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Article

A New Plant-Wearable Sap Flow Sensor Reveals the Dynamic Water Distribution during Watermelon Fruit Development

by
Runqing Zhang
1,
Yangfan Chai
2,
Xinyu Liang
1,
Xiangjiang Liu
2,
Xiaozhi Wang
3 and
Zhongyuan Hu
1,4,*
1
College of Agricultural and Biotechnology, Zhejiang University, Hangzhou 310058, China
2
College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China
3
College of Information Science and Electronic Engineering, Zhejiang University, Hangzhou 310058, China
4
Hainan Institute of Zhejiang University, Yazhou District, Sanya 572025, China
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(6), 649; https://doi.org/10.3390/horticulturae10060649
Submission received: 10 May 2024 / Revised: 31 May 2024 / Accepted: 6 June 2024 / Published: 17 June 2024
(This article belongs to the Special Issue Application of Smart Technology and Equipment in Horticulture)
Browse Figures
Versions Notes

Abstract

:
This study utilized a plant-wearable sap flow sensor developed by a multidisciplinary team at Zhejiang University to monitor water distribution patterns in watermelon fruit stalks throughout their developmental stages. The dynamic rules of sap flow at different stages of fruit development were discovered: (1) In the first stage, sap flow into the fruit gradually halts after sunrise due to increased leaf transpiration, followed by a rapid increase post-noon until the next morning, correlating with fruit expansion. (2) In the second stage, the time of inflow sap from noon to night is significantly shortened, while the outflow sap from fruit is observed with the enhancement of leaf transpiration after sunrise, which is consistent with the slow fruit growth at this stage. (3) In the third stage, the sap flow maintains the diurnal pattern. However, the sap flow that inputs the fruit at night is basically equal to the sap flow that outputs the fruit during the day; the fruit phenotype does not change anymore. In addition, a strong correlation between the daily mass growth in fruit and the daily sap flow amount in fruit stalk was identified, validating the sensor’s utility for fruit growth monitoring and yield prediction.

1. Introduction

Generally speaking, sap flow refers to the water flow within organs such as stems, leaf stalks, and fruit stalks that have transport tissues driven by water potential differences [1]. The water flow rate inside a plant is called the sap flow rate. Its measurement principle is to add a detection tracer to the water flowing inside the plant and calculate the sap flow rate by measuring the distance traveled by the detection tracer over a certain period of time. As an important water physiological indicator, the sap flow rate can reflect the transportation of water, minerals, and assimilates in plants. Therefore, monitoring the sap flow rate can provide clues for studying plant growth patterns [2,3]. In addition, compared to traditional phenotypic indicators, such as plant height, stem thickness, and leaf color, sap flow responds more quickly to environmental changes, providing a new perspective for studying the effects of environmental stresses such as water, temperature, light, and nutrients on plant growth and development [4,5]. Researchers often use temperature as a detection tracer; based on this, three methods have been developed to measure the sap flow rate, namely the thermal diffusion method, thermal equilibrium method, and thermal pulse method [6,7,8]. Traditional sap flow sensors require the probe to be inserted into the plant body to calculate the temperature difference between the two probes, which can cause certain damage to the plant. They are often used to measure the sap flow rate of tall woody plants and are not suitable for horticultural crops with a low biomass.
In 2020, the multidisciplinary team from Zhejiang University developed a new type of flexible wearable sensor for plant sap flow that was suitable for horticultural crops [9]. Chai et al. [10] deployed the new sap flow sensor on the surface of watermelon fruit stalks and conducted long-term and continuous monitoring. The plant condition was good, indicating that the sap flow sensor had good biocompatibility and could non-destructively monitor the plant sap flow rate. Compared with traditional sap flow sensors, the new sap flow sensor has excellent data collection capabilities and a simple and reliable structure, which is conducive to the high-throughput measurement of the plant sap flow rate in the field.
Watermelon (Citullus lanatus) is an annual herbaceous plant of the Cucurbitaceae family, originating from Africa [11]. It is widely cultivated worldwide and is one of the highest yielding fruits, known as the “king of summer fruits”. The development period of watermelon fruit starts from pollination to the end of fruit harvest, which is the most important period in the entire growth period of watermelon [12]. With the assistance of the new sap flow sensor, long-term monitoring of watermelon fruit development in the field is conducted to explore the water distribution law during fruit development, investigate the physiological characteristics related to sap flow, provide new theoretical clues for the breeding of high-yield and high-quality watermelon varieties or the research and development of cultivation techniques, and contribute to the sustainable and healthy development of the watermelon industry.

2. Materials and Methods

2.1. Test Location and Materials

From February to June 2023, the experiment was conducted at the base of Zhejiang Wuwangnong Co., Ltd., Hangzhou, China (30.25° N, 120.25° E). The tested Zhemi 8 was a watermelon variety, which was bred by our laboratory and widely cultivated around Zhejiang, Jiangsu, and surrounding areas. After disinfection on February 17, the seeds were planted in hole trays. When watermelon seedlings had four true leaves on March 15, they were planted in plastic greenhouses. The greenhouse was 45 m long and 8 m wide, with four rows covered with silver-black dual-color plastic film and irrigated under the film. The planting distance was 40 cm, and the pruning method was single-vine pruning. When the plant entered the vine extension period, a strong main vine was selected and left. Daily agricultural operations were managed by farm workers. On April 27, plants generally grew to 10 true leaves and differentiated into a second female flower, beginning artificial pollination.

2.2. Method

2.2.1. Sap Flow Rate (mg/min) of Fruit Stalk and Leaf Stalk

On the 7th day after pollination, when the watermelon fruit grew to the size of an egg (with a transverse diameter range of 56 cm and a longitudinal diameter range of 6–7 cm), three individual plants with similar fruit sizes were selected as three biological replicates. Sap flow sensors were installed on the fruit stalks (Figure 1), with the upstream temperature sensor corresponding to the direction near the root system and the downstream temperature sensor corresponding to the direction away from the root system (please see Appendix A for a detailed description). The sap flow sensor program was set to make a measurement every 30 min from the beginning until fruit harvesting, so the sap flow rate (mg/min) represented the average value over 30 min.
Studies have shown that fruit growth was influenced by plant transpiration [13,14]. Because all sap flow passing through the leaf stalks would evaporate into the air through the leaves, sap flow sensors installed on the leaf stalks could be used to study transpiration [15,16,17,18]. In this study, the sap flow rate of the leaf stalk was utilized to reflect the intensity of leaf transpiration. The preliminary experiment measured the sap flow rate of leaf stalks at multiple nodes and showed similar variation patterns. Herein, the leaf stalks closest to the fruit, namely the leaf stalks of the fruit-setting node, were used to demonstrate their impacts on the sap flow of the fruit stalks. At the same time as the sap flow sensors were installed on the fruit stalks, sap flow sensors were also installed on the leaf stalks of the fruit-setting node. The installation method and measurement interval of the sensors were as described above. Unless otherwise specified, the subsequent plotting data represented the average of three biological replicates.

2.2.2. Environmental Parameters

Data collection for total solar radiation (J/m2/h) utilized photoelectric solar radiation sensor (RS4854, Vemsee Co., Ltd., Shandong, China), with a range of 0–2000 W/m2 and an accuracy of ±5%. Measurements were automatically taken once every hour and transmitted to the cloud platform via a 4G signal. The sensor was mounted on the upper part of the greenhouse.
For air temperature (°C) data acquisition, external temperature and humidity sensor (ZL-TH10TP, CIMC Co., Ltd., Beijing, China) were employed, with a temperature measurement range of −40 °C to 80 °C and an accuracy of ±0.5 °C. Measurements were automatically taken once every half hour and sent to the cloud platform through a 4G signal. The sensor was positioned in the lower part of the greenhouse, near the fruits.

2.2.3. Daily Mass Growth (g) of Fruit

Destructive sampling was conducted every 24 h. Before sampling, the longitudinal and transverse diameters of the fruits containing sap flow sensors were measured using a tape measure with an accuracy of 0.1 cm. Subsequently, fruits matching their longitudinal and transverse diameters were selected and removed from the vine. These fruits were then weighed using an electronic balance, and the weights were recorded as Wx. The same procedure was repeated at the same time the following day to obtain the weight Wx + 1. Thus, the daily mass growth of fruit was calculated as Wx + 1 − Wx. This measurement was used to compare with the daily sap flow amount of fruit stalk during the same time period.

2.2.4. Daily Sap Flow Amount (g) of Fruit Stalk

The daily sap flow amount (g) was calculated based on the sap flow rate (mg/min), as shown in the following formula:
M = ∑(V × 30/1000)
M represented the daily sap flow amount (g) of fruit stalk. V represented the sap flow rate (mg/min) of fruit stalk measured by the sap flow sensor. The sap flow sensor program was set to measure every 30 min from the beginning until fruit harvesting. Therefore, V represented the average sap flow rate (mg/min) over a 30 min period. (V × 30/1000) represented the estimated sap flow amount (g) for the 30 min interval. The estimated sap flow amount from 48 measurements in a day was then summed up to obtain the daily sap flow amount (g). As watermelon fruits primarily grew at night [10], the total of 48 measurements within a 24 h period from 12:00 on day x to 12:00 on day x + 1 was considered as the daily sap flow amount (g) for day x + 1. Consequently, the diameter and weight of the fruit were measured at 12:00 each day.

2.3. Data Processing and Statistical Analysis

In this experiment, we used the R language (4.2.1) to organize and clean the raw data measured by the sap flow sensors, calculate the sap flow rate, conduct descriptive statistics analysis and correlation analysis, and visualize the data using R language (4.2.1) and EXCEL (Microsoft Office 2016).

3. Results

3.1. Sap Flow Rate of Leaf Stalk

Figure 2 shows the variation pattern of the leaf stalk sap flow rate (equivalent to leaf transpiration rate, mg/min) with days after pollination (DAP) in watermelon. Total solar radiation and temperature exhibited similar trends, with the temperature in the greenhouse rising rapidly as the sun rose and then decreasing after noon as total solar radiation decreased. After conducting correlation analysis on the real-time data of total solar radiation and temperature, a highly significant positive correlation (R = 0.882 ***) was found. To avoid redundancy, only the temperature curve was added to the graph, while the total solar radiation curve was omitted.
As shown in the figure, the curve of the leaf transpiration rate and the temperature curve were in very good agreement, both in terms of days and the entire fruit development period. At 9 DAP, 10 DAP, and 14 DAP, under low-temperature and low-light conditions, the leaf transpiration rate was very low. During 15–19 DAP, when the temperature was high, the transpiration rate could even reach 450 mg/min. After Pearson’s correlation analysis, a highly significant positive correlation (R = 0.903 ***) was found between the leaf transpiration rate and temperature.
The leaf transpiration rate exhibited a very distinct diurnal rhythm, regardless of weather conditions. Sap flow commenced around sunrise and peaked at noon due to the increase in total solar radiation. Subsequently, post-noon, as total solar radiation decreased, the transpiration rate weakened, approaching 0 mg/min around sunset, with no observed sap flow throughout the night. Following correlation analysis, the leaf transpiration rate and total solar radiation exhibited a highly significant positive correlation (R = 0.921 ***).

3.2. Sap Flow Rate of Fruit Stalk

According to the change rule of the sap flow rate in the fruit stalk and the time of appearance of negative-direction sap flow, the watermelon fruit development period was divided into three stages (stage 1 from 7 DAP to 20 DAP, stage 2 from 20 DAP to 29 DAP, and stage 3 from 29 DAP to 35 DAP):
The first stage began with the installation of sap flow sensors on the fruit stalks at 7 DAP and ended with the appearance of obvious negatively oriented sap flow at 20 DAP (Figure 3). The average value of the sap flow rate of fruit stalks in the first stage was 62 mg/min, and the total sap flow amount (area of blue shaded portion) was 1160 g.
The maximum value of the sap flow rate in this stage was 224 mg/min, which occurred around 18:00 at 16 DAP, and the sap flow rate remained high from 15 DAP to 19 DAP, with a daily average sap flow rate of 100–150 mg/min. Moreover, the area shaded in blue also showed that the sap flow into the fruit was very high during these days. At 10 DAP and 14 DAP, the overall sap flow rate as well as sap flow rate during these two days were significantly smaller in comparison to the two days prior and after, indicating that the low-temperature and low-sunshine weather would had a significant negative impact on fruit growth and development.
At this stage, the sap flow rate of fruit stalks showed a similar pattern of change nearly every day. Around 6:00 a.m., as the amount of light and temperature increased, the sap flow rate of fruit stalks rapidly approached 0 mg/min, and no sap flow was observed throughout the morning. After 12:00 a.m., as the temperature and total solar radiation decreased, sap flow reappeared between 13:00 and 16:00. The sap flow rate increased rapidly, reaching its maximum around sunset and gradually decreased after sunset, persisting until sunrise the next day.
During fruit development, the root system absorbed water from the soil, which was then transported to the fruit through the conductive tissues over a long distance, typically from the exterior to the interior of the fruit. However, the negative sap flow rate depicted in the figure indicated that water was flowing out of the fruit through the fruit stalk during certain periods. The sap flow rate calculations of the three biological replicates before 20 DAP also exhibited negative values, albeit with very small absolute magnitudes and infrequent occurrences, thus not being considered significant. Negative sap flow coincidentally occurred in all three biological replicates around 6:00 a.m. at approximately 20 DAP, with absolute sap flow rates exceeding 50 mg/min and lasting for about 3 h. This phenomenon persisted almost every morning from 20 DAP until the fruits were harvested.
The beginning of the second stage was marked by the appearance of significant negatively oriented sap flow at 20 DAP, and the end of the second stage was marked by the fact that the night-time sap flow amount into the fruit was essentially equal to the daytime sap flow amount out of the fruit at 29 DAP (first half of Figure 4). The average sap flow rate of fruit stalks in the second stage was 23.3 mg/min, and the total sap flow amount (area shaded blue above the x-axis minus the area shaded blue below the x-axis) was 335.3 g.
Compared to the first stage, the average temperature was higher in the second stage, but the sap flow rate was considerably lower, and the duration of positively oriented sap flow was significantly lower in this stage compared to the first stage, when water flowed into the fruit almost the entire night. In the first few days (20 DAP, 21 DAP, and 23 DAP), positive sap flow appeared around 16:00 and disappeared between 2:00 and 4:00. With the passing of developmental days, the disappearance of positive sap flow during the night began earlier and earlier, and the amount of water flowing into the fruit during the night decreased progressively (the blue shaded portion above the x-axis became smaller).
Negative-direction sap flow was observed almost every morning during this phase. On the initial days (20 DAP, 21 DAP, 23 DAP, and 24 DAP), the cessation of negative sap flow occurred around 9:00 a.m., with an approximate duration of 3 h from the onset to cessation. With the advancement of fruit development, the cessation of negative sap flow during daytime progressively delayed, accompanied by an increasing outflow of water from the fruit during daytime (the area shaded blue below the x-axis became larger and larger).
The beginning of the third stage was marked by the 29 DAP night-time sap flow into the fruit being essentially equal to the daytime sap flow out of the fruit, and the end of the stage was marked by the harvest of the fruit at 35 DAP (Figure 4, second half). The mean sap flow rate of fruit stalks in the third stage was 7.6 mg/min, and the total sap flow amount (the area shaded blue the x-axis minus the area shaded blue below the x-axis) was 60.6 g.
Positive sap flow in this phase occurred only around sunset and lasted less than 6 h. Negative sap flow occurred during the day for about 6 h and disappeared after 12:00 a.m. as temperature and total solar radiation decreased. The duration of positive-direction sap flow at night was basically equal to that of negative-direction sap flow during the day, and the amount of sap flow into the fruit at night was basically equal to the amount of sap flow out of the fruit during the day (the area shaded blue above the x-axis was basically equal to the area shaded blue below the x-axis), and the daily sap flow amount tended to be 0 g.

3.3. Daily Sap Flow Amount of Fruit Stalk and Daily Mass Growth in Fruit

As shown in Figure 5, the daily sap flow amount and daily mass growth showed an increasing and then decreasing trend versus the number of days of fruit development after pollination, and the difference between the daily sap flow amount and daily mass growth on the same day was not significant. Except for 10 DAP, 11 DAP, and 15 DAP, which were affected by low temperature and rain, the daily mass growth from 8 DAP to 20 DAP was more than 50 g, and the daily mass growth at 13 DAP, 16 DAP, and 17 DAP was even more than 150 g. From 20 DAP onwards, the daily mass growth gradually decreased, and the daily mass growth for the 6 days before harvest was around 0 g. By summing the daily sap flow amount, a total sap flow amount of 1479 g was obtained for the entire fruit development period. Additionally, summing the daily mass growth resulted in a mass increase of 1511 g during the same period. This represents that there was a small difference between the two values.
As shown in Figure 6 (left), the longitudinal and transverse diameters of watermelon fruits after pollination conformed to an S-shaped growth curve. Initially, the longitudinal diameter was greater than the transverse diameter. As the fruits grew and developed, the gap between the two gradually decreased. When growth ceased, the transverse diameter averaged 16.7 cm, and the longitudinal diameter averaged 16 cm. The longitudinal diameter ceased to grow around 22 DAP, while the transverse diameter ceased around 24 DAP. At 10 DAP and 15 DAP, there were two days of cold and rainy weather, resulting in significantly smaller increases in longitudinal and transverse diameters compared to the dates before and after.
The daily sap flow amount over these 28 days was compared and analyzed against the daily mass growth. As shown in Figure 6 (right), the daily mass growth and the daily sap flow amount were evenly distributed above and below the y = x line, with an R2 value of 0.817, indicating a good fit. After field verification, the sap flow sensor accurately predicted the sap flow rate of fruit stalk, which was essentially equivalent to the real-time growth rate of fruit mass. The daily sap flow amount of fruit stalk corresponded closely to the daily mass growth of the fruits.

4. Discussion

4.1. The Sap Flow Rate Is Sensitive to Environmental Factors and Can Reflect the Growth Status of Fruits

Water transport, traditionally focused on the plant stem and leaf, has been well developed to understand the soil–plant–atmosphere continuum (SPAC) [19]. However, research on water transport during fruit development has been limited, largely due to the lack of suitable technical means. Methods such as microscopy, high-pressure flow meters, microCT, and others [20,21,22,23], were often destructive and time-consuming, with significant drawbacks. In our study, we installed a new sap flow sensor on watermelon fruit stalk to investigate the sap flow patterns during watermelon fruit development. Previous studies have indicated that water accounted for more than 90% of the fresh weight in many fleshy fruits, and, hence, water content largely determined fruit size [24,25]. Our research results also confirmed this point, as the daily sap flow amount of the fruit stalk was essentially equal to daily fruit mass growth. Furthermore, we found that sap flow was highly sensitive to environmental changes: when encountering low-temperature and low-light conditions, the sap flow of the fruit stalk was notably weak, while under favorable weather conditions, the sap rate flowing into the fruit increased rapidly. Therefore, the sap flow rate of the fruit stalk can reflect the real-time growth rate of the fruit, and the new sap flow sensor can be used to monitor fruit growth status.

4.2. Employing the New Sap Flow Sensor to Examine Diurnal Shifts in Water Allocation during Watermelon Fruit Development

The plant root system relies on two different mechanisms for water uptake: one is passive water uptake through leaf transpiration, and the other is active water uptake that is dependent on the ion concentration in the reservoir [26]. In either case, the water potential difference is the fundamental driving force for water transportation in the plant, and water always passes from a higher water potential to a lower one [27]. Previous studies have shown that at different stages of fruit development, the partition of vascular flows in fleshy fruits varied [28,29,30,31]. According to the change rule of the fruit stalk sap flow rate and the duration of negative-direction sap flow, the watermelon fruit development period was divided into three stages. Moreover, based on the fundamental cause of water transportation and the synergistic changes of the sap flow rate of fruit stalks and leaf stalks, fruit mass, as well as the longitudinal and transverse diameters of the fruit observed in the experiments, the water distribution laws of watermelon fruit development in each stage are as follows (Figure 7):

4.2.1. The First Stage (7 DAP–20 DAP), as in Figure 7A

In the evening, transpiration is extremely weak, coupled with the transfer and accumulation of photosynthetic products from source to reservoir during the day. At this time, the water potential difference between the inside and outside the fruit is the greatest, and the sap flow rate of the fruit stalk reaches its maximum. Subsequently, with the inflow of water, the water potential inside the fruit increases, and the water potential difference between the inside and outside of the fruit decreases. The sap flow rate also decreases, but until the next morning, the sap flow rate does not reach 0 mg/min, indicating continuous water inflow into the fruit throughout the night. Morphologically, watermelon fruits expand significantly, and the longitudinal diameter, transverse diameter, and mass measured every other day increase greatly compared with those of the previous day.
After sunrise, with the increase in temperature and total solar radiation, leaf transpiration becomes active. The water potential outside of the fruit decreases, and the difference between the internal and external water potentials decreases until it reaches 0. The sap flow rate of the fruit stalk rapidly decreases to 0 mg/min, water stops flowing into the fruit, and the sap flow in the positive direction disappears. This phenomenon lasts until about 12:00 a.m.
After noon, as leaf transpiration weakens and the transpiration rate decreases, the water potential outside the fruit rises, allowing water to flow into the fruit. The sap flow sensor re-monitors the sap flow in the positive direction of the fruit stalk. With the continuous decline in the transpiration rate and the accumulation of assimilates in the fruit, the difference between the water potential inside and outside of the fruit increases. Finally, the sap flow rate of the fruit stalk reaches its maximum value around sunset.

4.2.2. The Second Stage (20 DAP–29 DAP), as in Figure 7B

The peak difference in water potential between the inside and outside of the fruit occurs in the evening, while the sap flow rate reaches its maximum value. Subsequently, as water flows in, the water potential inside the fruit increases, leading to a decrease in the water potential difference between the inside and outside of the fruit. The sap flow rate gradually decreases until it reaches 0 mg/min, and the water inflow into the fruit stops. Compared to the first stage, the water inflow is significantly reduced. Morphologically, watermelon phenotypic indexes exhibit slow growth. With the progression of developmental days, the positive sap flow disappears earlier and earlier. Night-time water inflow diminishes progressively. Morphologically, the longitudinal diameter, transverse diameter, and mass of fruits gradually cease to change.
After sunrise, as the temperature rises and the total solar radiation increases, leaf transpiration is initiated. The external water potential of the fruit begins to decrease, becoming lower than the internal water potential, resulting in water flowing out of the fruit. The sap flow sensor detects the sap flow in a negative direction, indicating the intense transpiration of the leaf “snatching” water from the fruit. As water flows out of the fruit, the water potential inside the fruit decreases, reducing the difference between the internal and external water potentials. After a few hours, the difference in water potentials tends to be 0, and the sap flow rate tends to be 0 mg/min. Water stops flowing out of the fruit, and the negative sap flow disappears. With the increase in developmental days, the sap flow in the negative direction disappears later and later, and the outflow amount becomes bigger and bigger.
After noon, the pattern of change of sap flow in the fruit stalk is the same as that of the first stage.

4.2.3. The Third Stage (29 DAP–35 DAP), as in Figure 7C

The diurnal variation in water allocation in this stage is the same as that of the second stage. However, the occurrence of positive-direction sap flow at night is basically equal to the occurrence of negative-direction sap flow during the day. The sap flow into the fruit at night is basically equal to the sap flow out of the fruit during the day, resulting in the daily sap flow amount approaching 0 g. The phenotype of watermelon fruits remains unchanged.
A comparison between the first and second stages reveals that even with high morning temperatures and total solar radiation in the first stage, there is almost no negative sap flow. However, in the second stage, the phenomenon of water outflow from the fruit occurs almost every morning. How can we explain this difference? During the pre-developmental period of watermelon fruits, it has been demonstrated that cell division and cell expansion are vigorous [32]. Watermelon fruits rapidly decompose assimilates into various components to enable cellular metabolism. The cytoplasm has a strong water-binding capacity, making it difficult for transpiration outside the fruit to “snatch” water [33]. As fruit expansion gradually stops, large amounts of sucrose, fructose, and other soluble sugars accumulate in the late stages of fruit development. Consequently, the free water content within the cells increases, facilitating transpiration from outside the fruit to “snatch” water.

4.3. It Was Firstly Discovered That Sap Flows out the Watermelon Fruit through the Fruit Stalk

It was firstly found that the direction of water transport during watermelon fruit development did not only occur from the outside to the inside of the fruit, but also from the inside of the fruit to the outside through the fruit stalk due to the intense transpiration of the leaves. Negative sap flow implies that watermelon fruit growth not only increases but also decreases, possibly resulting in a decrease in mass or diameter at certain times. However, capturing this small phenotypic change with conventional instruments is challenging.
In recent years, researchers have also observed similar phenomena in other crops using high-precision sensors. The linear variable displacement transducer (LVDT) is a distance sensor capable of measuring micrometer-level variations, and W. Conejero et al. mounted it on the trunk of a peach tree [34]. The trunk diameter was found to be smallest at noon, and the maximum daily trunk shrinkage was significantly positively correlated with the noon air temperature and transpiration rate. The maximum daily trunk shrinkage in the water deficit stress treatment was also significantly higher than that in the control group and returned to normal after normal irrigation. Sun Qing et al. installed linear variable displacement sensors on apple fruits, together with the Internet of Things, forming a fruit diameter dynamic monitoring system. After observing two growing seasons, it was found that the fruit diameter from young fruit to mature fruit exhibited obvious diurnal variation rules, generally peaking in the early morning and reaching a minimum in the evening, with a maximum daily shrinkage of 200 μm [35]. Through a real-time weighing system, Wang Dandan et al. found that changing tomato plants in solar greenhouses throughout the day causes an increase in plant growth at night. After sunrise, due to transpiration, plant weight begins to decline; after sunset, plant weight rises again [36]. In conclusion, the negatively oriented sap flow of watermelon fruits can be used as a new indicator to study the responses of watermelon fruits to water-deficit stress and high-temperature stress during their developmental period.

5. Conclusions

With the assistance of the new sap flow sensor, this study elucidated the dynamic changes in sap flow during watermelon fruit development, filling the gap in the research on water distribution during watermelon fruit development: (1) In the first stage, sap flow into the fruit gradually halts after sunrise due to increased leaf transpiration, followed by a rapid increase post-noon until the next morning, correlating with fruit expansion. (2) In the second stage, the time of inflow sap from noon to night is significantly shortened, while the outflow sap from fruit is observed with the enhancement of leaf transpiration after sunrise, which is consistent with the slow fruit growth at this stage. (3) In the third stage, the sap flow maintains a diurnal pattern. However, the sap flow into the fruit at night is basically equal to the sap flow out of the fruit during the day, and the fruit phenotype does not change anymore. In addition, the daily sap flow amount of the fruit stalk was essentially equal to the daily fruit mass growth, and the sap flow rate of fruit stalk was essentially equal to real-time fruit mass growth, indicating the sensor’s potential in fruit growth monitoring and yield prediction.

Author Contributions

Conceptualization, R.Z. and Z.H.; data curation, R.Z., Y.C. and X.L. (Xinyu Liang); methodology, R.Z. and Y.C.; software, X.L. (Xiangjiang Liu) and X.W.; validation, R.Z., Z.H. and Y.C.; formal analysis, R.Z.; investigation, R.Z., Y.C. and X.L. (Xinyu Liang); resources, Y.C., X.L. (Xiangjiang Liu) and X.W.; visualization, R.Z.; writing—original draft preparation, R.Z.; writing—review and editing, R.Z., Y.C. and Z.H.; supervision, Z.H.; seedling management, X.L. (Xinyu Liang); funding acquisition, Z.H. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Earmarked Fund for China Agriculture Research System (CARS25); the Project of Sanya Yazhou Bay Science and Technology City (SCKJ-JYRC-2022-18); and the Science and Technology Innovation Platform for Watermelon and Melon Breeding, Reproduction, and Spreading of Zhejiang Province (2020-KYY-NSFZ-0314).

Data Availability Statement

The data that support the findings of this study are available from the first author, upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

The detection principle of the new sap flow sensor is shown in Figure A1. When sap flows from the upstream temperature sensor to the downstream temperature sensor, it is heated by the thermistor, resulting in an increase in temperature. Thus, the temperature value measured by the downstream temperature sensor is higher than the temperature value measured by the upstream temperature sensor. As the thermistor continues to heat up, the heat is continuously transported from the upstream to downstream sensor, and the temperature difference (ΔT = Tdownstream − Tupstream) between the two sensors becomes larger and larger.
It has been shown that the sap flow rate was significantly negatively correlated with the time to reach the maximum ΔT: the larger the sap flow rate, the shorter the time to reach the maximum ΔT; the smaller the sap flow rate, the longer the time to reach the maximum ΔT. Therefore, a prediction model was developed to calculate the sap flow rate by inputting the time to reach the maximum ΔT [10].
When sap flows from the upstream temperature sensor to the downstream temperature sensor, the sap flow rate is positive, and we define this direction as the positive direction of sap flow. When sap flows from the downstream temperature sensor to the upstream temperature sensor, the sap flow rate is negative, and we define this direction as the negative direction of sap flow. Generally, the installation direction of the sap flow sensor on the surface of the plant material is such that the upstream temperature sensor corresponds to the direction near the root system, and the downstream temperature sensor corresponds to the direction away from the root system.
Horticulturae 10 00649 g0a1
Figure A1. Detection principle of the new sap flow sensor. There are three core elements of the sensor: the upstream temperature sensor, the thermistor, and the downstream temperature sensor.
Figure A1. Detection principle of the new sap flow sensor. There are three core elements of the sensor: the upstream temperature sensor, the thermistor, and the downstream temperature sensor.
Horticulturae 10 00649 g0a1

References

  1. Smith, D.M.; Allen, S.J. Measurement of sap flow in plant stems. J. Exp. Bot. 1996, 47, 1833–1844. [Google Scholar] [CrossRef]
  2. Busby, P.E.; Soman, C.; Wagner, M.R.; Friesen, M.L.; Kremer, J.; Bennett, A.; Morsy, M.; Eisen, J.A.; Leach, J.E.; Dangl, J.L. Research priorities for harnessing plant microbiomes in sustainable agriculture. PLoS Biol. 2017, 15, 134–156. [Google Scholar] [CrossRef] [PubMed]
  3. Forster, M.A. How significant is nocturnal sap flow. Tree Physiol. 2014, 34, 757–765. [Google Scholar] [CrossRef] [PubMed]
  4. Miner, G.L.; Ham, J.M.; Kluitenberg, G.J. A heat-pulse method for measuring sap flow in corn and sunflower using 3D-printed sensor bodies and low-cost electronics. Agric. For. Meteorol. 2017, 246, 86–97. [Google Scholar] [CrossRef]
  5. Fang, W.; Lu, N.; Zhang, Y.; Jiao, L.; Fu, B. Responses of nighttime sap flow to atmospheric and soil dryness and its potential roles for shrubs on the Loess Plateau of China. J. Plant Ecol. 2018, 11, 717–729. [Google Scholar] [CrossRef]
  6. Čermák, J.; Deml, M.; Penka, M. A new method of sap flow rate determination in trees. Biol. Plant. 1973, 15, 171–178. [Google Scholar] [CrossRef]
  7. Helfter, C.; Shephard, J.D.; Martínez-Vilalta, J.; Mencuccini, M.; Hand, D.P. A noninvasive optical system for the measurement of xylem and phloem sap flow in woody plants of small stem size. Tree Physiol. 2007, 27, 169–179. [Google Scholar] [CrossRef] [PubMed]
  8. Cohen, Y. Accuracy of Sap Flow Measurement Using Heat Balance and Heat Pulse Methods. Agron. J. 1993, 85, 1080–1086. [Google Scholar] [CrossRef]
  9. Chen, C.Y. Study of Non-Invaisve Plant Wearable Sap Flow Sensor. Master’s Thesis, Zhejiang University, Hangzhou, China, 2020. [Google Scholar]
  10. Chai, Y.; Chen, C.; Luo, X.; Zhan, S.; Kim, J.; Luo, J.; Wang, X.; Hu, Z.; Ying, Y.; Liu, X. Cohabiting Plant-Wearable Sensor In Situ Monitors Water Transport in Plant. Adv. Sci. 2021, 8, 2003642. [Google Scholar] [CrossRef]
  11. Guo, S.; Zhang, J.; Sun, H.; Salse, J.; Lucas, W.J.; Zhang, H.; Zheng, Y.; Mao, L.; Ren, Y.; Wang, Z. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 2013, 45, 51–58. [Google Scholar] [CrossRef]
  12. Yativ, M.; Harary, I.; Wolf, S. Sucrose accumulation in watermelon fruits: Genetic variation and biochemical analysis. J. Plant Physiol. 2010, 167, 589–596. [Google Scholar] [CrossRef] [PubMed]
  13. Morandi, B.; Losciale, P.; Manfrini, L.; Zibordi, M.; Anconelli, S.; Pierpaoli, E.; Grappadelli, L.C. Leaf gas exchanges and water relations affect the daily patterns of fruit growth and vascular flows in Abbé Fétel pear (Pyrus communis L.) trees. Sci. Hortic. 2014, 23, 106–113. [Google Scholar] [CrossRef]
  14. Carella, A.; Massenti, R.; Lo Bianco, R. Testing effects of vapor pressure deficit on fruit growth: A comparative approach using peach, mango, olive, orange, and loquat. Front. Plant Sci. 2023, 20, 1294195. [Google Scholar] [CrossRef] [PubMed]
  15. Forster, M.A. The importance of conduction versus convection in heat pulse sap flow methods. Tree Physiol. 2020, 40, 683–694. [Google Scholar] [CrossRef] [PubMed]
  16. Ma, Y.; Ren, R.; Fu, H.; Si, B.; Kinar, N.J.; Liu, G.; Steppe, K. Comparing dual heat pulse methods with Péclet’s number as universal switch to measure sap flow across a wide range. Tree Physiol. 2023, 43, 1691–1703. [Google Scholar] [CrossRef] [PubMed]
  17. Pradiko, I.; Rahutomo, S.; Farrasati, R.; Ginting, E.N.; Hidayat, F.; Syarovy, M. Transpiration of oil palm (Elaeis guineensis Jacq.) based on sap flow measurement: The relation to soil and climate variables. J. Oil Palm Res. 2023, 35, 168–184. [Google Scholar] [CrossRef]
  18. Bayona-Rodríguez, C.J.; Romero, H.M. Estimation of transpiration in oil palm (Elaeis guineensis Jacq.) with the heat ratio method. Agron. Colomb. 2016, 34, 172–178. [Google Scholar] [CrossRef]
  19. Hou, X.; Li, H.; Zhang, W. Water transport in fleshy fruits: Research advances, methodologies, and future directions. Physiol. Plant. 2021, 172, 2203–2216. [Google Scholar] [CrossRef] [PubMed]
  20. Ma, S.; Li, Y.; Li, X. Phloem unloading strategies and mechanisms in crop fruits. J. Plant Growth Regul. 2019, 38, 494–500. [Google Scholar] [CrossRef]
  21. Anderegg, W.R.; Venturas, M.D. Plant hydraulics play a critical role in Earth system fluxes. New Phytol. 2020, 226, 1535–1538. [Google Scholar] [CrossRef]
  22. Guo, X.M.; Wang, G.X.; Gao, R.F. Vascular anatomy of kiwi fruit and its implications for the origin of carpels. Front. Plant Sci. 2013, 16, 61185. [Google Scholar] [CrossRef] [PubMed]
  23. Rančić, D.; Quarrie, S.P.; Radošević, R.; Terzić, M.; Pećinar, I.; Stikić, R.; Jansen, S. The application of various anatomical techniques for studying the hydraulic network in tomato fruit pedicels. Protoplasma 2010, 246, 25–31. [Google Scholar] [CrossRef] [PubMed]
  24. Knipfer, T.; Fei, J.; Gambetta, G.A. Water transport properties of the grape pedicel during fruit development: Insights into xylem anatomy and function using microtomography. Plant Physiol. 2015, 168, 1590–1602. [Google Scholar] [CrossRef] [PubMed]
  25. Trifilò, P.; Raimondo, F.; Lo Gullo, M.A. Hydraulic connections of leaves and fruit to the parent plant in Capsicum frutescens (hot pepper) during fruit ripening. Ann. Bot. 2010, 106, 333–341. [Google Scholar] [CrossRef] [PubMed]
  26. Dubbert, M.; Couvreur, V.; Kübert, A.; Werner, C. Plant water uptake modelling: Added value of cross-disciplinary approaches. Plant Biol. 2023, 25, 32–42. [Google Scholar] [CrossRef] [PubMed]
  27. Choat, B.; Brodribb, T.J.; Brodersen, C.R. Triggers of tree mortality under drought. Nature 2018, 558, 531–539. [Google Scholar] [CrossRef]
  28. Brüggenwirth, M.; Winkler, A.; Knoche, M. Xylem, phloem, and transpiration flows in developing sweet cherry fruit. Trees 2016, 30, 1821–1830. [Google Scholar] [CrossRef]
  29. Morandi, B.; Manfrini, L.; Lugli, S.; Tugnoli, A.; Boini, A.; Perulli, G.D.; Bresilla, K.; Venturi, M.; Grappadelli, L.C. Sweet cherry water relations and fruit production efficiency are affected by rootstock vigor. J. Plant Physiol. 2019, 237, 43–50. [Google Scholar] [CrossRef] [PubMed]
  30. Morandi, B.; Manfrini, L.; Losciale, P. Changes in vascular and transpiration flows affect the seasonal and daily growth of kiwifruit (Actinidia deliciosa) berry. Ann. Bot. 2010, 105, 913–923. [Google Scholar] [CrossRef]
  31. Nordey, T.; Lechaudel, M.; Génard, M. The decline in xylem flow to mango fruit at the end of its development is related to the appearance of embolism in the fruit pedicel. Funct. Plant Biol. 2015, 42, 668–675. [Google Scholar] [CrossRef]
  32. Chen, J.W.; Zhang, S.L.; Zhang, L.C. Sugar Transport, Metabolism, Accumulation and Their Regulation in Fruits. J. Plant Physiol. Mol. Biol. 2004, 30, 1–10. [Google Scholar]
  33. Srivastava, M.K.; Dwivedi, U.N. Delayed ripening of banana fruit by salicylic acid. Plant Sci. 2000, 158, 87–96. [Google Scholar] [CrossRef] [PubMed]
  34. Conejero, W.; Alarcón, J.J.; García-Orellana, Y.; Abrisqueta, J.M.; Torrecillas, A. Daily sap flow and maximum daily trunk shrinkage measurements for diagnosing water stress in early maturing peach trees during the post-harvest period. Tree Physiol. 2007, 27, 81–88. [Google Scholar] [CrossRef] [PubMed]
  35. Sun, Q.; Zhao, Y.X.; Cheng, J.X.; Zeng, T.Y.; Zhang, Y. Fruit growth modelling based on multi-methods—A case study of apple in zhaotong, yunnan. Sci. Agric. Sin. 2021, 54, 3737–3751. [Google Scholar] [CrossRef]
  36. Wang, D. Research on Irrigation Model for Tomatoes in Solar Greenhouse Bag Culture Based on Real Time Growth. Master’s Thesis, Shenyang Agricultural University, Shenyang, China, 2017. [Google Scholar]
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Figure 1. Field application of sap flow sensors to monitor fruit development. ‘DAP’ represents days after pollination.
Figure 1. Field application of sap flow sensors to monitor fruit development. ‘DAP’ represents days after pollination.
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Figure 2. The variation of sap flow rate of leaf stalk at the fruit-setting node with the days after pollination. The black points represent the sap flow rate (mg/min) measured at 30 min intervals, and their values correspond to the y-axis on the left. The area marked by the blue shadow represents the sap flow amount (mg) passing through the leaf stalk between sequential time points. We will not consider the actual sunrise and sunset time here and use 6:00 as the sunrise time and 18:00 as the sunset time, which is shown as a black and white rectangular background in the figure. The red curve represents the temperature variation over time, and its value corresponds to the y-axis on the right.
Figure 2. The variation of sap flow rate of leaf stalk at the fruit-setting node with the days after pollination. The black points represent the sap flow rate (mg/min) measured at 30 min intervals, and their values correspond to the y-axis on the left. The area marked by the blue shadow represents the sap flow amount (mg) passing through the leaf stalk between sequential time points. We will not consider the actual sunrise and sunset time here and use 6:00 as the sunrise time and 18:00 as the sunset time, which is shown as a black and white rectangular background in the figure. The red curve represents the temperature variation over time, and its value corresponds to the y-axis on the right.
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Figure 3. The variation of sap flow rate of watermelon fruit stalk versus the days after pollination in the first stage. The black points represent the sap flow rate (mg/min) measured at 30 min intervals, and their values correspond to the y-axis on the left. The area marked by the blue shadow represents the sap flow amount (mg) passing through the fruit stalk between sequential time points. The explanation of other information elements is the same as Figure 2.
Figure 3. The variation of sap flow rate of watermelon fruit stalk versus the days after pollination in the first stage. The black points represent the sap flow rate (mg/min) measured at 30 min intervals, and their values correspond to the y-axis on the left. The area marked by the blue shadow represents the sap flow amount (mg) passing through the fruit stalk between sequential time points. The explanation of other information elements is the same as Figure 2.
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Figure 4. The variation of sap flow rate of watermelon fruit stalks versus the days after pollination in the second stage and third stage. The explanation of information elements is the same as Figure 3.
Figure 4. The variation of sap flow rate of watermelon fruit stalks versus the days after pollination in the second stage and third stage. The explanation of information elements is the same as Figure 3.
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Figure 5. Changes in daily sap flow amount and daily mass growth versus the days after pollination.
Figure 5. Changes in daily sap flow amount and daily mass growth versus the days after pollination.
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Figure 6. Changes in fruit longitudinal and transverse diameters versus the days after pollination (left); comparison of daily sap flow amount and daily mass growth with y = x straight line (right).
Figure 6. Changes in fruit longitudinal and transverse diameters versus the days after pollination (left); comparison of daily sap flow amount and daily mass growth with y = x straight line (right).
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Figure 7. Water distribution patterns during watermelon fruit development. Rows ((A–C) in figure) represent different stages of fruit development, while columns represent different time periods within the same day. The values next to the leaf stalks and fruit stalks represent the average sap flow rate (mg/min) of the leaf stalks and fruit stalks during the corresponding time period, respectively.
Figure 7. Water distribution patterns during watermelon fruit development. Rows ((A–C) in figure) represent different stages of fruit development, while columns represent different time periods within the same day. The values next to the leaf stalks and fruit stalks represent the average sap flow rate (mg/min) of the leaf stalks and fruit stalks during the corresponding time period, respectively.
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MDPI and ACS Style

Zhang, R.; Chai, Y.; Liang, X.; Liu, X.; Wang, X.; Hu, Z. A New Plant-Wearable Sap Flow Sensor Reveals the Dynamic Water Distribution during Watermelon Fruit Development. Horticulturae 2024, 10, 649. https://doi.org/10.3390/horticulturae10060649

AMA Style

Zhang R, Chai Y, Liang X, Liu X, Wang X, Hu Z. A New Plant-Wearable Sap Flow Sensor Reveals the Dynamic Water Distribution during Watermelon Fruit Development. Horticulturae. 2024; 10(6):649. https://doi.org/10.3390/horticulturae10060649

Chicago/Turabian Style

Zhang, Runqing, Yangfan Chai, Xinyu Liang, Xiangjiang Liu, Xiaozhi Wang, and Zhongyuan Hu. 2024. "A New Plant-Wearable Sap Flow Sensor Reveals the Dynamic Water Distribution during Watermelon Fruit Development" Horticulturae 10, no. 6: 649. https://doi.org/10.3390/horticulturae10060649

APA Style

Zhang, R., Chai, Y., Liang, X., Liu, X., Wang, X., & Hu, Z. (2024). A New Plant-Wearable Sap Flow Sensor Reveals the Dynamic Water Distribution during Watermelon Fruit Development. Horticulturae, 10(6), 649. https://doi.org/10.3390/horticulturae10060649

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