Seaweed Extract Improved Yields, Leaf Photosynthesis, Ripening Time, and Net Returns of Tomato (Solanum lycopersicum Mill.) (2024)

Overuse of chemical fertilizers inthe intensive greenhouse tomatocultivation system has limited the increase of plant production. Nowadays,seaweed extract has been gradually applied in agriculture as an effectiveway to achieve a higher yield of crops, but its effects on tomatocultivation have not been fully explored. In this study, a greenhouseexperiment was conducted in Shandong province of China with a novelseaweed extract (SES) originated from Sargassum horneri, to investigate the effects of different doses of SES (0, 30, 60,and 90 kg hm^–2) on yields, quality, ripening time,and net returns of tomato. The results indicated that the applicationof SES significantly increased tomato yield by 4.6–6.9% comparedto the control, which is attributed to the improved photosyntheticcapacity of tomato leaves. The yields of tomato increased first andthen decreased with increasing dosage of SES, and SES applied at thedose of 60 kg hm^–2 achieved the highest tomato yield.Compared to the control, SES at 60 and 90 kg hm^–2 significantly increased the hardness of tomato by 10.2 and 19.8%,respectively, and this can help to reduce losses during transportationand storage. Moreover, SES shortened the ripening time of tomato,and the coincidence between tomato harvest and sale price peak achieveda high net return.

2.1. Effects of Different Amounts of SES on SingleHarvest and Total Yield of Tomato

Tomato yields were obviouslyaffected by the amount of SES (Table 1). Compared to CK, SES30, SES60, and SES90 significantlyincreased the total yields of tomato by 4.6, 6.9, and 4.7%, respectively.Our results were consistent with the report described in previousstudies that seaweed extracts improved the yield of tomato,^10,17,30 but the increased yield was relativelylower than that reported by Crouch and van Staden.³⁰ The reason is that the long history for continuous growingof tomato with high nutrients input made it hard for yield improvementand the difference in application method of seaweed extract (foliaror soil application) had different yield improvement effect.³⁰ The increase of yield in the SES-treated plantcan be associated with the hormonal substances in SES, especiallycytokinin,¹⁰ which can promote the mobilizationof nutrients and trigger fruit set. Crouch¹³ also noted that seaweed extracts increased the root length of tomato,improved the uptake of nutrients, and then boosted the yield.

Considering the continuous harvest character of tomato,tomatoyields on every single harvest were also compared. The first harvestof tomato was on 14 January 2018, and SES30, SES60, and SES90 increasedthe yield by 82.1, 104.6, and 131.6% compared to CK treatment, respectively(Table 1). SES30, SES60,and SES90 treatments also significantly increased the second harvestyield of tomato by 43.8, 60.0, and 67.8% compared to CK treatment,respectively. On the third harvest, no significant difference wasobserved between the yield of SES90 treatment and CK treatment. Buton the fourth, fifth, and sixth harvests, tomato yields under SES30,SES60, and SES90 treatment were significantly reduced by 21.2–27.5,13.1–24.2, and 23.8–31.3% compared to CK treatment,respectively. The increased yield in the early harvest stages indicatedthat the application of SES shortened the fruit-ripening time (daysfrom anthesis to ripening) of tomato.³¹ The photos taken on 21 January 2018 further confirmed the resultsas more fully ripe red tomatoes existed on the plants applied withSES (Figure ​Figure11). Seaweedextracts contain cytokinins,^23,24 auxins,²⁵ and ABA-like growth substances¹⁰ and these hormonal substances have been shown to have astimulatory effect on plant growth and fruit maturity.²⁶⁻²⁹ We speculated that the precocity of tomato affected by SES may berelated to its capacity to trigger early flowing and fruit set,¹⁰ and then shortened the fruit-ripening time oftomato.

2.2. Effects of Different Amountsof SES on theEconomic Benefits of Tomato

The unit price of tomatoes isaffected by market factors, and this means that tomato will have disparateprofit due to the sale prices at different harvest times. In the presentstudy, the tomato harvest period lasted 42 days and across China’sSpring Festival. In China, the harvest time that is near the SpringFestival can get a relative higher price. The price of tomato fluctuatesbetween 0.62 and 1.11 $ kg^–1 according to the localsale price (Table 2). The maximum and minimum sale price gap is 1.8 times. In addition,the sale price of tomato in the early harvest stage was higher thanthat in the last three harvest stages. Eventually, the total profitsin SES30, SES60, and SES90 treatments were 10.1, 13.6, and 9.9 higherthan that in CK treatment, which means that the application of SEScan be a reliable means to achieve more benefits when cultivated inautumn and harvested during the Spring Festival.

2.3. Effects of SES Amountson SPAD, ChlorophyllContent, and Photosynthetic Characteristics of Tomato Leaves

The SPAD values were considerably affected by the application ofSES. Leaf SPADs in SES30, SES60, and SES90 treatment were significantlyincreased by 9.6, 8.5, and 9.5% compared to CK treatment, respectively(Table 3). The SPADvalue has a good correlation with chlorophyll content, and the chlorophyllcontent in SES30, SES60, and SES90 treatments was significantly increasedby 25.3, 18.9, and 16.6% compared to CK treatment, respectively. Numerousstudies also confirmed that leaf chlorophyll content positively increasedwith the application of seaweed extract,³²⁻³⁴ which preciselycoincided with our results. Blunden³⁵ foundthat the application of seaweed extract had a higher chlorophyll contentthan unapplied treatments, which might be attributed to the reductionin chlorophyll degradation caused by betaines in the seaweed extract.Besides, some researchers found that the application of seaweed increasedthe leaf surface area.²⁷ Nevertheless,there was no significant difference in both SPAD value and chlorophyllcontent between the treatments when applied with different amountsof SES.

Photosynthesis is the basis for crops to capture solarenergy andaccumulate nutrients. The photosynthetic capacity of leaves directlydetermines the level of plant productivity. In the present study,Pn in SES30, SES60, and SES90 treatments was significantly increasedby 17.5, 31.1, and 31.7% compared to CK treatment, respectively (Table 3). This may acceleratethe accumulation of nutrients in plants, thereby promoting the maturationand increasing the yield of tomatoes. Moreover, Pn has been widelyused as an indicator to estimate plant senescence, and the improvementof Pn in SES30, SES60, and SES90 indicated that the application ofSES delayed the leaf senescence of tomato. Gs of SES30, SES60, andSES90 was significantly increased by 23.0, 26.2, and 31.3% comparedto CK treatment, respectively, which means that SES can boost thegas exchange in tomato leaves. Moreover, Ci in CK acquired the highestsince more CO₂ is needed as the raw material in the treatmentwith high Pn. But there was no evidence that the SES application hasa significant effect on Tr in leaves.

2.4. Effectsof SES Amounts on Soil Physical/ChemicalProperties and Nutrient Supply Intensity

In actual greenhouseproduction, available soil nutrient contents were extremely higherowing to the habitually excessive soluble fertilizer input for higheryield.²⁻⁴ In this work, the average content of NO₃^–, available P, and available K of soil also reacheda very high level (more than 40, 90, and 430 mg kg^–1, respectively) after all of the tomatoes were harvested (Table 4). Previous papersreported that several seaweeds contained high ratios of elements likeCa, P, and K.³⁶ Although the K and ashcontents of the SES were up to 6.6 and 30.2%, respectively, no obviousdifference was observed in the NO₃^– content,NH₄⁺ content, available P, and available K ofsoil among all of the treatments (Table 4), which is precisely consistent with theconcept of biostimulants defined by European Biostimulant IndustryCouncil (EBIC): “Biostimulants operate through different mechanismsthan fertilizers, regardless of the presence of nutrients in the products”.¹¹ Under the condition of such fertile soil, theyield of tomatoes was markedly increased by 4.6–6.9% with theapplication of SES, providing an environment-friendly way for cropcultivation in greenhouse. In the future, whether the amount of fertilizercan be reduced by adding SES while maintaining the gain yield is worthto be validated.

Soil EC values in SES30, SES60, and SES90 treatmentswere significantlydecreased by 16.3, 25.3, and 26.0% compared to CK treatment (Table 4). The greater theEC value, the higher the content of soluble salts.^37,38 The decreased EC value in SES30, SES60, and SES90 treatments indicatedthat SES can reduce the leaching or runoff of nutrients into the environment.The decreased EC value may be attributed to the precipitate/chelatecharacter of SES with some alkaline ions in the soil and the existenceof polyuronides in SES with gelling, chelating, and hydrophilic propertiessuch as alginates and fucoidans.¹⁵

2.5. Effects of the Amount of SES on Tomato Quality

Qualityis an important factor for sustaining higher unit priceof tomato. Tomato quality includes appearance character such as singlefruit weight and hardness, as well as intrinsic aspect representedby nutrient content and mouthfeel. In the present study, althoughsingle tomato weight, soluble solids, titratable acid, and vitaminC content of tomato showed no significant difference in all of thetreatments, the soluble sugar content in tomato was markedly increasedwith the application of SES (Table 5), thereby increasing the sugar/acid ratio and achievinga better flavor and taste. But there was no significant differenceamong the treatments with different amounts of SES.

Moreover, the hardness of tomatowas markedly increased with theincreasing dose of SES (Table 5). The hardness of tomato in SES60 and SES90 was 10.2 and19.8% higher than that in CK treatment, respectively. Therefore, theapplication of SES can reduce the loss during transportation and storageby increasing the hardness of the tomato. Stasio³⁸ noted that seaweed extracts increased the Ca²⁺ content of tomato by more than 20%, which helps to explain the mechanismof SES for the increase of hardness.

2.6. ChemicalStructure and Composition of SES

The effectiveness of seaweedextracts was markedly influenced bytheir sources, structure, and composition.³⁹ Therefore, a thorough understanding of SES by characterization isnecessary for their efficient utilization. For instance, Stasio³⁸ confirmed via the gas chromatography-mass spectrometryanalysis that the seaweed extract was rich in bioactive compounds,which was possibly beneficial to the growth and stress adaptationof tomato. Khan¹⁰ summarized several chemicalanalyses of seaweeds and seaweed extracts and revealed the presenceof a wide variety of plant growth-promoting substances such as auxins,cytokinins, and betaines. Despite evidence from the literature forthe role/effects of these substances as single molecules on plantgrowth and stress protection, the diverse and complex nature of seaweedextracts makes it difficult to establish a univocal cause of the variousbiostimulant effects observed. Therefore, there is a need for an in-depthanalysis of the functional specificities.

SES contains 29.2%of alginic acid, 14.1% of crude protein, 10.9% of mannitol, 30.2%of ash, 6.6% of potassium, 0.024% of iodine, as well as a varietyof plant hormones (the date was provided by Worldfull AgriculturalTechnology Co., Ltd., Shandong, China). Furthermore, the analysisof size exclusion chromatography provided a clear insight into themolecular weight (MW) distribution of SES with a range of 179–11 949Da (Figure ​Figure22). Theproportion of the relatively low MW fraction (MW < 5 kDa) was upto 87.8%, and the higher MW (MW > 5 kDa) was only 12.2%. Therefore,SES was a biostimulant with lower MW than other seaweed extracts,⁴⁰ which can be easily absorbed by the tomato root.Detailed structural information and the relative distribution of mainstructures were obtained by ¹H NMR spectroscopy (Figure ​Figure33). SES exhibiteda stronger predominance of aromatic protons (δ(¹H)= 9.5–6.5 ppm) than alkyl protons (δ(¹H) =1.9–0.5 ppm). The proton content (δ(¹H) =4.9–3.1 ppm) on C atoms directly bonded to N, O, or carbohydratesis up to 57.87% (Table S1). The signalsat 4.5–3.2 ppm also can be the source of H in methylene groupsand/or aminomethine groups [−CH(NH−)]. The signals at6.5–6.0 ppm can be attributed to double bonds. Although manyof the various chemical components of SES and their modes of actionremain unknown, it is plausible that these components exhibit synergisticactivity.

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Figure 2

Size exclusion chromatography of SES.

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Figure 3

Solid-state ¹H nuclear magnetic resonance spectroscopyof SES.

4.1. Experimental Sites and Materials

The experimental siteis located at Fangcun town (117°20′37″E, 35°97′03″ N), Shandong Province, China, thelargest professional production and wholesale base for tomatoes. Itbelongs to the warm-temperature semihumid monsoon climate, with anannual mean temperature of 13 °C and precipitation of700 mm. The greenhouse has 12 years cropping history of continuousgrowing tomato two seasons per year. The rectangular greenhouses are70 m long and 10.5 m wide, with one side wall (3.6 m high) and twoend walls constructed from soil and brick (Figure S1). The main properties of top-layer soil (0–20 cm)at the experimental site in 2017 before tomato planting were: pH,6.65 (2.5:1, the ratio of water to soil), soil total N concentration,1.83 g kg^–1; organic matter concentration, 21.50g kg^–1; NO₃^––Nconcentration, 30.73 mg kg^–1; NH₄⁺–N concentration, 10.25 mg kg^–1;available P concentration; 25.71 mg kg^–1; and availableK concentration, 180.58 mg kg^–1, respectively.

Tomato (Solanum lycopersicum Mill,Jinpeng 11), a member of the pink tomato varieties, was selected asthe testing crop. The SES extracted from S. horneri was freely provided by Worldfull Agricultural Technology Co., Ltd.(Yantai, Shandong, China), and it contains 29.2% of alginic acid,14.08% of crude protein, 10.94% of mannitol, 30.16% of ash, 6.63%of potassium, 0.024% of iodine, as well as a variety of plant hormones.The extraction and production processes of SES by the company arepresented in Figure S2. The water-solublefertilizer (N–P₂O₅–K₂O: 20–20–20) applied in the experiment as the nutrientsource of tomato was provided by Kingenta Ecological Engineering Co.Ltd. (Linshu, Shandong, China).

4.2. ExperimentalDesign

A randomizedexperiment with three replicates was conducted on 20 August 2017 inplots considering four treatments: control without SES application(CK), applied SES at the dose of 30 kg hm^–2 (SES30),applied SES at the dose of 60 kg hm^–2 (SES60), andapplied SES at the dose of 90 kg hm^–2 (SES90). Everyplot was 8.5 m long and 1.8 m wide with an area of 15.3 m². Soil ridges (30 cm height, 30 cm width) were built to ensure independentirrigation and drainage between adjacent plots. The tomato was transplantedat the four-leaf stage with a density of 30 plants plot^–1 (90 cm between rows and 30 cm between plants).

Based on thelocal planting habits, all of the treatments were applied with organicfertilizer (70% rice hull and 30% chicken manure uniformly blendedin advance, 150 t hm^–2) as a base fertilizer 20days before the transplantation of tomato seedlings. Fertilizationand irrigation were carried out simultaneously during the growth oftomato. The water-soluble fertilizer (N–P₂O₅–K₂O: 20–20–20, 195 kg hm^–2 time^–1) was dissolved in 400 kgof water at a pool (Figure S3) and irrigatedby pipes every 15 days (achieve 90% of the field water-holding capacity,eight times in total). For the application of SES, weighed SES dependenton different treatments was dissolved in the pool and applied alongwith the water-soluble fertilizer on September 27, 2017, October 26,2017, November 26, 2017, and December 25, 2017. All replications withineach treatment were conducted according to the local agronomic practices,receiving identical irrigation, pruning, and control of insects andweeds.

4.3. Harvest

The harvesting process oftomatoes lasted from January 14, 2018 to February 18, 2018 for every7 days (six times in total). Tomatoes in each treatment were individuallyweighed, counted, and measured. Plant samples were derived from thetomatoes harvested in the third harvest stage, and the soil sampleswere collected after all of the tomatoes were harvested.

4.4. Soil and Plant Sampling and Measurement

Leaf SPAD valuewas estimated with a chlorophyll meter (SPAD–502,Minolta Co., Japan) on 14 January 2018. The photosynthesis parametersof leaves, including net photosynthetic rate (Pn), stomatal conductance(Gs), intercellular CO₂ concentration (Ci), and transpiration(Tr), were measured on 14 January 2018 between 9:00 to 11:00 h bya portable photosynthetic meter (Li-6400XT, LI-COR Co.). Subsequently,the leaves were taken off and brought back to the laboratory. Thechlorophyll of leaves was dissolved in acetone (80%)⁴¹ and measured by an ultraviolet spectrophotometer (UV-2700,Shimadzu Co., Japan).

Soil EC was measured by a conductivitymeter (DDS-11A, Inesa Co., China). Soil NO₃^––N and NH₄⁺–N concentrationswere extracted by 0.01 M CaCl₂⁴² and analyzed by an AA3 Auto-analyzer (AA3-A001-02E, Bran-LuebbeCo., Germany). Soil total N was measured by the Kjeldahl N determinationmethod (Douglas et al., 1980).⁴³ The availableP concentration in soil was extracted by 0.5 M NaHCO₃ atpH 8.5⁴⁴ and analyzed by a Discrete Auto-analyzer(Smart Chem 200, Alliance Co., France). The available K concentrationin soil was extracted by 1 M CH₃COONH₄ at pH7⁴⁵ and analyzed by a flame photometer(Model 410, Sherwood Co., England).

Tomato samples were hom*ogeneouslysmashed with a juice machineat room temperature. Vitamin C (Vc) content was measured by the colorimetricmethod.⁴⁶ The concentration of solublesolids was measured using a digital refractometer (RX-5000α,Atago Co., Japan).⁴⁷ The titratable aciditywas determined by titrating with 0.1 N NaOH of pH 8.2.⁴⁸ Soluble sugar content in tomato juice was determinedusing the anthrone reagent method.⁴⁹

Size exclusion chromatography was performed on solutions of theSES using a Sephadex G-100 medium gel (Code No. 17-0060-02 PharmaciaBiotech AB). Solid-state ¹H NMR spectroscopy was performedusing an Avance 600 MHz (Bruker, Karlsruhe Co., Germany) spectrometer.

4.5. Calculation of Every Single Profit and NetReturn

4.6. Statistical Analyses

The responseparameters were subjected to analysis of variance (ANOVA) and meanseparation test using the Statistical Analysis System 9.2 (2010, SASInstitute, Cary, NC). Mean and standard error values were assessedto assemble graphs using the SigmaPlot software 10 (MMIV Systat Software,Inc., San Jose, CA).

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