PHYSIOL. PLANT. 66: 521-526. Copenhagen 1986

Non-stomatal limitation of CO2 assimOatlon in three tree spedesduring natural drought conditions

G. M. Briggs, T. W. Jurik and D. M. Gates

Briggs, G. M., Jurik, T. W. and Gates, D. M. 1986. Non-stomatal limitation of COjassimilation in three tree species during natural drought conditions. - Physiol. Plant.66: 521-526.

The effect of drought on COj assimilation and leaf conductance was studied in threenorthern hardwood species: Quercus rubra L., Acer rubrum L. and Populus gran-didentata Michx. Leaf gas exchange characteristics at two CO' levels (320 aad 620 pjr ' ) and temperatures from 20 to 35°C were measured at the end of a dry period andshortly after 10 cm of rainfall. The effects of drought varied with spedes, temperatureand CO2 level. Calculated values of internal CO; concentration showed little or nodecline during drought. Differences in assimilation, before vs after the rains, weremost apparent at the higher CO2 level. These latter two observations indicate non-stomatal disruption of CO2 assimilation during the dry period, in P. grandidentatathere was a substantial interaction between drought and temperature, with a resultantshift in the temperature for maximum assimilation to lower temperatures duringdrought. Dnring drought, internal COj concentrations increased sharply in all threespecies under the combined conditions of high temperatures and the higher CO,level.

Additional key words - Acer rubrum, elevated CO, levels, internal CO,, Populusgrandidentata, Querctis rubra, temperature optima.

G. M. Briggs (reprint requests), T. W. Jurik and D. M. Gates, Univ. of Michigan Bio-logical Station, Pellston, MI 49769, USA.

Introduction

Drought has long been known to decrease CO, assimila-tion, but the precise mechanisms controlling this effectare not cotnpletely understood (Bradford and Hsiao1982, Hanson and Hitz 1982). As drougiit developsplants often exhibit parallel decreases in CO, assimila-tion and leaf conductance to water vapor. This ledworkers to propose a process of "stomatal control" dur-ing drought-water stress had sotnehow lowered leaf con-ductance, resulting in decreased CO, diffusion into theleaf, lowered internal CO, concentrations, and therebylower rates of CO, assimilation (Barrs 1968, O'Toole etal. 1977). Many of the studies showing stipport for sto-matal control during drought utilized a "linear resis-tance model" to arrive at these conclusions and this mo-del has been shown to be invalid under many circttni-stances (Farquhar and Sharkey 1982). Re-exattiination

Received 21 May, 1985; revised 26 August, 1985

Physjol. Plml. 66, 1986

of the studies thought to indicate stomatal control usingan analysis developed to evaluate the extent of stomatalcontrol (Farquhar and Sharkey 1982), has indicated thatstomatal limitation is not of primary importance in low-ering CO, assimilation daring drought. This same con-clusion was reached in two recent studies on sunflowergrown in growth chambers (Matthews atid Boyer 1984)and field-grown cotton (Huttnacher and Krieg 1983). fnthese studies reductions in COj assimilation during wa-ter stress were primarily caused by non-stomatal fac-tors. Complicating the situation is the observation thatCO, assimilation is indeed coupled to leaf conductance,but not, apparently, due to stomatal control of CO, as-similation (Wong et al. 1979). Thus it appears probablethat at least in some situations, it is the decrease in CO,assimilation during drought that results in stomatal clo-sure, rather than vice versa. Here we report evidence tosupport eoB-stomatal control of CO, assimilation in

521

three tree spedes growing under natural drought condi-tions. Also indicated are significant interactions be-tween drought and the response of CO, assimilation totemperature.

Abbreviations - PPFD, photosynthetic photon flux density;RuBP, ribulose-bis-phosphate; VPD, leaf-to-air vapor pressuredeficit.

Materials and methods

The study site was located at the University of MichiganBiological Station in northern lower Michigan, USA(45°33'N 84°42'W). The site represents a low-fertihtyhabitat common in the region, characterized by a dis-tinct spedes composition, low stand density and slowgrowth in comparison to adjacent high-fertility areasthat have a greater clay content in the soils (Koerperand Richardson 1980). The soil of the site consists ofgreater than 95% sand and is classified as a sandy,mixed, frigid Entic Haplorthod. The site was harvestedin 1972 and the trees studied are sprouts from the re-maining stumps {Quercus rubra L. and cer rubrum L.)or from underground structures {Populus grandidentataMichx.). Tree height averaged 3.5 m in relatively openstands. A scaffold was utilized to provide access toleaves near the tops of the trees. A single genotype ofeach species was studied. The P. grandidentata individ-ual was a single stem while both the A. rubrum and Q.rubra were clumps of about 5 stems emerging from astump.

Rates of CO, and H,O exchange were measured us-ing a gas exchange system described in Jurik et al.(1984). Intact, attached leaves were sealed in a clearplexiglass chamber coated internally with teflon (Du-Pont S-115) and connected in an open gas exchange sys-tem (Heinz Waltz Mess- tind Regeltechnik, Effeltrich,West Germany). The dewpoitits of air entering andleaving the chamber were measured using dewpointmirrors. The humidity of air entering the chamber wascontrolled with a cold trap. Temperature of the chamberwas controlled using Peltier blocks. Leaf temperaturewas measured with two copper-constantan thermocoup-les appressed to the lower side of the leaf. The differ-ence in CO, concentration between the in-going andout-going air was measured with an Analytical Deve-lopment Company Type 225 Mkfl gas analyzer in thedifferential mode. The gas analyzer was calibrated withcommercially prepared bottled air of known CO, con-centration, checked previously against the output ofWosthoff mixing pumps using pure gases. A single gasof given CO, concentration was used for both zero andspan calibration of the gas analyzer; for span calibra-tions, the construction of the analyzer allowed a volum-etric depletion of 5% of the reference gas by COi-freeair. Air flow rates were measured with a Teledyne Hast-ings-Raydst NALI^SK mass flow meter aod averaged4-5 1 min"'. Experiments were conducted at two CO,

levels. The use of ambient air resulted in chamber CO,levels of 315-325 \il 1"'. A higher carbon dioxide levelwas obtained by mixing CO,-free air (CO, removed bysoda lime and monitored with a Beekman 864 gas ana-lyzer to assure CO, removal) and pure CO,. Mixing wasregulated by a Matheson model 8250 modular dyna-blender and flow controller. This system produced anair supply with 630 |il 1"' CO,, resulting in chamber CO,concentrations of 615-625 (il 1"'. Light was maintainedat approximately 1000 |imol m" s"' by naeans of an Os-ram PowerStar lamp (HOI-TS 400W/D).

The responses of CO, assimilation rate and leaf con-ductance to water vapor were studied at both CO, lev-els. Sttidies were made during a drought period and inthe week following nearly 10 cm of rainfall. For eachleaf a temperature response curve was obtained, withtemperature usually starting at 20°C and incremented in5° steps to 35°C. It took 2 to 3 min for the temperatureto increase 5°C. Measurements were taken after rates ofCO, assimilation and transpiration had stabilized (0.5 to1.25 h). Atmospheric pressure during these experi-ments averaged 96.4 kPa. In-going absolute humiditywas held constant at 0.93 kPa during a temperature se-quence. Boundary layer conductance, estimated byevaporation rates from moistened cardboard models,ranged from 1000 to 40(K) mmol m" s"' depending uponleaf size and shape. Calculation of internal CO, was asdescribed in Farquhar and Sharkey (1982) with a correc-tion for transpiration. The leaves were harvested after asingle temperature run at either of the CO, levels andthe leaf area determined with a Licor LI-300O leaf areameter. The leaves of all three species were distinctly hy-postomatous and the area of only one side of the leafwas used in calculations of CO, assimilation and leafconductance to water vapor. Values reported are aver-ages of three, or occasionally two, leaves for each spe-cies in the four combinations of CO, level and drought/post-drought conditions.

Drought stress was monitored using mid-afternoonpressure bomb readings of xylem tension. To minimizetranspirational effects from excision to measurement(Turner and Long 1980), leaves were enclosed in a mois-tened plastic bag just prior to excision.

On 5,15, and 25 September, soils were sampled at 10and 30 cm for gravimetric determination of percentagemoisture. The relationship between gravitnetrically de-termined percentage moistitre and soU water potentialwas determined with a pressure plate by the Utah StateUniversity Plant and Soil Analysis Laboratory. Soil wa-ter potential was then estimated from this relationship.

Results

The summer of 1983 was one of the driest on record atthe Biological Station, with less than 3 cm of rain duringJune and July. The drought was partially relieved bymid-August rains but the soil was not totally recharged,and a second drought pedod developed during Septem-

522 Physiol. Plant. 66.1986

Tab. 1. Soil water potential and mid-afternoon xylem pressure potential (MPa) at the study site in September (valuesior trees aremeans of three samples taken on each of three trees per spedes ± SD).

ParameterDate

3 Sept.

-0.10-0.03

-1.76±0.06-1.68±0.08-1.8710.01

14 Sept.

-1.50-0.10

-2.01±0.19-1.63±0.13-2.20+0.21

26 Sept.

-0.03-0.03

-0.71+0.05-0.78±0.04-0.84+0.04

Soil water potential10 cm-30 cm

Xylem pressure potentialQuercus rubraPopultts grandidentataAcer rubrum

ber with xylem pressure potentials reaching their lowestvalues for the summer (unpublished data). The droughtended with nearly 10 cm of rain falling during Septem-ber 16-22. Table 1 shows the mean mid-afternoon xylempressure potential during September for the species

POPULUS

~ 16

O <"

K E

o E2 E 40O ~ '

5 0 0

oO ^300

111 ^ 100I-

QUERCUS ACER

f-+~-4

20 30 20 30 20 30

LEAF TEMPERATURE ( "O

Fig. 1. Comparison of gas exchange characteristics for Populusgrandidentata, Quercus rubra, and Acer rubrum. Studies wereconducted during a dry period (open symbols) and after 10' cmof rain (closed symbols). Measurements were made at two CO,concentrations: 320 nl 1"' (solid lines) and at 620 [»11"' (dashedlities). Each point is the mean ±SD (error bars tiot shown whenless than the symbol width); n = 3 except for the followingwhere n = 2: P. grandidentata-umtressed, 620 nl I"', P. gran-didentata-dmught, 620 nl I"', Q. ruftra-drought, 320 nl 1"'.

studied and the estimated soil water potential at twodepths.

Between 10 and 15 September the leaves of all threespecies were studied at both ambient and elevated CO,levels. Similar studies were made in the week followingthe rainfall. Pre-rain (drought) and post-rain gas ex-change characteristics are shown in Fig. 1. Carbon di-oxide assimilation decreased in al! species duringdrought; the largest decreases occurred in P. grandiden-tala, especially at higher temperatures. In all speciesdrought caused proportionally greater decreases in as-similation when measured at the higher CO, level thanwhen measured at near normal levels of CO,; e.g., as-similation oi A. rubrum under ambient conditions wasvirtually the same during both drought and post-rainconditions, but assimilation in high CO, was substati-tially increased after the rains.

Leaf conductance to water vapor was more variablethan CO, assimilation, especially after the rains(Fig. 1). In both A. rubrum and Q. rubra conductancewas decreased by drought, higher CO,, and, to a lesserextent, by increased temperature. The combination ofdrought and elevated CO, drastically lowered leaf con-ductance in Q. rubra. In P. grandidentata drought re-sulted in the largest decreases in leaf conductance; in-creased CO, had little effect on leaf conductance, es-pecially dnring drought conditions.

Figure 1 shows calculated values for internal CO,concentration. In A. rubrum, an approximate two-foldincrease in external CO, concentration caused internalCO, concentration to increase roughly 100 (il 1"' underboth drought and post-rain conditions. Internal CO,levels were constant with temperature, except duringdrought at the higher CO, level when internal CO, in-creased sharply at 35°C. For P. grandidentata, internalCO, concentrations during drought rose with tempera-ture at both external CO, levels; after the rains internalCO, concentration changed little with temperature. Thetemperature response of Q. rubra was comparable tothat of J4. rubrum, with no significant response to tetn-perature except under the combined conditions ofdrought and high external CO, levels, when internalCO, concentration rose sharply at 30°C. Q. rubra was

Physiol. Plant. 66, 19S6 523

unique in that dtmng droaglit the internal CO, concen-tration apparently was lower at the high CO, level, ex-cept at the highest temperature (it should be noted thatcalculation of internal CO, concentration at low leafconductance values is very sensitive to errors in the es-timation of conductance). Under post-rain conditionsthis phenomenon did not occur.

Discussion

The most likely cause of the changes in the characteris-tics of gas exchange observed in this study is droughtand its subsequent relief by rains. Two features indicatethat the drop in assimilation seen during the droughtperiod was not due to stomatal control. First, there wasno consistent drop in internal CO, concentration duringthe drought period (Fig. 1). Second,, and perhaps evenmore compelling, is the fact that elevated CO, levels didlittle to alleviate the decrease in assimilation duringtimes of water stress (Fig. 1). In fact, stimulation of as-similation in the enriched CO, atmosphere was greaterafter the rains. In the case oiA. rubrum a drop in assim-ilatioti during drought was not observed at ambient CO,levels, but was apparent at the higher CO, concen-trations; drought apparently impaired the ability of theleaf to utilize higher CO, levels. Sharkey and Badger(1982) observed similar behavior in osmotically stressedmesophyll cells of Xanthium strumarium L. These ob-servations are difficult to reconcile with the hypothesisthat drought effects are due to stomatal closure and theresultant lower values for internal CO, concentration(except perhaps for Q. rubra, see below). Non-stomatallimitation of CO, assimilation during drought has beenrecognized for some time, but it has not been observedconsistently (reviews in Boyer 1976, Bradford andHsiao 1982, Hanson and Hitz 1982). Recent re-analysisof data has failed to indicate a dominant stomatal com-ponent to the decrease of assimilation during drought,thereby implying that non-stomatal factors must be im-portant (Farquhar and Sharkey 1982). The predse na-ture of these non-stomatal factors is not known. Shar-key and Badger (1982) felt that the aspect of pho-tosynthesis most sensitive to water stress wasphotophosphorylation. Matthews and Boyer (1984)showed that changes in chloroplast activity, includingchanges in in vitro PS II activity, accounted for most ofthe decrease in assimilation caused by drought. Theyfurther demonstrated that acclimation to drought in-volved changes in chloroplast activity.

An anomalous situation occurred with Q. rubra. Dur-ing drought, elevated CO, levels resulted in a drastic de-crease in conductance, resulting in an internal CO, con-centration that was lower in the high COj atmospherethan in the low CO, atmosphere (Fig. 1). In Q. rubra itis probable that this stomatal behavior lowered assimila-tion at the higher CO, level during drought. Under am-bient conditions the evidence for stooiatal control isequivocal: at 20°C, internal CO, concentration values

were lower during drought,, but at 25 and 30°C, wheredecreases in assimilation during drought were larger, in-ternal CO, concentrations were not lower duringdrought. The combined effects of drought and elevatedCO, on conductance of Q. rubra is unusual. Manyplants have lower leaf condnctances in atmospheres en-riched in CO,, but the extent of stomatal closure is in-sufficient to bring internal CO, concentrations down be-low those found at ambient CO, levels. It should also benoted that both Q. rubra and A. rubrum occasionallyexhibited a slight inhibition of assimilation by elevatedCO, levels under drought conditions. A similar highCC, inhibition has been observed by T. D. Sharkey(personal communication) under conditions of waterstress and by Woo and Wong (1983) under conditions oflow fertility and low temperatures. The trees of thisstudy were growing in a low fertility situation btit the in-hibition was found only at higher temperatures in A. ru-brum and showed no consistent temperature pattern inQ. rubra. The cause for this inhibitory effect of elevatedCO, is discussed by Woo and Wong (1983), but remainsa mystery.

ITie effect of temperature on CO, assimilationchanged during drought, with the most dramatic effectsin P. grandidentata, where drought conditions loweredthe temperature for maximum assimilation. Similarshifts in the temperature response pattern of assimila-tion have been reported (Boyer 1971, Nobel et al. 1978,Osonubi and Davies 1980) and attributed to changes inmesophyll conductatice. Unstressed P. grandidentataleaves exhibited a typical Q temperature response witha broad temperature maximum for assimilation fromabout 22 to 28°C at ambient CO,. The maximum shiftedto higher temperatures at elevated CO, levels. Such apattern has beeo found previously for this spedes (Juriket al. 1984) and for other C, species (Berry and Bjork-man 1980, Ehleringer and Bjorkman 1977). The drop inassimilation at higher temperatures is thought to resultfrom a decreased ratio of RuBP carboxylation to oxy-getiation. This can be partially offset by elevated CO,levels (Pearcy and Bjorkman 1983). Under droughtconditions the temperature for maximum assimilationshifted to lower temperatures, and elevated CO, levelsdid little to alleviate this temperature effect (Fig. 1).This lack of response argues against the temperature ef-fect being caused by changes in RuBP carboxylase activ-ity. In von Caemmerer and Farquhar's (1981) model ofC3 photosynthesis, the temperature for maximum as-similation can be related to the ratio between the maxi-mum rate of photosynthetic electron transport and themaximum rate of RuBP carboxylation. Their modelshows a decreased temperature for maximtim assimila-tion as this ratio decreases. Therefore the drought-in-duced lowering of the temperature for maximum assimi-lation could be associated with a lowering of the hght-saturated rate of electron transport. Such an explana-tion is consistent with the lack of response to elevatedCO, levels and with the apparent non-stomatal nature

524 Physiol. Plant. 66, 1986

of the drought effects. However, Sharkey and Badger(1982) felt that electron transport was insensitive to wa-ter stress. The shift in the temperature response couldalso involve changes in respiration.

In A. rubrum and Q. rubra, the effects of water stresson the temperature response of assimilation were not asdramatic as in P. grandidentata. At normal CO, levelsQ. rubra showed only a slight shifting of the tempera-ture response with relief from drought and A. rubrumshowed no change in response at all. At higher CO, lev-els both Q. rubra and A. rubrum did show a greater de-crease in assimilation at the higher temperatures duringdrought conditions (similar to the pattern of P. gran-didentata), but the response was of reduced magnitude.

Another explanation for the drought-temperature in-teraction involves changes in VPD. In these experi-ments, changes in temperature were confounded withchanges in VPD (as they are in nature): VPD increasedwith temperature (from 0.8 to 3.3 kPa). The stomates ofmany species are known to close in response to highVPD and the sensitivity of stomates to VPD has beenfound both to increase and to decrease in response todrought (Losch and Tenhunen 1981). As argued above,assimilation does not appear to be limited by stomatalfactors (with the possible exception of Q. rubra); thus,the shifting response to temperature with drought isprobably not due to a shifting sensitivity of the stomatesto VPD. Vapor pressure deficit apparently can also af-fect assimilation in a more direct manner, not involvingstomatal changes and changes in internal CO, concen-tration (Bunce 1984, Sharkey 1984, Morison and Gif-ford 1983, Reseman and Raschke 1984). The mecha-nism for such a response is unknown. High VPD couldresult in lowered leaf water potential that could inhibitassimilation (Sharkey 1984, Bunce 1983, Morison andGifford 1983); if this mechanism operates, an enhancedVPD (temperature) effect might be expected in water-stressed plants with lower water potentials. In such amechanism, assimilation is actually responding to trans-piration, not to VPD; this has been found to be the casein some studies (Sharkey 1984) but not in others (Bunce1984).

At elevated CO, levels the combination of high tem-peratures and drought disrupted the coupling of assimi-lation and conductance that normally results in rela-tively constant internal CO, concentrations (Wong et al.1979) (Fig. 1). The mechanism that couples assimilationand stomatal conductance is still unknown, and the un-coupling caused by temperature and drought may proveto be a useful tool in studying the process.

Acknowledgements - We are grateful to M. M. Samson for avariety of aid during this project and to the comments of ananotiymous reviewer. Supported by the U.S. Dept of Energyunder contract DE-ACO2-79EV10091.

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Edited by L. O. Bjorn

5 2 6 Physiol. Plant. 66, 1986