Next Article in Journal
A World of Gorse: Persistence of Ulex europaeus in Managed Landscapes
Next Article in Special Issue
Effects of Arbuscular Mycorrhizal Fungi on Yield, Biochemical Characteristics, and Elemental Composition of Garlic and Onion under Selenium Supply
Previous Article in Journal
Responses of Rice Growth to Day and Night Temperature and Relative Air Humidity—Dry Matter, Leaf Area, and Partitioning
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 8
Issue 11
10.3390/plants8110522
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Plant-Based Biostimulants Influence the Agronomical, Physiological, and Qualitative Responses of Baby Rocket Leaves under Diverse Nitrogen Conditions

by
Ida Di Mola
1,*,
Lucia Ottaiano
1,
Eugenio Cozzolino
2,
Mauro Senatore
1,
Maria Giordano
1,
Christophe El-Nakhel
1,
Adriana Sacco
3,
Youssef Rouphael
1,
Giuseppe Colla
4 and
Mauro Mori
1
1
Department of Agricultural Sciences, University of Naples Federico II, 80055 Portici, Italy
2
Council for Agricultural Research and Economics (CREA)—Research Center for Cereal and Industrial Crops, 81100 Caserta, Italy
3
Council National Research (CNR), 80055 Portici, Italy
4
Department of Agriculture and Forest Sciences, University of Tuscia, 01100 Viterbo, Italy
*
Author to whom correspondence should be addressed.
Plants 2019, 8(11), 522; https://doi.org/10.3390/plants8110522
Submission received: 18 October 2019 / Revised: 4 November 2019 / Accepted: 7 November 2019 / Published: 19 November 2019
(This article belongs to the Special Issue Factors Affecting Yield, Quality, Antioxidants, Mineral Composition and Residual Biomass Valorization of Vegetable Crops)
Browse Figures
Versions Notes

Abstract

:
Nitrogen is the primary technical means responsible for food production increase, but on the other hand, wise management is needed because its excessive use can have a negative impact on the environment and on green leafy vegetable quality, such as that rocket. Rocket has the characteristics of accumulating nitrate in leaves with possible impacts on human health. In order to overcome this issue, researchers are focusing their attention on the use of alternative means, such as plant biostimulant application. The scope of this study was to assess the effect of legume-derived protein hydrolysate(LDPH) and tropical plant extract(TPE), combined with various doses of nitrogen (0 kg ha−1 non-fertilized; N0); 60 kg ha−1 (sub-optimal; N1); 80 kg ha−1 (optimal; N2); and 100 kg ha−1 (supra-optimal; N3)), in order to reduce nitrogen use, boost yield, and enhance the chemical and nutritional value of leaves without significantly accumulating nitrate. Both vegetal-based plant biostimulants enhanced plant growth, boosted the marketable yield (especially at N0 and N1 levels, by 38.2% and 28.2%, respectively, compared to the non-treated control), and increased the SPAD (Soil Plant Analysis Development) index and leaf pigments content, such as chlorophyll and carotenoids, especially in treated-LDPH rocket. The plant-based biostimulants also produced a major amplification in lipophilic antioxidant activity (+ 48%) and total ascorbic acid content (average + 95.6%), especially at low nitrogen fertilization levels, and maintained nitrate content under the legal European Comission limits.

1. Introduction

In the last decades, world food demand has been increasing due to global population growth. In order to satisfy this concern, growers around the globe are intensifying food crop production by increasing the use of resources, in particular, fertilizers [1]. A large number of crops, including leafy vegetables, require large quantities of nitrogen to reach maximal productivity, notwithstanding that high nitrogen availability is not correlated with higher quality of produce. Conversely, excessive nitrogen fertilization can trigger superfluous vegetative growth, making plants prone to pathogen attacks [1]. Furthermore, uncurbed nitrogen presence usually induces nitrate accumulation in leafy vegetables to levels that exceeds the EU regulation limits [2,3]. Exorbitant nitrogen fertilizer rates can also have deleterious impacts on human health [4,5,6] and on the environment through nitrate leaching into water resources and greenhouse gas emissions, such as nitrous oxide [7]. In fact, after intake into the human body, nitrate can be converted into nitrite, and the latter can cause methemoglobinemia or be used to produce the cancer-causing compounds nitrosamine and nitrosamide [8,9].
Among leafy vegetables, rocket production for use in ready-to-eat salads is increasing in response to market demand. Rocket belongs to the Brassicaceae family and it is known for diverse plant metabolites such as polyphenols, ascorbic acid, and glucosinolates [10,11,12]; however, as is the case in other leafy vegetables, rocket is known as a nitrate hyper-accumulating species. Nevertheless, nitrate accumulation depends on nitrogen availability, but also on specific environmental conditions, such as low radiation, which reduces the nitrate reductase activity [13,14,15]. In order to overcome this issue, the scientific community is focusing its attention especially on the accurate management of nitrogen fertilization, also through the use of alternative methods, such as natural biostimulants, for stimulating early growth and yields.
Plant biostimulants are extracted from organic fresh substances accommodating bioactive compounds. Biostimulants mainly include minerals, humic compounds, vitamins, chitin/chitosan, amino acids, and poly- and oligosaccharides [16,17,18].
The mechanisms activated by biostimulants are still not completely known, and therefore they are under intensive investigations [19,20,21]. Biostimulants act either directly on plant metabolism and physiology or indirectly by enhancing soil-conditions [22] by affecting its microflora that can positively influence plant growth. Nonetheless these natural products modify root conformations and boost their development [16,23,24,25]. Based on the biostimulant composition and purpose of use, the application can be foliar or by irrigation [26]. Furthermore, plant biostimulants act differently on different species and/or cultivars of the same species, and their action is environmentally-, dosage-, and application time-dependent [26]. Such variability of effects can impede generalization.
Biostimulant use has been on the rise and their implementation is gaining popularity in sustainable agriculture. Utilization of these natural products triggers numerous physiological processes that stimulate plant growth and tolerance to abiotic stresses, but simultaneously reduce fertilizer application by improving plant nutrient use efficiency without collateral effects on yield and quality [26].
Our hypothesis is that plant-based biostimulant application can improve produce quality by enhancing the antioxidant content and leaf pigments and trigger plant performance by stimulating root growth. However, the abundance of available products in the market, such as fertilizers, growth regulators, and biostimulants, can negatively influence growers’ reasonable choices and applications, leading to disappointing outcomes [27,28]. In view of this approach, the purpose of the present study was to verify the potential of two vegetal-based biostimulants, combined with various doses of nitrogen, on plant growth parameters, yield, biochemical parameters, and chemical and nutritional value of baby rocket leaf grown under plastic tunnel conditions.

2. Results

2.1. Influence of N Fertilization Levels and Plant-Based Biostimulants on Yield and Plant Growth Parameters

The findings concerning total and single harvest marketable fresh yields of baby rocket leaf are reported in Table 1. A significant interaction between N levels (N) and biostimulant application (B) was observed for the three harvest dates as well as for total fresh yield. Irrespective of biostimulant application, the marketable fresh yield of rocket was positively affected by increasing N fertilization levels, reaching the higher value at N3 (100 kg N·ha−1) in all three harvests (Table 1) but progressively decreasing from the first to the third harvest.
In particular, at the first harvest, marketable yields of N2 and N3 plants (optimal and supra-optimal levels of nitrogen) were similar, and no significant differences between treated and control plants were recorded (Table 1). Contrarily, in the second and third harvest dates, at optimal and supra-optimal levels of nitrogen, the plants sprayed with the two biostimulants exhibited higher fresh yield values than control plants, with no significant difference between legume-derived protein hydrolysates (LDPH) and tropical plant extract (TPE) (Table 1).
No significant interaction between N fertilization rates and biostimulant application was recorded for plant growth parameters: leaf area index (LAI), leaf succulence, and specific leaf weight (SLW) (Table 2). Particularly, the plant growth parameters were highly influenced by nitrogen fertilization levels and to a lesser extent by the biostimulant application (Table 2).
When averaged over biostimulant application, the leaf area index and leaf succulence showed a similar trend to marketable fresh yield with increasing nitrogen levels from 0 to 100 kg ha−1. Moreover, from the first to the third harvest dates, the differences between the N treatments were more pronounced. The highest values of SLW were recorded in untreated rocket plants.
Irrespective of N fertilization, the foliar application of plant-based biostimulants (i.e., LDPH and TPE) enhanced the leaf surface expansion by 66% and 80%, in the second and third harvest dates, respectively, in comparison to control, with no significant differences between the two commercial products. Additionally, for leaf succulence and SLW, no differences between the two biostimulants were recorded; the increase in succulence over control treatment was 5.6% and 4.1% in the second and last harvest, respectively (Table 2).

2.2. Influence of N Fertilization Levels and Plant-Based Biostimulants on SPAD index and Leaf Colorimetry

Soil Plant Analysis Development (SPAD) index was significantly affected by both factors (nitrogen-N and biostimulant application-B), but without significant interaction N × B (Table 3). When averaged over biostimulant application, the increasing nitrogen levels positively affected the SPAD index, with the highest values recorded in the N3 fertilization level, irrespective of the harvest date (Table 3). Nitrogen doses determined an increase of 16.0%, 27.0%, and 33.9% (average of the three harvests) in N1, N2, and N3 plants, respectively, over non-fertilized plants. Moreover, irrespective of nitrogen fertilization, the foliar application of biostimulants also highlighted an increase of SPAD index (+ 9.3% mean value of the two biostimulants in the three harvest dates) in comparison to untreated plants, but with differences between the two commercial biostimulants only at the third harvest, where the LDPH exhibited the best performance.
Among the physical properties that may orient consumer choices is the produce aspect, particularly the color [29]. In our study, the leaf colorimetric Commission internationale de l’éclairage (CIELAB) parameters were only affected by fertilization levels, with no significant effect of biostimulant application nor N × B interaction (Table 4). Notably, augmenting N fertilization levels from 0 to 100 kg ha−1 decreased a* values, therefore increasing the green intensity, and increased b* values (Table 4). Both leaf colorimetric traits (a* and b*) decreased from the first to the last harvest. For both parameters, the differences between the three fertilization levels were stronger in the second and especially in the third harvest.

2.3. Influence of N Fertilization Levels and Plant-Based Biostimulants on Nitrate Accumulation and Biochemical Parameters

Nitrate content, total chlorophyll, chlorophyll a and b, and carotenoids were affected by both nitrogen levels (N) and biostimulant application (B), but not by their interaction (Table 5). Nitrate content is essential for leafy vegetable quality. In the present paper, nitrate accumulation in leaves increased linearly when N fertilization levels increased from 0 to 100 kg ha−1, with the highest value set in N3 fertilized plants.
Additionally, chlorophyllous pigments, particularly total chlorophyll, chlorophyll a and b, and carotenoid content were positively influenced by nitrogen level increases, especially under N2 and N3 regimens (Table 5). Furthermore, when averaged over N fertilization, the foliar application of biostimulants elicited an increase in chlorophyll and carotenoid content with the highest value recorded in plants treated with the LDPH product (Table 5).

2.4. Influence of N Fertilization Levels and Plant-Based Biostimulants on Lipophilic Antioxidant Activity and Total Ascorbic Acid

The highest values of lipophilic antioxidant activity (LAA) were recorded in biostimulant-treated rocket at both N0 and N1 treatments, with no significant difference between the two commercial biostimulants (Figure 1). On the other hand, the marked effect of vegetal-based biostimulants on total ascorbic acid (TAA) was recorded in non-fertilized treatments. Particularly, foliar application of TPE and LDPH elicited a significant increase (112.0% and 79.2%, respectively) of TAA content compared to untreated rocket plants (Figure 2).

3. Discussion

The use of natural plant biostimulants including LDPH and TPE have been proven, when applied at low concentrations, to boost plant growth, yield, and quality, and to increase tolerance to abiotic stressors [30,31]. In the current study, the stimulation effect of the two plant-based biostimulants was more evident in the non-fertilized (N0) and sub-optimal (N1) treatments. Particularly, the biostimulant application led to significant yield increases in rocket sprayed with LDPH and TPE in comparison to untreated plants, (by 38.2% and 28.2% for N0 and N1 treatments, respectively) with no significant differences between the two commercial products. Positive effects of biostimulant application (TPE and LDPH) on fresh yield of rocket were also reported by Caruso et al. [30] and by several authors on a wide range of fruit and leafy vegetables grown under greenhouse conditions, such as baby leaf lettuce [31], tomato [32], zucchini squash [33], and spinach [34]. Similar to the effects on rocket yield, the increase in LAI recorded in the present work due to biostimulant application was more pronounced than those reported by Rouphael et al. [34] and Caruso et al. [30] on spinach and perennial wall rocket, showing a species-specific response [35], especially when the same two commercial plant biostimulants were tested. Therefore, our findings highlight the need to investigate further this issue for elucidating the physiological and molecular mechanism(s) behind these stimulation effects. In addition, several authors have pointed out that biostimulant application can activate a transduction signal pathway through elicitation of endogenous phytohormone synthesis (i.e., auxin- and gibberellin-like activities), thus leading to a higher yield [36,37]. Moreover, the stimulation of LAI and succulence could be due to the increase of root biomass, volume, length, and higher branching triggered by biostimulant application, which enhanced nutrient uptake/translocation/assimilation, helping in a major nitrogen uptake efficiency and utilization, and consequently higher agronomical performance [33,34,38,39].
The leaf SPAD measurements recorded in LDPH- and TPE-treated plants were significantly higher than in untreated rocket plants. Our data obtained on the SPAD index are consistent with those mentioned for many leafy vegetable species, such as lettuce, perennial wall rocket, jute, and spinach [30,34,40,41]. Two different mechanisms could have caused the higher SPAD values: (i) enhanced N uptake efficiency, and (ii) limited chlorophyll degradation and leaf senescence [36,42,43]. Indeed, this index is considered a major indicator of green pigment biosynthesis efficiency, and thus improved crop outcomes.
Nitrate content is essential for the quality of fresh leafy vegetables, in particular rocket, which is considered a hyper-accumulator species. In the current study, nitrate content in all treatments was below the European Union upper limits for safe rocket marketing EU No 1258/2011 of 6000 to 7000 mg NO3− kg−1 for wild and salad rocket (depending on growing season and cultivation conditions). Moreover, irrespective of nitrogen fertilization levels, the foliar application of biostimulants determined a significant increase of nitrate content (avg. 94.0%) in rocket leaves sprayed with LDPH and TPE, without violation of EU nitrate limits. The higher accumulation of nitrate in biostimulant-treated plants has been observed previously by several authors [44,45], probably due to a more developed root system (in terms of biomass and root branching), which may have increased nitrate uptake and translocation to the shoots.
The different changes induced by biostimulant application on agronomical traits (yield and LAI) may be reflected at the biochemical level. This was the case in the current experiment, since the beneficial response of plant biostimulant application, in particular LDPH, on chlorophyllous pigment has been recorded also in baby lettuce, eggplant, and corn [40,46,47,48], probably due to amino acid abundance in the LDPH-treated plants, which help to enhance chlorophyll pigment content and augment net photosynthesis rate.
Leafy vegetables are considered an important sources of antioxidant molecules. In the current study, lipophilic antioxidant activity (LAA) and total ascorbic acid (TAA) were significantly affected by N × B interaction. The importance of antioxidant activity, as a functional quality parameter of food, is related to the beneficial effects of antioxidant molecules (hydrophilic and lipophilic) on human health, due to their role in delaying or/inhibiting oxidative damage, hence evading a broad range of diseases [49,50,51,52,53]. Irrespective of biostimulant application, the rocket plants in the optimal (N2) and supra-optimal (N3) treatments were characterized by the lowest quality traits (i.e., lowest LAA). Similar to our findings, Wang and co-workers [54] reported that a high level of nitrogen can result in damage in terms of commercial, nutritional, and functional quality of fruit and leafy vegetables. Furthermore, it is notable that stress conditions, such as low nitrogen input, may stimulate the antioxidant system leading to an increase in antioxidant molecule production in plants [39].
Concerning the effects of plant biostimulants on leaf quality traits, the plant-based biostimulants also determined a major amplification in LAA (+ 48%) and TAA content (+ 95.6%), especially at low nitrogen fertilization levels. These findings are in line with our previous research on baby leaf lettuce sprayed with three different biostimulants at four different levels of nitrogen, in which we found an LAA increase in non-fertilized and low-fertilized regimens [30]. The positive effects of plant biostimulant application on synthesis of antioxidant molecules can be attributed to two putative mechanisms: (1) activation of key enzymes activation that are involved in cell antioxidant homeostasis, and (2) an increase of macro and micronutrients assimilation in plants treated with biostimulants that can play a part in amino acid synthesis such as phenylalanine and tyrosine [55,56].

4. Materials and Methods

4.1. Growing Conditions, Rocket Cultivar, and Experimental Design

During the 2018 spring season, an experiment was conducted at the experimental site of “Gussone Park” of the University of Naples-Federico II (40°48.870’ N; 14°20.821’ E; 70 m a.s.l.; in Portici, Naples, Southern Italy).
The plastic tunnel was open on both sides and covered on top by polyethylene. The rocket plants were cultivated in large lysimeters (0.70 m diameter and 0.60 m depth). The soil was sandy (69.1% coarse sand, 21.9% fine sand, 4.5% silt, and 4.5% clay) with a pH of 6.6, an electrical conductivity of 0.68 dS m−1, an organic matter of 2.6% (w:w), a total N of 1.1 g kg−1 (Kjeldhal method), 127.2 mg kg−1 of P (Olsen method), and 471.8 mg kg−1 of K (Tetraphenylborate method).
The baby rocket leaf (Diplotaxis erucoides L.) cultivar ‘Reset’ (Maraldi Sementi S.r.l., Cesena, Italy) was the tested crop. This cultivar is widely used by leafy vegetable growers due to its good adaptability to different environmental conditions.
The experimental design was a factorial combination of four fertilization levels of nitrogen (N) and three treatments of biostimulants (B) (the untreated control did not receive any product). The N levels were: 0 kg ha−1 (non-fertilized control—N0); 60 kg ha−1 (N1—sub-optimal level); 80 kg ha−1 (N2—optimal level); and 100 kg ha−1 (N3—supra-optimal level). The biostimulants used were an untreated control, tropical plant extract (TPE), and legume-derived protein hydrolysate (LDPH). Treatments were arranged in a randomized complete-block design and replicated three times each.

4.2. Nitrogen Fertilization Management and Biostimulant Characteristics and Application

A density of 3500 plants per square meter (about 0.8 g m−2 of seeds) was adopted to hand seed baby rocket leaf on 16 April 2018. Calcium nitrate (26% N) was the nitrogen source; it was distributed as follows: (i) first treatment 50% of the total amount applied ten days after sowing; (ii) second treatment 25% after the first harvest; (iii) third treatment 25% after the second harvest. During the growing cycle, lysimeters were irrigated with an amount of water corresponding to the complete replacement of water lost by evapotranspiration.
The two commercial biostimulants, legume-derived protein hydrolysate-LDPH (Trainer®) and tropical plant extract-TPE (Auxym®) were supplied by Italpollina S.p.a. (Rivoli Veronese, Italy). An enzymatic hydrolysis process was used to produce the LDPH that contained free amino acids and peptides, carbohydrates, and mineral nutrients with the following percentages of 75%, 22%, and 3%, respectively [57,58]. A fermentation process of tropical plants such as hibiscus was used to produce the TPE biostimulant, which contained free amino acids/peptides, carbohydrates, mineral nutrients, vitamins, and phytohormones with the following percentages of 54%, 17%, 23%, 6%, and 0.22%, respectively, as reported in detail by Rouphael et al. [59] and Caruso et al. [60].
The treatments with biostimulants started 21 days after the sowing; a total of four applications were applied on a weekly basis. A solution containing 3 mL L−1 of LDPH and 2 mL L−1 of TPE-based biostimulant was used to spray rocket leaf plants, and control plants were sprayed with water.

4.3. Morphological Parameters and Leaf Colorimetry

Rocket plants were harvested at three different dates during the growing period (on 14 May, 30 May, and 13 June). A sample area of 0.40 × 0.40 m was harvested from each lysimeter to avoid the edge effect. At all harvest dates, leaf area of rocket was measured with an electronic leaf area meter (Li-Cor3000, Li-Cor, Lincoln, NE, USA) and then the leaf area index (LAI) was calculated based on the crop density. The marketable yield was determined and expressed in tons per hectare; a sample was oven dried at 70 °C until reaching a steady weight; then samples of dried leaves were used for determining leaf succulence (mg water cm−2), specific leaf weight (mg dw cm−2), and nitrate content determination.
The color space parameters, L*, a*, and b*, were determined by a Minolta CR-300 Chroma Meter (Minolta Camera Co. Ltd., Osaka, Japan) by measuring on the upper side of ten leaves per replicate. On ten undamaged and fully developed leaves, the Soil Plant Development Analysis (SPAD) index was also measured using a portable chlorophyll meter (SPAD-502, Konica Minolta, Tokyo, Japan). After harvest, leaf samples from all treatments were frozen in liquid nitrogen and then lyophilized with the means of a Crist, Alpha 1-4 (Osterode, Germany), to be stored at −80 °C for future chemical analysis.

4.4. Lipophilic Antioxidant Activity and Total Ascorbic Acid Analysis

The lipophylic antioxidant activity was determined on 200 mg of freeze-dried material using methanol. It was assessed spectrophotometrically (Hach DR 2000, Hach Co., Loveland, CO, USA) according to the methods of Re et al. [61], and the absorbance of the solution was measured at 734 nm. Lipophylic antioxidant activity was expressed as mmol of Trolox per 100 g of dry weight (dw) [62].
The total ascorbic acid (TAA) was also assessed spectrophotometrically according to the protocol stated by Kampfenkel et al. [63]. The solution absorbance was measured at 525 nm.

4.5. Chlorophyll, Carotenoid, and Nitrate Analysis

Rocket leaf chlorophyll and carotenoid content was also measured by means of a spectrophotometer after the extraction with ammoniacal acetone according to the method described by Wellburn [64], whereas the nitrate content was assessed based on the protocol of Sah [65]. Solution absorbances were measured at 662 and 647 for chlorophyll a and b, at 470 nm for carotenoids, and at 550 nm for nitrate. Total chlorophyll, chlorophyll a and b, and carotenoids were expressed as mg g−1 fw, whereas nitrate content was expressed in mg kg−1 fw.

4.6. Statistical Processing

Morphometric, physiological, and qualitative data were subjected to variance analysis (two-way ANOVA) using SPSS 21 for Windows 2007. In case of interaction between the two tested factors, mean comparisons were made between the N rate × biostimulant application, and letters separated by Duncan’s test (significance level 0.05) were used to denote comparisons between these one-way means. On the other hand, when non-significant interaction was recorded between the two tested factors, the letters separated by Duncan’s test (significance level 0.05) were used to denote statistical differences between the main effects.

5. Conclusions

Fertilizers, in particular nitrogen, are a crucial part of agriculture, being a tool farmers use to enhance yield and guarantee continuous productivity all year long [66,67]. Simultaneously, their synthetic/chemical characteristics can influence human health and ecosystems. Therefore, finding sustainable means of production, such as use of plant biostimulants to boost yield and quality under both optimal and sub-optimal conditions, is an urgent need for horticulturists and scientists. In this study, the foliar application of vegetal-based biostimulants stimulated plant growth and boosted the marketable yield. The better agronomical performance was attributed to an improved physiological (higher SPAD index) and biochemical (higher chlorophyll and carotenoids content) status of plants, especially with LDPH use. Interestingly, foliar application of biostimulants enhanced the functional quality of baby rocket leaf in terms of lipophilic antioxidant activity and total ascorbic acid content, especially under a sub-optimal nitrogen regimen. The results displayed in the current study will contribute to understanding the biostimulant effects behind the variation in yield and quality of rocket and will assist the leafy vegetable industry in identifying optimum biostimulant–nitrogen fertilization regimens for achieving higher productivity and functional quality.

Author Contributions

Conceptualization, M.M.; methodology, M.S., I.D.M., and E.C.; software, L.O., A.S., and M.S.; validation, M.M., I.D.M., E.C., and L.O.; formal analysis, M.G. and L.O.; investigation, I.D.M.; resources, M.M.; data curation, I.D.M. and L.O.; writing—original draft preparation, I.D.M.; writing—review and editing, Y.R., C.E.-N., and G.C.; visualization, M.G. and G.C.; supervision, Y.R., G.C., and M.M.; project administration, M.M.; funding acquisition, M.M.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Liebman, M.; Davis, A.S. Integration of soil, crop and weed management in low-external-input farming systems. Weed Res. 2000, 40, 27–47. [Google Scholar] [CrossRef]
  2. Alberici, A.; Quattrini, E.; Penati, M.; Martinetti, L.; Gallina, P.M.; Ferrante, A.; Schiavi, M. Effect of the reduction of nutrient solution concentration on leafy vegetables quality grown in floating system. Acta Hortic. 2008, 801, 1167–1176. [Google Scholar] [CrossRef]
  3. Cavaiuolo, M.; Ferrante, A. Nitrates and glucosinolates as strong determinants of the nutritional quality in rocket leafy salads. Nutrients 2014, 14, 1519–1538. [Google Scholar] [CrossRef] [PubMed]
  4. Luo, J.K.; Sun, S.B.; Jia, L.J.; Chen, W.; Shen, Q. The mechanism of nitrate accumulation in pakchoi [Brassica campestris L. ssp. Chinensis L.]. Plant Soil 2006, 282, 291–300. [Google Scholar] [CrossRef]
  5. Parks, S.E.; Huett, D.O.; Campbell, L.C.; Spohr, L.J. Nitrate and nitrite in Australian leafy vegetables. Aust. J. Agric. Res. 2008, 59, 632–638. [Google Scholar] [CrossRef]
  6. Cavaiuolo, M.; Cocetta, G.; Spadafora, N.D.; Müller, C.T.; Rogers, H.J.; Ferrante, A. Gene expression analysis of rocket salad under pre-harvest and postharvest stresses: A transcriptomic resource for Diplotaxis tenuifolia. PLoS ONE 2017, 12, e0178119. [Google Scholar] [CrossRef]
  7. Mattner, S.W.; Wite, D.; Riches, D.A.; Porter, I.J.; Arioli, T. The effect of kelp extract on seedling establishment of broccoli on contrasting soil types in southern Victoria, Australia. Biol. Agric. Hortic. 2013, 29, 258–270. [Google Scholar] [CrossRef]
  8. Gangolli, S.D.; Van den Brandt, P.A.; Feron, V.J.; Jan-Zowsky, C.; Koeman, J.H.; Speijers, G.J.A.; Spiegelhalder, B.; Walker, R.; Winshnok, J.S. Nitrate, nitrite and N-nitroso compounds. Eur. J. Pharmacol. Environ. Toxicol. Pharmacol. 1994, 292, 1–38. [Google Scholar] [CrossRef]
  9. Walker, R. Nitrate, nitrite and N-nitroso compounds: A review of the occurrence in food and diet and the toxicological implications. Food Addit. Cont. 2000, 7, 717–768. [Google Scholar] [CrossRef]
  10. Lazzeri, L.; Baruzzi, G.; Malaguti, L.; Antoniacci, L. Replacing methyl bromide in annual strawberry production with glucosinolate containing green manure crops. Pest. Manag. Sci. 2003, 59, 983–990. [Google Scholar] [CrossRef]
  11. Kim, J.S.; Chung, T.Y.; King, G.J.; Jin, M.; Yang, T.J.; Jin, Y.M.; Kim, H.I.; Park, B.S. A sequence-tagged linkage map of Brassica rapa. Genetics 2006, 174, 29–39. [Google Scholar] [CrossRef] [PubMed]
  12. Martínez-Sánchez, A.; Gil-Izquierdo, A.; Gil, M.I.; Ferreres, F. A comparative study of flavonoid compounds, vitamin C, and antioxidant properties of baby leaf Brassicaceae species. J. Agric. Food Chem. 2008, 56, 2330–2340. [Google Scholar] [CrossRef] [PubMed]
  13. Gonnella, S.F.; Santamaria, P. Fattori genetici e contenuto di nitrato degli ortaggi. Colt. Protette 2002, 12, 14–19. [Google Scholar]
  14. Steingrover, E.; Ratering, P.; Siesling, J. Daily changes in uptake, reduction and storage of nitrate in spinach grown at low light intensity. Physiol. Plant. 1986, 66, 550–556. [Google Scholar] [CrossRef]
  15. Blom-Zandastra, M.; Lampe, J.E.M. The role of nitrate in the osmoregulation of lettuce (Lactuca sativa L.) grown at different light intensities. J. Exp. Bot. 1985, 36, 1043–1052. [Google Scholar] [CrossRef]
  16. Russo, R.O.; Berlyn, G.P. The Use of Organic Biostimulants to Help Low Input Sustainable agriculture. J. Sustain. Agric. 1990, 1, 19–42. [Google Scholar] [CrossRef]
  17. Hamza, B.; Suggars, A. Biostimulants: Myths and realities. Turfgrass Trends 2001, 10, 6–10. [Google Scholar]
  18. Kauffman, G.L.; Kneivel, D.P.; Watschke, T.L. Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass. Crop. Sci. 2007, 47, 261–267. [Google Scholar] [CrossRef]
  19. Ertani, A.; Schiavon, M.; Altissimo, A.; Franceschi, C.; Nardi, S. Phenol-containing organic substances stimulate phenylpropanoid metabolism in Zea mays. J. Plant Nutr. Soil. Sci. 2011, 174, 496–503. [Google Scholar] [CrossRef]
  20. Ertani, A.; Schiavon, M.; Muscolo, A.; Nardi, S. Alfalfa plant-derived biostimulant stimulate short-term growth of salt stressed Zea mays L. plants. Plant Soil 2013, 364, 145–158. [Google Scholar] [CrossRef]
  21. Guinan, K.J.; Sujeeth, N.; Copeland, R.B.; Jones, P.W.; O’Brien, N.M.; Sharma, H.S.S.; Prouteau, P.F.J.; O’Sullivan, J.T. Discrete roles for extracts of Ascophyllum nodosum in enhancing plant growth and tolerance to abiotic and biotic stresses. Acta Hortic. 2013, 1009, 127–136. [Google Scholar] [CrossRef]
  22. Nardi, S.; Carletti, P.; Pizzeghello, D.; Muscolo, A. Biological activities of humic substances. In Biophysico-Chemical Processes Involving Natural Nonliving Organic Matter in Environmental Systems; Senesi, N., Xing, B., Huang, P.M., Eds.; Wiley: Hoboken, NJ, USA, 2009; Volume 2, pp. 305–340. [Google Scholar]
  23. Nardi, S.; Carletti, P.; Ertani, A.; Pizzeghello, D. Knowledge and evaluation of plant growth stimulants. Inform. Agrario 2006, 45, 41–44. [Google Scholar]
  24. Petrozza, A.; Summerer, S.; Di Tommaso, G.; Di Tommaso, D.; Piaggesi, A. Evaluation of the effect of Radifarm w treatment on the morpho-physiological characteristics of root systems via image analysis. Acta Hortic. 2013, 1009, 149–153. [Google Scholar] [CrossRef]
  25. Petrozza, A.; Summerer, S.; Di Tommaso, G.; Di Tommaso, D.; Piaggesi, A. An evaluation of tomato plant root development and morpho-physiological response treated with VIVA w by image analysis. Acta Hortic. 2013, 1009, 155–159. [Google Scholar] [CrossRef]
  26. Kunicki, E.; Grabowska, A.; Sekara, A.; Wojciechowska, R. The effect of cultivar type, time of cultivation, and biostimulant treatment on the yield of spinach (Spinacia oleracea L.). Folia Hortic. 2010, 22, 9–13. [Google Scholar] [CrossRef]
  27. Vernieri, P.; Borghesi, E.; Ferrante, A.; Magnani, G. Application of biostimulants in floating system for improving rocket quality. J. Food. Agric. Environ. 2005, 3, 86–88. [Google Scholar]
  28. Vernieri, P.; Borghesi, E.; Tognoni, F.; Serra, G.; Ferrante, A.; Piagessi, A. Use of biostimulants for reducing nutrient solution concentration in floating system. ISHM Acta Hortic. 2006, 718, 477–484. [Google Scholar] [CrossRef]
  29. Kyriacou, M.C.; Rouphael, Y.; Colla, G.; Zrenner, R.M.; Schwarz, D. Vegetable grafting: The implications of a growing agronomic imperative for vegetable fruit quality and nutritive value. Front. Plant Sci. 2017, 8, 741. [Google Scholar] [CrossRef]
  30. Caruso, G.; De Pascale, S.; Cozzolino, E.; Giordano, M.; El-Nakhel, C.; Cuciniello, A.; Cenvinzo, V.; Colla, G.; Rouphael, Y. Protein Hydrolysate or Plant Extract-based Biostimulants Enhanced Yield and Quality Performances of Greenhouse Perennial Wall Rocket Grown in Different Seasons. Plants 2019, 5, 208. [Google Scholar] [CrossRef]
  31. Di Mola, I.; Cozzolino, E.; Ottaiano, L.; Giordano, M.; Rouphael, Y.; Colla, G.; Mori, M. Effect of Vegetal- and Seaweed Extract-Based Biostimulants on Agronomical and Leaf Quality Traits of Plastic Tunnel-Grown Baby Lettuce under Four Regimes of Nitrogen Fertilization. Agronomy 2019, 9, 571. [Google Scholar] [CrossRef]
  32. Colla, G.; Cardarelli, M.; Bonini, P.; Rouphael, Y. Foliar Applications of Protein Hydrolysate, Plant and Seaweed Extracts Increase Yield but Differentially Modulate Fruit Quality of Greenhouse Tomato. HortScience 2017, 52, 1214–1220. [Google Scholar] [CrossRef]
  33. Rouphael, Y.; De Micco, V.; Arena, C.; Raimondi, G.; Colla, G.; De Pascale, S. Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J. Appl. Phycol. 2017, 29, 459–470. [Google Scholar] [CrossRef]
  34. Rouphael, Y.; Giordano, M.; Cardarelli, M.; Cozzolino, E.; Mori, M.; Kyriacou, M.C.; Bonini, P.; Colla, G. Plant- and Seaweed-Based Extracts Increase Yield but Differentially Modulate Nutritional Quality of Greenhouse Spinach through Biostimulant Action. Agronomy 2018, 8, 126. [Google Scholar] [CrossRef]
  35. Colla, G.; Rouphael, Y.; Lucini, L.; Canaguier, R.; Stefanoni, W.; Fiorillo, A.; Cardarelli, M. Protein hydrolysate-based biostimulants: Origin, biological activity and application methods. Acta Hortic. 2016, 1148, 27–34. [Google Scholar] [CrossRef]
  36. Ertani, A.; Schiavon, M.; Nardi, S. Transcriptome-wide identification of differentially expressed genes in Solanum Lycopersicon, L. in response to an alfalfa-protein hydrolysate using microarrays. Front. Plant Sci. 2017, 8, 1159. [Google Scholar] [CrossRef] [Green Version]
  37. Colla, G.; Rouphael, Y.; Canaguier, R.; Svecova, E.; Cardarelli, M. Biostimulant action of a plant-derived protein hydrolysate produced through enzymatic hydrolysis. Front. Plant Sci. 2014, 5, 448. [Google Scholar] [CrossRef] [Green Version]
  38. Trevisan, S.; Manoli, A.; Quaggiotti, S.A. Novel biostimulant, belonging to protein hydrolysates, mitigates abiotic stress effects on maize seedlings grown in hydroponics. Agronomy 2019, 9, 28. [Google Scholar] [CrossRef] [Green Version]
  39. Szczepanek, M.; Siwik-Ziomek, A. P and K accumulation by rapeseed as affected by biostimulant under different NPK and S fertilization doses. Agronomy 2019, 9, 477. [Google Scholar] [CrossRef] [Green Version]
  40. Lucini, L.; Rouphael, Y.; Cardarelli, M.; Canaguier, R.; Kumar, P.; Colla, G. The effect of a plant-derived biostimulant on metabolic profiling and crop performance of lettuce grown under saline conditions. Sci. Hortic. 2015, 182, 124–133. [Google Scholar] [CrossRef]
  41. Carillo, P.; Colla, G.; Fusco, G.M.; Dell’Aversana, E.; El-Nakhel, C.; Giordano, M.; Pannico, A.; Cozzolino, E.; Mori, M.; Reynaud, H.; et al. Morphological and physiological responses induced by protein hydrolysate-based biostimulant and nitrogen rates in greenhouse spinach. Agronomy 2019, 9, 450. [Google Scholar] [CrossRef] [Green Version]
  42. Battacharyya, D.; Babgohari, M.Z.; Rathor, P.; Prithiviraj, B. Seaweed extracts as biostimulants in horticulture. Sci. Hortic. 2015, 196, 39–48. [Google Scholar] [CrossRef]
  43. Jannin, L.; Arkoun, M.; Etienne, P.; Laîné, P.; Goux, D.; Garnica, M.; Fuentes, M.; Francisco, S.S.; Baigorri, R.; Cruz, F. Brassica napus growth is promoted by Ascophyllum nodosum L. Le Jol. seaweed extract: Microarray analysis and physiological characterization of N, C, and S metabolisms. J. Plant Growth Regul. 2013, 32, 31–52. [Google Scholar] [CrossRef]
  44. Tsouvaltzis, P.; Koukounaras, A.; Siomos, S.A. Application of amino acids improves lettuce crop uniformity and inhibits nitrate accumulation induced by the supplemental inorganic nitrogen fertilization. Int. J. Agric. Biol. 2014, 16, 951–955. [Google Scholar] [CrossRef]
  45. Colla, G.; Kim, H.J.; Kyriacou, M.C.; Rouphael, Y. Nitrate in fruits and vegetables. Sci. Hortic. 2018, 237, 231–238. [Google Scholar] [CrossRef]
  46. Tadros, M.J.; Omari, H.J.; Turk, M.A. The morphological, physiological and biochemical responses of sweet corn to foliar application of amino acids biostimulants sprayed at three growth stages. Aust. J. Crop Sci. 2019, 13, 412–417. [Google Scholar] [CrossRef]
  47. Ali, M.; Cheng, Z.H.; Hayat, S.; Ahmad, H.; Ghani, M.I.; Liu, T. Foliar spraying of aqueous garlic bulb extract stimulates growth and antioxidant enzyme activity in eggplant (Solanum melongena L.). J. Integr. Agric. 2019, 18, 1001–1013. [Google Scholar] [CrossRef]
  48. Carillo, P.; Colla, G.; El-Nakhel, C.; Bonini, P.; D’Amelia, L.; Dell’Aversana, E.; Pannico, A.; Giordano, M.; Sifola, M.I.; Kyriacou, M.C.; et al. Biostimulant application with a tropical plant extract enhances Corchorus olitorius adaptation to sub-optimal nutrient regimens by improving physiological parameters. Agronomy 2019, 9, 249. [Google Scholar] [CrossRef] [Green Version]
  49. Khanam, U.K.S.; Oba, S.; Yanase, E.; Murakami, Y. Phenolic acids, flavonoids and total antioxidant capacity of selected leafy vegetables. J. Funct. Foods 2012, 4, 979–987. [Google Scholar] [CrossRef]
  50. Kyriacou, M.C.; Rouphael, Y.; Di Gioia, F.; Kyratzis, A.; Serio, F.; Renna, M.; De Pascale, S.; Santamaria, P. Micro-scale food production and the rise of microgreens. Trends Food Sci. Technol. 2016, 57, 103–115. [Google Scholar] [CrossRef]
  51. Kyriacou, M.C.; El-Nakhel, C.; Graziani, G.; Pannico, A.; Soteriou, G.A.; Giordano, M.; Ritieni, A.; De Pascale, S.; Rouphael, Y. Functional quality in novel food sources: Genotypic variation in the nutritive and phytochemical composition of thirteen microgreens species. Food Chem. 2019, 277, 107–118. [Google Scholar] [CrossRef]
  52. Kyriacou, M.C.; Rouphael, Y. Towards a new definition of quality for fresh fruits and vegetables. Sci. Hortic. 2018, 234, 463–469. [Google Scholar] [CrossRef]
  53. Rouphael, Y.; Kyriacou, M.C. Enhancing quality of fresh vegetables through salinity eustress and biofortification applications facilitated by soilless cultivation. Front. Plant Sci. 2018, 9, 1254. [Google Scholar] [CrossRef]
  54. Wang, Z.H.; Li, S.X.; Malhi, S. Effects of fertilization and other agronomic measures on nutritional quality of crops. J. Sci. Food Agric. 2008, 88, 7–23. [Google Scholar] [CrossRef]
  55. Colla, G.; Nardi, S.; Cardarelli, M.; Ertani, A.; Lucini, L.; Canaguier, R.; Rouphael, Y. Protein hydrolysates as biostimulants in horticulture. Sci. Hortic. 2015, 196, 28–38. [Google Scholar] [CrossRef]
  56. Colla, G.; Hoagland, L.; Ruzzi, M.; Cardarelli, M.; Bonini, P.; Canaguier, R.; Rouphael, Y. Biostimulant action of protein hydrolysates: Unraveling their effects on plant physiology and microbiome. Front. Plant Sci. 2017, 8. [Google Scholar] [CrossRef] [Green Version]
  57. Paul, K.; Sorrentino, M.; Lucini, L.; Rouphael, Y.; Cardarelli, M.; Bonini, P.; Reynaud, H.; Canaguier, R.; Trtílek, M.; Panzarová, K.; et al. Understanding the biostimulant action of vegetal-derived protein hydrolysates by high-throughput plant phenotyping and metabolomics: A case study on tomato. Front Plant Sci. 2019, 10, 47. [Google Scholar] [CrossRef]
  58. Paul, K.; Sorrentino, M.; Lucini, L.; Rouphael, Y.; Cardarelli, M.; Bonini, P.; Miras Moreno, M.B.; Reynaud, H.; Canaguier, R.; Trtílek, M.; et al. A combined phenotypic and metabolomic approach for elucidating the biostimulant action of a plant-derived protein hydrolysate on tomato grown under limited water availability. Front Plant Sci. 2019, 10, 493. [Google Scholar] [CrossRef]
  59. Rouphael, Y.; Colla, G.; Giordano, M.; El-Nakhel, C.; Kyriacou, M.C.; De Pascale, S. Foliar applications of a legume-derived protein hydrolysate elicit dose dependent increases of growth, leaf mineral composition, yield and fruit quality in two greenhouse tomato cultivars. Sci. Hortic. 2017, 226, 353–360. [Google Scholar] [CrossRef]
  60. Caruso, G.; De Pascale, S.; Cozzolino, E.; Cuciniello, A.; Cenvinzo, V.; Bonini, P.; Colla, G.; Rouphael, Y. Yield and nutritional quality of Vesuvian Piennolo tomato PDO as affected by farming system and biostimulant application. Agronomy 2019, 9, 505. [Google Scholar] [CrossRef] [Green Version]
  61. Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved abts radical cation decolorization assay. Free. Radic. Biol. Med. 1999, 26, 1231–1237. [Google Scholar] [CrossRef]
  62. Fogliano, V.; Verde, V.; Randazzo, G.; Ritieni, A. Method for measuring antioxidant activity and its application to monitoring the antioxidant capacity of wines. J. Agric. Food Chem. 1999, 47, 1035–1040. [Google Scholar] [CrossRef]
  63. Kampfenkel, K.; Van Montagu, M.; Inzé, D. Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal. Biochem. 1995, 225, 165–167. [Google Scholar] [CrossRef]
  64. Wellburn, A.R. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994, 144, 307–313. [Google Scholar] [CrossRef]
  65. Sah, R.N. Nitrate-nitrogen determination: A critical review. Commun. Soil Sci. Plant Anal. 1994, 25, 2841–2869. [Google Scholar] [CrossRef]
  66. Ruggeri, R.; Provenzano, M.E.; Rossini, F. Effect of mulch on initial coverage of four groundcover species for low input landscaping in a Mediterranean climate. Urban For. Urban Green. 2016, 19. [Google Scholar] [CrossRef]
  67. Rossini, F.; Provenzano, M.E.; Sestili, F.; Ruggeri, R. Synergistic effect of sulfur and nitrogen in the organic and mineral fertilization of durum wheat: Grain yield and quality traits in the Mediterranean environment. Agronomy 2018, 8, 189. [Google Scholar] [CrossRef] [Green Version]
Plants 08 00522 g001 550
Figure 1. Lipophilic antioxidant activity (LAA) in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer). Different letters indicate significant differences at p ≤ 0.05.
Figure 1. Lipophilic antioxidant activity (LAA) in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer). Different letters indicate significant differences at p ≤ 0.05.
Plants 08 00522 g001
Plants 08 00522 g002 550
Figure 2. Total ascorbic acid (TAA) in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer). Different letters indicate significant differences at p ≤ 0.05.
Figure 2. Total ascorbic acid (TAA) in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer). Different letters indicate significant differences at p ≤ 0.05.
Plants 08 00522 g002
Table
Table 1. Baby rocket leaf marketable yield at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
Table 1. Baby rocket leaf marketable yield at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
TreatmentsI HarvestII HarvestIII HarvestTotal
(t ha−1)
N0Control6.35 e1.73 g2.01 e10.09 f
TPE7.75 d3.56 ef2.40 de13.71 e
LDPH8.10 d3.15 f2.93 cd14.18 de
N1Control10.15 c3.64 ef2.10 e15.89 d
TPE10.73 bc4.35 ce5.09 b20.17 c
LDPH10.93 b4.53 cd5.11 b20.57 c
N2Control11.65 a3.92 df3.19 c18.76 c
TPE11.80 a7.38 b5.49 b24.67 b
LDPH11.87 a7.15 b5.08 b24.10 b
N3Control11.73 a4.82 c3.57 c20.13 c
TPE11.57 a9.04 a7.18 a27.79 a
LDPH11.70 a8.35 a7.40 a27.44 a
Significance
Nitrogen (N) ********
Biostimulants (B) NS***
N × B ********
NS, *, ** Non-significant or significant at p < 0.05 and 0.01, respectively. Different letters within each column indicate significant differences at p ≤ 0.05.
Table
Table 2. Baby rocket leaf plant growth parameters (leaf area index (LAI), leaf succulence and specific leaf weight (SLW)) at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
Table 2. Baby rocket leaf plant growth parameters (leaf area index (LAI), leaf succulence and specific leaf weight (SLW)) at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
TreatmentsLAISucculenceSLW
I HarvestII HarvestIII HarvestI HarvestII HarvestIII HarvestI HarvestII HarvestIII Harvest
(mg H2O cm−2)(mg d.m. cm−2)
Nitrogen (N)
N03.5 c1.0 d0.9 c51.5 b66.9 b65.2 c4.4 a6.0 a7.4 a
N14.6 b1.5 c1.5 b55.9 a68.8 b68.7 bc4.4 a5.6 b5.4 b
N25.2 a2.0 b1.6 b55.8 a74.2 a70.6 ab4.1 b5.6 b5.5 b
N35.1 a2.4 a2.0 a56.5 a74.7 a73.1 a4.0 b5.6 b5.8 b
Biostimulants (B)
Control4.51.2 b1.0 b54.568.6 b67.9 b4.25.86.8 a
TPE4.72.1 a1.8 a55.171.9 a70.8 a4.35.75.7 b
LDPH4.71.9 a1.8 a55.673.0 a70.6 a4.15.65.7 b
Significance
N*************
BNS**NS**NSNS**
N × BNSNSNSNSNSNSNSNSNS
NS, *, ** Non-significant or significant at p < 0.05 and 0.01, respectively. Non-significant interaction was recorded between the two tested factors; the letters separated by Duncan’s test (significance level 0.05) were used to denote statistical differences between the main effects.
Table
Table 3. Baby rocket leaf plants Soil Plant Analysis Development (SPAD) index at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
Table 3. Baby rocket leaf plants Soil Plant Analysis Development (SPAD) index at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
TreatmentsSPAD Index
I HarvestII HarvestIII Harvest
(%)
Nitrogen (N)
N022.9 d31.8 d23.8 d
N127.4 c34.1 c29.3 c
N229.1 b36.4 b33.2 b
N331.1 a37.5 a35.2 a
Biostimulants (B)
Control26.1 b32.6 b28.7 c
TPE28.1 a35.8 a30.7 b
LDPH28.6 a36.4 a31.7 a
Significance
N******
B****
N × BNSNSNS
NS, *, ** Non-significant or significant at p < 0.05 and 0.01, respectively. Non-significant interaction was recorded between the two tested factors; the letters separated by Duncan’s test (significance level 0.05) were used to denote statistical differences between the main effects.
Table
Table 4. Baby rocket leaf plants hunter color parameters (L*, a*, and b*) at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
Table 4. Baby rocket leaf plants hunter color parameters (L*, a*, and b*) at different harvest dates in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
TreatmentsI HarvestII HarvestIII Harvest
L*a*b*L*a*b*L*a*b*
Nitrogen (N)
N042.83–16.20 b25.15 b39.82−14.26 c20.38 b41.73–13.01 c20.39 c
N142.96–16.85 a25.69 a39.74–14.75 b20.68 b41.81–13.30 bc20.71 bc
N242.96–16.90 a25.96 a39.77–14.91 ab21.23 a41.63–13.69 ab20.91 ab
N342.96–17.07 a27.15 a39.83−15.07 a21.40 a41.66–13.85 a21.30 a
Biostimulants (B)
Control42.87–16.7526.2039.71–14.6420.8441.74–13.4620.83
TPE43.00–16.7226.3339.79–14.7720.9441.67–13.5620.89
LDPH42.91–16.7926.1839.87–14.8320.9841.72–13.3820.77
Significance
NNS***NS****NS****
BNSNSNSNSNSNSNSNSNS
N × BNSNSNSNSNSNSNSNSNS
NS, *, ** Non-significant or significant at p < 0.05 and 0.01, respectively. Non-significant interaction was recorded between the two tested factors; the letters separated by Duncan’s test (significance level 0.05) were used to denote statistical differences between the main effects.
Table
Table 5. Baby rocket leaf plants nitrate, chlorophyll, and carotenoid content as mean value of the three harvests, in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
Table 5. Baby rocket leaf plants nitrate, chlorophyll, and carotenoid content as mean value of the three harvests, in relation to N fertilization rates (N0 = 0, N1 = 60, N2 = 80, and N3 = 100 kg ha−1) and biostimulant application (Control, tropical plant extract (TPE): Auxym and legume-derived protein hydrolysate (LDPH): Trainer).
TreatmentsNitrateChlorophyll aChlorophyll bTotal ChlorophyllCarotenoids
(mg kg−1 fw)(mg g−1 fw)(mg g−1 fw)(mg g−1 fw)(µg g−1 fw)
Nitrogen (N)
N01049.3 d0.741 c0.464 b1.205 b232.0 c
N12417.9 c0.843 bc0.572 ab1.415 a254.0 b
N23036.5 b0.873 ab0.555 ab1.427 a265.0 ab
N34417.4 a0.883 a0.624 a1.507 a280.0 a
Biostimulants (B)
Control1650.0 b0.814 b0.524 b1.338 b253.0 b
TPE3504.2 a0.784 b0.507 b1.291 b247.0 b
LDPH2900.1 a0.907 a0.630 a1.537 a274.0 a
Significance
N******
B*****
F × BNSNSNSNSNS
NS, *, ** Non-significant or significant at p < 0.05 and 0.01, respectively. Non-significant interaction was recorded between the two tested factors; the letters separated by Duncan’s test (significance level 0.05) were used to denote statistical differences between the main effects.

Share and Cite

MDPI and ACS Style

Di Mola, I.; Ottaiano, L.; Cozzolino, E.; Senatore, M.; Giordano, M.; El-Nakhel, C.; Sacco, A.; Rouphael, Y.; Colla, G.; Mori, M. Plant-Based Biostimulants Influence the Agronomical, Physiological, and Qualitative Responses of Baby Rocket Leaves under Diverse Nitrogen Conditions. Plants 2019, 8, 522. https://doi.org/10.3390/plants8110522

AMA Style

Di Mola I, Ottaiano L, Cozzolino E, Senatore M, Giordano M, El-Nakhel C, Sacco A, Rouphael Y, Colla G, Mori M. Plant-Based Biostimulants Influence the Agronomical, Physiological, and Qualitative Responses of Baby Rocket Leaves under Diverse Nitrogen Conditions. Plants. 2019; 8(11):522. https://doi.org/10.3390/plants8110522

Chicago/Turabian Style

Di Mola, Ida, Lucia Ottaiano, Eugenio Cozzolino, Mauro Senatore, Maria Giordano, Christophe El-Nakhel, Adriana Sacco, Youssef Rouphael, Giuseppe Colla, and Mauro Mori. 2019. "Plant-Based Biostimulants Influence the Agronomical, Physiological, and Qualitative Responses of Baby Rocket Leaves under Diverse Nitrogen Conditions" Plants 8, no. 11: 522. https://doi.org/10.3390/plants8110522

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop