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    Gas exchange and water relations of young potted loquat cv. Algerie under progressive drought conditions

    2018-06-06 09:13:05StellfeldtMaldonadoHuesoCuevas
    Journal of Integrative Agriculture 2018年6期

    A. Stellfeldt, M. A. Maldonado, J. J. Hueso, J. Cuevas

    1 Department of Agronomy, University of Almeria, ceiA3 Almeria 04120, Spain

    2 Experimental Station of Cajamar Las Palmerillas, ceiA3 Almeria 04710, Spain

    1. Introduction

    Plants need large amounts of water to grow and reproduce.When soil water content does not match these plant demands, water stress appears. If plant water demand is not satisfied, root water potential and turgor reach very low values, stimulating the synthesis of several plant growth regulators, including abscisic acid (ABA) (Davies and Zhang 1991). ABA, formed in roots, is then transported to the leaves and induce partial or complete stomatal closure to limit water losses due to transpiration (Davieset al. 2005;Lissoet al. 2011). The closure of stomata has a drastic effect on reducing photosynthetic CO2fixation and, in turn,on plant growth and productivity (Davies and Lakso 1978;Floreet al. 1985; Chaveset al. 2002; Medranoet al. 2002;Díaz-Espejoet al. 2006). However, the magnitude of these negative effects depends on the severity and duration of water stress and also on the drought tolerance of the crop and the phenological stage in which the plant is. Some species have developed mechanisms to maintain the turgor of photosynthetic tissues and the stomatal aperture in order to preserve certain levels of photosynthesis (Matthews and Boyer 1984; Nuneset al. 1989).

    Among those plants tolerant to severe water deficits,we might cite loquat (Eriobotrya japonicaLindl.). Loquat is an evergreen subtropical fruit crop native to southeast China (Linet al. 1999) that belongs to the family Rosaceae subtribe Pyrinae (Potteret al. 2007). Despite its origin,loquat seems well-adapted to the Mediterranean climate where drought periods during summer are very frequent.During this period, loquat can withstand prolonged periods of water stress to which responds in terms of early blooming once irrigation (or rain) comes (Cuevaset al. 2007). Loquat is, in fact, a crop model for the application of regulated deficit irrigation, since the plant responds to irrigation withholding in summer producing a more profitable crop due to the advancement of harvest dates (Hueso and Cuevas 2008,2010). In the last years, our research team refined the best strategy of regulated deficit irrigation for Algerie loquat as that suspending irrigation starting in early June, and prolong it until plants reach a level of water stress integral (SΨ) of around 47 MPa, usually after 8-9 weeks of no irrigation(Fernándezet al. 2010; Cuevaset al. 2012). These levels ofSΨwere measured in commercial plots, where individual trees never exceeded values of stem water potential below–2.2 MPa despite suffering periods of drought of up to 3 months.

    With the aim of determining the maximum level of water stress that a loquat plant may survive, we suspended irrigation in young Algerie loquats grown in pots of reduced volume as long as possible. On these plants, we carefully monitored plant water status and gas exchange parameters in response to the increasing levels of water stress in order to check its effect on CO2assimilation rates and see which levels of water stress may provoke complete stomatal closure and cancel photosynthesis. We also pretended to determine the relationships among soil and plant water status and gas exchange parameters by means of correlation and regression analyses to guide irrigation practice linking photosynthesis rate to soil and plant water status.

    2. Materials and methods

    2.1. Plant materials and experimental conditions

    Measurements of leaf gas exchange and water relations were performed during summer 2012 in an irrigation experiment carried out on 5-year-old potted loquat trees(Fig. 1), located at the Cajamar Experimental Station in Almeria, Southeast Spain (36°48′N, 2°43′W). This area presents a semi-arid subtropical climate with an average rainfall of 241 mm and no rain in summer. The annual evaporation, measured with a Class A pan placed on bare soil at the vicinity of the experimental orchard, averages 1 940 mm yr-1, with extreme values of 8.7 mm d-1on July,2012.

    Fig. 1 Irrigated (I) (A and C) and non-irrigated (NI) (B and D)plants and details of leaves at the end of the experiment.

    The loquat trees were grafted on Provence quince and were grown in pots with a volume of 50 L (outside diameter 0.5-m, and height of 0.41-m) filled with a mixture of sandyloam soil typical of the area (2/3) and peat (1/3). On these plants, we established 2 treatments, a control treatment in which the trees were maintained near field capacity, that is,irrigated (I) and a treatment in which the trees were nonirrigated (NI) until they were near wilting point. The effects of the treatments were analyzed following a randomized complete design with 5 trees (replicates) per treatment. To keep control irrigation treatment close to field capacity, drip irrigation was daily performed providing 6 L pot-1and day.There was no rain at all during the experimental period.The experiment was designed to last 2 weeks. However,the harsh conditions suffered during that summer (see results) forced us to shorten irrigation withholding period,and restart the irrigation 10 days after the beginning of the experiment. The time course of ambient temperature and relative humidity and therefore vapor pressure deficit is provided in Appendix A.

    2.2. Soil and plant water status and gas exchange measurements

    To determine the relationships of gas exchange with the conditions suffered by the trees, we carefully monitored the environmental conditions, soil water content, plant water status, gas exchange parameters and leaf temperature during the experimental period (from June 17 to July 6). Measurements were performed just before irrigation suspension (0 day), and 2, 4, 7, and 9 days after irrigation withholding (DAIW). A new measurement was performed one week after irrigation was restarted.

    Weather (air temperature, relative humidity and vapor pressure deficit) parameters were recorded every 5 min using a data logger HOBO (model U23-001, Onset Computer Co., Bourne, MA, USA). The averages during the period of measurement are provided in Appendix A. Changes in soil moisture were followed recording pot weight changes due to evapotranspiration and for changes in volumetric soil water content during the experiment. The changes in the weight of the pots were recorded using a weighing scale of 0.1 kg precision (Cobos Serie K-Rekord, Barcelona, Spain). No drainage or runoff took place in the pots of I or NI plants.The volumetric soil water content was determined with a time domain reflectometry (TDR) system (Trase 6050X1,Soil Moisture Equipment Co., Santa Barbara, CA, USA).Readings were taken on 5 trees per treatment during the water deficit period and after re-irrigation using 15 cm long waveguides.

    Plant water status was monitored by measuring midday stem water potential (Ψst) with a pressure chamber (Model 3000, Soil Moisture Equipment Co., Santa Barbara, CA,USA). Each time, measurements were performed in 5 fully expanded leaves (one per tree and treatment) located in branches near tree trunk and randomly selected. Leaves were bagged and covered with aluminum foil early in the morning, more than 2 h before leaf detachment (McCutchan and Shackel 1992).

    Pnand stomatal conductance(Gs) were measured using a portable open infrared gas analyzer (CIRAS-2; PP System, Hitchin, Herts, UK) on fully expanded leaves.Readings were taken after steady-state conditions in gas exchange were achieved (around 1 min). The CO2concentration inside the chamber was automatically controlled by the CIRAS-2 porometer at 400 ppm (ambient CO2concentration, approximately), whereas the radiation,temperature and evaporative demands were those of the environment too. CO2and water vapor concentration differences, as well as leaf temperature obtained from energy balance equations, were used to calculate leaf area based onPn, transpiration rate (E) andGsusing von Caemmerer and Farquhar’s equation (von Caemmerer and Farquhar 1981). For gas exchange measurements, 3 fully expanded sunlit leaves in 5 trees per treatment (15 leaves per treatment) were randomly selected and tagged for continuous measurements. The measurements ofPnandGswere made during the period of water stress and after re-irrigation. Irrigation was restarted 10 days after the beginning of the experiment. Daily variations of leaf gas exchange were measured between 10:00 and 13:00 h Greenwich mean time (GTM).

    In order to establish the relationships among soil and plant water status and gas exchange parameters, correlation and regression analyses were performed. Statistical analyses were done using Statgraphic and Sigmaplot software.

    3. Results

    3.1. Soil and plant water status

    The suspension of irrigation caused a rapid and significant loss in pot weight, more acute in the first 7 d of the experiment when a daily average of 0.88 kg of water was lost in the pots of non-irrigated loquats (Fig. 2-A). Pot weight losses continued at a lower rate from 7 to 9 DAIW. Once irrigation was restored, potted loquats regained original weight (Fig. 2-A). The weight of the pots in irrigated plants remained constant along the whole period of the experiment.Initial measurements of I and NI plants showed that the treatments did not differ in this regard, as they did not do it at the beginning of the experiment for any other parameters under control (Fig. 2).

    Volumetric soil water content measured using TDR also diminished as the dry period advanced, showing significant differences between I and NI plants at 2 DAIW (I=40.59vs.NI=30.79 mm), coinciding with the first significant loss of pot weight. The differences became higher at 4 DAIW (I=38.31vs.NI=13.36 mm) and after (Fig. 2-B). Soil water content in I plants did not show large variations during the period of the experimentation, oscillating around field capacity value (Fig. 2-B). Since runoff and drainage were not observed, lack of changes in pot weight in I plants confirm the adequacy of the irrigation program.

    Ψstclearly reproduced the changes in water availability showing significant differences between treatments also beginning at 2 DAIW (Fig. 2-C). The differences remained significant for the entire dry period, but diminished in a great extent a week after irrigation was restarted (Fig. 2-C). In the last day of the dry period, the averageΨstvalue in NI plants was –4.05 MPa. At that time, the measurements made with the pressure chamber became very difficult, since the emergence of the water drop through the petiole of the leaf was largely delayed, even at very high pressures, causing in occasions the tearing of the leaf blade inside the chamber. In these circumstances, the displacement of the petiole out of the pressure chamber made the measurements dangerous,given the high pressures applied. A single plant reached a negative value ofΨst=–5.00 MPa, before we decided to cancell the dry period. I plants showed values ofΨstbetween–0.70 and –1.15 MPa all the time.

    Fig. 2 Changes in pot weight (A), volumetric soil water content (SWC, B) and stem water potential (Ψst, C) during the experiment (from June 18 to July 6, 2012) in irrigated (I)and non-irrigated (NI) plants. The different letters in each measurement date indicate significant differences at 0.05 level.ns, not significantly different. Bars indicate SE.

    3.2. Gas exchange parameters

    Water stress did indeed affect gas exchange parameters,but the changes were not observed. From equivalent values of stomatal conductance before irrigation withholding(I=150.40vs.NI=148.60 mmol m–2s–1),Gsrecords dropped in NI plants, while remained more or less stable in I plants(Fig. 3-A). The differences became significant at 4 DAIW and increased afterwards, sinceGsvalues plummeted in NI loquats as the dry period progressed. At the end of the dry period,Gsrecords in NI plants averaged only 5.37 mmol m–2s–1.Gswas occasionally reduced in I plants, probably due to the harsh environmental conditions suffered during the experiment (high temperatures and low relative humidity leading to high vapor pressure deficits, Appendix A). In any case,Gsdifferences between I and NI plants remained significant until the end of the dry period. Once irrigation was restarted, these differences disappeared.

    The effects of irrigation withholding on photosynthesis were also noted at 4 DAIW, whenPnvalues in NI plants were barely a 50% of those measured in I plants (I=16.23vs.NI=8.74 μmol m–2s–1). In the last day of irrigation withholding, thePnin NI plants averaged 3.49 μmol m–2s–1,which was much lower than the value measured in control plants (20.35 μmol m–2s–1). After watering was reassumed,NI reached an averagePnvalue of 14.98vs.an average of 14.93 μmol m–2s–1measured in I plants, informing of the fast recovery of NI loquats. Minor oscillations inPnlinked to changes in the environment were also observed in I plants (Fig. 3-B).

    In line with previous argument, the transpiration (E) in NI plants was largely reduced due to the severe water stress.The differences between I and NI plants became significant at 4 DAIW too (I=1.94vs.NI=1.01 mmol m–2s–1) (Fig. 3-C).The differences were even larger at the end of the dry period (I=1.48vs.NI=0.52 mmol m–2s–1), but once again disappeared 1 week after reirrigation (I=0.77vs.NI=0.76 mmol m–2s–1). Stomatal closure has been often linked to an increase in leaf temperature since the lack of transpiration through the closed stomata makes the refrigeration of the leaf tissues difficult. Daily morning temperature during the experiment was between 28.7 and 32.9°C. At solar noon,when measurements were taken, temperatures rose to 30.7-36.7°C (Appendix A). Leaf temperature did not show a clear trend during the experiment. In occasions, leaf temperature was above ambient (approximately 2°C above in both treatments), while in some other moments readings taken in the leaves were below ambient temperatures. The differences between treatments in leaf temperature were not significant and scarcely reached a few tenths of a degree(Appendix A).

    Fig. 3 Changes in stomatal conductance (gs, A), net photosynthetic rate (Pn, B) and transpiration rate (C) during the experiment (from June 17 to July 6, 2012) in irrigated (I) and non-irrigated (NI) plants. The different letters mean significant differences at 0.05 level. ns, no significant different. Bars indicate SE.

    Multiple linear regressions were performed to detect the main environmental and physiological determinants of photosynthetic rates in Algerie loquats. The analyses show significant relationships betweenPnandGs(P=0.007), and betweenPnandΨst(P=0.008). The highest coefficient of determination ofPnrate was obtained forGs(r2=0.759).Non-linear regressions confirmed the significant relationship between these 2 parameters (P<0.0001). The best fitting(r2=0.794) was observed for a logistic model (Fig. 4), in which 3 parts can be identified. In the first part of the curve,forGsvalues close to zero,Pnwas minimal. In the second part of the curve, a linear relationship betweenGsandPncan be deduced. Finally, asGsvalues were higher than 80 mmol m–2s–1,Pndid not increase much, but showed instead a plateau around values of 20 μmol m–2s–1. The highest single measurement ofPnwas 25.6 μmol m–2s–1in control fully irrigated plants measured at the beginning of the experiment in leaves with a value ofGsof 253 mmol m–2s–1.Photosynthesis was never zero. The minimum value ofPnmeasured was 1.8 μmol m–2s–1in NI plants at the end of the dry period when stomata seemed almost close (Gs=1.0 mmol m–2s–1). The comparison of the slopes of the regression equations explaining the relationships betweenPnandGsin different sections of the range showed significant differences(P<0.001) (Fig. 4). The slope of central section was 10 times higher (m=0.1777) than the increase rate observed in the region of the plateau (m=0.0178), meaning a much higher increase ofPnin the central section of the curve.

    On the contrary, no significant relationships were found betweenPnand pot weight, or soil water content,Eand leaf temperature (data not shown). The significant relationship betweenGsandΨstwas not lineal either, but exponential,meaning in this case that higher (less negative) values ofΨstallowed a much higher stomatal aperture (Fig. 5). In other words, a better water status of Algerie loquat plants allows higher stomatal aperture which in turn favors a higher photosynthesis rate. On the contrary, whenΨstfell below–1.5 MPa,Gsdiminished very rapidly precluding then CO2fixation asPndrops acutely. IfΨstdropped to values lower than –3.0 MPa,Gsbecame almost zero (Fig. 5).

    4. Discussion

    Irrigation withholding caused a rapid reduction in water availability in young Algerie trees that were planted in small pots with a limited soil volume. This reduction was reflected in a drastic diminution of the weight of the pots, consequence of the water losses that in turn affected plant water status.Soil water content as well asΨstvalues were extremely low at the end of the irrigation withholding period forcing us to cancel the dry period before the 2-week duration scheduled.The strong water losses and the negative effects observed on plant water status must be the result of the difference between the reduced availability of water in the small pots and the evaporative demand (Boyer 1995), quite high during summer in Almeria, Spain (Appendix A). Detrimental effects on plant water status caused by days with high evaporative demand are often reported in the Mediterranean climate,even for fully irrigated trees of many crops (Morianaet al.2003; Tognettiet al. 2009; Martín-Vertedoret al. 2011).Nonetheless, the main force reducingΨstin NI loquats seems the complete suspension of irrigation. If rapid negative effects were noted on NI plants when irrigation was suspended, equally rapid was the recovery of them when irrigation was restarted, demonstrating thus the extraordinary capacity of loquat to endure severe water restrictions.

    Progressive stomatal closure was the response of NI plants to adapt to the drastic water losses in the soil and to the compromised plant water status. In accordance to this response,Gswas progressively diminished in NI plants reaching the lowest values at the end of the dry period. The significant relationships betweenΨstvalues andGsrecords is shown in Fig. 5, from which it can be deduced that whenΨstfalls below –1.5 MPa,Gsdiminishes rapidly. IfΨstdrops to values lower than –3.0 MPa,Gsbecomes almost zero. This indicates notable effects of moderate levels of water stress on gas exchange parameters, and extreme if water stress is severe. This response is compatible with the remarkable capacity of water-stressed loquats to fully recover once irrigation was restarted.

    Fig. 4 Relationship between net photosynthetic (Pn) and stomatal conductance (Gs). The whole set of data significantly fitted a logistic curve and a linear increase of Pn was found for values of Gs<80 mmol m–2 s–1. For values above this level, a plateau region was observed with the slopes of these regions being significantly different (P<0.001).

    Fig. 5 Relationship between stomatal conductance (Gs) and stem water potential (Ψst).

    Stomatal closure in response to ABA accumulation in the leaves is a common response to water deficits (Lissoet al.2011), since one of the most important function of ABA is to avoid water losses and regulates the tolerance to osmotic stress (Boudsocq and Lauriere 2005). In this sense, it seems that ABA accomplishes a double function in response to drought: it diminishes guard cells turgor and, in addition,induces the expression of genes involved in the tolerance to severe water deficits (Zhu 2002). Low water availability is the main environmental factor limiting photosynthesis and growth in flowering plants (Boyer 1982). This effect often causes severe yield reductions in crops growing in arid and semi-arid zones such as in the Mediterranean climate (Chaveset al. 2003). When water availability is limited after drought episodes, the negative effects on plant water status might lead to progressive stomatal closure and to lower rates of photosynthesis (Lawlor 1995). In this regard, a lineal relationship between stomatal closure and photosynthetic rates has often been reported. In our case,Gsreduction in potted loquats caused a rapid fall ofPnrates(Fig. 4) and a diminution ofE. However, in some species,the relationship between these parameters is more complex.In this regard, Farquhar and Sharkey (1982) conclude that althoughGssubstantially reduces transpiration, rarely limits significantly photosynthesis, because this process is more often limited for other factors contributing to stomatal closure. For instance, under high CO2levels, the limiting factor for photosynthesis is the regeneration of Rubisco.

    In our study,Pnrate showed a significant relationship withGs. The best fitting was observed for a logistic model.Logistic model suggests a maximum level ofPnestablished around an asymptote. That asymptote was around 20 μmol m–2s–1when stomata were fully open. In the logistic curve, 3 parts were identified. The closerGsvalue was to zero, the lessPnwas, althoughPnwas not zero but 2 μmol m–2s–1. In the second part of the curve, a linear relationship betweenGsandPnwas found. Finally, forGsvalues higher than 80 mmol m–2s–1,Pndid not increase much, but instead it showed a plateau, meaning than higher aperture of stomata scarcely increasesPnin young potted Algerie loquats (Fig. 4). Low CO2levels within the leaves often limit photosynthesis in cases of severe water stress. In this regard, Flexaset al. (2004) concluded after a detailed study that water stress mostly affects CO2diffusion in leaves. This decreasing in CO2diffusion could be a consequence of the reduction inGs, but in any case, water deficit would affect the biochemical capacity of the leaves for CO2assimilation. Our experiment shows that despite severe water stress strongly reduced photosynthesis, CO2assimilation never dropped to zero, indicating that the closure of stomata largely reduced,but did not suspend completely photosynthesis in ‘Algerie’loquats. This suggests that some CO2diffused through the cuticle despite stomata are almost closed. This CO2entry would allow a slight photosynthetic rate, even at severe water stress. Boyeret al. (1997) assure that leaf cuticle protects efficiently leaves from dehydration, but that even when stomata are sealed, CO2and water vapor diffuse slowly through the cuticle.

    After restoring irrigation,Pnlevels were rapidly recovered reinforcing the hypothesis that photosynthetic machinery remained intact, after such a severe water stress.Similarly, olive trees subjected to severe water stress had photosynthesis values between 0 and 2 μmol m–2s–1, but also recovered rapidly after irrigation (Morianaet al. 2002).Young apricot trees subjected to 2 periods of water deficit only diminished photosynthetic rate at the end of the dry periods, showing also a fast recovery afterwards. These results suggest that stomata behavior is not a passive response to water deficit. On the contrary, it seems that the aperture and closure of stomata is under a more complex regulation (Ruiz-Sánchezet al. 1997), at least in species well-adapted to the Mediterranean climate such as olive,apricot and loquat. Additionally, in avocado, photosynthesis is inhibited under mild water stress due to a reduction in CO2diffusion linked to stomata closure and to changes in the structure of the mesophyll of the leaf.(Chartzoulakiset al. 2002).

    In this study, we did not find an effect of irrigation withholding on leaf temperature. In this sense, leaf temperature differences between treatments were not significant and scarcely reached a few tenths of a degree.Leaf temperature is directly determined by leaf energy and water balance, but radiation, air temperature, humidity and wind speed modify leaf temperature (Fuchs 1990). High values ofPnwere observed in control plants even when leaf temperature was very high. On the contrary, in a previous study conducted on adult trees in a loquat orchard, very lowPnvalues were observed at midday for fully irrigated plants (Stellfeldtet al. 2011). It is widely known that in Mediterranean climate,Pnat midday strongly decreases during summer due to high temperature, high vapor pressure deficit and high irradiance (Tehnunnenet al. 1984; Ogaya and Pe?uelas 2003; Llusiaet al. 2016). This behavior is a consequence of the strong stomatal control exerted by the plant to avoid large water losses during summer. In this experiment, control plants were fully irrigated in the morning allowing the maintenance of a high enough stomatal conductance and high photosynthetic rates at midday.

    Finally, it is worth mentioning that all NI plants bloomed at the same period, which was regular than I plants did. In previous field experiments, water-stressed loquats during summer bloomed well in advance to control fully irrigated trees (Cuevaset al. 2007, 2008). The lack of effects of the dry period on phenology may be due to NI plants did not reach the threshold level ofSΨneeded to modify flowering dates (SΨ>29 MPa days; Fernándezet al. 2010). In this experiment,SΨin NI plants scarcely reached 20 MPa days, because the dry period was too short to successfully advance blooming dates, despite of the water stress intensity.

    5. Conclustion

    Even though deficit irrigated plants wilted and dropped some leaves, all water stressed plants survived. Furthermore,1 week after irrigation was restored, water stressed plants reachedPnvalues very like those of non-stressed plants confirming the remarkable water stress tolerance of loquat and suggesting that photosynthesis machinery remain intact even after severe levels of water stress in ‘Algerie’ loquat.These results also confirm the good adaptation of loquat to the summer dry periods typical of the Mediterranean climate.No unexpectedly, Spain is the second largest producer of loquat in the world after China.

    Acknowledgements

    This research was partially financed by the Junta de Andalucía with European Union (FEDER) funds (AGR-03183).

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