Effects of changes in the photosynthetic photon flux density on net gas exchange of Citrus limon and Nicotiana tabacum

Oscilação cíclica da condutância estomática em Citrus limon e Nicotiana tabacum

Abstracts

The objective of this study was to evaluate the effects of changes in the photosynthetic photon flux density (PPFD) on net gas exchange of Citrus limon, a woody species, and Nicotiana tabacum, an herbaceous species. When PPFD was increased from 50 to 350 mumol.m-2.s-1 and returned to 50 mumol.m-2.s-1 after 60 min, the CO2 assimilation rate (A) increased and stabilized after 15 min in both species. Stomatal conductance (g s), however, continued to increase. After returning to low PPFD, A immediately diminished to a low value for both lemon and tobacco. Stomatal conductance of lemon diminished slowly over 60 min, whereas g s for tobacco took only 15 min to decrease. This difference in behavior is probably due to over-sensitivity of stomata of woody species, such as Citrus, when exposed to high light, retarding stomatal closure on return to low PPFD. Furthermore, when lemon, growing at a PPFD of 300 mumol.m-2.s-1, was submitted to a step increase of 600 mumol.m-2.s-1, there was an oscillatory behavior of A and g s requiring 150 min to stabilize. The causes of this behavior are discussed with respect to improved intrinsic water use efficiency by stomatal closure.

CO2 assimilation rate; gas exchange; stomata; intrinsic water use efficiency

O objetivo desse estudo foi avaliar o efeito da variação da densidade de fluxo de fótons fotossintéticos (DFFF) nas trocas gasosas de Citrus limon, uma espécie lenhosa, e Nicotiana tabacum, uma espécie herbácea. Quando a DFFF foi aumentada de 50 para 350 mimol.m-2.s-1 durante 60 min, retornando em seguida a 50 mimol.m-2.s-1, a taxa de assimilação de CO2 (A) aumentou e estabilizou após 15 min, mas a condutância estomática (g s) continuou crescendo, em ambas as espécies. Quando se retornou à baixa DFFF, A diminuiu instantaneamente nas duas espécies, mas a g s do limoeiro diminuiu lentamente durante 60 min, enquanto em tabaco, a g s levou apenas 15 min para decrescer. Essa diferença nas respostas é provavelmente devida à hipersensibilidade dos estômatos de espécies lenhosas, como Citrus, quando submetidas à alta DFFF, retardando o seu fechamento, quando de volta à baixa DFFF. Além disso, quando o limoeiro, crescendo sob DFFF de 300 mimol.m-2.s-1, foi submetido subitamente a 600 mimol.m-2.s-1, iniciou-se uma flutuação de A e g s, levando 150 min para se estabilizar. As causas dessa oscilação são discutidas em função do ajuste da eficiência intrínseca no uso de água, devido ao controle estomático.

eficiência intrínseca no uso de água; estômatos; taxa de assimilação de CO2; trocas gasosas

RESEARCH ARTICLE

Effects of changes in the photosynthetic photon flux density on net gas exchange of Citrus limon and Nicotiana tabacum

Oscilação cíclica da condutância estomática em Citrus limon e Nicotiana tabacum

Carlos Pimentel^{I, *}; Rafael Vasconcelos Ribeiro^II; Mauro Guida dos Santos^II; Ricardo Ferraz de Oliveira^II; Eduardo Caruso Machado^III

^IDepartamento de Fitotecnia, Instituto de Agronomia, Universidade Federal Rural do Rio de Janeiro, CEP 23851-970, Itaguaí, RJ, Brasil

^IIDepartamento de Ciências Biológicas, CP 09, Escola Superior de Agricultura "Luiz de Queiroz"-USP, CEP 13419-110, Piracicaba, SP, Brasil

^IIICentro de Pesquisa e Desenvolvimento em Ecofisiologia e Biofísica, CP 28, Instituto Agronômico de Campinas, CEP 13001-970, Campinas, SP, Brasil

ABSTRACT

The objective of this study was to evaluate the effects of changes in the photosynthetic photon flux density (PPFD) on net gas exchange of Citrus limon, a woody species, and Nicotiana tabacum, an herbaceous species. When PPFD was increased from 50 to 350 mmol.m^-2.s^-1 and returned to 50 mmol.m^-2.s^-1 after 60 min, the CO₂ assimilation rate (A) increased and stabilized after 15 min in both species. Stomatal conductance (g_s), however, continued to increase. After returning to low PPFD, A immediately diminished to a low value for both lemon and tobacco. Stomatal conductance of lemon diminished slowly over 60 min, whereas g_s for tobacco took only 15 min to decrease. This difference in behavior is probably due to over-sensitivity of stomata of woody species, such as Citrus, when exposed to high light, retarding stomatal closure on return to low PPFD. Furthermore, when lemon, growing at a PPFD of 300 mmol.m^-2.s^-1, was submitted to a step increase of 600 mmol.m^-2.s^-1, there was an oscillatory behavior of A and g_s requiring 150 min to stabilize. The causes of this behavior are discussed with respect to improved intrinsic water use efficiency by stomatal closure.

Key words: CO₂ assimilation rate, gas exchange, stomata, intrinsic water use efficiency.

RESUMO

O objetivo desse estudo foi avaliar o efeito da variação da densidade de fluxo de fótons fotossintéticos (DFFF) nas trocas gasosas de Citrus limon, uma espécie lenhosa, e Nicotiana tabacum, uma espécie herbácea. Quando a DFFF foi aumentada de 50 para 350 mmol.m^-2.s^-1 durante 60 min, retornando em seguida a 50 mmol.m^-2.s^-1, a taxa de assimilação de CO₂ (A) aumentou e estabilizou após 15 min, mas a condutância estomática (g_s) continuou crescendo, em ambas as espécies. Quando se retornou à baixa DFFF, A diminuiu instantaneamente nas duas espécies, mas a g_s do limoeiro diminuiu lentamente durante 60 min, enquanto em tabaco, a g_s levou apenas 15 min para decrescer. Essa diferença nas respostas é provavelmente devida à hipersensibilidade dos estômatos de espécies lenhosas, como Citrus, quando submetidas à alta DFFF, retardando o seu fechamento, quando de volta à baixa DFFF. Além disso, quando o limoeiro, crescendo sob DFFF de 300 mmol.m^-2.s^-1, foi submetido subitamente a 600 mmol.m^-2.s^-1, iniciou-se uma flutuação de A e g_s, levando 150 min para se estabilizar. As causas dessa oscilação são discutidas em função do ajuste da eficiência intrínseca no uso de água, devido ao controle estomático.

Palavras-chave: eficiência intrínseca no uso de água, estômatos, taxa de assimilação de CO₂, trocas gasosas.

INTRODUCTION

Oscillatory transpiration is a rhythmic fluctuation that has been described in several species (Barrs, 1971), with an average cycle periodicity of 15 to 120 min (Kramer and Boyer, 1995). Stomatal cycling can be triggered by environmental signals such as changes in photosynthetic photon flux density (PPFD) (Zipperlen and Press, 1997) or changes in xylem water potential and hydraulic conductivity (L_p) (Rose and Rose, 1994). Stomatal cycling is common in Citrus under field conditions, when the PPFD, vapor pressure deficit (VPD) of air or soil water deficit increase. This cycle has a period of about one hour, and increases in amplitude and decreases in duration as the daytime progresses (Levy and Kaufmann, 1976). Stomatal closure can also be induced by a non-hydraulic root signal from roots, usually ABA (Kramer and Boyer, 1995), or changes in L_p, a hydraulic signal, especially under high transpiration rates (Steudle, 2001). This change in L_pis caused, among others factors, by an apoplastic water movement through the endodermis cell wall in addition to that passing along the cellular pathway under high transpiration rates (Hartung et al., 2002). In maize under high transpiration rates, despite the increase in radial water flow, the ABA concentration in the xylem remained constant or even increased (Hose et al., 2001). This is due to transport of the root apoplastic and symplastic ABA by solvent drag (Hartung et al., 2002).

Low CO₂ assimilation rate (A) and leaf diffusive conductance (g_s) often characterize leaves of perennial species, as in Citrus. Although most agricultural and herbaceous C₃ plants have A in the range 20-40 mmol CO₂.m^-2.s^-1, in mature leaves of Citrus, under near optimal environmental conditions, A greater than 12 mmol CO₂.m^-2.s^-1 is rarely observed (Lloyd et al., 1992). Although g_s of Citrus are also relatively low (generally less than 0.2 mol.m^-2.s^-1), under optimal or near optimal conditions intercellular CO₂ partial pressure (C_i) is typically in the range of 200-250 mmol.mol^-1 (Lloyd et al., 1992), while for herbaceous plants C_ican vary from 250 to 350 mmol.mol^-1 (Long and Hällgren, 1993). Thus, the stomatal limitation of A in woody species can be higher than 20%, as reported by Jones (1998) for herbaceous plants.

Citrus and others woody species have a low maximum rate of carboxylation (V_cmax) because of the low chloroplastic CO₂ partial pressure (Lloyd et al., 1992), resulting from a low mesophyll conductance to CO₂ diffusion (Syvertsen and Lloyd, 1994). In Citrus, Rubisco accounts for only 10% of the nitrogen in the leaf (Lloyd et al., 1987). Therefore, for long-lived leaves of woody shade-tolerant rain forest species exposed to light, the mean time to attain 90% full photosynthetic induction fell in the range of 11-36 min, as opposed to 1-3 min for short-lived species (Zipperlen and Press, 1997).

Presently in Brazil there is an increased interest in gas exchange studies with Citrus, especially after the incidence of citrus variegated chlorosis (CVC), a vascular disease caused by the bacterium Xylella fastidiosa, which causes reduction in photosynthesis and productivity of Citrus (Ribeiro et al., 2003). However, gas exchange measurements need to be carefully done to avoid environmental changes during measurements, which induce stomatal oscillations.

Thus, the aim of this study was to evaluate the different effects of changing PPFD on A and g_s behavior of lemon, an evergreen woody plant with low mesophyll conductance to CO₂ diffusion, compared to an annual herbaceous plant, specifically tobacco, with its higher mesophyll conductance to CO₂ diffusion.

MATERIAL AND METHODS

The plants of Citrus limon Burm. f. (two years old) and of Nicotiana tabacum cv. W38 (45 days old) germinated and grown in a greenhouse, in 1.5 L and 5 L pots, for tobacco and lemon, respectively, with a soil-less growth medium (Sunshine Mix #1, SunGro Horticulture, Inc., Bellevue, WA USA), at the University of Illinois, IL, USA (40º01"N, 88º16"W). The plants were watered regularly and were fertilized weekly with approximately 300 mL.L^-1 of NPK 15:5:15 (Peters Excel, The Scotts Co., Marysville, OH USA) to pot saturation. Greenhouse air temperature was set at 25ºC for the 16 h complemented photoperiod and 18ºC for night. One week before measurements three plants were transferred to a cabinet (E15, Conviron, Winnipeg, Manitoba, Canada), with a PPFD of 300 mmol.m^-2.s^-1 at canopy height, a photoperiod of 14 h, a day/night air temperature of 25/20ºC, and a VPD of 0.7 kPa.

Leaf gas exchange rates were measured using an open gas exchange system with independent [CO₂] control, using a 6 cm² clamp-on leaf cuvette (LI-6400, LI-COR, Lincoln, NE USA). The gas-exchange system was calibrated for CO₂ with a source of air containing a precisely known concentration of CO₂ in the range to be analyzed, and for H₂O vapor with a dew point generator (LI-610, LI-COR, Lincoln, NE USA), as proposed by Long and Hällgren (1993). It was zeroed daily using CO₂-free air, and the VPD in the cuvette was maintained between 0.5 and 1.0 kPa to prevent stomatal closure. All the measurements were carried out at 25ºC and 360 mL.L^-1 of CO₂ on the youngest fully expanded leaf prior to stem elongation.

The lemon response of CO₂ assimilation rate (A) to PPFD (the A/Q curve, as stated by Long and Hällgren, 1993) was conducted on plants from the cabinet, using an artificial quartz halide light source (LI-6400-02 LED light source, LI-COR, Lincoln, NE USA) controlled with a quantum sensor located inside the leaf cuvette. The A/Q curve was obtained after one hour at the higher PPFD used. It was done diminishing the PPFD by 100 mmol.m^-2.s^-1 after 5 min at each value of PPFD, from 1,500 to 500 mmol.m^-2.s^-1, so as to avoid photoinhibition, and by 50 mmol.m^-2.s^-1 from 500 to zero mmol.m^-2.s^-1, to obtain the curve inflexion. On the other hand, lemon and tobacco responses of A, g_s, C_iand Intrinsic Water Use Efficiency (IWUE = A.g_s^-1) were evaluated under a change of PPFD from 50 to 350 mmol.m^-2.s^-1, after stabilizing under 50 mmol.m^-2.s^-1 (data shown for the last 10 min). The PPFD was lowered again to 50 mmol.m^-2.s^-1 after 60 min under 350 mmol.m^-2.s^-1, as used by Barradas and Jones (1996) on Phaseolus vulgaris, an annual herbaceous plant. Finally, the cycling of A and g_s measurements in lemon were obtained after gas exchange parameters were stabilized (after at least 2 h) at 300 mmol.m^-2.s^-1 (data showed for the last 20 min), and then increasing the PPFD to 600 mmol.m^-2.s^-1 during 130 min.

The measurements were all carried out with one leaf using three replicate plants in a completely randomized statistical design. Data were subjected to analysis of variance.

RESULTS AND DISCUSSION

Typical of a C₃ plant, the photosynthetic light response curve (A/Q curve) of C. limon (figure 1) produced a saturation of A at 600 to 800 mmol.m^-2.s^-1, which represents 25-30% of full sunlight (Long and Hällgren, 1993). Consequently, high light intensities over 600 to 800 mmol.m^-2.s^-1 may cause photoinhibition reducing A (Bolhàr-Nordenkampf and Öquist, 1993), and therefore, for environmental-controlled assays with Citrus, the ideal light intensities for maximal A are in this range (Bernacchi et al., 2001). An increase of 20% of the integrated daily A was obtained with nursery trees of Citrus sinensis, by using a reflective net over the greenhouse during midday to avoid photoinhibition by high PPFD (Medina et al., 2002).

The response of A, g_s and C_iof lemon to changing PPFD from 50 to 350 and returning to 50 mmol.m^-2.s^-1 (figure 2), produced values in the same range as those for bean (Barradas and Jones, 1996). After 15 min of changing PPFD from 50 to 350 mmol.m^-2.s^-1, A stabilized around 10.0 mmol CO₂.m^-2.s^-1 (figure 2A). On the other hand, the Citrus g_s values increased constantly when changing the PPFD to 350 mmol.m^-2.s^-1 reaching a value of 0.17 mol.m^-2.s^-1 at 60 min (figure 2B). However, when returning the PPFD from 350 to 50 mmol.m^-2.s^-1, A decreased instantly to 2.5 mmol CO₂.m^-2.s^-1 and stabilized at this value. However, g_s diminished slowly, from 0.17 to 0.054 mol.m^-2.s^-1, tending to stabilize only after 60 min. These results are in agreement with those obtained with long-lived leaves (Zipperlen and Press, 1997), but contrast data for bean, an herbaceous plant, where a more rapid decrease of g_s was recorded when returning to 50 mmol.m^-2.s^-1 (Barradas and Jones, 1996). The C_i values for lemon increased as for A when changing to a higher PPFD (figure 2C), but when returning to a low PPFD, the C_i values diminished more slowly than A. In addition, the lemon C_i values, after stabilization at low or higher PPFD, were low, around 250 mmol.mol^-1, in agreement with Lloyd et al. (1992). On the other hand, the IWUE shows a step increase when changing to a higher PPFD (figure 2D) because the increase of A is greater than that of g_s. After 60 min under high light, it diminished to values close to those under low light due to the slower increase of g_s compared to A. When returning to low light, the IWUE diminished rapidly but returned to initial values after the slow decrease of g_s.

Tobacco, with higher values of A, g_s and C_i than lemon, produced the same response patterns to PPFD as shown for bean (Barradas and Jones, 1996). After 15-20 min under 350 mmol.m^-2.s^-1, A was stabilized around 15 mmol CO₂.m^-2.s^-1 (figure 3A), but g_s continued to increase reaching a value of 0.576 mol.m^-2.s^-1 at 60 min (figure 3B). When returning to 50 mmol.m^-2.s^-1, A diminished to 2.8 mmol CO₂.m^-2.s^-1 immediately and g_s took only 15 min to decrease to 0.307 mol.m^-2.s^-1, thereafter decreasing slowly to 0.255 mol.m^-2.s^-1 over 70 min at 50 mmol.m^-2.s^-1. On the other hand, the C_ivalues for tobacco (figure 3C) were between 250 to 350 mmol.mol^-1 after stabilizing at low or high PPFD, and on return to low PPFD, stabilized as for g_s. As seen for lemon, the IWUE produced a step increase under high light (figure 3D), and then diminished gradually during the 60 min under this condition, but it stabilized at a value greater than those under low light. On return to low light, it decreased suddenly but after a while, it returned to the same initial values. On the other hand, values of A, g_s and Ci for tobacco were much higher than for lemon, whereas IWUE was much lower than for lemon.

Thus, for tobacco, as for bean (Barradas and Jones, 1996), the changes of A in response to either increasing or decreasing PPFD were significantly faster than changes in g_s. However, this is not the case for a woody plant such as lemon, at least when changing the PPFD from a high to a low value showing that the changes in g_s of lemon are slower and the transpiration rates higher than for herbaceous plants. The slower reduction of g_s in Citrus, compared to tobacco, when reducing the PPFD is probably due to over sensitivity of the stomatal response to light for woody species (Zipperlen and Press, 1997), which did not occur in tobacco or bean, both herbaceous plants. In Citrus, as for other woody species, the CO₂ mesophyll conductance is considerably lower (1.1 to 2.2 mmol CO₂.m^-2.s^-1.Pa ^-1) than those reported for unstressed herbaceous plants (Lloyd et al., 1992). However, the low mesophyll conductance of Citrus can be due to the lower C_i values, which is due to the lower g_s values of lemon, because the C_i values are proportional to g_s values (Long and Hällgren, 1993). Thus, for C. limon g_s increases can affect A probably because of the low mesophillic conductance and the need of very high P_CO2 for saturation of A (Lloyd et al., 1992). As a result, the response of A and g_s, and consequently of IWUE, to changing PPFD from 50 to 350 and back to 50 mmol.m^-2.s^-1 in Citrus (figure 2), a perennial woody species, was quite different from tobacco or bean (Barradas and Jones, 1996). The A and g_s values for lemon varied from 3 to 10 mmol CO₂.m^-2.s^-1 and from 0.04 to 0.17 mol.m^-2.s^-1, respectively (figures 2A and 2B), whereas for tobacco, these values varied from 2.8 to 15 mmol CO₂ m^-2.s^-1 and from 0.19 to 0.61 mol.m^-2.s^-1 respectively (figures 3A and 3B). By contrast, the IWUE values for lemon varied from 15 to 170 mmol CO₂.mol^-1H₂O (figure 2D), while for tobacco, these values varied from 5 to 55 mmol CO₂.mol^-1H₂O (figure 3D). Therefore, in woody perennial species such as Citrus, with much lower g_s values than annual herbaceous species such as tobacco, the g_s control of A will be more important (Lloyd et al.,1992), especially when reducing the PPFD, improving their IWUE. Also, the IWUE of lemon was always higher than for tobacco, and under high light it stabilizes at values close to those under low light, but for tobacco, the IWUE values under high light are greater than that under low light.

Increasing the light intensity to 600 mmol.m^-2.s^-1, for plants growing at 300 mmol.m^-2.s^-1, induce an oscillatory stomatal behavior in lemon (figure 4). The g_s values increased from 0.07 to a maximal g_s value of 0.1 mol.m^-2.s^-1 in 10 min at 600 mmol.m^-2.s^-1, while A did not change and was maintained around 7.5 mmol CO₂.m^-2.s^-1. This response is in agreement with data obtained for long-lived leaves, where a faster increase for g_s than for A was found, which takes 11-36 min to reach 90% of full photosynthetic induction with increasing light intensity. This contrasts the 1-3 min for the species with short-lived leaves. In the former, g_s increased at a much greater rate than photosynthesis due to a low mesophyll conductance and thus a slower full photosynthetic induction (Zipperlen and Press, 1997). However, a high g_s value means a high transpiration rate, and if there is no parallel increase in A (figure 4A), it tends to diminish the IWUE (figure 4D). Afterwards, g_s decreased (figure 4B), due to excessive transpiration, and consequently A will also decrease, and the minimal A and g_s values were 3.0 mmol CO₂.m^-2.s^-1 and 0.04 mol.m^-2.s^-1, respectively, after 60 min of saturating light intensity. The rapid initial increases in g_s at 600 mmol CO₂.m^-2.s^-1, without changes in A, lowers the IWUE because g_s increased (figure 4D). Then, there is an induction of stomatal closure and increase in IWUE, probably due to the increased amount of ABA carried by the increased transpiration stream (Hartung et al., 2002). Thus, the reduction in g_s, and consequently in transpiration rate, will improve the IWUE and prevent wilting. However, A became too low and g_s began to increase again because stomatal movement favours maximum possible A values with lower transpiration rates (Kramer and Boyer, 1995). Then, A and g_s stabilized at values of 7.1 mmol CO₂.m^-2.s^-1 and 0.07 mol.m^-2.s^-1, respectively, and the total oscillatory cycle in C. limon took two and half hours.

The temporal dynamics of the circadian control of stomatal movements indicate that it may benefit the plant by increasing IWUE (Kramer and Boyer, 1995). The extra carbon obtained during peaks can outweigh the reduced carbon gain during troughs, resulting in greater net carbon assimilation with a lower loss of water (Webb, 1998) than would be obtained during a steady rise to a maximum, where transpiration would increase without an increase in A (Zipperlen and Press, 1997). The patterns of stomatal oscillations, obtained with potted Citrus trees in these assays, are in agreement with the observations in field-grown trees of C. sinensis (Levy and Kaufmann, 1976). This oscillation can occur in water-stressed plants and is initiated by a sudden shock such as water shortage in the soil, a short period of darkness, cooling of the soil, or changes in humidity and temperature (Kramer and Boyer, 1995).

Therefore, the results presented here for different g_s and C_i values and behavior when changing the PPFD, in the woody species Citrus as compared to the herbaceous species tobacco, highlight the necessity of great care when carrying out gas exchange measurements, especially with woody species. To avoid confusing cyclical plant response with random noise in measurements of an average gas exchange rate of a group of plants, especially when growing in pots, frequently determined by taking just one measurement per plant, repetitive measurements at 10 min intervals can determine whether transpiration is stable or oscillating when environmental conditions are varying (Rose and Rose, 1994). Also, simultaneous measurements of gas exchange with light adapted fluorescence analysis (the measurement of the efficiency of Photosystem II photochemistry - F_PSII) can also be used because fluorescence can vary faster than gas exchange, from static to oscillating, indicating stomatal oscillation and or patchy stomatal closure, or some environmental stress (Cardon et al., 1994).

Received: 01/11/2003, Accepted: 28/03/2004

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Publication Dates

• Publication in this collection
  01 Oct 2004
• Date of issue
  Aug 2004

History

• Accepted
  28 Mar 2004
• Received
  01 Nov 2003