Defining biological thresholds associated to plant water status for monitoring water restriction effects: Stomatal conductance and photosynthesis recovery as key indicators in potato

Agricultural Water Management 177 (2016) 369–378

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Agricultural Water Management journal homepage: www.elsevier.com/locate/agwat

Defining biological thresholds associated to plant water status for monitoring water restriction effects: Stomatal conductance and photosynthesis recovery as key indicators in potato David A. Ramírez a,b,∗ , Wendy Yactayo a , Libby R. Rens c , José L. Rolando a , Susan Palacios a , Felipe De Mendiburu a,b , Víctor Mares a , Carolina Barreda a , Hildo Loayza a , Philippe Monneveux a , Lincoln Zotarelli c , Awais Khan a , Roberto Quiroz a a

International Potato Centre (CIP), P.O. Box 1558, Lima 12, Peru Universidad Nacional Agraria La Molina, Av. La Molina s/n, Lima, Peru c Horticultural Science Department, University of Florida, 241 Fifield Hall, Gainesville, FL 32611, USA b

a r t i c l e

i n f o

Article history: Received 13 April 2016 Received in revised form 22 July 2016 Accepted 24 August 2016 Keywords: Carbon isotope discrimination Crop water stress index Drought Photochemical reflectance index Solanum tuberosum

a b s t r a c t The definition of irrigation schedules depends on the understanding of the response of key plant traits to different water restriction characteristics with the aim to avoid physiological impairment. In this study, different timings (at tuber initiation and bulking) and intensities (four soil moisture levels) of water restriction were tested in the potato crop. The temporal patterns of mid-morning or maximum, light saturated stomatal conductance (gs max ), recovery of net photosynthesis (Arecovery ), stem water potential (stem ), carbon isotope discrimination in tubers (tuber ), plant water concentration (PWC), photochemical reflectance index (PRI) and crop water stress index (CWSI) were analyzed. Early-severe water restriction caused a drastic yield reduction, with low recovery of physiological responses (gs max , tuber , stem , CWSI, Arecovery ) after 15 days of post-restriction irrigation and even a continued reduction of some of them (PWC, PRI). It also caused a prolonged gs max reduction below 0.05 mol H2 O m−2 s−1 (≈ 5 ␮mol CO2 m−2 s−1 of net photosynthesis) suggesting that this value defines a physiological severity threshold in potato, under which a metabolic impairment occurs. CWSI and PRI showed a close linear (R2 = 0.76) and no linear (natural logarithm function, R2 = 0.67) relationship with gs max respectively. In cloudless dry environments, irrigation schedules in potato should aim to avoiding CWSI values higher than 0.4, especially until before of maximum canopy cover establishment. A close relationship between Arecovery at maximum stress moment and yield reduction was found. The strong relationship between the measured traits (except PWC and stem ) and final yield at maximum stress moment found in the present study warrants further research on drought phenotyping immediately before post-restriction irrigation or when the defined severity threshold in potato is reached. © 2016 Elsevier B.V. All rights reserved.

1. Introduction

Abbreviations: An , net photosynthesis; Amax , Average maximum net photosynthesis; Arecovery , Recovery of net photosynthesis; D, duration of irrigation; DAP, days after planting; CWSI, crop water stress index; gs , stomatal conductance; gs max , maximum light-saturated stomatal conductance; IWQ, irrigated water quantity; PRI, photochemical reflectance index; PWC, plant water concentration; Tcanopy , Canopy temperature; Tdry , dry temperature (7 ◦ C over the dry bulb temperature); Twet , wet artificial reference surface temperature; VPD, vapour pressure deficit; tuber , carbon isotope discrimination in tubers; stem , stem water potential;  v , soil volumetric water content;  vT , the target  v established for each treatment. ∗ Corresponding author at: International Potato Centre (CIP), P.O. Box 1558, Lima 12, Peru. E-mail address: [email protected] (D.A. Ramírez). http://dx.doi.org/10.1016/j.agwat.2016.08.028 0378-3774/© 2016 Elsevier B.V. All rights reserved.

Potato, the fourth most important edible crop in the world (FAO, 2016) is expanding to drought prone areas affected by climate change (Monneveux et al., 2013). Because it has a high water requirement, which amounts to an estimated 3500–6500 m3 ha−1 (Sood and Singh, 2003), strategies for saving water while maintaining yields are needed. Several irrigation techniques such as deficit irrigation, partial root-zone drying and drip irrigation conserve water and increase water use efficiency with no significant yield reduction compared to conventional, water wasteful irrigation methods (Erdem et al., 2006; Liu et al., 2006; Sasani et al., 2006; Shahnazari et al., 2007, 2008; Saeed et al., 2008; Kumar et al.,

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2009; Ahmadi et al., 2010; Jensen et al., 2010; Jovanovic et al., 2010; Ati et al., 2012; Xie et al., 2012; Yactayo et al., 2013). In general, soil-based water content methods (potential evapotranspiration, pan evaporation, soil moisture or tensiometers) are used for determining irrigation schedules. However, using physiological descriptors of plant water status for a more precise definition of optimal irrigation timing has been suggested (Medici et al., 2014). Since mid-morning or maximum, light-saturated stomatal conductance (gs max ) response integrates a complex interaction between internal and external plant factors (Medrano et al., 2002), Flexas et al. (2004) postulated that this trait is a more appropriate indicator of water stress intensity than either leaf potential or relative water content. Thus, gs max values between 0.1 and 0.15 mol H2 O m−2 s−1 have been proposed as an optimum threshold at which to irrigate the crop (Flexas et al., 2004, 2006). Highly variable physiological traits have been used as indicators of plant water status for managing irrigation in potato (Byrd et al., 2014; Zakaluk and Ranjan, 2006; Zakaluk and Sri Ranjan, 2008; Rud et al., 2014) but assessing gs max for scheduling irrigation in this crop is still a pending issue. Photosynthesis recovery after an irrigation pulse is another physiological descriptor that has been proposed for monitoring water demand by the crop (Flexas et al., 2004, 2006, 2012). However, photosynthesis recovery depends on the timing, duration and intensity of water restriction before the water pulse (Xu et al., 2010). In potato, carbon isotope discrimination measured in tubers (tuber ) is an integrative trait that reflects photosynthetic carbon balance over time (Jefferies and MacKerron, 1997) and it has proven to be useful for assessing the physiological performance of potato under both well-watered and water restriction conditions (Ramírez et al., 2015a). As the relationship between gs max thresholds and the recovery of photosynthesis (Flexas et al., 2004) is not thoroughly studied, tuber is so far the most reliable indicator of physiological processes affected by water restriction and the way for maximizing potato water use efficiency. Canopy temperature (Tcanopy ), detected by proximal sensing methods has been proposed to analyse drought tolerance in potato (Stark et al., 1991; Prashar et al., 2013). On the other hand, Tcanopy based Crop Water Stress Index (CWSI) closely correlates with stomatal conductance, a key trait affected by the water status of the plant (Rud et al., 2014). The water restriction effect on potato depends on its timing, intensity and duration and their combination (Jefferies, 1995), thus severe water restriction can negatively affect tuber yield if it occurs just before or during tuber initiation (Mackerron and Jefferies, 1986; Monneveux et al., 2013) or bulking (Van Loon, 1981). In this study, the effects of the timing (water restriction starting at tuber initiation and bulking) and intensity (from well-irrigated to no watered plants) of water stress on physiological traits (gs max , stem , tuber , plant water content) commonly used to test drought effects in potato, and their relationship with indexes based on proximal sensed Tcanopy and reflectance were assessed. The study was carried out in a desert area to avoid the interfering effect of rainfall. The planted variety was UNICA, previously used to test irrigation techniques (Yactayo et al., 2013) and drought tolerance in potato (Ramírez et al., 2014, 2015a, 2015b; Rolando et al., 2015). The objectives of the study were to: i) define

a threshold value of a plant physiological trait that indicates water restriction but at a level that precludes physiological impairment and yield reduction, ii) compare the reliability of the identified physiological trait with proximal sensed indexes as indicators for monitoring plant water status, and iii) analyse photosynthesis recovery after early drought and its relationship with yield. As metabolic impairment has been observed in crops other than potato when gs max drops below 0.05 mol H2 O m−2 s−1 (Flexas et al., 2004, 2006), it is hypothesized that this value could represent a physiological threshold in potato, which if surpassed during sensitive phenological stages, no recovery of plant water status and photosynthesis will occur, leading to a subsequent tuber yield reduction. 2. Materials and methods 2.1. Study area and plant material The field trial was carried out at the “Santa Rita de Siguas” Experimental Station from September to December 2014. The station, owned by the Peruvian National Institute of Agrarian Innovation, is located in the Arequipa Region – Southern Peru (16◦ 29.6 S, 72◦ 05.7 W, 1292 m.a.s.l.)- in a desert area on the western flanks of the Andes. The area has an average yearly precipitation and monthly air temperature of 0 mm year−1 and 17.7 ± 1.4 ◦ C respectively, with maximum (27.6 ± 0.48 ◦ C) and minimum (10.0 ± 0.34 ◦ C) monthly temperatures during November and July, respectively (data for 2011–2014, from La Joya Meteorological Station, 16◦ 35 33 S, 71◦ 55 9 W). During the trial, the average air temperature, global solar radiation, relative atmospheric humidity and vapour pressure deficit (VPD) were 19.1 ± 0.16 ◦ C, 26.04 ± 0.24 MJ m−2 day−1 , 49.7 ± 1.36% and 1.14 ± 0.08 kPa respectively (data recorded with a HOBO U12 Outdoor/Industrial Model and Silicon pyranometer sensor S-LIB-M003 Model, Onset Computer Corporation, Bourne, MA, USA, see details in Table 1). The maximum hourly VPD recorded ranged between 3.3 and 4.4 kPa. The textural soil class was loamy sand (880 g kg−1 of sand and 60 g kg−1 of clay and silt) with 4.35 ± 0.17 dS m−1 , 0.65 ± 0.03%, 1.61 g cm−3 and 0.14 m3 m−3 average water electrical conductivity, soil organic matter content, soil bulk density and volumetric water content ( v ) at field capacity, respectively. The planted potato variety was UNICA (CIP code: 392797.22), a genotype adapted to the Peruvian coast drylands with resistance to virus and heat, and slightly tolerant to salinity (Gutiérrez-Rosales et al., 2007). 2.2. Experimental design A randomized complete block design, with 7 treatments repeated in 4 blocks was used. The factorial treatments included two water restriction timings (early and late) and three intensity levels (low, medium, severe) along with one fully irrigated control. Each plot (14.0 m × 3.2 m) contained 120 plants sown at a distance of 0.38 m in-row spacing and 0.80 m between rows. Plots were further sectioned into 6 sub-plots (3.2 m × 1.5 m) for sequential plant samplings throughout the season. Each sub-plot was comprised of five plants in each of four rows, for a total of 20 plants. The cen-

Table 1 Environmental conditions during the experimental period 2014. Average daily values ± standard error. VPD = Vapour pressure deficit.

Minimum Temperature (◦ C) Maximum Temperature (◦ C) Average Temperature (◦ C) Average Relative Humidity (%) Global Solar Radiation (MJ m2 d−1 ) (kPa) Average VPD Maximum VPD recorded (kPa)

September

October

November

December

11.1 ± 0.43 26.3 ± 0.77 18.7 ± 0.46 45.3 ± 3.10 23.1 ± 0.81 1.21 ± 0.09 3.59

11.5 ± 0.35 27.7 ± 0.41 19.6 ± 0.30 39.3 ± 2.11 25.8 ± 0.29 1.41 ± 0.07 4.14

10.6 ± 0.43 26.9 ± 0.28 18.8 ± 0.29 53.6 ± 2.31 27.3 ± 0.29 1.03 ± 0.06 3.27

11.5 ± 0.29 26.8 ± 0.37 19.1 ± 0.28 58.9 ± 2.02 26.8 ± 0.32 0.93 ± 0.05 3.26

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6.1 L m−1 h−1 at 0.055 MPa were placed on each side of the row (about 0.1 m away from the plants). Each block had one valve and one pressure gauge to control the operating pressure and each row within a plot had its own control valve. Each morning, soil samples were collected from each plot at the soil depth layer (0–0.3 m) where the majority (>90%) of root biomass is concentrated in UNICA variety, as shown by previous studies (Ramírez, unpublished data). Soil samples were weighed and dried in a microwave oven (CQ1570 Model, Samsung, Bangkok, Thailand) to calculate  v using the following equation: v =

 mass of soil water × b w mass of dry soil

(1)

Where bulk density (b ) was measured as 1.6 g cm−3 and water density (w ) considered as 1 g cm−3 . The duration of irrigation (D, in hours) and irrigated water quantity (IWQ, in mm) at each treatment were calculated using the following equations: D = (vT − v ) × RZd × RZw × IWQ =

Fig. 1. Average value of soil volumetric water content ( v ) measured before the irrigations (A) and irrigated water quantity (B) for each water restriction treatment. DAP = days after planting.

1 × 1000 emitter rate

emitter rate ×D RZw

(2) (3)

where RZw was root-zone width (0.35 m), RZd was root-zone depth (0.3 m),  vT was the target  v for each treatment, and 6.1 is the emitter rate in L m−1 h−1 . At hilling, a second drip tape was installed. Immediately after planting (0 DAP) an intense irrigation pulse was supplied (17 mm of IWQ) and the following days  v was monitored to estimate D and IWQ. The irrigation was scheduled to occur (Fig. 1A) when the reduction of  v was in average between −20 to −30% of  vT for each treatment (Fig. 1B). During the final period of the trial i.e. from the end of late water restriction treatments (93 DAP) until harvest (117 DAP), all plots were irrigated 5 times with 6.7 mm every 2 days. After that, there were no more irrigations until the plants reached natural maturity and were harvested. 2.4. Eco-physiological and biomass measurements

tre six plants were used for evaluations throughout the season (see below). The early water restriction started 46 days after planting (DAP), one week after tuber initiation, and finished 72 DAP when plants reached maximum canopy cover which is considered as the beginning of senescence in crops (Yin, 2013). The late water restriction started 67 DAP during the tuber bulking phase, and ended 93 DAP when the crop showed a decrease of ≈ −45% relative to maximum canopy cover (beginning of late senescence phase). During plant establishment, all plots were irrigated at the field capacity (0.14 m3 m−3  v ). However, as average values of gs max lower than 0.15 mol H2 O m−2 s−1 (which is considered a physiological threshold over which the plant is at an optimum water status; Flexas et al., 2006) were recorded, soil water status at the beginning of water restriction was adjusted to 0.20 m3 m−3  v (see Fig. 1A) for the control plots, which caused average values of gs max higher than 0.15 mol H2 O m−2 s−1 . The intensity of water restriction was based on  v targeting 0.20, 0.14, 0.10 m3 m−3 and no irrigation for the control, low, medium and severe water restriction treatments respectively. 2.3. Crop management Composted manure was applied at planting along with 100–200–100 kg ha−1 of granular N-P-K supplied by (NH4 )2 HPO4 , NH4 NO3 , and K2 SO4 . In addition, 100 kg ha−1 of N and K2 O as Urea and KCl were applied at hilling (35 DAP). The crop was irrigated via drip irrigation, beginning immediately after planting. The drip tapes with emitters spaced at 0.2 m and emitter flow rate of

Eco-physiological variables were measured from 11:00 to 13:00 h, before the biomass sampling (explained below), in an apical leaflet of a young, sun-exposed and expanded leaf at each of three target plants located at the centre of the sub-plot. Net photosynthesis (An ) and gs max were measured with a portable photosynthesis system (LI6400-TX model, LI-COR Bioscience, NE, USA). The parameters fixed in the chamber were: 1200 ␮mol m−2 s−1 of photosynthetically active radiation which is the light saturation point for the UNICA variety (Rolando et al., 2015), CO2 concentration of 400 ppm, boundary layer conductance of 9.29 mol m−2 s−1 and air flow rate of 300 ␮mol s−1 . After assessing gas exchange and canopy temperature (see below), stem water potential (stem ) was measured using a pressure chamber (80325 model, Labconco, Kansas City, MO USA). For the measurement, leaf and xylem water potentials were equilibrated by enclosing the stems in a plastic bag 1 h before the assessments, following the procedure of Byrd et al. (2014) in potato. Ecophysiological and reflectance (see 2.5 sub-section) measurements were carried out 8 times, one at 33 DAP and the other seven were taken every week, following the initiation of water restriction treatments (at 46 DAP). Biomass samples were taken every two weeks from 36 to 117 DAP for a total of six samplings. The six centre plants from each sub-plot were individually harvested and separated into leaves, stems, and tubers. Fresh tissues were weighed and then subsamples were dried at 60 ◦ C to calculate dry biomass per plant. Plant ˜ water concentration (PWC) was determined as follows (Penuelas et al., 1997): PWC = ((FW − DW ) /DW ) ∗ 100

(4)

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where FW is the fresh weight and DW is the dry weight of the whole plant. Composite dried samples from tubers corresponding to the 3rd, 4th, 5th and 6th sequential samplings were ground using a ball mill (BMIX-100 model, MRC, Holon, Israel). Using plastic gloves to avoid contamination, 2.7–3.4 mg composite samples from each sub-plot were enclosed in tin capsules and sent to University of California − Davis, Stable Isotope Facility (David, CA, USA) for 13 C analysis with a PDZ Europa ANCA-GSL elemental analyser coupled to a PDZ Europa 20-20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK). Deviation of the sample 13 C isotopic composition from the reference was reported (␦13 C) with a precision of ±0.2‰:



13

␦ C(‰) =

Rsample Rreference



−1

 (‰) =

ıatm − ısample 1 + ısample

Reflectance measurements were recorded for each target plant (three readings per plant, three plants per plot) at wavelengths from 325 to 1075 nm with a spectral sampling interval of 1 nm, using a FieldSpec FR spectroradiometer (Model FSHH 325–1075P, Analytical Spectral Devices Inc., Boulder, CO, USA). The Photochemical Reflectance Index (PRI,) was estimated as follows (Gamon et al., 1992; R stands for reflectance and the subscript number is the wavelength in nm): PRI =

× 1000

(5)

where Rsample and Rreference are the 13 C/12 C isotopic ratio in the sample and the reference Pee Dee Belemnite standard (0.011237), respectively. Discrimination against 13 C () was calculated as defined by Farquhar et al. (1989):



2.5. Proximal sensing-based indexes

 × 1000

(6)

where ␦atm, and ␦sample are the atmospheric (−8‰) and sample ␦13 C values, respectively. Tuber  (tuber ) was calculated for each subplot composite sample.

R531 − R570 R531 + R570

(7)

After gas exchange measurements, canopy temperature was gauged using an 18 mm infrared thermal camera (model FLIR B335, FLIR Systems, Sweden) equipped with an uncooled microbolometer sensor (focal plane array), sensitive in the 7.5–13 ␮m spectral range and with a resolution of 320 × 240 pixels. The infrared camera incorporates a 3.1 Mpixel built-in RGB digital camera, taking both infrared and RGB images in every shot. Image acquisition was done at a vertical distance of 3 m from each sub-plot canopy so that the three target plants and a wet artificial reference surface were captured in each image. This reference surface was similar to that described by Möller et al. (2007): an expanded polystyrene sheet floating in a 0.32 m × 0.22 m × 0.10 m plastic tray filled with water. The sheet was coated with a 2 mm water-absorbent microfiber non-

Fig. 2. Average value (±standard error) of physiological measurements: (a) maximum, light-saturated stomatal conductance (gs max ), (b) tuber carbon isotope discrimination (tuber ), (c) plant water concentration (PWC) and (d) stem water potential (stem ) for each assessed water restriction treatment along the growing season. **, * and n.s. means p < 0.01, <0.05 and >0.05 (no significant) respectively in the ANOVA analysis. DAP = days after planting.

D.A. Ramírez et al. / Agricultural Water Management 177 (2016) 369–378 Table 2 F-values of ANOVA with repeated measurements in time comparing irrigation treatments for gs, stem, PRI, CWSI, PWC and tuber . Variable s stem PRI CWSI PWC tuber

Irrigation Treatment

Time

30.2** 8.34** 30.2** 14.6** 8.57** 6.77**

34.2** 3.12** 44.3** 19.1** 128.4** 8.02**

* p < 0.05,**p < 0.01, n.s. p > 0.05. gs max = Maximum, light-saturated stomatal conductance, stem = stem water potential, PRI = Photochemical Reflectance Index, CWSI = crop water stress index, tuber = tuber carbon isotope discrimination, PWC = plant water concentration.

woven cloth, with its edges inside the water in order to replace evaporating water. Camera parameters were set up as following: thermal emissivity was set to 0.96 according to Wang et al. (1994) findings for potato leaves. Reflected apparent temperature was calculated every four images by the direct method (for detailed information see FLIR, 2011), while atmospheric temperature and relative humidity were recorded by the HOBO meteorological station installed in the field. In order to discriminate canopy from bare soil temperature, visible and thermal images alignment was done using the Image Processing Toolbox Release Notes of Matlab scripts (R2014a, MathWorks, Natick, MA, USA). Three control points represented by easily recognizable features in both images were selected by an expert. A transformation matrix was obtained using fitgeotrans functions in Matlab based on the three control points. The transformation matrix was applied to visible images for aligning it with the thermal images using imwarp function. Once aligned, crop canopy from the RGB image was thresholded in Hue, Saturation and Brightness colour spaces with an image processing software (ImageJ, version 1.48, U.S. National Institute of Health, MD, USA). A Matlab script was written to automate the extraction of canopy temperature values from the thermal image of each target plant. This script multiplied the thermal with the thresholded image allowing to draw a polygon to point out each target plant. Crop Water Stress Index (CWSI) was estimated for each target plant using the empirical method applied to potato (Jones, 1992; Rud et al., 2014) CWSI =

Tcanopy − Twet Tdry − Twet

(8)

where Tcanopy is the measured crop canopy temperature, Twet is the wet artificial reference surface measured temperature and Tdry is 7 ◦ C over the dry bulb temperature.

2.6. Photosynthesis recovery analysis The mean photosynthesis recovery (Arecovery , %) after the water pulse following the water restriction period was calculated as the ratio of the mean net photosynthesis (An ) to the average maximum net photosynthesis (Amax ) value obtained in the control (23 ␮mol CO2 m−2 s−1 ) during the trial as follows (Resco et al., 2009): Arecovery =

 A  n Amax

373

2.7. Statistical analysis The effects of irrigation treatments and time on the physiological variables were assessed by ANOVA with repeated measures over time running the PROC GLM procedure using SAS/STAT v. 8.02 software (SAS Institute Inc. USA). Simultaneous test for General Linear Hypotheses was performed to do a multiple comparison of means between early and late water restriction treatments and the control. A Spearman correlation matrix was performed using SAS/STAT v. 8.02 software (SAS Institute Inc. USA) to assess the relationship between the response variables, and functions among plant traits were fitted using a linear regression analysis. Significance of all statistical tests were assessed at p < 0.05 and p < 0.01 and satisfying the Shapiro-Wilk normality test using R v3.1.3 software (R Core Team, 2015). 3. Results 3.1. Response variables along the growing period All physiological variables responded highly significantly (p ≤ 0.01) to treatments and time (Table 2). After defining target  v for the control treatment (56 DAP), the overall averages for gs , tuber , PWC, stem , PRI and CWSI in the control were 0.21 ± 0.025 mol H2 O m−2 s−1 , 15.3 ± 0.5‰, 713 ± 27%, −0.24 ± 0.03 MPa, −0.03 ± 0.002 and 0.53 ± 0.05 respectively (Figs. 2, 3). Compared to the control, the early and late water restriction periods showed reductions in gs max that ranged between 23.3–91.1% and 0.0–92.1%, respectively. The average gs dropped below 0.05 mol H2 O m−2 s−1 in plants under the severe treatments in both periods of water restriction (Fig. 2a). During both early and late water restriction periods, the tuber average reduction in comparison with the control ranged between 3.9–20.3% and 1.1–17.7% respectively (Fig. 2b). The tuber was reduced in plants under the early severe treatment (an average of 13.1 ± 0.4‰), and did not return to the original levels when irrigation was re-established (Fig. 2b). PWC differences between the water restriction treatments and the control ranged between −3.1 to 464.7% for the early restriction period and −22.7 to 384% for the late restriction period (Fig. 2c). A progressive PWC fall in plants under early and severe stress occurred even after irrigation was re-initiated (Fig. 2c). Significant differences in stem were observed in three assessments at the early severe treatment, which showed an average reduction of 168% in comparison with the control (Fig. 2d). The reduction ranged between 15.1–170.8% and −14.4 to 167.8% for the early and late water restriction periods respectively compared to the control (Fig. 3a). The severe water restriction treatment caused a progressive decrease in PRI that, for the early water restriction, continued even after the end of the restriction period (Fig. 3a). During the early and late water restriction periods, CWSI increase compared with the control ranged between 9.8–99.3% and 7.3–77.5% respectively (Fig. 3b). The CWSI rise in plants under the early severe treatment (an average of 0.88 ± 0.03) never reverted after irrigation was re-established (Fig. 3b). No significant differences in CWSI were detected among treatments during the last assessment. 3.2. Relationship between response variables and gs max

∗ 100

(9)

As plants after the late water restriction treatment were in the late senescence stage, which has an effect on Arecovery response (Flexas et al., 2012), this variable was only assessed for early treatments during the period from 4 days before to 15 days after re-watering.

The magnitude of the correlation between measured traits and gs max had the following pattern: CWSI » PRI > tuber > PWC > stem , with positive relationships except for CWSI (Table 3). Important correlations (|rSpearman > 0.7|) were found between tuber − PWC, PRI − CWSI, PRI − tuber , and PRI − PWC. stem showed the weaker correlation with most variables (Table 3). The gs max significantly accounted for the variability of proximal sensed variables as fit-

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Fig. 3. Average value (±standard error) of proximal sensed variables: (a) Photochemical Reflectance Index (PRI) and (b) crop water stress index (CWSI) for each assessed water restriction treatment along the growing season. **, * and n.s. means p < 0.01, <0.05 and >0.05 (no significant) respectively in the ANOVA analysis. DAP = days after planting.

Table 3 Spearman correlation matrix among the assessed response variables: maximum, light-saturated stomatal conductance (gs max ), stem water potential (stem ), Photochemical Reflectance Index (PRI), crop water stress index (CWSI), tuber carbon isotope discrimination (tuber ) and plant water concentration (PWC). gs stem PRI CWSI tuber PWC ∗

max

0.45* 0.83** −0.88** 0.77** 0.76**

stem 0.47** −0.42** 0.59** 0.05

PRI −0.77** 0.83** 0.76**

CWSI −0.69** −0.67**

tuber 0.82**

p < 0.05, **p < 0.01.

ted functions between gs max − CWSI and gs max − PRI were linear (R2 = 0.76) and natural logarithm (R2 = 0.67) respectively (Fig. 4). 3.3. Yield reduction, photosynthesis recovery and yield prediction based on physiological variables The average fresh tuber yield was 705.0 ± 84.5, 573.9 ± 75.8, 327.9 ± 50.3, 240.9 ± 38.7, 211.3 ± 37.0, 205.5 ± 38.1 and 80.5 ± 21.2 g plant−1 for the control, late-low, early-low, latemedium, early-medium, late-severe and early-severe treatments, respectively. The reduction of fresh tuber yield with respect to the control caused by all water restriction treatments was significant (F-value=12.66, p < 0.01), being the late-low and early-severe the treatments that showed the lowest (32.2%) and highest (93.2%) yield reductions, respectively (Fig. 5). After the irrigation pulse the Arecovery in early treatments showed the following pattern: low restriction (72.2 ± 9.1%) > medium restriction (43.2 ± 6.8%) > severe restriction (16.5 ± 7.4%) (Fig. 6A). At the moment of maximum stress (before the irrigation pulse) the average Arecovery showed higher correspondence with tuber yield relative to the average yield of the control i.e. 36.7 ± 5.1, 26.5 ± 4.6, and 6.8 ± 2.6% for low, medium and severe early treatments, respectively (Fig. 6A). The linear response function (y = 104.0 x, R2 = 0.98, p < 0.01) fitted between gs max and An for the early restriction treatments showed that 5 and 16 ␮mol CO2 m−2 s−1 of An values corresponded to 0.05 and 0.15 mol H2 O m−2 s−1 of gs max, respectively (Fig. 6B). Tuber yield prediction based on the

Fig. 4. Fitted functions between the mean of proximal sensed variables and maximum, light-saturated stomatal conductance (gs max ) along the growing season including all the assessed treatments of water restriction. CWSI = Crop Water Stress Index, PRI = Photochemical Reflectance Index.

linear relationship of yield with the assessed responses variables at the moment of maximum stress showed the following pattern of R2 : tuber > gs max > CWSI > PRI > PWC > stem (Table 4), and

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Table 4 Dry tuber yield (y) prediction based on its linear relationship with the plant traits (x) of each assessed treatment before the irrigation finishing the water restriction period at maximum stress moment. Where “a” and “b” are the intercept and slope of the linear function (y = a+bx) and R2 is the determination coefficient. See caption of Table 2 to define each trait’s abbreviation. Trait (x)

a

b

R2

tuber gs max CWSI PRI PWC stem

−26.2 0.06 8.02 6.86 −1.84 3.91

2.00 25.5 −7.78 90.0 0.007 5.46

0.97** 0.95** 0.92** 0.63* 0.42 n.s. 0.33 n.s.

n.s. p > 0.05. * p < 0.05. ** p < 0.01.

the relationship with PWC and stem were the only ones not significant. 4. Discussion 4.1. Severity threshold under water restriction signalling physiological impairment and yield reduction in potato After the irrigation pulse, lack of recovery (gs max , tuber , stem and CWSI) and continued reduction (PWC and PRI) of the values of some physiological traits were observed in plants under severe water restriction during early developmental stages. Interestingly, these plants reduced their average gs max below 0.05 mol H2 O m−2 s−1 which correspond to values < 5 ␮mol CO2 m−2 s−1 of An (Figs. 2, 6 B), value recognized as a “severity threshold” beyond which a metabolic impairment affecting photochemical and biochemical components of photosynthesis occurs (Flexas et al., 2004, 2006). As reported by Monneveux et al. (2013), yield reduction in potato caused by severe water restriction is larger when the stress occurred at early rather than at later phenological stages (Fig. 3). Flexas et al. (2006, 2012) pointed out that the consequences of surpassing the severity threshold depends on the acclimation capacity and light intensity. Plant acclimation during early growth stages in the variety UNICA has been observed (Yactayo et al., 2013). However, the results in this study suggest that prolonged exposure below this severity threshold disrupted the acclimation capability. Since a positive correlation between tuber yield and root biomass has been reported in potato (Iwama, 2008; Wishart et al., 2013), it is hypothesized that the low and persistent PWC of plants submitted to early severe water restriction was caused by a low water absorption capacity driven by a likely reduced root system. Low tuber values have been associated with high maintenance respiration rates that support water stress tolerance mechanisms in potato (Ramírez et al., 2015a). This argument is supported by the findings of this study in which tuber reduction occurred in periods of water stress with subsequent recovery after the water pulse in the low and medium water restriction treatments (Fig. 2b). The lack of tuber recovery after the water stress period in the early severe treatment suggests a continuous energy supply from tubers to repair severe damage likely caused by oxidative stress which occurs when gs max falls below the severity threshold (Flexas et al., 2006). Under the early severe water restriction, the average tuber value (13.4‰) was lower than the average values of 16.7 and 14.9‰ reported for UNICA variety by Ramírez et al. (2015a; b). On the other hand, the average tuber (15.2‰) and dry biomass per plant (118 g plant−1 , data not shown) found in the control treatment were similar to those reported by Ramírez et al. (2015b; 15.2 ± 0.2‰ and 81.2 ± 2.45 g plant−1 respectively) under mild water restriction a result that suggests that plants in the control treatment were not in optimum physiological status. We inferred three likely factors

Fig. 5. Average percentage of reduction for fresh tuber yield in relation with the average control plots obtained by each treatment. Different letters means significant differences in ANOVA at p < 0.05.

affecting physiological performance of control plants: i) Although UNICA has been described as slightly salt tolerant (GutiérrezRosales et al., 2007) and osmotic adjustments mechanisms has been reported in this variety (Yactayo et al., 2013), the relative high water electrical conductivity (>4 dS m−1 ) in soil indicates potentially salt effects. ii) Plants were irrigated based on field capacity until the beginning of water restriction, however plants showed gs max lower than the recommended threshold for crop irrigation (0.15 mol H2 O m−2 s−1 ; see Fig. 2a) which means that plants could have been at sub-optimum physiological condition before tuber initiation onset. It has been shown that water restriction before tuber initiation reduces final tuber number which is closely related with final tuber yield (Mackerron and Jefferies, 1986; Mackerron et al., 1988; Jefferies and Mackerron, 1987). iii) Although the irrigation scheduling was defined by a soil moisture level slightly higher than field capacity, water retention in coarse-textured sandy soils does not adequately meet the evapotranspiration demand by the potato crop (Van Loon, 1981). The foregoing arguments point out to the inadequacy of soil-based methods to define good watering conditions for plants (Jones, 2004) and the convenience of using a plant-based descriptor like gs max for characterizing the water status of the plant-soil system, particularly in sandy soils. The gs max as a water status descriptor also allows comparisons with other studies assessing water restriction; for instance, Rolando et al. (2015) reported a 64.2% reduction of fresh yield in a water stress treatment, similar to the early medium water restriction treatment in this study (Fig. 5). Interestingly, the gs max average (≈0.09 mol H2 O m−2 s−1 ) was also similar in both cases of yield reduction. 4.2. Proximal sensed plant attributes as proxies of physiological indicators of water status in potato Stomatal closure in potato occurs well before any noticeable change in leaf water potential or content (Van Loon, 1981; Wilcox and Ashley, 1982; Martinez and Moreno, 1992; Tourneux et al., 2003; Liu et al., 2005), likely leading to yield reductions due to mild water stress. Maximum, light-saturated stomatal conductance indicates physiological performance related to water status, and is considered as a more pertinent trait than leaf water potential and content to define irrigation schedules (Medrano et al., 2002; Flexas et al., 2004, 2006, 2012). This assumption is supported by this study, as gs max was the first variable showing significant responses to water restriction (Fig. 2). However, some confounding factors affect

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under mild stress varied between 0.30 and 0.67 in soybean (Glycine max L.) and between 0.38 and 0.46 in cotton (Gossypium hirsutum L.), depending on the variety and weather conditions. Because its high correlation with gs max , in potato, we strongly suggest the use of CWSI as an indicator for defining irrigation schedules, stressing the importance of preventing values (mainly during the maturity phase) higher than 0.7 which corresponds with gs max values close to the severity threshold (0.05 mol H2 O m−2 s−1 , Fig. 4). In our study, CWSI values lower than 0.6 corresponded to gs max values higher than 0.15 mol H2 O m−2 s−1 (which in turn corresponds to values >15.6 ␮mol CO2 m−2 s−1 of An , Fig. 6B), which has been identified as the signal for opportune irrigation in crops other than potatoes (Flexas et al., 2004, 2006). As other measurements of CWSI in potato, using the empirical method for Twet calculation, found that 0.15 mol H2 O m−2 s−1 of gs max corresponds to values between 0.4–0.6 approximately (Rud et al., 2014), 0.4 of CWSI could be conservatively considered a threshold for irrigation of a potato crop. However, more research is required to adjust the suggested threshold to CWSI measured in other potato cropping areas where diffuse light caused by clouds could be dominant (see for example Jones, 1999). Concurrently with the effect of N stress in potato (Jemberu, 2013), PRI at canopy level showed a high sensitivity to water restriction (Fig. 4). A close correlation between PRI and canopy temperature-based index (RSpearman = −0.77, p < 0.01; data not shown) was found in this study, in agreement with results reported by Suárez et al. (2008). The close positive relationship between PRI and gs max (Fig. 4) indicates the relationship between the photochemical and diffusive components of photosynthesis. Because PRI has been associated with some photosynthesis photochemical processes (non-photochemical quenching, xanthophyll cycle and photochemical efficiency of Photosystem II; see Garbulsky et al., 2011), it would be useful to compare canopy indicators related to photosystem II status against canopy temperature, for early stress detection in potato. Fig. 6. (A) Mean photosynthesis recovery (Arecovery ) after the early water restriction period and final tuber yield in relation to the control at harvest (TYC). (B) Relationship between average maximum, light-saturated stomatal conductance (gs max ) and net photosynthesis (An ) in early water restriction treatments. White, gray and black symbols and bars correspond to low, medium and severe intensity of water restriction.

the value of this trait as a good indicator for irrigation monitoring, in particular its high intra-plant and intra-population variability due to differences in leaf senescence and exposition, and the long time required to measure it in the field (see Jones, 2004). The close relationship found between gs max on the one hand and PRI and CWSI on the other (Fig. 4) suggests that the last two are appropriate for estimating water status in potato plants. Particularly, the high correlation of CWSI with gs observed also in other work with potato (Rud et al., 2014) is consistent with the hypothesis that canopy temperature variation caused by plant water exchange is a crucial variable to discriminate potato drought tolerant materials (Stark et al., 1991; Prashar et al., 2013). The higher CWSI values (≈0.4, see Fig. 3b) in our control plants compared with the values observed by Rud et al. (2014) in well irrigated potato (CWSI < 0.2) means that this index was able to detect the sub-optimum physiological performance of our control plants as discussed in the 4.1 sub-section. In order to obtain high yields, stomata closure must be continuously avoided through opportune irrigation of the crop. Nevertheless, the relation between CWSI values and yield loss under water stress varies between species and environmental conditions. In drip-irrigated broccoli (Brassica oleracea L. var. italica) in Turkey, CWSI values above 0.39 resulted in decreased yields (Erdem et al., 2010). On the other hand, O’shaughnessy et al. (2011) conducted a sprinkler irrigation trial and showed that CWSI

4.3. Photosynthesis recovery analysis for physiological assessments in water restriction trials As reported by Xu et al. (2010), the level of Arecovery following the post-restriction irrigation pulse depends on the intensity and duration of the stress, which determine a complete or partial compensatory recovery. In potato, Van Loon (1981) reported a full Arecovery after three days of re-watering permanently wilted plants. This result concurs with Vos and Groenwold’s (1989) study, who found that Arecovery under 50% deficit irrigation was complete in a short time, even after 30 days of water restriction. Watkinson et al. (2006) reported a high genetic variability in Arecovery in four open-pollinated Solanum tuberosum ssp. Andigena varieties after re-watering them once photosynthesis rates dropped to 1 ± 1 ␮mol CO2 m−2 s−1 . Post-stress photosynthesis rate ranged from complete recovery to no recovery at all. In the severe water restricted conditions of the present experiment, the low Arecovery 15 days after the post-restriction irrigation pulse (<30%, Fig. 6A) in plants showing gs max values below the severe threshold during the early stages of water restriction, supports the hypothesis of metabolism impairment (Flexas et al., 2006; 2012). The Arecovery analysis could consequently help in defining the most appropriate irrigation timing for subsequent crops in conditions of water restriction. It could also be useful for defining when well-irrigated plants should be watered for maintaining an optimum photosynthetic activity and sustain high yield (see Medici et al., 2014). Finally, based on Arecovery analysis and its relationship with yield reduction (Fig. 6A and Table 4), this study pointed out the moment of maximum stress

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as the most appropriate for carrying out the characterization of physiological traits during the study of drought effects in potato. 5. Conclusion Maximum, light-saturated stomatal conductance is the most pertinent physiological trait to characterize water status in potato for defining appropriate irrigation schedules for this crop. During early stages of plant development, values of gs max lower than 0.05 mol H2 O m−2 s−1 led to severe impairments in the photosynthetic apparatus (diffusive and biochemical photosynthetic processes) and reduced water absorption, photosynthesis recovery and yield. This study showed the convenience of using plantbased instead of soil-based methods to define water status in the plant-soil system in coarse-textured sandy soils. CWSI, based on canopy temperature, is useful for defining physiological thresholds at canopy level and for detecting early water stress in cloudless dry environments with low diffuse radiation, as was the case of our study area. In this sort of environment, irrigation schedule in potato should aim at avoiding CWSI values higher than 0.4, especially until before of maximum cover establishment. However, other canopy traits related to photosynthesis biochemistry, like chlorophyll fluorescence, must be further investigated to test the hypothesis that biochemical factors react faster than the diffusive factors of photosynthesis that determine canopy temperature. Finally, the moment of maximum stress was identified as the most appropriate time to carry out physiological assessments in potato. It occurred right before the irrigation pulses in the case of intermittent water restriction or when gs max is close to 0.05 mol H2 O m−2 s−1 or 5 ␮mol CO2 m−2 s−1 of An in other drought situations. Acknowledgement This research was conducted under the CGIAR Research Programs (CRP) on Climate Change, Agriculture and Food Security (CCAFS), Root, Tuber and Bananas (RTB) and Dryland Systems, and the bilateral projects: – BMZ/GIZ “Improved potato genotypes and water management technologies to enhance water use efficiency, resilience, cost-effectiveness, and productivity of smallholder farms in stress-prone Central Asian environments”, – PNIA-N◦ : 016-2015-INIA-PNIA/UPMSI/IE “Uso efectivo del agua en el cultivo de papa en zonas áridas: Mejorando el manejo del riego mediante el monitoreo del estatus hídrico para enfrentar al Cambio Climático”. The authors gratefully acknowledge research fellowship for Libby R. Rens and research grants from the U.S. Borlaug Fellow in Global Food Security Program (Grant No. 206766) and the University of Florida Horticultural Sciences Department. Authors thank Eng. Javier Ramos and Eng. Valeriano Huanco from INIA-Arequipa for giving us all the facilities to work in “Santa Rita de Siguas” Experimental Station, and Gaby Savina, Nikolai Alarcón, Jesús Zamalloa and Luis Silva for their assistance in field assessments. References Ahmadi, S.H., Andersen, M.N., Plauborg, F., Poulsen, R.T., Jensen, C.R., Sepaskhah, A.R., Hansen, S., 2010. Effects of irrigation strategies and soils on field-grown potatoes: gas exchange and xylem (ABA). Agric. Water Manag. 97, 1923–1930. Ati, A.S., Iyada, A.D., Najim, S.M., 2012. Water use efficiency of potato (Solanum tuberosum L.) under different irrigation methods and potassium fertilizer rates. Ann. Agric. Sci. 57 (2), 99–103. Byrd, S.A., Rowland, D.L., Bennett, J., Zotarelli, L., Wright, D., Alva, A., Nordgaard, J., 2014. Reductions in a commercial potato irrigation schedule during tuber bulking in Florida: physiological, yield, and quality effects. J. Crop Improv. 28, 660–679. Erdem, T., Erdem, Y., Orta, H., Okurso, H., 2006. Water-yield relationships of potato under different irrigation methods and regimens. Sci. Agric. 63 (3), 226–231.

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