Short Communication Environ. Control Biol., 51 (4), 215
220, 2013 DOI: 10.2525/ecb.51.215 Use of Air Circulation to Reduce Wet Leaves under High Humidity Conditions

1 1 2 1 Takeshi KUROYANAGI , Hisashi YOSHIKOSHI , Takafumi KINOSHITA and Hiroki KAWASHIMA

1 NARO Western Region Agricultural Research Center, Zentsuji, Kagawa 765
0053, Japan 2 NARO Tohoku Agricultural Research Center, Morioka, Iwate 020
0123, Japan

(Received August 16, 2013; Accepted November 21, 2013)

The wetting of plants due to guttation (i.e., drops of xylem sap that exude onto the leaves) represents a potential risk for incidence and outbreak of pathogens. Here, we investigated the effect of air circulation on guttation of tomato leaves under dark and high humidity conditions. The tomato plants were grown in a container and pinched above the second truss and were then separately placed in a darkened and constantly humidified growth cabinet that was exposed to three levels of air circulation intensity (air velocities of 0.05 m s1, 0.16 m s1, and 0.29 m s1). The evaporation rate increased in direct proportion to air velocity around the plants regardless of differences in leaf area. The guttation rate varied with leaf area; specially, tomato plants with small leaf areas secreted larger amounts of guttation water than those with large leaf areas. However, guttation was completely suppressed in both large and small leaves under well-circulated conditions (i.e., a veloc- ity of 0.3 m s1). This study indicates that air circulation reduces the wetting of plants by guttation under dark and high humidity conditions, which is likely to suppress the secondary spread of pathogens. Keywords : circulator, greenhouse, guttation, tomato, transpiration, wetting

commercial-like greenhouse conditions, the secondary INTRODUCTION spread of C. michiganensis subsp. michiganensis is caused by workers touching the guttation droplets exuded from in- The wetting of plants is regarded as an undesirable oculated source plants. In comparison, once the guttation condition in greenhouses because of an increased risk of droplets have dried, spread does not occur by touching in- fungal and bacterial-incited diseases (Csizinszky et al., oculated plants (Sharabani et al., 2013). Tomato mosaic 2005). Droplets form on plants as a result of 3 factors as- virus (ToMV) and pepper mild mottle virus (PMMV) have sociated with the high humidity of greenhouses: (1) con- also been identified in the guttation water of infected to- densation falling from greenhouse covers; (2) condensation mato and green pepper plants, with the concentrations of on the leaf or fruit surface; and (3) guttation, which is the the virus particles being sufficient to lead to the infection of exudation of drops of xylem sap due to root pressure. The healthy plants (French et al., 1993). Since hydathodes presence of water on plants is often unavoidable in green- serve as efficient infection routes via guttation, the imple- houses. mentation of certain greenhouse air conditions that inhibit Among growers, guttation is widely believed to be a guttation might prevent the secondary spread of critical sign of plants having good root spread. Depending on plant pathogens. species and weather conditions, guttation on a plant may be Water droplets on leaf margins due to guttation are comparable to condensation on the leaves (Hughes and brought through the intercellular spaces of the leaf, called Brimblecombe, 1994), with this phenomenon being fre- the epithem, which results in these droplets being in con- quently observed under greenhouse conditions tinuous contact with the water in the vascular system (Joachimsmeier et al., 2011). Since guttation water is de- (Wilkinson, 1979). This channel through the leaf becomes rived from xylem sap through hydathodes (the structure active in darkness, when almost all the stomata close. through which water exudation occurs), it has a similar Guttation might be effectively suppressed by dehumidify- composition to the exudates that flow from the root to the ing greenhouse air and increasing transpiration rates. shoot in healthy plants (such as tomato and cucumber), and However, dehumidification is not unavailable for more than contains various minerals, such as P, K, Ca, and Mg half of the greenhouses in Japan, which are not equipped (Masuda, 1989). However, the appearance of droplet with dehumidifiers or heaters. Therefore, circulating air through hydathodes is regarded as a major invasion route of around the leaves, which decreases the thickness of leaf pathogens into host plants (Huang, 1986). For example, boundary layer (Yabuki and Harazono, 1978), might pro- Clavibacter michiganensis subsp. michiganensis, which vide an alternative means of increasing transpiration. causes bacterial canker in tomato plants, is transported into The present study aimed to examine methods to sup- the leaves via guttation droplets containing bacteria, and press the appearance of droplets on leaves by circulating air causes marginal necrosis (Carlton et al., 1998). Under the around plants. Guttation was provoked by placing individ-

Corresponding author : Takeshi Kuroyanagi, fax: 81
877
62
1130, e-mail : [email protected]

Vol. 51, No. 4 (2013)

 T. KUROYANAGI ET AL.

ual tomato plants in a closed growth cabinet under constant and the chamber was taken under conditions being passive. dark and high humidity conditions. A stable temperature The fluorescent lamps in the chamber were not used during was produced in the cabinet and root zone, with three dif- the experiments. ferent air circulation intensities being created in the cabinet Measurement by adjusting the number of active fans attached to the floor Eight tomato plants were used in the experiments, of and the ceiling. The transpiration rate was monitored auto- which 4 were grown in 2011 and the other 4 were grown in matically, whereas the amount of droplets on the leaf mar- 2012. The experiments were conducted from November 8 gins was manually collected after subjecting plants to each to 18 in 2011, and from December 4, 2012 to January 11, air circulation level. Based on the findings of this study, 2013. The leaf area and fresh weight of the fruits of all the mechanism of transpiration under dark and high humid- plants were measured destructively after the experiments. ity conditions, along with the relationship between plant Individual plants were exposed to the three-level air characteristics and guttation, were considered towards im- circulation intensity: “No” (no fan running), “Low” (1 fan proving greenhouse management protocol. running on the ceiling), and “High” (all 8 fans running). Plants were subjected to each air circulation intensity for 1, MATERIALS AND METHODS 3, 6, and 15 h, to examine the effect of the exposure time on the magnitude of guttation and transpiration. One plant Plant and experimental system was subjected to 3 to 11 treatments, consisting of a combi- Non-grafted tomato (Solanum lycopersicum) cultivars nation of the air circulation intensity and the exposure time. (Reiyo, Sakata Seed Corporation, Kanagawa, Japan), which Between treatments, plants were rested for an interval of 1 was at the fruit developmental stage after being pinched h and more, during which time the cabinet and the chamber above second fruit truss, were used for the experiments. were not saturated with water vapor. Water with the same The individual seedlings were transplanted on September temperature to the room was supplied to the substrate be- 20, 2011, and October 5, 2012, into plastic containers with fore each treatment until drainage was observed at the bot- bars to support the stems and a rockwool substrate (200 tom of the container. Evaporation from the substrate was mm
200 mm
75 mm). The tomato plants were grown in prevented by the presence of a plastic board and a thin plas- an unheated greenhouse located at Kagawa, Japan (34.1°N, tic film. The droplets that formed on leaves as a result of 133.5°E), until use in the experiments. A mixture of guttation were collected by a researcher using about 15 Otsuka House No. 1 and No. 2 nutrient solutions (Otsuka pieces of cotton (66 mm
50 mm
2 mm) per treatment. Chemical Co., Ltd., Osaka, Japan) adjusted to 0.6 to 1.6 dS Droplets on the floor of the upper compartment were also m1 was supplied to the plants. 4-Chlorophenoxy acetate collected, as they were also regarded as guttation droplets. (Tomato Tone, ISK Biosciences K. K., Tokyo, Japan) was Droplets were collected from the chamber within 1 h, while sprayed onto young flowers to promote fruit set. The humidification lasted. The amount of the droplets on each leaves of the plants were not pruned; however, the fruit was leaf was derived from the difference of weight on each pruned to retain less than 5 fruits per truss. Apical and lat- piece of cotton before and after collection, using an electric eral buds were removed at least 1 week before the onset of balance (Adventurer Pro AV4102CU, Ohaus Corporation, each experiment. NJ, USA; repeatability 0.01 g). Moisture absorption of the A growth cabinet (680 mm
680 mm
1990 mm) in a cotton was negligible, as the cotton did not increase weight thermostatic chamber (MBCR-C5040, Sanyo Electric Co., after being left for 1 h in the humidified chamber. Ltd.; 2600 mm
3250 mm
2200 mm) was used to pro- The arrangement of measurement devices in the cabi- vide the three-level air circulation conditions under dark net is presented as a schematic in Fig. 1. The transpiration and high humidity conditions. The cabinet was composed rate of individual plants was measured using an electric of transparent PVC rigid plates which were sealed with balance (XP8002S, Mettler-Toledo International Inc., transparent adhesive tape. A perforated PVC rigid plate Greifensee, Switzerland; repeatability 0.008 g) placed in separated the cabinet into an upper and lower compartment. the upper compartment of the cabinet. The weight of the For air circulation, the upper compartment was equipped plant and container was recorded every minute on a PC via with 8 axial fans (ASEN 60511, Panasonic Corporation; software (Balance Link, Mettler-Toledo International Inc., 0.26 m3 min1); 4 of the fans were attached to the ceiling to Greifensee, Switzerland). Air temperature and relative hu- generate downward airflow and 4 were attached to the floor midity in the upper and lower compartments of the cabinet to generate upward airflow. Each fan could be operated were measured via probes containing a platinum resistance separately. A humidifier (HD-RX 509, Dainichi Co., Ltd., thermometer and capacitance sensor, respectively (2119A, Niigata, Japan) was placed in the lower compartment. In Eto Denki Co., Tokyo, Japan). Air velocities in the cabinet addition, a humidifier (HD-RX 512, Dainichi Co., Ltd., were measured by 4 omnidirectional hot-wire anemometers Niigata, Japan) was placed in the chamber, which had the (Climomaster 6533, Kanomax Japan, Inc., Osaka, Japan) same capacity as the one placed in the cabinet. The hy- attached to the walls of the cabinet. Leaf temperatures grometers of both humidifiers were exposed at all times to were measured by 2 radiation thermometers (FT-H30 and air that had been dried by a pack of silica gel (sodium sili- FT-55A, Keyence Corp., Osaka, Japan) which were cali- cate) for continuous operation. Saturated vapor pressure brated in advance by comparing them against the tempera- condition in the cabinet could be maintained more than 15 ture measured on a black metal board surface using a

h. Air temperature and CO2 concentration in the cabinet thermocouple. The emissions of the radiation

 Environ. Control Biol. AIR CIRCULATION REDUCES WET LEAVES

following equations (Campbell and Norman, 1998):

f(pl
pa) E
(1) rlrb 1 rl
(2) 1/rs1/rc where E is the transpiration rate (kg m
2 s
1), f is a function

converting water vapor pressure to absolute humidity, pl

and pa is water vapor pressure in stomata and air (Pa), rb,

rc, rl, and rs represent the leaf boundary layer resistance, cuticula diffusive resistance, total leaf resistance, and stomatal resistance (s m
1). The leaf boundary layer resis- tance of single leaves for a mixed convection regime in a greenhouse is represented by (Stanghellini and de Jong, 1995):

0.5
1174d rb 2 0.25 (3) (dTl
Ta207u )

where d is the leaf dimension (m), Ta and Tl are the tem- peratures of the air and leaf (K), respectively, and u is the air velocity (m s
1).

RESULTS AND DISCUSSION

Plant materials The plants had different characteristics in the 2011 and 2012 crops (Table 1). The plants in 2011 had significantly smaller leaf area compared to those in 2012 (P0.001). This difference in leaf area was attributed to both the growth period and the amount and concentration of nutrient solution provided to the plants, which was determined manually. The number of fruits in 2011 was significantly smaller compared to 2012 (P0.01) because a half and Fig. 1 Schematic of the growth cabinet equipped with the more flowers of the subjects in 2011 did not reach fruiting measurement devices. *1 denotes the fan which ran for stage. the treatment of “Low” air circulation intensity. Air and root zone environment in the cabinet Air velocity in the upper compartment of the cabinet thermometers were fixed at 0.95. The temperature of the was kept stable, except when all fans were active (Tables 2 rockwool slab at a depth of 0.02 m from the surface was and 3). Air velocity in the “High” setting was fluctuated measured and recorded every minute using a thermistor and it was assumed to result from interference caused by temperature sensor (RTR-52A, T&D Corp., Nagano, the airflow of each fan, with the upper compartment possi- Japan). A data logger (Cadac 21, Eto Denki Co.) recorded bly being in a continually turbulent state. However, the air the air temperature, relative humidity, air velocity and leaf circulation intensity in each treatment was significantly dif- temperature every minute. ferent because the fluctuation was small. Air movement In addition to the measurement of guttation, air veloc- was also observed when none of fans were operational. ity was measured at 27 points in the cabinet in the absence This phenomenon was attributed to the underlying airflow of plants, with the points being evenly distributed over the in the lower compartment, generated by the continuous upper compartment. Three omnidirectional hot-wire ane- moisture supply from the humidifier. As shown in Tables mometers (Climomaster 6533, Kanomax Japan, Inc., 2 and 3, the effect the presence of the plant on the air circu- Osaka, Japan) were attached vertically to a 900-mm-stick. lation intensity was negligible, supposing that the protocol The stick was moved from place to place in 9 points on the of the airflow measurement for Tables 2 and 3 were differ- floor of the upper compartment. The air velocity profile of ent from each other. This would be explained by the ex- the “High” and “Low” air circulation treatments in the ab- perimental condition that a plant was placed in the sence of plants was recorded on a data logger (Thermic continually turbulent state resulted from the combination of 2300A, Eto Denki Co., Ltd., Tokyo, Japan) for 1 min at 0.2 small fans. sec intervals. The air temperature, leaf to air vapor pressure deficit Mathematical form of water vapor transport from a (VPD), and root zone temperature in the upper compart- leaf ment of the cabinet were kept in a semi-constant even for The transpiration rate of a leaf is estimated by the 15 h, and were hardly affected by the air circulation

Vol. 51, No. 4 (2013) 
 T. KUROYANAGI ET AL.

Table 1 Leaf area, fruit number per plant, and fruit fresh weight (FW) of the plant material used for the ex- periments in 2011 and 2012. Year Leaf area (m2 plant
1) Fruit number (plant
1) Fruit FW (g fruit
1) 2011 0.190.01 3.01.4 17.311.8 2012 0.640.13 7.51.0 59.141.8 *** ** N.S. Means  standard deviation (n4). Double and triple asterisks indicate a significant difference at P 0.01, P 0.001, respectively, using Welch’s t test.

Table 2 Mean air velocity and hygrothermal environment in the cabinet during the experiments.

Root zone temperature Circulation intensity Air velocity (m s 1) Air temperature (°C) Leaf to air VPD (kPa) (°C) 2011 No 0.050.01 a 20.51.2 a 0.030.01 a 20.90.9 a Low 0.160.01 b 20.80.7 a 0.030.00 a 20.31.2 a High 0.29 22.8 0.06 22.1 2012 No 0.050.01 a 19.61.1 a 0.030.01 ab 20.01.5 a Low 0.160.02 b 20.30.8 a 0.020.01 a 19.51.5 a High 0.340.03 c 21.31.2 a 0.050.02 b 19.91.9 a Circulation intensities of “No”, “Low”, and “High” represent 0, 1, and 8 active fans, respectively. Meansstandard deviation with different letters in each column were significantly different (P 0.05) based on Welch’s t test in the 2011 experiment, and the Tukey-Kramer test in the 2012 experiment. VPD is an abbreviation for vapor pressure deficit.

Table 3 Frequency of guttation under different air circulation conditions.

Guttation observations / Sample number Circulation intensity Air velocity (m s 1) 2011 2012 No 9/9 10/16 Low 0.150.07 a 8 / 9 10 / 16 High 0.310.07b 0/1 0/4 Circulation intensities of “No”, “Low”, and “High” represent 0, 1, and 8 active fans, respectively. Air velocity was mean  standard deviation, which was measured at 27 points in the upper compartment of the growth cabinet containing no plant. Different letters in the column of air velocity are significantly different (P 0.05) based on Welch’s t test.

intensity under the continuous operation of the humidifier. (Table 2), the difference in transpiration among “No”, The change of the air temperature, leaf to air VPD, and root “Low”, and “High” was attributed to an increase in air cir- zone temperature during 15-h-treatments in 2012 experi- culation. However, our observations conflicted with two ment were within 1.1°C, 0.03 kPa, 1.2°C, respectively. established principles. First, saturated water vapor pressure The air temperature decreased slowly when the fans were conditions prevent the gasification of water. In the present not operational, which was caused by heat loss to outside of experiments, it was unclear why transpiration occurred the chamber; however, the activation of all fans minimally under semi-saturated water vapor pressure. It is possible increased the air temperature in the cabinet. The leaf to air that condensation on the door of the chamber might have VPD was low but not zero, because the leaf temperature driven water vapor transfer from the plant, through leakage was slightly higher compared to the air around the leaves. from the cabinet. Despite the continuous supply of water The hygrothermal environment in the upper compartment vapor by the humidifiers, transpiration might have partly of the cabinet fell within a similar range for all treatments, compensated for the decrease in water vapor in the cham- except for air velocity in all treatments and the leaf to air ber, especially in the air-circulated treatments. Regarding VPD in the 2012 experiment (Table 2). sinks of water vapor, such as condensation or leakage in ac- Transpiration tual greenhouses, we suggest that air circulation might pro- Plant transpiration lasted stably under dark and high mote the transpiration or evaporation of droplets on leaves, humidity conditions even for 15-h-treatments. The aver- even under semi-saturated water vapor pressure conditions. aged transpiration rate of “No”, “Low”, and “High” condi- The second confliction was that most stomata close in tions during 15-h-treatments were 0.35 g m
2 h
1 ,1.88 the dark, with transpiration rates declining to almost zero. gm
2 h
1, and 6.24 g m
2 h
1, respectively, which were Although stomata closure considerably decreases transpira- considerably lower compared to that observed under light tion, water vapor is able to transfer from the inner tissue of and unsaturated water vapor pressure conditions (209
308 a leaf to the ambient air through the cuticle and partially
2
1 gm h for C3 plants, Hasegawa, 1977). Under “Low” opened stomata (Bakker, 1991). Yet, a previous publica- and “High” conditions, the transpiration rate was 5.3 times tion found that the total leaf resistance of tomato in the dark
1 and 17.8 times higher, respectively, compared to the “No” period (rl was about 225 s m , Bakker, 1991), which may condition. also be interpreted as cuticula diffusive resistance, was sev- Regarding the similar conditions of leaf to air VPD eral times larger compared to the leaf boundary layer

 Environ. Control Biol. AIR CIRCULATION REDUCES WET LEAVES

Fig. 2 Leaflet with guttation droplets associated with hydathodes at 15 h after “No” air circulation in the 2012 experiments.

resistance, when calculated using Eq. 3 in the present ex-
1 periments (rb ranged from 26 to 77 s m , assuming a leaf dimension of 0.04 m in a unidirectional airflow). Thus, the total leaf resistance was dominant in the coupled resistance (calculated from Eq. 1) in the present experiments. This es- timate indicates that Eq. 1 could not explain the 18-fold in- crease in transpiration due to the decrease in the leaf boundary layer resistance by air circulation. The difference Fig. 3 Mean transpiration and guttation rate per leaf area of in transpiration between “Low” and “High” might be ex- tomato plants in the 2011 experiments, A; and the 2012 plained in part, by the observed increase in leaf to air VPD experiments, B. For the “No” and “Low” air circulation (Table 2). In addition, it is possible that the guttation water conditions, the respective data represented the mean of on the leaf margins evaporated through the hydathodes. 9 or 16 replications in 2011 and 2012, respectively. For However, the measurement system of the present study was the “High” air circulation condition, 1 observation was made in the 2011 experiments, and 4 in the 2012 ex- not enough to elucidate this mechanism. Further studies periments. Symbols with different letters were signifi- about water movement in the leaf and the variation of the cantly different (P0.05) based on Welch’s t test in leaf boundary layer resistance of leaves in complex airflow the 2011 experiments, and based on the Tukey-Kramer are required to clarify the route of water transfer from the test in the 2012 experiments. Error bars, which indicate the standard deviations, were only assigned to plots plant under dark conditions in relation to air circulation. with the same number of observations in each experi- Guttation ment. Guttation was observed in most plants under the “No” and “Low” air circulation conditions, whereas it was not observed under “High” air circulation conditions (Table 3, leaf area and fruit number, caused the observed difference Fig. 2). The guttation rate was inversely proportional to the between the 2 study years (Table 1). The fruit of a tomato evaporation rate (Fig. 3). Despite difference in the re- plant uptakes xylem water in the dark, and has a sufficient corded guttation rates between 2011 and 2012, air circula- water potential gradient for water accumulation, regardless tion with an air velocity of 0.3 m s
1 or more suppressed of fruit transpiration rates (Ehret and Ho, 1986). In addi- the appearance of dewdrops on the leaf margins (Table 3). tion, more hydathodes would have been present on the leaf The magnitude of guttation was 20 times greater in the margins of plants in 2012 compared to 2011, due to the 2011 experiments compared to the 2012 experiments under leaveshavingalargerleafareain2012(Table1). “No” air circulation conditions. The magnitude of Although the fresh weight of the terrestrial part of a plant, guttation might have been affected by a combination of hu- which reflects the root mass and respiratory activity, has a midity around plants and root zone temperature, because close positive correlation to the magnitude of exudation, this phenomenon is driven by the development of root pres- the increment of the exudation rate with weight is barely

sure in the same way of exudation (Grossenbacher, 1939; observed under normal CO2 environmental conditions Hughes and Brimblecombe, 1994; Taiz and Zeiger, 2010). (Nakano et al., 2013). Thus, the positive effect of plant However, the air temperature, leaf to air VPD, and root weight on guttation would have been negligible in the cur- zone temperature in the cabinet had a similar range be- rent experiments, even though the weight of individual tween the 2011 and 2012 experiments (Table 2). The auto- plants in 2012 was probably larger compared to 2011. We nomic cycle of root pressure, which is initiated by light and hypothesize that an increase in the leaf area and fruit num- decapitation (Grossenbacher, 1939), was also negligible, ber would cause a greater dispersal of xylem water flow due to the identical protocol in the experiments. Therefore, into each organ, thus reducing the appearance of droplets the effect of the hygrothermal environment was unlikely to on the leaf margins in the 2012 experiments. Our findings have caused the difference in the magnitude of guttation were partially supported by the observations of a previous between in the 2011 and 2012 experiments. study that demonstrated a greater frequency of guttation It is more likely that plant characteristics, including during early growth stages of some crops (Joachimsmeier

Vol. 51, No. 4 (2013) 
 T. KUROYANAGI ET AL.

et al., 2011). French, C. J., Elder, M., Skelton, F. 1993. Recovering and iden- tifying infectious plant viruses in guttation fluid. HortScience CONCLUSIONS 28: 746
747. Grossenbacher, K. A. 1939. Autonomic cycle of rate of exudation of plants. Am. J. Bot. 26:107
109. The appearance of droplets on the leaf margins due to Hasegawa, S. 1977. Agro-climatological studies on C3 -plants guttation was affected by both plant characteristics (leaf and C4-plants (3) Transpiration rates and leaf temperatures. (in area and fruit number) and the air velocity around a plant. Japanese with English abstract) J. Agr. Met. 33: 129
136. More water was secreted on the leaf margins of tomato Huang, J. S. 1986. Ultrastructure of bacterial penetration in plants with a smaller leaf area and fewer fruits. Regardless plants. Ann. Rev. Phytopathol. 24: 141
157. plant characteristics, evaporation was accelerated by air cir- Hughes, R. N., Brimblecombe, P. 1994. Dew and guttation: for- culation under dark and high humidity conditions, with air mation and environmental significance. Agric. For. Meteorol.  67
circulation of
0.3 m s 1 resulting in the complete sup- : 173 190. Joachimsmeier, I., Pistorius, J., Heimbach, U., Schenke, D., pression of droplet secretion from the hydathodes of tomato Kirchner, W., Zwerger, P. 2011. Frequency and intensity leaves. In conclusion, the spread of pathogens via of guttation events in different crops in Germany. Hazards of guttation, particularly during the early growth stages of pesticides to bees - 11th International Symposium of the ICP- crops, could be reduced using air circulators or perforated BR Bee Protection Group, November, Wageningen, Julius- airflow ducts that are adequately arranged in a greenhouse. Kühn-Archiv (abstract) 437:87
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