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Net CO2 assimilation (A) of four birch genotypes (Betula nigra L. ‘Cully’, B. papyrifera Marsh., B. alleghaniensis Britton, and B. davurica Pall.) was studied under varied photosynthetic photon flux density (PPFD) and CO2 concentrations (CO2) as indicators to study their shade tolerance and potential for growth enhancement using CO2 enrichment. Effect of water-deficit stress on assimilation under varied PPFD and (CO2) was also investigated for B. papyrifera. The light saturation point at 350 ppm (CO2) for the four genotypes varied from 743 to 1576 μmol·m−2·s−1 photon, and the CO2 saturation point at 1300 μmol·m−2·s−1 photon varied from 767 to 1251 ppm. Light-saturated assimilation ranged from 10.4 μmol·m−2·s−1 in B. alleghaniensis to 13.1 μmol·m−2·s−1 in B. davurica. CO2-saturated A ranged from 18.8 μmol·m−2·s−1 in B. nigra ‘Cully’ to 33.3 μmol·m−2·s−1 in B. davurica. Water-deficit stress significantly reduced the light saturation point to 366 μmol photon m−2·s−1 but increased the CO2 saturation point in B. papyrifera. Carboxylation efficiency was reduced 46% and quantum efficiency was reduced 30% by water-deficit stress in B. papyrifera.
There are various light conditions in landscape situations, i.e., full sun, partial sun, or shade, and plants have different requirements for light. Photosynthetically active irradiance is an important ecological factor on which all photoautotrophic plants depend (Lambers et al., 1998). Photosynthesis is highly correlated with photosynthetic photon flux density (PPFD), and thus net carbon gain and biomass production, if other factors are optimal such as water and nutrient supply. Low PPFD could limit the photosynthesis rate in sun plants and therefore limit plant growth. High PPFD may result in photoinhibition under certain growing conditions when excess energy could not be dissipated through photochemistry (Lambers et al., 1998). Excess excitation energy may cause damage to the photosynthetic apparatus when it exceeds the capacity of other dissipation mechanism. Ambient CO2 concentration (CO2) is a limiting factor to net CO2 assimilation (A) in C3 plants (Lambers et al., 1998). Thus, increasing (CO2) could potentially enhance photosynthesis and growth in C3 plants. Supplemental CO2 has been applied to improve production of vegetables or fruits in controlled environments (Edwards et al., 2004; Gao et al., 2004; Wei et al., 2004). Birch trees (Betula L.) are normally produced outdoors; however, vegetative propagation of some selections might benefit from supplemental CO2 application in a greenhouse. No previous research has been conducted on CO2 enrichment during nursery production of birch.
Light and CO2 responses are commonly used to explore the photosynthesis mechanism of plants. Single-leaf photosynthesis measurement (Peng and Krieg, 1992) provides a good estimate of a plant's maximum photosynthetic potential, although intracanopy shading may affect the accuracy of the single leaf as an indicator of the whole-plant photosynthesis responses (Makino and Mae, 1999).
Birch consists of ≈50 deciduous species throughout the northern hemisphere (Krussmann, 1984). Birch trees are popular landscape trees for the attractive white bark, fall foliage, or pendulous catkins. Most birch trees are pioneer species in their natural habitat (Atkinson, 1992; Kobe and Coates, 1997; O'Hanlon-Manners and Kotanen, 2004) and rarely exist in the inner canopy of forests, which indicates that they may not be shade-tolerant. Previous research (Gu et al., 2003) suggested that there was a range of A under identical PPFD within the Betula genus. A better understanding of shade intolerance would contribute in selection and improvement among the birch trees for varied light conditions in the landscape. Although B. papyrifera was found to be the most shade-intolerant compared with other forest species based on models of sampling mortality in existing woods (Kobe and Coates, 1997), applying such an approach to Betula species in the landscape would not be feasible simply because of their diverse provenance. Four birch genotypes from diverse origins were selected for the experiment (B. nigra L. ‘Cully’ from the eastern United States, B. papyrifera Marsh. from North America, B. alleghaniensis Britton from eastern North America, and B. davurica Pall. from northeast China), and B. papyrifera was selected to study the water status effect on light and CO2 responses resulting from its popularity in the landscape.
There have been no previous reports on light response or CO2 response of birch genotypes. The objectives of this research were to: 1) compare light and CO2 responses in the four birch genotypes; and 2) evaluate water status effect on light and CO2 responses in B. papyrifera. The hypotheses were that there is a difference in light and CO2 responses among the four birch genotypes and that water deficit could affect quantum efficiency and carboxylation efficiency in B. papyrifera, which could serve as a basis for recommending birch genotypes for landscapes with various light conditions, plant water status management in the landscape, and CO2 enrichment for birch production under controlled environments.
Four birch genotypes (B. nigra ‘Cully’, B. papyrifera, B. alleghaniensis, and B. davurica) obtained as rooted cuttings or bare-root plants were potted in 3.8-L pots with SunGro SB 300 Universal Mix (Pine Bluff, AR) in Winter 2003 and placed in an outdoor lathe house at the Arkansas Agriculture Research and Extension Center at Fayetteville.
The container plants were transported to the greenhouse at the Rosen Alternative Pest Control Center in June 2004. Five grams of Osmocote® 18N–2.6P–9.9K were topdress-applied to each container. Plants were grown in the greenhouse with ambient (CO2) and the supplemental metal halide high-intensity discharge lights, which were automatically turned on when the ambient light level decreased to below 60 Klux. Photosynthetic photon flux density was ≈750 μmol·m−2·s−1 photon at the upper canopy level when the supplemental lights were turned on. The greenhouse conditions were programmed at day/night temperatures of 25 ± 2/20 ± 2 °C and relative humidity of 50%. Plants were trained to a single shoot and the height of the plants was ≈1.2 m before the initiation of the experiments.
Six trees of similar size were selected for each genotype and the experiment was conducted on the 8, 9, and 10 Sept. 2004. Gas exchange measurements were taken between 900 hr and 1330 hr (CDST; 1 to 4.5 h after sunrise) using a portable gas exchange analyzer (CIRAS-1 Analyzer; PP Systems, Haverhill, MA). The cuvette conditions were set at 25 °C and 350 ppm (CO2). The air in the cuvette was maintained at ≈70% relative humidity to minimize stomatal heterogeneity (Griffin et al., 2004b).
Measurements were taken on a 2.5-cm2 section on the center of the fifth unfolded leaf from the apex of each tree as described by Pettersson and McDonald (1992), and the midvein was avoided from being included in the cuvette. One measurement was taken on each leaf to get one data point in both light and CO2 responses. Dark respiration (Rd) was recorded when the light supply unit was detached from the cuvette head and aluminum foil was used to cover the cuvette to avoid scattered radiation on the leaf (PPFD = 0 μmol·m−2·s−1 photon). The light supply unit was replaced back to the cuvette head and irradiance increased incrementally (25, 50, 100, 250, 500, 750, 1000, 1250, 1500, 1750, 2000 μmol·m−2·s−1 photon). After an ≈15-min acclimation period, A was recorded at each light level and fitted to the model equation
as given by Lambers et al. (1998) in which A is the net CO2 assimilation rate, Φ is the quantum efficiency, PPFD is the incident irradiance, Amax is the light-saturated rate of gross CO2 assimilation (light-saturated net CO2 assimilation plus Rd) at infinitely high irradiance, and k is the curvature factor describing the convexity of the curve, which can vary between 0 and 1. When k is close to 1, the curve changes directly from the initial line determined by Φ to a plateau (called Blackman type) determined by Amax and Rd (Leverenz, 1987; Ogren, 1993). When k is close to 0, the curve is a rectangular hyperbola (Leverenz, 1987).
Light compensation point at ambient (CO2) (350 ppm), referred to as PPFDcomp, was calculated when A was equal to 0. The value of PPFDsat at ambient (CO2) was calculated as the PPFD associated with 90% of Amax like by Jurik et al. (1988). Light-saturated A at ambient (CO2) was calculated when PPFD was equal to PPFDsat. The PPFD associated with a 50% reduction in Amax (PPFD50%) was also calculated.
A/(CO2) of each genotype was measured on the same fifth leaf between 900 hr and 1330 hr (CDST; 1 to 4.5 h after sunrise) on 11, 12, and 13 Sept. 2004. The cuvette condition started as 0 ppm (CO2), 25 °C, 70% relative humidity, and 1300 μmol·m−2·s−1 photon PPFD. This level of PPFD was close to the PPFDsat estimated from A/PPFD for the four birch genotypes. Pettersson and McDonald (1992) applied 600 μmol·m−2·s−1 photon PPFD on B. pendula in a similar study, which was not adopted in this study because it was significantly lower than the sunlight level on a sunny day or the PPFDsat estimated in Expt. 1. (CO2) was incrementally increased from 0 to 1100 ppm (50, 100, 200, 300, 400, 500, 600, 700, 800, 900, 1000, 1100 ppm). Net CO2 assimilation was recorded after an ≈15-min acclimation at each (CO2) level. Data were fitted to the negative exponential model adjusted from Reid and Fiscus (1998): A = a (1 − e −bCa ) + c, where a is the potential assimilation capacity, b is the initial slope or carboxylation efficiency, Ca is the ambient CO2 concentration, and c is the intercept on the ordinate [A at the level when (CO2) = 0 ppm].
CO2 compensation point at 1300 μmol photon m−2·s−1 PPFD, referred to as (CO2)comp, was calculated when A was equal to 0. The value of (CO2)sat at 1300 μmol photon m−2·s−1 PPFD was calculated in a similar way as PPFDsat [(CO2) associated with 90% of a]. (CO2)-saturated A at 1300 μmol·m−2·s−1 photon PPFD was calculated when (CO2) was equal to (CO2)sat. The (CO2) associated with a 50% reduction in a [(CO2)50%] was also calculated.
Eight trees of B. papyrifera of similar size were selected for the experiment conducted on 12 and 13 Sept. 2005. Water was withheld from four randomly selected trees until the average predawn water potential (Ψpredawn) reached ≈–2.5 MPa measured psychrometrically (Oosterhuis and Wulleschleger, 1987). A/PPFD and A/(CO2) response curves were generated for well-watered (WW; Ψpredawn ≈ –0.5 MPa) and water-deficit-stressed (WS; Ψpredawn ≈ –2.5 MPa) B. papyrifera as described in Expts. 1 and 2.
The experimental design for A/PPFD and A/(CO2) responses of four birch genotypes was a completely randomized design with the genotype as the main factor and six replication trees per treatment. Data were subjected to SAS PROC NLIN procedure (SAS Institute, Cary, NC) to generate light and CO2 response equations for each genotype. The variables of light and CO2 response equation (A, Φ, Amax, Rd, a, b, and c) and the calculated values [PPFDcomp, PPFD50%, PPFDsat, light-saturated A, (CO2)comp, (CO2)50%, and (CO2)sat, (CO2)-saturated A] were subjected to analysis of variance to investigate difference among genotypes and means were separated with a protected least significant difference at P ≤ 0.05.
Data from A/PPFD and A/(CO2) responses of B. papyrifera were analyzed similarly like in Expts. 1 and 2, except with the plant water status as the main factor.
There was a close relationship between PPFD and A of the four birch genotypes (r2 = 0.97–0.99, Fig. 1). In the four birch genotypes, net CO2 assimilation increased linearly at low PPFD, where it was limited by electron transport rate, and gradually reached a plateau where A would be limited by Rubisco capacity (Ogren, 1993). Detectable decrease in assimilation at high PPFD, an indication of photoinhibition, was not observed in any of the four genotypes for the PPFD range studied (0 to 2000 μmol·m−2·s−1 photon). Therefore, all data were used for analysis of the relationship between PPFD and A.
Citation: HortScience horts 43, 2; 10.21273/HORTSCI.43.2.314
The four birch genotypes reached PPFDcomp at ≈20 μmol·m−2·s−1 photon (Table 1). The PPFDcomp was similar for the four genotypes. Net CO2 assimilation increased rapidly as PPFD was increased from 0 to ≈200 μmol·m−2·s−1 photon (≈10% of full sunlight), where four birch genotypes reached PPFD50%. PPFDsat occurred from 743 to 1576 μmol·m−2·s−1 photon (Fig. 1; Table 1), which is ≈30% to 70% of full sunlight. PPFD50% and PPFDsat were significantly different among the four birch genotypes. PPFD50% and PPFDsat of Betula davurica were 51% and 112% greater than B. papyrifera, respectively.
There were no differences in the photosynthetic quantum efficiencies (Φ) among the four genotypes (Table 1), which indicated that the four birch genotypes use light in photochemistry at similar efficiency at low irradiance when Rubisco is saturating and light is the limiting factor of photosynthesis.
The light response variables of B. papyrifera were similar to a previous study (Gu et al., 2003). No difference was detected for Rd among the genotypes, which ranged from 0.9 μmol·m−2·s−1 CO2 in B. alleghaniensis to 1.3 μmol·m−2·s−1 CO2 in B. nigra ‘Cully’. The birch genotypes differed in light-saturated A and Amax (Table 1). Betula davurica and B. nigra ‘Cully’, which had greater PPFD50% and PPFDsat, had greater Amax and light-saturated A than B. alleghaniensis and B. papyrifera. Betula davurica and B. nigra ‘Cully’ are from warmer origins than B. alleghaniensis and B. papyrifera, which could have affected their light response. Amax of B. papyrifera (11.9 μmol·m−2·s−1 CO2) was similar to a previous report (Jurik et al., 1988). Amax of B. davurica and B. nigra ‘Cully’ (14.2 and 14.1 μmol·m−2·s−1 CO2 , respectively) was ≈20% higher than those of B. alleghaniensis and B. papyrifera. Higher PPFDsat and Amax in B. davurica and B. nigra ‘Cully’ indicates their ability to convert a greater portion of the absorbed light energy to photochemistry and may lower the amount of excess energy needed to be dissipated by plants, as indicated in a similar study on Illicium (Griffin et al., 2004a). The greater ability observed in B. davurica and B. nigra ‘Cully’ to make use of sunlight than B. alleghaniensis and B. papyrifera might enable them to grow faster under full sun situations in the landscape and was consistent with field evaluation at Fayetteville, AR (Gu et al., 2007). On the other hand, the fact that B. alleghaniensis and B. papyrifera reached PPFDsat and Amax sooner indicated that they are more suitable for landscape situations with lower light levels than B. davurica and B. nigra ‘Cully’.
Light compensation point (PPFDcomp), Rd, and Amax are significantly greater in high-light-acclimated plants compared with low-light-acclimated plants (Lambers et al., 1998). This experiment did not find significant differences in PPFDcomp or Rd among four birch genotypes. However, PPFDsat of B. davurica and B. nigra ‘Cully’ were significantly higher than B. alleghaniensis or B. papyrifera, which might indicate their lower shade-tolerance level. Although it was found to be the most shade-intolerant compared with other forest species (Kobe and Coates, 1997), B. papyrifera might not be the most shade-intolerant among Betula species based on the A/PPFD response under greenhouse conditions.
The value of curvature factor (k) determines the photosynthetic efficiency in the intermediate light range above the linear region (Ogren, 1993). The position of the breaking points between the two limits (electron transport rate and Rubisco capacity) determines k, and the Rubisco limitation/light saturation setting at low light levels could result in a higher value of k (Ogren, 1993). Betula papyrifera had a significantly greater k value than the other genotypes (Table 1), which was consistent with the observation that B. papyrifera reached Rubisco limitation/light saturation faster (as indicated by PPFDsat) than the other three genotypes.
At 1300 μmol·m−2·s−1 photon PPFD, the net CO2 assimilation of four birch genotypes increased rapidly to a value of 15 to 20 μmol·m−2·s−1 CO2 with the cuvette (CO2) elevated to 700 ppm (Fig. 2). The A/(CO2) responses indicated that initial linear regions at low (CO2) were Rubisco-saturated and CO2-limited, which changed to CO2-saturated and Rubisco-limited regions at high (CO2) (Farquhar and Sharkey, 1982).
Citation: HortScience horts 43, 2; 10.21273/HORTSCI.43.2.314
The (CO2)comp, which was not significantly different among the four genotypes, was reached at ≈60 ppm (Table 1). This was similar to a previous report on B. pendula under 600 μmol·m−2·s−1 photon PPFD (Pettersson and McDonald, 1992). The (CO2)50% was significantly different among the four birch genotypes. Betula nigra ‘Cully’ and B. papyrifera had the lowest (CO2)50%, 271 ppm and 309 ppm, respectively. Betula davurica had the greatest (CO2)50% of 417 ppm. At 1300 μmol·m−2·s−1 photon PPFD, B. davurica had the greatest (CO2)sat, which was 63% higher than B. nigra ‘Cully’ (Table 1).
The carboxylation efficiency, b, was negatively correlated with (CO2)50% and (CO2)sat in four birch genotypes (Table 1). Betula nigra ‘Cully’, which had the greatest value of b (0.0033) and reached the CO2-saturated stage faster than the other three genotypes, had the lowest (CO2)50% and (CO2)sat. It also had the lowest a (potential assimilation capacity) and CO2-saturated A (22.6 and 18.8 μmol CO2 m−2·s−1, respectively). By contrast, B. davurica, which had the lowest value of b (0.0020) and reached CO2-saturated stage slower, had the greatest (CO2)50% and (CO2)sat. Promotion of assimilation by increasing (CO2) would be more detectable on B. davurica relative to the other genotypes. The greatest (CO2)50% (417 μmol CO2 m−2·s−1) and (CO2)sat (1251 μmol·m−2·s−1 CO2) associated with B. davurica allowed it to continue CO2 assimilation at high (CO2), whereas the other three birch genotypes could not. Betula davurica had the greatest a (37.2 μmol·m−2·s−1 CO2). Betula davurica, which had the greater Amax in the light response experiment, had the CO2 assimilation 60% greater than the other three genotypes at (CO2)sat. On the contrary, Betula nigra ‘Cully’, which also had the greatest Amax in light response, had the least assimilation at (CO2)sat.
Birch selections such as B. nigra ‘Cully’ are usually vegetatively propagated in controlled environments before planted outside, which made CO2 enrichment possible during the early stage of propagation. This might also be applicable to the other vegetatively propagated birch selections such as B × ‘Royal Frost’, B. nigra ‘BNMTF’, B. pendula ‘Laciniata’, and B. platyphylla ‘Fargo’ and selections of the other woody ornamental genera.
Well-watered plants had significantly greater A than WS plants under PPFD from 100 to 2000 μmol·m−2·s−1 photon (Fig. 3A). Amax and light-saturated A of WW plants (15.4 and 14.0 μmol·m−2·s−1 CO2) were ≈3 times greater than WS plants (5.3 and 4.0 μmol CO2 m−2·s−1; Table 2). Water-deficit stress did not affect PPFDcomp. PPFD50% and PPFDsat of WW plants and values were approximately twice as high as the values for WS plants. Calculated Φ was greater in WW plants than WS plants. There was no significant effect on Rd or k between WW and WS plants. Therefore, although WW plants reached light saturation stage faster than WW plants, water-deficit stress did not significantly affect the starting point (determined by the Rd) or the shape (determined by k) of A/PPFD curve. Water-deficit-stressed plants reached light saturation at 366 μmol·m−2·s−1 photon under 350 ppm (CO2), which is ≈20% of full sun conditions. Full sun conditions would more likely cause photoinhibition in WS than WW plants, which reached light saturation at 752 μmol·m−2·s−1 photon. Under full sun conditions in the landscape, WS B. papyrifera might experience one more stress, photoinhibition stress, than WW plants in addition to water deficit.
Citation: HortScience horts 43, 2; 10.21273/HORTSCI.43.2.314
WW plants had significantly greater A than WS plants under (CO2) from 100 to 1100 ppm (Fig. 3B). Potential assimilation capacity (a), CO2-saturated net CO2 assimilation, and c of WW plants were ≈1.5 times greater than WS plants (Table 2). (CO2)comp was similar for both WW and WS plants (70 and 43 ppm, respectively). (CO2)50% of WW plants was approximately twice as high as WS plants and (CO2)sat was half of WS plants. The b value was greater in WW plants than WS plants. Water deficit might have impaired the ability to respond actively to increased CO2 level through both stomatal closure and other nonstomatal regulations. Sage (1994) suggested that stomata would become more conservative under water-deficit stress in elevated CO2 environments. Therefore, water status of plants might be one key factor for successful CO2 enrichment programs to promote plant photosynthesis and growth in controlled environments.
Photosynthetic activity was significantly affected by water deficit in B. papyrifera as indicated by less assimilation in both light and CO2 responses (Table 2). In light response, water stress decreased Φ (quantum efficiency) by 30% and Amax by 66%, and in CO2 response, water stress decreased b (carboxylation efficiency) by 48% and decreased a by 31%, which both indicated nonstomatal limitation of assimilation under water stress. Reduction of photosynthesis by water stress was observed in field-grown soybean; however, quantum efficiency and carboxylation efficiency were unaffected by water stress (Sullivan and Teramura, 1990). The discrepancy between the two studies might result from different levels of water stress. Stomatal closure is the dominant limitation to photosynthesis at mild to moderate water stress, and decreased Rubisco content becomes the dominant limitation on photosynthesis at severe water stress (Flexas and Medrano, 2002), which may have caused decreased quantum efficiency and carboxylation efficiency in the current study (Ψpredawn ≈ –2.5 MPa). CO2 enrichment was found to significantly increase water use efficiency in rice exposed to water stress (Baker et al., 1997). Less reduction in photosynthesis of B. papyrifera under a high level of (CO2) compared with under a high light level agreed with Baker et al.’s finding that increased (CO2) might be able to alleviate water stress or improve water use efficiency under ambient light level.
Based on our results, k, PPFDsat and Amax in photosynthesis light response appeared to be good indicators of shade tolerance of birch genotypes, and k is unaffected by water-deficit stress, whereas PPFDsat and Amax were reduced by water-deficit stress. These values could serve as a basis for recommending birch genotypes for landscapes with various light conditions in the landscape. Almost all birch species are considered shade-intolerant, and special attention might need to be paid to their shade tolerance in landscape situations. Based on our results, B. davurica had the highest Amax in both light and CO2 responses among the four birch genotypes examined under greenhouse conditions. Despite its northern origin of northeastern China, active responses of B. davurica to a high light level and (CO2) in the greenhouse were confirmed by field performance at two locations in Arkansas representing U.S. Department of Agriculture cold hardiness Zone 7 and 8 (Gu et al., 2007). CO2 enrichment could potentially increase plant growth of birch genotypes in a controlled environment, and it might be important to manage water status to maximize the benefit of CO2 enrichment.
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Current address: Mississippi State University, Plant and Soil Sciences, Department of Plant Soil Sciences, Box 9555, Mississippi State, MS 39762.
To whom reprint requests should be addressed; e-mail mgu@pss.msstate.edu
