rant, Call anc Environment (1996) 19, 182-190 Leaf gas exchange and carbon isotope composition responses to drought in a drought-avoiding (Pinus pinaster) and a drought-tolerant (Quercus petraea) species under present and elevated atmospher C. PICON,' J. M. GUEHL! & A. FERHE. COz concentrations “Unité d’Ecophysiologie Forestiere, Equipe Bioclimatologie-Ecophysiologie. INRA Nancy, F-54280 Champenous, France, and *Cenure de Recherches Géodynamiques, Université Paris VI, 47, Avenue de Corzent, F-74203 Thononles- Bains, France ABSTRACT ‘The responses of predawn leaf water potential (Vg), leaf conductance to water vapour diffusion (g) CO; assimilation rate (A) and carbon isotope competition (5"C) to a soil drying cycle were assessed in Pious pinaster, a drought- avoiding species with high stomatal sensitivity to drought, and Quercus petraea, a drought-tolerant species with lower stomatal sensitivity to drought, under present (350 mol mol") and elevated (700 molmol™') atmospheric CO; concentrations ({COs"). In P. pinaster, decreasing A in response to drought was associated with increasing plant intrinsic water use efficiency (A/p) and with decreasing calculated intercellular (CO;] (Ci), suggesting a stomatal limitation of A. In contrast in Q. petraea, A/g declined and G; imereased during the drying cycle, which suggests a non-stomatal origin forthe decrease in A. In P. pinaster, a negative relationship was observed between the gat ‘exchange-derived values of G/C, and 52°C, which conforms fo the classical two-step carbon isotope discrimination model. In Q. petraea, the relationship between C/C, and 3C was positive. Possible causes of this discrepancy are discussed. Lower g values were observed under elevated (COg] than under present [COs] in Q. petraea, whereas g was unaffected in P. pinaster. A stimulation of A by elevated [CO;] was found in P. pinaster but not in Q. petraes. In both species, Ag was markedly higher under elevated than under present (CO;]. Whether the differences in the g response to elevated (CO3] found here can be generalized to other drought-avoiding and non-avoiding species remains to be assessed. Key-words: forest trees; drought; elevated [CO]; gas ‘exchange; carbon isotope composi Correspondence: Jean-Marc Guehl, Unité de recherches en Ecophysiologie Foresére, Equipe de Bioclimatologie et Eco- physiologic, INRA Nancy, F-54280 Champenous, France. INTRODUCTION Plants differ widely in their stomatal sensitivity to drought. This variability is atleast partly associated with the existence of drought adaptation strategies based on: (1) drought avoidance, which is generally found in species with high stomatal sensitivity to drought, or (2) drought tolerance, which is found in species with lower stomatal sensitivity but displaying structural and func- tional adaptive traits such as osmoregulation, allowing the plant improved tolerance of reduced water status. ‘The mechanisms underlying the stomatal responses 10 drought might differ in these two groups of species, as suggested by Jensen, Henson & Turner (1989). In Pinus pinaster Quercus petraea 32 03 03 328 a4 bo 02 He 2” 01 4 2 00 00 40 35-30 -25 -20 -15 -10 05 00 -35 30 25 -20 -15 -1.0 -05 00 Predawn leaf water pote (CY upp MPa) Figure 3. Relationships between instantaneous intrinsic water use efficiency and predawn leaf water potential obtained during a soit drying cycle in Pinus pinster and Quercus petraea plants grown under 350 and 700,mmol mol” {CO.}. For P. pinaster. each experimental point corresponds to a different plant: for Quercus petraea a given plant was used two or thee times during the experiment. All felationships were fited by second-order polynomials. (© 1996 Blackwell Science Ld, Plant, Cell nd Ensiomment. 19. 182-190Leaf gas exchange responses to drought and elevated CO; 187 700 jmol mot! 380 pot mot! ‘A Wellwaered A Well-watered . © Droughted —--O Droughied 25 25 Pinus pinaster Quercus petraea a 27 eA Peosipeoor | [ =064,r001 | 5 2 % g3l : x ° ° 331 - [ ° o 7 4 ° 73 a 13 5 2 35 35 3 Pinus pinaster ° Quercus petraea B39 39 § é 2 065,Pe0.01 #72040, Pe0.05 g al 41 43 “43 AS 45 47 “47 “40-35 30 25 20-15 -10 05 00 -35 30 25 -20 -15 -10 05 00 Predawn leaf water potential (yp, MPa) Figure 4. Relationships between leaf carbon isotope composition and predawn leaf water potential obtained during 2 soil drying cycle in Pinus pinaster and Quercus petraea plants grown under 350 and 700 umotmol~ [COs]. Experimental points correspond to distinct plants. Leaves were harvested and conditioned forthe isotopic measurements inthe late afternoon ofthe day on which water potential was measured, parison between species and to the assessment of drought effects within each of the tunnels in which common 6, prevailed. This analysis cannot be extended to assess the CO; effects. In both species. and for both (CO), leaf carbon isotope composition (8,) increased with increasing drought intensity (Fig. 4). This reflects the effect of drought on carbon isotope discrimination and on isotope composition of the carbon photoassimilated during the drying cycle (Brugnoli etal. 1988; Borland etal. 1994. Relationship between 5, and the gas exchange- derived G/C, Because ofthe lag in time-integration scales between the © 1906 Blackwell Science Lud, Plant, Cell and Environment 19. 182-190 Afg (instantaneous scale) and isotopic data (function of the isotope discrimination from the beginning of the drying cycle), no quantitative interpretation can be derived from the 8, versus C/C, relationships obtained in the present study (Fig.5), as can be done when isotope discrimination is assessed simultaneously with ‘gas exchange (Lloyd er al. 1992). However, qualitative conclusions can be drawn from the comparison between the two species. In P. pinaster, 8, was negatively correlated with the CJC, values derived from leaf gas exchange (Fig. 5). which is consistent with the two-step carbon isotope discrimination theory (Farquhar et al. 1989) presented above (Eqn2). In contrast, in Q. petraca, a positive correlation between these two variables was observed188 ©. Picon et al opmoieat! sprain! A Melee Webi ore as E Pinus pinaster Quereus petraca 2” n treats 29 a 5 29 oe < 3 af : a oN a co fa é a 3 3 non 33 gon 9 a Pinus pinaster Quercus petraea . i» » 2-09, 0 os. nats a 4 a 3 a 43 anne 43 z 4 é s 1 4s 0 03 4 0s 06 07 08 09 03 04 05 0S 07 08 09 10 cre, . Figure 5. Relationships between leaf carbon isotope composition and the gas exchange-derived values of C/C, obtained during a soil drying cycle in Pinus pinaster and Quercus peraea plats grown under 380 and 700 molmol~' [CO:|. Experimental points correspond to distinct plants which are the same asin Fig. 4, Leaves were harvested and conditioned fr the iotopic measurements in the late afternoon ofthe day on which gas exchange was measured (Fig. 5), which is not in accord with the simple two-step weighted value of C/C,., will then be superior to discrimination model. Meinzer et al. (1992) found a the isotopic discrimination-derived C/C,, a local similar discrepancy between gas exchange-derived C/C, CO; assimilation-weighted value of CJC, (Far- values and leaf carbon isotopic composition in plants of quhar 1989). This hypothesis is to be considered Coffea arabica subject to soil drought. here since oak leaves are heterobaric, i.e. leaves The discrepancy between gas exchange and isotopic are subdivided by the leaf veins into small pneu- data observed in oak can be ascribed to three possible ‘matically isolated units, and pine leaves have a causes: free lateral diffusional structure. In this case the (1) The difference in time-integration scale between consequences of patchy stomatal function would the instantaneous gas exchange data and the be alleviated (Farquhar 1989). time-integrated nature of isotopic signatures. (3) Decreasing conductance for CO: diffusion in (2) Increasing spatial stomatal and photosynthetic liquid phase from the intercellular air spaces to heterogeneity in the leaves during the drought the sites of carboxylation inthe chloroplasts (gq) cycle (Terashima et al. 1988; Downton, Loveys & during drought. Such an effect would also tend to Grant, 1988; Epron & Dreyer 1993). The gas decrease leaf carbon isotope discrimination ~ and exchange-derived C/C,, a local conductance- thus to increase 6, while decreasing the A/g ratio © 1996 Blackwell Science Lid, Plat, Cel ad Environment 19.183 190Lear gas exchange responses to drought and elevated CO; 189 (or increasing the gas exchange-derived C/C,) (Lloyd et al. 1992; Parkhurst 1994). No clear experimental evidence has been provided so far showing a negative effect of drought on gj. We do not have decisive evidence at this stage that could enable a choice to be made between these hypotheses. However, in another study (Picon, Guehl & Aussenac 1995) using Q. robur, a species with a leaf structure identical to that of Q. petraea, we found a good agreement between season-long WUE determined gravimetrically and , using the simple two-step dis- crimination model. This suggests that the effects due to patchy leaf function and to gm were negligible in this ‘The effects of elevated [C0] Elevated CO; did not affect the shape of the A, g and C, responses to drought exhibited by the two species (Figs 1 & 2). In Q. petraea, g was lowered by elevated [CO], whereas g remained unaffected in P. pinaster. In a review on the sensing of CO» by plants, Mott (1990) proposed that the decrease in g generally observed in response to rising CO: is linked to the higher values of intercellular [CO,]. However, no effect of elevated {CO2] on g was found in experiments performed using Pinus nigra ssp. laricio (Kaushal, Guehl & Aussenac 1989). Liriodendron tulipifera (Norby & O'Neill 1991) or Malus domestica, Quercus prinus and Quercus robur (Bunce 1992). The decrease in A relative to C, obtained in P. pinaster grown at 700 mol mol~' as compared with 350 umol mol”! (Fig. 2) reflects a downward acclimation cof photosynthesis (Stitt 1991), but A remained stimu- lated by the elevated [COs] (Fig. 1). In Q. petraea no stimulation in A was found throughout the drying cycle although the C values were higher at C, = 700umol- mol". In Quercus robur, Vivin et al. (1995) also observed an absence of stimulation of A that was associated with an absence of relative growth rate stimulation after July Despite the differential responses of g and A to elevated CO>, intrinsic water use efficiency was increased in both species (Fig. 3). This isa quite general result in CO: enrichment studies with C; plants (see reviews by Eamus 1991; Morison 1993; Tyree & Alexan- der 1993) and with trees (Ceulemans & Mousseau 1994) {In conclusion, the results obtained here show that, in the drought-tolerant species, drought avoidance was increased in the elevated CO; conditions as a result of stomatal closure in the moderately constrained situa- tions. This could favour the maintenance of satisfactory water status in the context of altered climatic conditions and rising CO; and could allow this species to colonize drier sites than it does presently. In contrast, stomatal function was not affected in the drought-avoiding species. but CO2 assimilation was increased. For this species, a higher productivity might be expected in the next decades, but the sensitivity to drought might not be {© 1996 Blackwell Science Lid Plant, Cell and Encironment, 19 182 alleviated. 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(1995) Whole-plant ‘CO; exchange, carbon parttioningand growthin Quercus robur seedlings exposed 10 elevated CO; Plant Physiology and Biochemistry 3, 201-211 Received 24 January 1995; received in revised orm 25 May 1995 ‘accepted for publiaion 7 June 1995 {© 1996 Blackwell Science Lu, Plant. Celt und Environment 19. 182-190