearly support the flooded tomato plants. Plant Physiol 73, 480-483 hypothesis of important disorders induced in Childers NF, White DG (1942) Influence of submersion the photosynthesis at the chloroplast level, of the roots on transpiration, apparent photosynthe-
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