Cultivating plants is a human activity involving several sectors. Agriculture deals with cultivation of crops for human consumption as well as animal production. Horticulture strictly involves the cultivation of plants for food consumption, as well as plants not for human consumption. Horticulture differs from floriculture. The former involves different types of garden crops, while the latter involves flowering and foliage plants. Ornamental horticulture is the cultivation of decorative plants of all kinds, including not only plants with attractive flowers, but also plants with decorative leaves, stems, bark, or fruit. Basically, floriculture and ornamental horticulture have decorative and aesthetic purposes. Aside from categories’ definitions and differences in the cultivated species, all these categories’ activities share similar problems.
Common farming practice is to boost plant production with a fertilizer dose higher than that adsorbed by soil and plant. Thus, noxious fertilizers’ components accumulate in soil, reach the food chain, leach through soil into ground water, and ultimately affect human and animal health. Mineral and organic fertilizers are used. The global fertilizer market is 156 billion USD/year. [1
]. Major ones are urea and mineral phosphates (80% of the EU fertilizers’ market value), with 0.11–0.46 €/kg production cost. They are based on energy-intensive production processes or manufactured from non-renewable feedstock imported from third countries [2
]. Organic fertilizers belong to a niche market (0.15% of the total fertilizer market) [3
]. The world consumption of mineral fertilizers containing N, P and K is ca. 200 Mt/year [4
]. EU consumption of mineral fertilizers is 16 Mt/year [5
]. From 70 to 250 kg/ha nitrates leaching may occur depending on fertilizer dose, soil, and plant type [6
]. Based on average 51 kg/ha applied surplus and total 175 Mha cultivated area, 9 kt/year nitrate leach through soil and water. To improve the balance between fertilizers dose and crop requirement, the max EU ruled dose is 150–350 kg/ha. Major organic fertilizers are composts of biowastes from urban, animal, or agriculture sources, manure, peat and leonardite hydrolysates. Composts are commonly applied to soil at 10–30 t/ha.year [7
]. High doses that obtain the desired effects are due to compost insolubility causing slow nutrients’ uptake by plants. This causes leaching of excess major and trace metal components through soil and water. Similarly, manure is applied at 70 t/ha dose. In addition to leaching, manure causes greenhouse-gases emission due to fermentation in soil. For example, typical aerial NH3
concentration in a pig farm is 5–35 ppm against a 25 ppm threshold level [8
]. A higher NH3
level harms both animal and human health. Emission of 420,000 t/year NH3
is estimated from a total 1400 Mt/year EU manure production [9
]. Peat and leonardite hydrolysates contain soluble organic and mineral matter. EU consumption is 240 kt/year. These hydrolysates are obtained from fossil source. Based on average 40% C content, their use causes 355 kt/year CO2
emission from fossil C and depletion of fossil sources. Except for municipal biowastes (MBW), a common problem of all fertilizers is that their sources are found in restricted sites, not available worldwide. This poses the problem of product supply and cost. The problem is highly relevant in Europe, which imports most of its mineral consumption from third countries.
One other important restraint on plant productivity is pests and diseases. These are highly relevant for food plants. Food production loss due to plant diseases is estimated to be 10–50%/year [10
]. Plant protection relies on pesticides use, which increases food cost and may cause hormonal disruption in human. A common problem of all fertilizers is the need to use them together with pesticides. Together with lowering cost, there is much concern for decreasing the exploitation and depletion of natural resources to produce fertilizers.
In the last ten years, relevant research has been focused on bio-stimulants. These belong to a new functional product category (FPC6) contemplated in the New European Fertiliser Regulation [11
]. Bio-stimulants are supposed to stimulate the plant metabolism, regardless of their nutrient content, and so improve plant growth, even under abiotic stress, and resistance to diseases [13
]. Applied at much lower doses than common mineral and organo-mineral fertilisers, bio-stimulants are expected to induce plant resistance to pathogens and provide high crop productivity at the same time. In this fashion, they reduce/minimize the negative environmental impact of the excessive application of commercial fertilisers and pesticides.
Work by the authors in the past fifteen years proves that soluble bioorganic substances (SBS) obtained from urban and agriculture biowastes have both biostimulant and antifungal properties [14
]. No other known products have both properties. The research hypothesis was that, by virtue of the solubility properties and organo-mineral composition, the SBS could increase plant growth and crop production compared to current commercial mineral and organo-mineral agrochemicals. The present paper reports the critical review of work performed by the authors with SBS for the cultivation of food and non-food plants. The review proves the research hypothesis. It demonstrates the SBS biostimulant properties for all tested plants and discusses the economic and environmental benefits for agriculture and horticulture.
2. SBS Composition and Properties
The SBS are obtained by hydrolysis at 60–90 °C and pH 13 of several different mixes of urban food, green and sewage sludge wastes fermented under anaerobic and aerobic conditions [14
]. Under these conditions, the SBS were obtained together with the secondary insoluble (IR) product. The fermented wastes yielding the SBS described in the present review were sampled from different streams of the Italian ACEA Pinerolese MBW treatment plant. The SBS contain organic and mineral matter. The organic matter is a mix of molecules with molecular weight from 5 to over 750 kDa. These molecules are constituted by several different organic moieties made by aliphatic and aromatic C substituted by acid and basic functional groups of different strengths. Mineral elements of groups 1 to 4 are bonded to or complexed by the organic moieties. These chemical features are inherited from the pristine biowastes. The molecules contained in SBS are water soluble memories of the native recalcitrant lignocellulosic polysaccharides, proteins, fats, and lignin proximates still present in the biowastes after anaerobic and aerobic fermentation. It is no wonder that, due to their origin, richness of mineral elements, organic functional groups and acquired water solubility, the SBS molecules exhibit a wide range of properties as plant biostimulants, plant resistance inducers, bio-photosensitizers, oxidation catalysts, polymers for manufacturing mulch films, composite pellets, composite plastic articles, and high performance surfactants. Table 1
, Table 2
, Table 3
and Table 4
report the compositional details of the SBS, IR and the pristine fermented biowastes. Table 5
list the plants cultivated with the SBS and summarizes the main SBS effects on the cultivated plants. All data in Table 1
, Table 2
, Table 3
, Table 4
and Table 5
are extrapolated from the references cited in Table 5
. The data reported in Table 1
, Table 2
, Table 3
and Table 4
were obtained through a specifically designed analytical protocol [14
]. This included calculation of moisture, ash and volatile solids (VS) contents from the sample weight losses determined after heating to 105 and 650 °C, inorganic elements analysis by AAS and/or ICP, microanalyses for C, H, N determination performed with a C. Erba (Rodano, Milan, Italy) NA-2100 elemental analyser. The C types and functional groups reported in Table 4
were determined by solid-state 13C NMR spectroscopy. Solid-state 13C NMR spectra were acquired at 67.9 MHz on a JEOL GSE 270 spectrometer equipped with a Doty probe. The cross-polarization magic angle spinning (CPMAS) technique was employed, and for each spectrum, about 104 free induction decays were accumulated. The pulse repetition rate was set at 0.5 s, the contact time at 1 ms, the sweep width was 35 KHz, and MAS was performed at 5 kHz. Signals assignment as a function of the resonance range were: 0–53 ppm aliphatic C, 53–63 ppm O-Me or N-alkyl C, 63–95 ppm O-alkyl C, 95–110 ppm di-O-alkyl C, 110–140 ppm aromatic C, 140–160 ppm phenol or phenyl ether C, 160–185 ppm carboxyl C, and 185–215 ppm ketone C.
6. SBS Economic and Environmental Benefits, and Perspectives for Agriculture and Horticulture
Mineral and organic products are marketed as fertilizers, plant biostimulants, and plant disease suppressing agents. Prices of these products cover a wide range. Benzothiadiazole, used as plant disease suppressants [29
], is the most expensive product. Its price is at 800 USD/kg level [30
]. By comparison, the production cost of mineral fertilizers is in the 0.11–0.46 €/range. The increasing demand of mineral fertilizers depletes fossil sources. The excessive applied doses to boost crop production causes accumulation in and leaching through soil into natural waters, and consequent eutrophication. In the last few decades, biostimulants have emerged as a new product category for agriculture [31
]. This category includes substance or microorganism that, regardless of their mineral nutrients content, are supposed to enhance plant nutrition efficiency, abiotic stress tolerance and/or crop quality traits. They are supposed to modify the plant physiology, and so to enhance the plant growth and stress response. Compared with biofertilizers, biostimulants act at much lower applied doses. Humic substances (HS), extracted from soil and fossil deposits, belong to the biostimulants’ category.
The SBS, described in Section 3
, Section 4
and Section 5
of the present review, bear similar origin and chemical features as humic substances [32
]. The advantages of SBS compared to HS and other commercial products claimed or reported in the literature as biostimulants is that the SBS are obtained from municipal biowastes available worldwide [33
]. They do not cause depletion of soil organic matter or fossil deposits, and their production cost is very low. Thus, new eco-friendly and low cost perspectives are opening for novel SBS-based farm practices to replace and/or decrease mineral fertilizers consumption in agriculture.
At the present time, the market turnover of organic fertilizers is small, compared to the mineral fertilizers’. The US total fertilizer market is around 40 billion USD, with only 60 million USD contributed by organic fertilizers. Prices for various organic fertilizers range [3
] range from 140 USD/t for solid products containing 10% soluble organics to 3000 USD/t for products sold in solution containing 35% organics and other mineral elements. Based on information collected by the authors of the present review, through interviews with major Italian distributors of peat derived organic fertilizers, the European market turnover is 20–25 million EUR/year., the minimum sale price is 1000 EUR/t, equivalent to 20–25 kt/year. sale. By comparison, the Euphorbia [15
], Lantana [16
] and Murraya [18
] studies demonstrate that SBS are more efficient biostimulants than commercial products derived from Leonardite. The latter products containing 30% dry matter are sold for 7 EUR/kg [15
], which corresponds to over 23 EUR/kg dry matter. The SBS production cost has been estimated about 0.1–0.5 EUR/kg [32
]. The figures prospect attracting economic benefits deriving from the allocation of SBS in the organic fertilizer market. Further commercial opportunity for SBS may derive from the growth of the bio-stimulants market [38
], estimated to reach 5 billion euros in the current decade.
To fully appreciate the economic perspectives of marketing SBS in biostimulants’ product category, it should be considered that SBS contain all mineral nutrients needed by plants (see Section 2
above). These are bonded to the soluble lignocellulosic matter. The research results (see Section 3
, Section 4
and Section 5
) point out that the reason of the observed effects on plant growth and productivity is that the SBS supply the plants with the mineral nutrients in a readily available soluble form, thus facilitating the nutrients uptake by the plant. Thus, the SBS fall into the high price organic fertilizers’ category. It is also important to be aware of the following fact exemplified for the Italian market. The SBS are obtained from composted urban bio-wastes. Italy produces 4.2 million t/year. organic humid bio-waste [40
]. This can potentially yield 300–400 kt/year. SBS. This potential production exceeds the above estimated organic fertilizers market size. It is evident that, at the present time, this market cannot absorb all organic fertilizers that can be obtained from the produced compost.
It should also be considered that the SBS have been proven efficient plant disease suppressants (see Section 5
). The capacity to induce plant protection against pathogens adds significant higher value to the potential SBS market [30
], in comparison with fertilizers that only enhance plant growth [36
], but do not have at the same time antifungal properties.
The above literature survey however points out that the organic fertilizers market is in the early stage. In this context, the SBS might be favoured for their capability to provide an integrated complete plant nourishment, which contains both mineral and organic matter of renewable sources. In principle, these products could replace current commercial mineral and organic fertilizers, and also antifungal agents. To appreciate the full potential of SBS uses in agriculture, it should be taken also in consideration the work [41
] reporting SBS as potential components of new composite mulch films. Used in agriculture, these films might have multiple function, i.e., protecting plants against negative external influences, creating an ideal microclimate, and slowly releasing the SBS into the soil to stimulate plant and crop growth.
Environmental benefits from using of SBS derive mainly from the substitution of mineral fertilizers. The tomato Micro-Tom [21
] and maize [23
] cultivation studies showed that performance-wise 1 kg SBS is equivalent to 5–7 kg NPK fertilizers. The Euphorbia [15
], Lantana [16
] and Murraya [18
] studies showed that 1 kg SBS yields equal or better plant productivity of at least 1 kg of organic fertilizers derived from fossil source. On this basis, using 1 kg SBS in place of 5–7 kg mineral fertilizers or 1 kg of organic fertilizers from fossil source would allow large reductions of nitrate leaching into natural waters and 100% CO2
emission in air, respectively.
7. Results’ Summary and Discussion
Five SBS have been tested as organo-mineral fertilizers in the cultivation of thirteen food and ornamental plants (Table 5
). The studies have been carried out in comparison with their IR co-products and the pristine sourcing PFB materials (Table 2
, Table 3
and Table 4
), with conventional NPK fertilizers, commercial organo-mineral fertilizers claimed by the vendor for their biostimulant properties, and with synthetic controlled release fertilizers and antifungal agents. The collected data demonstrate the performance of SBS as biostimulants (Section 3
) and antifungal agents (Section 5.2
), and the replicability of their effects over the different tested plants (Section 4
The results of the trials described in Section 3
, Section 4
and Section 5
evidenced that the performance ranking order of the applied SBS products depended on the cultivated plant species. Overall, ten not commercial SBS and IR research products, five different PFB pristine sourcing materials, and several commercial fertilizers and biostimulants were used for the cultivation of thirteen plants. For each plant, several performance indicators were measured. The ranking order of the applied products also depended on the plant performance indicators. Under these circumstances, it is not possible to summarize the results of the present review results in form of comprehensive figures. Specific data plots are given in each of the references cited above for each trial. The authors feel that the results of the present review are more easily and clearly summarized in form of the following text.
The first trial carried out for the cultivation of tomato [7
] demonstrated that CVD SBS performed better than CVD IR, CVD PFB and the commercial RCP product. The second tomato trial [20
] demonstrated that CV SBS performed better than D and CVDF SBS, and CVD SBS in the first trial, even though the applied N, P and K doses with CV SBS were the lowest ones. Thus, the CV SBS seems the best choice for farmers adopting the SBS-based practice for the cultivation of tomato Lycopersicon
as part of their business activity. On the other hand, potential stakeholders of the SBS-based practice should take in consideration the results of the trials carried out for the cultivation of tomato Microtom and red pepper. In the former case [21
], the CVDF SBS performed better than the CV and CVD SBS. In the case of red pepper [22
], the results demonstrated that the plants cultivated in presence of CVD SBS performed much better than tomato Lycopersicon cultivated in the presence of CVD SBS [7
], and tomato Lycopersicon cultivated in the presence of CV, D and CVDF SBS [20
], even though the CVD SBS dose applied in the red pepper study was much lower than that applied in the first tomato study [7
], and the same as the CV, D and CVDF SBS doses applied in the second tomato study [20
]. The four case studies [7
] definitely prove that the all three CV, CVD and CVDF SBS obtained from composted biowastes represent the best choices depending on the type of food plant to cultivate.
The trials performed for the cultivation of maize, spinach and of the ornamental plants disclosed a somewhat different product hierarchy, particularly in relation to D SBS that never ranked first in the tomato and red pepper studies. The Euphorbia [15
], Lantana [16
] and Murray [18
] studies showed that the CVDF SBS performed better than the D SBS and the commercial LND product. However, the first Hibiscus study [17
] showed that D SBS performed better than D IR and PFB, CV SBS, IR and PFB, and the commercial CB product. The second Hibiscus study [10
] showed that under nutrient deficiency conditions, both the CV and D SBS treatments compensated the negative effects of the nutrient deficiency on the plant performance indicators well, and that the CV SBS was more effective than the D SBS treatment. The maize cultivation study [23
] showed that CVDF SBS performed better than CVDF IR and PFB. The spinach [26
] and oilseed rape [10
] studies demonstrated D and/or CVDF SBS as regulators of the N release and oxidation and/or antifungal agents. As for tomato and red pepper [7
], the Euphorbia [15
], Lantana [16
], Murray [18
], maize [23
] studies confirmed the optimum performance of the CVDF and CV SBS obtained from the composted biowastes, whereas the hibiscus [10
], spinach [26
] and oilseed rape [10
] studies disclosed useful important effects by the D SBS.
summarizes the SBS ranking order, based on the indicator that for each plant was mostly affected by the applied SBS. It may be observed that, generally, the CVDF SBS produced the highest increase of total biomass and crop production in all plants, which were cultivated in its presence. The biomass and crop production increase ranged from 6% in the case of tobacco to 331% in the case of Euphorbia. Generally, the ornamental plants were more sensitive to the SBS application than the food plants. The other CV, CVD and D SBS were also effective, although at lower level than the CVDF SBS. The former ones produced biomass and crop production increases, which ranged from zero in the case of tobacco to 117% in the case of Euphorbia cultivated in the presence of D SBS.
Although not as effective as CVDF SBS on biomass and crop production, the D SBS exhibited other relevant effects, such as reduction of nitric to total N ratio in spinach leaves and of lesions caused by Leptosphaeria maculans in oilseed rape. In the spinach trial [25
], the D SBS was used as a component of a composite pellet also containing urea and sunflower protein concentrate. Although the SBS was a minor component in the pellet and was not a significant source of N, relatively to N supplied by the other two components, the D SBS was found to cause a number of effects. It slowed down the formation of ammonia from urea hydrolysis and enhanced the release of organic nitrogen from the sunflower protein concentrate in the cultivation substrate, and strongly affected the mineralization of the total N supplied by the pellet. These effects were ascribed to the interaction of the D SBS functional groups with urea and the protein concentrate. The hypothesis is quite plausible considering the relative high content of carboxylate functional group coupled to the other NR, OR and PhOY in the D SBS (Table 4
). From the practical point of view, the final effect of D SBS was 24–40% reduction of nitric to total N ratio in leaves and the production of the safest crop coupled with high biomass production.
The oilseed rape study [10
] investigated the mechanism of the disease suppression effect reported by both CVDF and D SBS. The two SBS did not show any antimicrobial effect against L. maculans
in vitro. This suggested different mechanisms underlying the observed reduction of lesions caused by Leptosphaeria maculans
reported in Table 5
, among which the induced resistance characterized by an increased resistance to infection occurring after a previous pathogen attack.
Quantitatively, the most remarkable effects were exhibited by the ETP SBS. This product produced 109–1750% increase of the of the enzyme activities and soluble proteins concentration in the leaves and roots of bean plants. This effect demonstrated undoubtedly the biostimulant properties of the applied product.
Reasons for the SBS performances have been proposed. These are based on chemical and biochemical interactions/reactions catalysed by SBS thanks to their chemical composition. The SBS contain 15–30% minerals together with organic matter. They can, therefore, add soluble plant nutrients to soil. They can also perform as bio-effectors, stimulate the uptake from roots of soil nutrients with a hormone-like effect and/or plant growth by promoting rhizobacteria, and catalyse the plant photosynthetic activity (see all references in Section 3
). Applied in mixtures [22
] with urea, other organic fertilizers and NPK conventional mineral fertilizers, they can regulate the release of N, P and K to the soil and taken up by the plant, and so reduce the amount of nitrates leaching through the soil into natural waters and taken up by the plant crop.
Whereas from the basic science point of view, the collected data do not allow demonstrating the action mechanism for the observed performances of SBS in agriculture, from the practical point of view, the most relevant result is that the highest SBS effect on the plant performance indicators occurs at about 140 kg/ha applied dose to the cultivation soil or substrate. Depending on the plant and the type of applied SBS, increases up to three order of magnitude for the plant performance indicators are measured relatively to the control plants. At higher dose levels, no further increases are observed. The remarkable high effects occurring at relatively low treatment dose prospect using the SBS to augment plant growth and productivity, and at the same time reduce the consumption and negative environmental impact of conventional fertilizers applied at high dose.
The collected data offer ground to attempt establishing case-by-case correlations between the composition and the effects of the different SBS used for the cultivation of the same plants. However, the SBS are complex mixtures of organic molecules differing for molecular weight and chemical features. These molecules are in turn bonded to different mineral elements. Under these circumstances, correlations between SBS chemical composition and effects as given in Section 2
, Section 3
, Section 4
and Section 5
do not help much to identify the active molecules, which are responsible for the observed effects. These difficulties are inherent to products obtained from materials of biological origin.