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Article

Flowering, Quality and Nutritional Status of Tropaeolum majus L. ‘Spitfire’ after Application of Trichoderma spp.

by
Roman Andrzejak
1,
Beata Janowska
2,*,
Agnieszka Rosińska
1,
Sylwia Skazińska
1 and
Orsolya Borsai
3
1
Department of Phytopathology, Seed Science and Technology, Faculty of Agronomy, Horticulture and Biotechnology, Poznań University of Life Sciences, Dąbrowskiego 159, 60-594 Poznań, Poland
2
Department of Ornamental Plants, Dendrology and Pomology, Faculty of Agronomy, Horticulture and Biotechnology, Poznań University of Life Sciences, Dąbrowskiego 159, 60-594 Poznań, Poland
3
Department of Horticulture and Landscape, Faculty of Horticulture and Business in Rural Development, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, 400372 Cluj-Napoca, Romania
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(11), 4672; https://doi.org/10.3390/su16114672
Submission received: 9 May 2024 / Revised: 28 May 2024 / Accepted: 28 May 2024 / Published: 30 May 2024
(This article belongs to the Special Issue Sustainable Agroecosystem: Interactions between Plants and Microorganisms)
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Abstract

:
The aim of this study was to compare the influence of three species of fungi of the Trichoderma genus (T. aureoviride Rifai—Ta8, T. hamatum/Bonord/Bainier—Th15, and T. harzianum Rifai—Thr2) on the quality, flowering, and nutritional status of Tropaeolum majus L. ‘Spitfire’. Early flowering was only influenced by T. hamatum, which delayed it by 6 days. T. aureoviride, T. hamatum, and T. harzianum stimulated the flowering of the ‘Spitfire’ cultivar but did not affect the size of the flowers. The plants treated with T. harzianum after being planted in pots flowered the most abundantly. Trichoderma spp. caused the plants to grow more intensively, producing longer and more leafy shoots with a greater number of offshoots. Trichoderma spp. stimulated the uptake of macronutrients, except for phosphorus (P). In the case of calcium (Ca) and sodium (Na), this phenomenon was only observed in plants treated with T. aureoviride and T. hamatum, and for magnesium (Mg), only when T. hamatum was applied to sown seeds. As for the developed root systems, as far as the micronutrients are concerned, Trichoderma spp. stimulated the uptake of zinc (Zn) and manganese (Mn). Apart from that, there was a higher iron (Fe) content in the plants treated with T. harzianum on both dates and T. aureoviride after planting the plants in pots.

1. Introduction

Tropaeolum majus belongs to the Tropaeolaceae family. It grows wild in South America. In the 16th century, it was brought from Peru to Europe by the Spanish [1,2]. It is a perennial, but in many countries with a temperate climate it is grown as an annual plant, because it dies at freezing temperatures [3]. T. majus plants produce well-branched shoots up to a length of 3 m. They have shield-shaped leaves with long petioles and dorsiventral, yellow or orange flowers, which are 3 cm in diameter. The flowers with long spurs are placed individually on long pedicels in the leaf axils. T. majus plants flower for a long time and abundantly. The fruit is a ribbed, gray and beige nut with a rough surface. The name of the genus derives from Greek and means ‘trophy’, a symbol of victory. It refers to the shield-shaped leaves and flowers with spurs; the specific epithet derives from Latin and means ‘big’ [4]. T. majus is grown as an ornamental, medicinal, and edible plant. Its flowers, leaves, and fruits, with a characteristic, sharp taste, reminiscent of cress (Cardamine), are used for culinary purposes. It is planted in suspended containers, in flower beds and is used for screening on fences and pergolas [3,5,6]. In folk medicine, it was used as a disinfectant to accelerate wound healing, as an antibiotic, as a remedy for chest diseases [5,6], and as an antiscorbutic [6]. T. majus leaves and flowers are used for the production of aqueous, ethanol, and acetate extracts, syrups based on herbal infusions and macerates, as well as spirits. The preparations have strong antibacterial and antifungal properties. Nasturtium leaf extracts are used to treat tonsillitis, bronchitis, and urinary tract inflammations [7,8,9]. Flower extracts are also used as natural dyes in the pharmaceutical and food industries. They contain anthocyanins, especially in the orange flower petals. Anthocyanins are not only dyes but also antioxidants [10].
Plants are a natural source of readily available micro- and macronutrients. This is particularly true of herbs that are incorporated into the diet. Dietary supplements of plant origin and herbal medicines usually have a higher bioavailability of elements than synthetic medicines. Knowing the elemental content of herbal raw materials used in treatment is an important factor in assessing their quality. The elemental content of the individual organs of T. majus is still largely unknown. Its flowers are the only source that has been studied in this respect [1]. The flowers of T. majus contain macronutrients such as potassium (K), phosphorus (P), calcium (Ca) and magnesium (Mg), and micronutrients, especially zinc (Zn), copper (Cu) and iron (Fe) [11,12].
Unfortunately, in some countries, T. majus is classified as an invasive species. The plant has spread rapidly in coastal California and Malta, where it forms large, invasive populations, which are detrimental to the native flora and ecosystems. The species is considered invasive but under control in the Hawaiʻi Volcanoes National Park and on Kauai, Molokai, Maui, and Hawaiʻi, as well as in forests and rangelands on Mauna Loa [4].
Fungi of the Trichoderma genus are increasingly often used to improve the quality, flowering, and nutrition of ornamental plants [13,14,15]. They inhabit plant roots and become symbionts stimulating the flowering and elongation of plant shoots and roots. Symbiosis enables plants to absorb nutrients more easily or to use them more efficiently [16,17]. Plants also become more resistant to biotic and abiotic stresses [17]. Trichoderma spp. probably stimulate plant growth because apart from enabling plants to take up more nutrients, they also stimulate the production of vitamins and plant growth regulators (PGRs) [16,18,19,20]. Growth stimulation can be highly variable due to several limiting factors, such as the crop type and conditions, inoculum dose and type of formulation [21]. According to Nieto-Jacob et al. [22], communication between plants and Trichoderma spp. involves the recognition of fungal-derived molecules such as auxins and microbial volatile organic compounds; however, this communication is highly dependent on the environment. Contreras-Cornejo et al. [23] suggest that Trichoderma spp. induce growth through an auxin-dependent mechanism. Trichoderma spp. fungi can mobilize and absorb nutrients from the substrate better and more efficiently than other organisms. These fungi obtain adenosine-5’-triphosphate (ATP) from the metabolism of various carbohydrates derived from polymers that are widely distributed in the soil environment, i.e., cellulose, glucan, chitin, and other sources [24]. As a result of the increase in nutrient uptake, the root system grows intensively. The increased root surface enables plants to access a larger volume of soil, which is important when competing with other organisms for nutrients or if there are small amounts of mineral compounds in the soil [18].
Trichoderma spp. are classified as biostimulants, which are applied to plants to increase the nutrient efficiency, abiotic stress tolerance and/or plant quality traits, regardless of the nutrient content of the plant organs [25]. The widespread use of Trichoderma spp. is very important for improving sustainable horticulture, as these fungi stimulate increased production with less environmental impact [26].
Biostimulants are small amounts of organic or inorganic substances that promote plant growth and development in ways that plants could not achieve without the addition of these compounds [27]. In 2018, the European Commission classified biostimulants in the CE category (the CE category indicates that the product in question has been tested by the manufacturer and found to comply with EU health, safety and environmental requirements), which means that they are fertilizer products that promote plant growth and development regardless of the amount applied [28]. The Council of the European Union [29] further clarified the definition by emphasizing that certain substances, mixtures and microorganisms, referred to as plant biostimulants, are not nutrients but stimulate the natural nutritional processes of plants. If the sole purpose of such products is to improve the efficiency of nutrient use by plants, to increase the tolerance to abiotic stress or plant quality traits, to break down organic compounds in the soil or to increase the nutrient availability in the rhizosphere, they are inherently more similar to fertilizers than to most categories of plant protection products. They act as a complement to fertilizers with the aim of optimizing their effectiveness and reducing fertilizer application rates [29].
The development of new molecular biotechnological methods helps us to understand the mechanisms and possible modes of action of biostimulants. The biostimulants have positive or neutral impacts on the environment and human health [30,31]. Their widespread use can be very important in improving sustainable horticulture, as they can stimulate increased production with less environmental impact [26].
The goal of this study was to assess the effect of three species of the Trichoderma spp. on the growth, flowering, and nutrition of Tropaeolum majus L. ‘Spitfire’ plants.

2. Materials and Methods

2.1. Cultivation of Plants

This research was conducted at the Department of Phytopathology and Seed Science, Poznań University of Life Sciences, Poland. On 18 March 2022, Tropaeolum majus L. ‘Spitfire’ (Figure 1) seeds were sown individually in multi-pot trays with a pot size of 2 × 2 cm into a peat substrate (pH = 6.2), enriched with 0.5 g of Peters Professional Allrounder multi-component fertilizer (20:20:20 + microelements). They were covered with a thin layer of sifted sand because they germinate in the light. The micronutrients contained in this fertilizer are boron (B), copper (Cu), iron (Fe), manganese (Mn), molybdenum (Mo) and zinc (Zn).
One month after sowing the seeds, the young plants (Figure 2) were planted in pots with a diameter of 9 cm (Figure 2 and Figure 3). The substrate was the same as the one into which the seeds had been sown, but the amount of the fertilizer was increased to 2 g∙dm−3. Three plants were planted in one pot.
There were 9 treatments (3 dates of Trichoderma spp. application × 3 species of fungi) and 3 replicates of the experiment. In each, there were three plants growing in one pot. The influence of three species of fungi of the Trichoderma genus (T. aureoviride Rifai—Ta8, T. hamatum/Bonord/Bainier—Th15, T. harzianum Rifai—Thr2) (Figure 4) on the quality, flowering, and nutrition of the Tropaeolum majus L. ‘Spitfire’ plants was compared. Each species of fungi was administered on two dates: after sowing the seeds (5 mL/pot in a tray) and/or after planting the plants in pots (20 mL/plant). The plants that, after sowing the seeds, were grown without Trichoderma spp. were used as the control.

2.2. Inoculum of Trichoderma spp.

An inoculum of the Trichoderma spp. (T. aureoviride Rifai—Ta8, T. hamatum/Bonord/Bainier—Th15, T. harzianum Rifai—Thr2) was prepared at the Department of Phytopathology and Seed Science according to the method described by Andrzejak et al. [13].

2.3. Conditions for Conducting the Experiment

The experiment was conducted in a plant growth chamber, with a 16 h day (Figure 5). The temperature was maintained at 18 °C during the day and at night. The relative air humidity was maintained at 65–70%. As the plants grew, the lamps were gradually raised to a higher position. The sown seeds and emerging seedlings were regularly sprayed with water so that the substrate was constantly moist. After the plants had been planted in the pots, apart from regular watering, every 10 days they were fertilized with aqueous solutions of the multi-component fertilizer (concentration: 0.2) used for basic fertilization (Peters Professional Allrounder multi-component fertilizer—20:20:20 + microelements).

2.4. Parameters

While the plants were growing, the earliness of their flowering was measured by counting the number of days from sowing the seeds to the development of the first flower. When three flowers developed on the plants, the number of buds and flowers and their diameter, the number of lateral branches of the shoot and the length of the shoots were measured. Two months after sowing the seeds, the content of macro- (nitrogen—N, phosphorus—P, potassium—K, calcium—Ca, magnesium—Mg, sodium—Na) and micronutrients (Fe, Zn, Mn, Cu) was measured. After the end of the experiment (after 8 months of cultivation), the percentage of root colonization by Trichoderma spp. was measured.

2.5. Root Colonization

At the end of the experiment, root fragments were taken from each treatment to determine their colonization by Trichoderma spp. This followed the method described by Andrzejak et al. [13].

2.6. Content of Macro- and Microelements

The total contents of the macroelements (N, P, K, Ca, Mg and Na) and microelements (Fe, Mn, Zn and Cu) were determined according to the method described by Andrzejak et al. [13].

2.7. Data Analysis

In order to determine the significance of the differences, a two-factor analysis of variance was carried out, followed by the assessment of the significance of the differences using the Duncan’s test at a significance level of α = 0.05. The Statistica 13.3 program (Statsoft Polska, Kraków, Poland) was used for the statistical analyses.

3. Result and Discussion

3.1. Root Colonization

The percentage of colonization of the roots of the Tropaeolum majus ‘Spitfire’ plants by the three species of fungi of the Trichoderma genus was measured in our study. There were no significant differences between the individual species of fungi or the dates of their application. The percentage of root colonization was high, as it ranged from 48.5% to 51.4% in all the treatments where Trichoderma spp. had been applied (Table 1).
Studies have shown that the degree of root colonization by Trichoderma spp. depends on the plant species treated with these fungi. For example, Andrzejak and Janowska [14] observed that during the two years of the study, Trichoderma spp. colonized 46.6% and then 48.2% of the roots of Gladiolus hybridus ‘Advances Red’ plants. The same fungi colonized 32–33% of the roots of Freesia reflacta ‘Argentea’ [32] and 29.5–30.5% of the roots of Begonia × tuberhybrida ‘Picotee Sunburst’ [13]. However, it is noteworthy that a mixture of fungi of the Trichoderma genus (T. viride, T. harzianum, T. hamatum) was used in the aforementioned experiments and the researchers provided the average value of the root colonization by the fungi, without distinguishing individual species. Prisa et al. [33] made interesting observations in their experiment on Limonium sinuatum. They found that Trichoderma spp. completely colonized the roots of this species. However, in most other studies, Trichoderma spp. colonized the roots to a much lesser extent. Trichoderma spp. are the most common fungi for improving the value of the substrate. Strains colonize the rhizosphere. When the spores come into contact with the roots, they germinate into the mycelium, which quickly colonizes them. Not all Trichoderma strains have the same properties. Some strains colonize the roots intensively and for a long time, penetrating the epidermis. Błaszczyk et al. [34] found that Trichoderma spp. colonized not only the outer layers of the roots of annual and perennial plants and trees in the rhizosphere but were also capable of penetrating the roots and colonizing them inside or they may exist as endophytes. According to Souza et al. [35], Trichoderma spp. can colonize the roots because the roots synthesize metabolites recognized by microorganisms. In addition, fungi also benefit from the sucrose secreted by the roots. It is a source of energy for microorganisms [36,37].

3.2. Earliness of Flowering and Quality of Flowers and Plants

The comparison of the research results showed that the earliness of blooming of the Tropaeolum majus ‘Spitfire’ was only influenced by T. hamatum. When the fungi had been applied after sowing the seeds, they delayed the blooming of the plants by six days. The plants in the other treatments flowered after 55.7–60.3 days (Table 2).
It is very important to provide information about the earliness of flowering of ornamental plants, because most species and cultivars are grown to produce flowers at a specific date [15]. Producers of ornamental plants must know whether to expect delayed or earlier flowering after the application of stimulants, including fungi of the Trichoderma genus [25,38]. Thanks to this information, they can start cultivation earlier or later and finish it at the right time. A lack of information about delayed or earlier flowering may cause losses if producers cannot sell their products. Although scientists around the world have conducted numerous studies on the effect of Trichoderma spp. on crop plants, so far there have been few studies on ornamental plants [15]. The authors of most studies on ornamental plants found that Trichoderma spp. influenced the earliness of flowering, because when they were applied, the plants usually bloomed earlier. This effect was observed in Tulipa gesneriana ‘Golden Parade’ [39], Freesia reflacta ‘Argentea’ [32], Begonia × tuberhybrida ‘Picotee Sunburst’ [13], and Gladiolus hybridus ‘Advances Red’ [14]. Sisodia et al. [40] did not observe the effect of fungi on the earliness of flowering of several Gladiolus cultivars after the application of Trichoderma spp., but the flowering period was longer.
T. aureoviride, T. hamatum, and T. harzianum stimulated the flowering of the ‘Spitfire’ cultivar, regardless of the date of their application, but they had no effect on the size of the flowers. In comparison with the control plants, the number of buds and flowers on the plants treated with individual species of the fungi after sowing the seeds increased by 95.1% (T. aureoviride), 127.6% (T. hamatum), and 154.5% (T. harzianum). The plants treated with the fungi after being planted in pots flowered significantly more abundantly, increasing by 190.2%, 187.0%, and 209.0%, respectively (Table 2). Breeders and producers are particularly interested in the plants that flower more abundantly and can be sold as cut flowers or in pots. Researchers observed that after the application of Trichoderma spp., the following plants flowered more abundantly: Pachypodium ovifera and Crassula falcata [41], Freesia reflacta ‘Argentea’ [28], Begonia × tuberhybrida ‘Picotee Sunburst’ [13], and Gladiolus hybridus ‘Advances Red’ [14]. The latter plants also developed longer inflorescences. Sisodia et al. [40] also observed longer inflorescences on nine cultivars of Gladiolus after the application of Trichoderma spp. However, Trichoderma spp. do not always affect the quality of flowers and inflorescences in Gladiolus. The experiment conducted by da Cruz et al. [42] on the ‘Peter’s Pear’ cultivar showed no effect of the fungal treatment on the plants. The researchers stressed the fact that Freesia reflacta ‘Argentea’ produced inflorescences with the most flowers after Trichoderma fungi had been applied in treatment with plant lighting. Scientific experiments also showed that there were more flowers in the inflorescences of plants exposed to low light and treated with Trichoderma fungi [32]. These research findings are important because in areas with low light intensity, it is only possible to grow Freesia cultivars to flower in winter when the plants are illuminated with artificial light, which generates extra costs. The researchers observed that light could be partially replaced by Trichoderma spp. Andrzejak et al. [13] found that Trichoderma spp. not only caused Begonia × tuberhybrida ‘Picotee Sunburst’ to flower more abundantly but also resulted in the larger diameters of the flowers.
There was a significant dependence between the length of the shoots of the ‘Spitfire’ plants and the species of the Trichoderma fungi as well as the date of their application. The control plants had significantly shorter shoots. The plants that had been treated with the Trichoderma fungi after sowing the seeds as well as those that had been treated with T. aureoviride after being planted in pots had significantly longer shoots than the control plants. The plants that had been treated with T. hamatum and T. harzianum after being planted in pots had significantly longer shoots (Table 2). According to Lorito et al. [20], it is a fact that plants produce longer shoots when treated with Trichoderma spp. fungi. Although the mechanisms of this phenomenon have not been fully investigated, it is associated with increased uptake of nutrients and, consequently, with the better nutrition of plants. However, not all species of Trichoderma spp. stimulate shoot elongation, as evidenced by Andrzejak et al. [13] in their research on Begonia × tuberhybrida ‘Picotee Sunburst’. Yahya et al. [43] observed that T. harzianum T-22 stimulated the elongation of shoots of Lantana camara. After the application of the fungi, the shoots also grew thicker. Prisa [44] observed a similar effect in three species of the Kalanchoe genus (K. pinnata, K. tubiflora, and K. gastonis-bonnieri) after they had been treated with T. viride. According to Nieto-Jacobo et al. [22], communication between plants and Trichoderma spp. involves the recognition of fungal-derived molecules such as auxins and microbial volatile organic compounds (VOCs); however, this communication is highly dependent on the environment. Contreras-Cornejo et al. [23] suggested that Trichoderma spp. induce growth through an auxin-dependent mechanism. They showed that some Trichoderma fungi can synthesize indolyl-3-acetic acid (IAA) and some of its derivatives, allowing the root system to vigorously develop. According to these authors, many Trichoderma strains are capable of synthesizing IAA, but only a few can stimulate plant growth.
In this research, the plants treated with Trichoderma spp. tillered more intensively, regardless of the stage of the plants’ development at which the fungi had been applied. The control plants had the fewest side shoots. The plants treated with T. harzianum after being planted in the pots had the most side shoots. There was also a significantly large number of side shoots on the plants treated with T. harzianum after their seeds had been sown. There was also a greater number of side shoots on the plants treated with T. aureoviride and T. hamatum. These species of fungi were significantly more effective when applied to the plants after being planted in the pots (Table 2). The intensity of the plant tillering after the application of Trichoderma spp. has rarely been analyzed in studies on ornamental plants. Andrzejak et al. [13] showed that Trichoderma spp. had no effect on the number of shoots of Begonia × tuberhybrida ‘Picotee Sunburst’. However, according to Prisa [44], T. viride increased the number of shoots and the vegetative mass of Kalanchoe pinnata, K. tubiflora, and K. gastonis-bonnieri.
In this research, more leaves developed on the shoots after the application of Trichoderma spp., but there were no significant differences between the fungal species and the dates of their application. The plants treated with the Trichoderma fungi developed 70.3–81.3 leaves, i.e., 30–50.5% more than the control plants (Table 2). The results of our experiment were similar to the results of earlier studies on other species of ornamental plants. Andrzejak et al. [13] found that fungi of the Trichoderma genus stimulated the development of Begonia × tuberhybrida ‘Picotee Sunburst’ leaves. The fungi had no effect on the number of leaves of Tulipa gesneriana ‘Golden Parade’. However, some species of Trichoderma spp. stimulated while others inhibited the elongation of the lamina and influenced its width [39]. Yahya et al. [43] also observed that T. harzianum T-22A stimulated the development of leaves of Lantana camara. Prisa [44] found that T. viride stimulated the development of leaves of Kalanchoe sp. Additionally, the Kalanchoe sp. plants treated with T. viride had a higher leaf vitamin C content and the leaves had a greater dry weight.

3.3. Macroelements Content

In this research, the fungi of the Trichoderma genus significantly stimulated the uptake of macronutrients, except phosphorus (P). However, the uptake of calcium (Ca) and sodium (Na) was only stimulated in the plants treated with T. aureoviride and T. hamatum, whereas the uptake of magnesium (Mg) improved in those plants whose seeds had been treated with T. hamatum when sown. The plants treated with T. hamatum after sowing the seeds had the highest significant nitrogen (N) content. The content of this element in the other treatments ranged from 3.34% to 3.56% in the dry weight of the leaves. It was 16.4–24.0% greater than in the leaves of the control plants. The most intensive uptake of potassium (K) was observed in the plants treated with T. aureoviride on both dates. The K content was similar in the other treatments, but it was significantly higher than in the control plants (Table 3).
When plants are stimulated with Trichoderma fungi, they take up nutrients more intensively because their root system develops better, occupies a larger volume of the substrate, and thus reaches a greater amount of nutrients. In consequence, these plants win the competition for minerals against other plant species with less developed root systems. What is more, a more developed root system means that plants can grow in places that are not abundant in mineral compounds [18]. Some compounds, e.g., P compounds, are dissolved and retained in the biomass of Trichoderma fungi. When the fungi decompose, the compounds are released in a form available to plants near the roots [41]. Andrzejak and Janowska [14] observed better P uptake in Gladiolus hybridus ‘Advances Red’, whereas Janowska et al. [32] observed it in Freesia refracta ‘Argentea’. However, in this experiment, P was the only macronutrient whose uptake was not stimulated by the three species of fungi of the Trichoderma genus. However, like in the studies by Janowska et al. [32] and Andrzejak and Janowska [14], our experiment showed that the flowering ornamental plants took up K and Ca more intensively. Plants treated with T. harzianum were the exception.

3.4. Microelements Content

The comparison of the results of the uptake of micronutrients in the experiment showed that the Trichoderma spp. stimulated the uptake of zinc (Zn) and manganese (Mn). There was higher iron (Fe) content in the plants treated with T. harzianum on both dates and in those treated with T. aureoviride after being planted in the pots (Table 4).
Plants need small but specific amounts and proportions of microelements for proper growth and development. If any of the micronutrients is missing or deficient, the plant metabolism is disrupted. Plants take up much smaller amounts of micronutrients than macronutrients. These compounds indirectly affect plants by activating or controlling various life processes [45,46]. For example, Fe is the main component of enzymes and participates in the processes of photosynthesis and N fixation. It is also involved in the synthesis of chlorophyll and some proteins [47]. Mn activates decarboxylase, dehydrogenase, and other enzymes. It also takes part in water (H2O) decomposition and oxygen release (O2) in the photosynthesis, chlorophyll synthesis and metabolism of proteins, sugars, and lipids. Copper (Cu), which can be found in chlorophylls, is involved in the processes of photosynthesis, respiration, and lignification of the cell wall, and in the transformation of N compounds, proteins, and saccharides. Boron (B) participates in the formation of cell wall structures and the metabolism of sugars in plants. As B is not transferred from older to younger tissues, during the growing season, plants, especially those with high nutritional needs, need to take up this element to build new organs. It also influences the development of generative organs and plays an important role in the process of pollen germination and pollen tube growth. This micronutrient stimulates the development of the root system, mainly the root hair zone [47]. Studies conducted on ornamental plants showed that Trichoderma spp. affected the uptake of Zn, Fe, and B by Gladiolus hybridus ‘Advances Red’ [14] and Begonia × tuberhybrida ‘Picotee Sunburst’ [13]. Janowska et al. [32] observed that these fungi improved the uptake of Fe, Mn, and Zn by Freesia reflacta ‘Argentea’ plants grown in winter in natural light as well as by the plants illuminated with artificial light. The researchers also found that the treatment of plant illumination and Trichoderma spp. stimulated the uptake of Cu. According to Benítez et al. [24], Trichoderma spp. are able to quickly absorb the elements whose trace amounts can be found in the rhizosphere. For example, Fe is chelated by Trichoderma spp., producing siderophores. According to Altmore et al. [48], the T. harzianum T-22 isolate facilitates the absorption of insoluble or poorly soluble elements such as Fe, Cu, Zn, and Mn. It increases the solubility of minerals by acidifying the root microenvironment and reducing oxidized metal ions (Fe, Cu).
Soil microorganisms such as Trichoderma spp. should be commonly applied to improve the uptake of nutrients because, thanks to them, it is possible to reduce the amount of artificial fertilizers and thus protect the environment [49,50,51]. Biological fertilizers can be used as a complement or alternative to mineral fertilizers in sustainable plant production [51]. The practical use of Trichoderma spp. isolates in the field is mainly limited by the instability of the features responsible for their antagonism against native microflora. The practical use of Trichoderma spp. fungi in the field is also significantly limited by the fact that it is necessary to use large amounts of the biopreparation. It is much more likely that biopreparations will be applied to crops grown under cover on substrates with specific physicochemical properties [52].

4. Conclusions

The three species of Trichoderma spp. fungi influenced the flowering, quality, and nutritional status of the Tropaeolum majus ‘Spitfire’ plants. Early flowering was only influenced by T. hamatum, which delayed it by 6 days. T. aureoviride, T. hamatum, and T. harzianum stimulated the flowering of the ‘Spitfire’ cultivar but did not affect the size of the flowers. The plants treated with T. harzianum after being planted in pots flowered most abundantly. Trichoderma spp. caused the plants to grow more intensively, producing longer and more leafy shoots with a greater number of offshoots. The plants treated with T. hamatum and T. harzianum after planting in pots grew most intensively. Those treated with T. harzianum had the most offshoots. The fungi of the Trichoderma genus stimulated the uptake of macronutrients, except for phosphorus (P). In the case of calcium (Ca) and sodium (Na), a phenomenon only observed in plants treated with T. aureoviride and T. hamatum, and for magnesium (Mg), only when T. hamatum was applied to sown seeds. As far as the micronutrients are concerned, these fungi stimulated the uptake of zinc (Zn) and manganese (Mn). Apart from that, there was a higher iron (Fe) content in the plants treated with T. harzianum on both dates and T. aureoviride after planting the plants in pots. Research on Tropaeolum majus ‘Spitfire’ confirms that Trichoderma spp. have a beneficial effect on the growth and nutritional status of ornamental plants. Their use in this group of plants is beneficial to the environment and meets the requirements of sustainability. The benefits of using Trichoderma spp. to improve nutrient uptake represent an opportunity for the latest horticultural crop production methods by reducing the use of fertilizers. The use of biological fertilizers based on microorganisms is an alternative to maintain high production with a low environmental impact. Biological fertilizers can be used as a complement or alternative to mineral fertilizers in sustainable crop production.

Author Contributions

Conceptualization: R.A. and B.J.; methodology: R.A. and B.J.; formal analysis: R.A., B.J., A.R., S.S. and O.B.; funding acquisition: R.A., B.J., A.R. and S.S.; writing—original draft: R.A., B.J., A.R., S.S. and O.B.; writing—review and editing: R.A., B.J., A.R., S.S. and O.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Flowering Tropaeolum majus L. ‘Spitfire’ plant.
Figure 1. Flowering Tropaeolum majus L. ‘Spitfire’ plant.
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Figure 2. Graphical description of the experiment.
Figure 2. Graphical description of the experiment.
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Figure 3. Young plants of Tropaeolum majus L. ‘Spitfire’.
Figure 3. Young plants of Tropaeolum majus L. ‘Spitfire’.
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Figure 4. Trichoderma aureoviride (A), T. hamatum (B), and T. harzianum (C).
Figure 4. Trichoderma aureoviride (A), T. hamatum (B), and T. harzianum (C).
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Figure 5. Young plants in the growth chamber.
Figure 5. Young plants in the growth chamber.
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Table 1. Root colonization (%) of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Table 1. Root colonization (%) of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Application DateT. aureoviride (%)T. hamatum (%)T. harzianum (%)
Control0.0 a0.0 a0.0 a
After sowing the seeds48.5 b49.0 b50.0 b
After planting the plants into pots48.9 b50.7 b51.4 b
Table 2. Flowering earliness (days) and quality of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Table 2. Flowering earliness (days) and quality of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Application DateT. aureovirideT. hamatumT. harzianum
Earliness of flowering (days)
Control55.7 a55.7 a55.7 a
After sowing the seeds58.7 ab61.7 b59.7 ab
After planting the plants into pots56.7 ab58.7 ab60.3 ab
Number of buds and flowers
Control12.3 a12.3 a12.3 a
After sowing the seeds24.0 b28.0 bc31.3 cd
After planting the plants into pots35.7 de35.3 de38.0 e
Flower diameter (cm)
Control4.8 a4.8 a4.8 a
After sowing the seeds5.0 a5.0 a4.9 a
After planting the plants into pots4.9 a5.0 a5.0 a
Shoot length (cm)
Control88.1 a88.1 a88.1 a
After sowing the seeds98.1 b98.7 b100.7 b
After planting the plants into pots96.8 b101.3 c112.2 c
Number of lateral shoots
Control3.0 a3.0 a3.0 a
After sowing the seeds5.0 b5.0 b7.4 cd
After planting the plants into pots6.2 bc6.4 bc8.4 d
Number of leaves
Control54.0 a54.0 a54.0 a
After sowing the seeds70.3 b74.2 b78.6 b
After planting the plants into pots75.0 b76.8 b81.3 b
Table 3. The quantity of macroelements (% in dry weight—DW) in the leaves of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Table 3. The quantity of macroelements (% in dry weight—DW) in the leaves of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Application DateT. aureovirideT. hamatumT. harzianum
N
Control2.87 a2.87 a2.87 a
After sowing the seeds3.38 b3.68 c3.34 b
After planting the plants into pots3.56 bc3.41 b3.50 bc
P
Control0.33 a0.33 a0.33 a
After sowing the seeds0.32 a0.38 a0.29 a
After planting the plants into pots0.32 a0.38 a0.37 a
K
Control1.97 a1.97 a1.97 a
After sowing the seeds2.74 c2.31 b2.30 b
After planting the plants into pots2.75 c2.37 b2.30 b
Ca
Control1.05 ab1.05 ab1.05 ab
After sowing the seeds1.28 c1.38 d0.99 a
After planting the plants into pots1.49 e1.67 f1.12 b
Mg
Control1.28 ab1.28 ab1.28 ab
After sowing the seeds0.31 b0.41 c0.22 a
After planting the plants into pots0.22 a0.26 ab0.26 ab
Na
Control0.35 a0.35 a0.35 a
After sowing the seeds0.63 c0.48 b0.32 a
After planting the plants into pots0.49 b0.47 b0.37 a
Table 4. The quantity of microelements (mg·kg−1 in DW) in the leaves of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Table 4. The quantity of microelements (mg·kg−1 in DW) in the leaves of Tropaeolum majus ‘Spitfire’ after application of Trichoderma spp. Means followed by the same letter do not differ significantly at α = 0.05.
Application DateT. aureovirideT. hamatumT. harzianum
Fe
Control103.53 a103.53 a103.53 a
After sowing the seeds106.50 ab104.60 a123.33 cd
After planting the plants into pots117.50 bc113.30 abc133.32 d
Zn
Control30.97 a30.97 a30.97 a
After sowing the seeds45.90 cd46.27 d46.80 d
After planting the plants into pots43.57 b44.57 bc49.60 e
Mn
Control52.30 a52.30 a52.30 a
After sowing the seeds92.00 c89.80 b108.20 e
After planting the plants into pots92.37 c92.40 c98.1 d
Cu
Control3.90 ab3.90 ab3.90 ab
After sowing the seeds4.13 b4.03 ab3.73 ab
After planting the plants into pots3.63 ab3.53 a3.60 ab
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Andrzejak, R.; Janowska, B.; Rosińska, A.; Skazińska, S.; Borsai, O. Flowering, Quality and Nutritional Status of Tropaeolum majus L. ‘Spitfire’ after Application of Trichoderma spp. Sustainability 2024, 16, 4672. https://doi.org/10.3390/su16114672

AMA Style

Andrzejak R, Janowska B, Rosińska A, Skazińska S, Borsai O. Flowering, Quality and Nutritional Status of Tropaeolum majus L. ‘Spitfire’ after Application of Trichoderma spp. Sustainability. 2024; 16(11):4672. https://doi.org/10.3390/su16114672

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Andrzejak, Roman, Beata Janowska, Agnieszka Rosińska, Sylwia Skazińska, and Orsolya Borsai. 2024. "Flowering, Quality and Nutritional Status of Tropaeolum majus L. ‘Spitfire’ after Application of Trichoderma spp." Sustainability 16, no. 11: 4672. https://doi.org/10.3390/su16114672

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