Response of Lettuce Cultivars to Inoculation with Trichoderma spp

Journal of Scientific Research & Reports 28(2): 7-14, 2022; Article no.JSRR.84852 ISSN: 2320-0227 Response of Lettuce Cultivars to Inoculation with Trichoderma spp. Rejayne Barbosa Lima a, Cleia Santos Cabral b, Lincon Rafael da Silva c, Luis Alberto Martins Palhares de Melo c, Paulo Henrique Pereira Costa Muniz d and Sueli Corrêa Marques de Mello c* a Department of Phytopathology, University of Brasilia, Brasília/Federal District, Brazil. b Unidesc University Center, Valparaíso de Goiás/Goiás, Brazil. c Embrapa Genetic Resources and Biotechnology, Brasília/Federal. District, Brazil. d Laboratory of Phytopathology, State University of Goiás, Ipameri/Goiás, Brazil. Authors’ contributions This work was carried out in collaboration among all authors. All authors read and approved the final manuscript. Article Information DOI: 10.9734/JSRR/2022/v28i230496 Open Peer Review History: This journal follows the Advanced Open Peer Review policy. Identity of the Reviewers, Editor(s) and additional Reviewers, peer review comments, different versions of the manuscript, comments of the editors, etc are available here: https://www.sdiarticle5.com/review-history/84852 Original Research Article Received 19 January2022 Accepted 24 March 2022 Published 29 March 2022 ABSTRACT Fungi of the Trichoderma genus are present in practically all types of soil and they have the ability to establish a beneficial relationship with plants. In addition to acting as direct biological control agents, they also act as plant growth promoters, by an indirect biological control mechanism. Because of these, many products containing Trichoderma strains are used to improve seed health, providing better development of roots and aerial parts of plants. In view of this fact, research work was carried out in a greenhouse with the aim of evaluating the effect of five Trichoderma strains, belonging to the species T. virens, T. asperellum, T. asperelloides, in addition to a strain unidentified at the species level T. koningiopsis, in three new crisp lettuce cultivars (BRS Lélia, BRS Leila, and BRS Mediterrânea). A conidial suspension of each of the strains was prepared (1.0 7 -1 x 10 conidia mL ) and applied at the time of sowing the lettuce in pots. The experiment was completely randomized in a factorial 5x3 design (Trichoderma spp. x cultivars). Control treatments consisted of pots containing plants without any of the fungi. All Trichoderma strains applied increased fresh mass and length of root, fresh mass of aerial part and lettuce height in comparison to the controls treated just with water. The cultivar BRS Leila showed an increase of 44% in fresh root mass, 45% in fresh mass of aerial part, with T. virens; 15% in plant height with T. koningiopsis, _____________________________________________________________________________________________________ *Corresponding author: E-mail: sueli.mello@embrapa.br; Lima et al.; JSRR, 28(2): 7-14, 2022; Article no.JSRR.84852 and 23.94% in root length, with Trichoderma sp. For ‘BRS Lélia’ the highest values of fresh root mass, fresh mass of aerial part and root length were 30%, 36.71%, and 13.33% with T. asperellum. Trichoderma asperelloides provided 13.72% increase in height compared to the control. ‘BRS Mediterrânea’ showed increments of 75% of fresh root mass, 78.45% of fresh mass of aerial part, and 44.37% of height with T. virens. With T. asperelloides, 40.61% was observed in root length. The strain T. virens performed better in all the analyzed variables, except for root length. Keywords: Biological control; lettuce genotypes; antagonistic fungi; plant growth promotion; lactuca sativa; microbiolization. 1. INTRODUCTION same time. Among these mechanisms are the synthesis of growth-stimulating substances, such as phytohormones and the ability to solubilize nutrients present in soil and make them available to be absorbed by the roots of plants, while reducing costs of mineral and organic fertilizers [5]. Given the above, the purpose of work was to analyze the effect of Trichoderma spp. applied in the planting furrow, using distinct lettuce cultivars. Lettuce (Lactuca sativa L.) is among the most cultivated and consumed leafy vegetables worldwide. Its short cycle allows planting throughout the year in different production and cultivation systems [1,2,3]. However, some aspects influence the development of this vegetable species, from the establishment of the culture to the harvest. For example, good germination generates vigorous seedlings for transplanting and will have an effect on the volume and quality of the product to be marketed. Thus, the proper treatment of seeds before being sown in the substrate is of great importance [4]. In this context, a study was carried out in the greenhouse with the aim of evaluating the effect of five Trichoderma strains, belonging to the species T. virens, T. asperellum, T. asperelloides, and T. koningiopsis, in addition to a strain unidentified at the species level, in three new crisp lettuce cultivars. Among the products available for use in seed treatment there are several biofungicides and biostimulators based on Trichoderma. This important genus contains more than 300 accepted species. Besides, these fungi are considered cosmopolitan, inhabiting different ecological niches, and they are able to colonize practically all types of soil [5,6]. Several Trichoderma species perform antagonism against phytopathogenic agents, especially bacteria and fungi. Their various mechanisms of action have been widely studied in recent decades, supporting the development and use of these products with relative success among food producers on farms [7]. Plant growth promotion is an indirect biological control mechanism, by which the action of these fungi improves germination and seedling health in lettuce by various paths. They promote the development of roots and aerial parts and make plants more resistant to invasion by phytopathogens [8]. 2. MATERIALS AND METHODS 2.1 Lettuce Cultivars and Trichoderma Strains used The experiments were conducted under greenhouse conditions with five strains of Trichoderma spp. (Trichoderma sp., T. virens, T. asperellum, T. koningiopsis, and T. asperelloides) and three crisp varietal types of lettuce (‘BRS Leila’, ‘BRS Lélia’ and ‘BRS Mediterrânea’). The strains used belong to the Collection of Biological Control Agents from Embrapa Genetic Resources and Biotechnology, Brasilia, Federal District, Brazil. They were multiplied in Petri dishes (90 x 15 mm) containing Potato Dextrose Agar (PDA) in a BOD incubator ® (Nova Técnica ) at 25±1 ºC for seven days. After this period, the spores were collected in sterilized distilled water, by scraping the surface of the colonized medium to obtain the full suspension. Fungal suspensions were homogenized by stirring in a magnetic stirrer (Vortex type). An aliquot of 200 μL of this suspension was used to fill the Neubauer chamber and count the spores in each sample. Numerous research papers report positive effects of Trichoderma application as a plant growth promoter in different cultivated plant species [9,10,11,12]. Strains of this fungus are able to establish interactions with plant roots, enabling an increase in quality and quantity of biomass, through different mechanisms at the 8 Lima et al.; JSRR, 28(2): 7-14, 2022; Article no.JSRR.84852 2.2 In vivo Growth Promotion Tests root mass in cultivar BRS Leila was verified with T. virens, whose average value of 11.97 g meant an increase of 44% in relation to the control (Table 1). This treatment differed from the control, as well as from the treatment with Trichoderma sp. For the cultivar BRS Lélia, there was no statistical difference among species used, for which the averages ranged from 7.43 to 9.92 g. Also, no differences were observed in relation to the control treatment. As for the cultivar BRS Mediterrânea, once again the treatment with T. virens was higher, with a mean value of 13.28 g, although it did not differ statistically from T. koningiopsis, whose mean value was 9.94. This last species, in turn, did not differ significantly from the other three, Trichoderma sp., T. asperelloides and T. asperellum, achieving averages of 7.26, 7.88 and 8.60 g, respectively, of fresh root mass. Suspensions of Trichoderma spp. were evaluated as described in the previous paragraph and spore concentrations adjusted to 1 x 107 conidia mL-1. The lettuce seeds disinfected by immersing them in 70% ethanol for 1 minute, a 2% sodium hypochlorite solution for 1 minute, were rinsed twice in distilled and autoclaved water. Pots with a 1 L capacity were filled with autoclaved substrate (BioPlant Plus®) and three lettuce seeds were sown per pot. Then, the substrate was inoculated with 2 mL of suspension representing each treatment. The pots containing lettuce plants with water were used as control. The pots were randomly distributed on the benches of the greenhouse. Irrigation was daily and no fertilizer was used. In order to keep one plant per pot, thinning was conducted after germination of the seeds. The plant height, root length, fresh mass of root and aerial part were checked and measured with a millimeter ruler and weighed on a precision balance 30 days after inoculation of Trichoderma spp. [11]. Considering the variable fresh mass of aerial parts of lettuce plants, there was no significant difference amount Trichoderma strains when tested with the cultivars, except with ‘BRS Mediterrânea’. For this cultivar, a better performance was observed (20.14 g) when treated with T. virens, meaning an increase of 80% compared to the control treatment, also differing from Trichoderma sp. The latter did not differ from T. asperellum, T. asperelloides and T. koningiopsis treatments, nor from the control (Table 2). 2.3 Statistical Analysis This trial was designed with 15 treatments, consisting of three cultivars, five strains of Trichoderma spp. Five repetitions were performed for each treatment. The arrangement adopted was a 3 x 5 factorial randomly distributed. The values of root and fresh mass of aerial part, plant height and root length were subjected to analysis of variance (ANOVA) and the means were compared by the Tukey test (P≤0.05), using the R software [13]. Regarding the variable height of plants, there was no statistical difference amount the treatments with Trichoderma, for the three cultivars tested. The cultivar BRS Mediterrânea was the only one for which there was a significant difference in treatments with Trichoderma spp. in relation to the control treatment. Nonetheless, the height averages ranged from 14.04 to 16.00 cm, meaning an increase of 36 to 45%, compared to the treatment without Trichoderma (Table 3). 3. RESULTS AND DISCUSSION Thirty days after inoculation, positive differences in root fresh mass, fresh mass of aerial part, plant height and root length varied according to cultivar, as well as in relation to Trichoderma strains. The best performance in terms of fresh Table 1. Fresh root mass (F.R.M) for different lettuce cultivars 30 days after inoculation (DAI) with Trichoderma spp. Strains of Trichoderma Trichoderma sp. T. virens T. asperellum T. asperelloides T. koningiopsis Control F.R.M per cultivar (g) BRS Lélia BRS Mediterrânea 9.15±2.71a 7.26±2.27bc 7.43±3.13a 13.28±2.01a 9.92±1.77a 8.60±1.33b 8.85±2.03a 7.88±2.99b 8.53±2.22a 9.94±1.22ab 6.96±3.05a 3.30±1.79c BRS Leila 6.80±1.66b 11.97±3.38a 7.90±1.19ab 8.18±2.37ab 8.30±2.23ab 6.72±2.38b Means followed by the same letter in the same column do not differ significantly at the 5% level by the Tukey test 9 Lima et al.; JSRR, 28(2): 7-14, 2022; Article no.JSRR.84852 Table 2. Fresh mass of aerial part (F.M.A.P) of different lettuce cultivars 30 days after inoculation (DAI) with Trichoderma spp. Strains of Trichoderma Trichoderma sp. T. virens T. asperellum T. asperelloides T. koningiopsis Control F.M.A.P per cultivar (g) BRS Lélia BRS Mediterrânea 11.57±4.80a 11.66±3.33bc 9.83±7.63a 20.14±4.66a 15.17±5.79a 16.30±4.35ab 12.58±3.05a 15.14±5.31ab 13.20±2.89a 16.54±3.69ab 9.60±4.54a 4.34±2.26c BRS Leila 11.62±3.46a 13.70±2.02a 10.78±1.33a 10.90±3.73a 12.40±1.90a 7.48±2.52a Means followed by the same letter in the same column do not differ significantly at the 5% level by the Tukey test Table 3. Plant height (P.H) of different lettuce cultivars at 30 days after inoculation (DAI) with Trichoderma spp. Strains of Trichoderma Trichoderma sp. T. virens T. asperellum T. asperelloides T. koningiopsis Control P.H per cultivar (cm) BRS Lélia BRS Mediterrânea 11.78±2.02a 14.04±1.44a 10.28±3.25a 16.00±1.15a 11.43±1.65a 15.30±1.10a 12.75±1.72a 15.30±1.60a 11.83±2.77a 15.06±0.44a 11.00±1.00a 8.90±1.02b BRS Leila 13.00±0.00a 14.00±0.82a 11.50±1.29a 13.00±1.41a 14.25±0.96a 12.10±0.22a Means followed by the same letter in the same column do not differ significantly at the 5% level by the Tukey test Table 4. Root length (R.L) of different lettuce cultivars at 30 days after inoculation (DAI) with Trichoderma spp. Strains of Trichoderma Trichoderma sp. T. virens T. asperellum T. asperelloides T. koningiopsis Control R.L per cultivar (cm) BRS Lélia 15.25±0.76b 18.03±2.00ab 19.50±3.27a 17.33±0.52ab 17.00±1.26ab 16.90±3.13ab BRS Leila 17.75±2.75a 15.75±2.22ab 16.50±1.29ab 15.75±2.22ab 15.75±1.50ab 13.50±1.94b BRS Mediterrânea 16.24±2.15bc 16.58±1.43bc 17.02±1.15b 22.06±2.12a 15.46±1.34bc 13.10±3.25c Means followed by the same letter in the same column do not differ significantly at the 5% level by the Tukey test With respect to the length of the roots, considering the cultivar BRS Leila, all treatments with Trichoderma differed from the control, although they did not differ from each other. For the cultivar BRS Lélia, T. asperellum showed to be statistically different from Trichoderma sp., the latter presenting a lower mean value (15.25 g). For the cultivar BRS Mediterrânea, the best result was obtained with T. asperelloides, which differed statistically from the others, with an average value of 22.06 cm. This result showed 40% more root length compared to the control. T. asperellum also showed a 23% increase in root length (17.02 cm) and thus also differed significantly from the control (Table 4). germination, rooting, sprouting of cuttings, growth of branches, increase in leaf area, delay in senescence, accumulation of organic matter (fresh and dry mass) and increase in crop yield [12,14]. These effects are highly variable, due to a number of factors, including crop type, growing conditions, inoculum rate, and formulation type. Ozdemir et al. [15] showed that the application of T. harzianum in lettuce plants promotes higher chlorophyll content in the leaves, a photosynthetic pigment that is directly related to the production of plant biomass. This attests to the growing interest in the study of Trichoderma spp. both in the control of plant diseases and in the promotion of plant growth by these fungi. The effect of Trichoderma spp. development can be observed In this present study, there was a higher fresh root mass in two of the cultivars tested, BRS on in plant seed 10 Lima et al.; JSRR, 28(2): 7-14, 2022; Article no.JSRR.84852 The data obtained here regarding the promotion of root length in lettuce plants are in accordance with Silva et al. [22]. These authors suggested that Trichoderma spp. act as root growth promoters as well. According to Altomare et al. [26], there is a balance of nutrients in the soil that is influenced by the microflora, directly affecting nutrient absorption by plant roots. These authors postulate that plant growth promoted by Trichoderma may result from the ability of this fungus to provide essential nutrients for the plant`s healthy development. Leila and BRS Mediterrânea. The fitness of Trichoderma spp. in promoting plant root development has been reported with other plant species, including vegetables such as cucumber, strawberry, tomato, pepper, cabbage and beet [16-20). Yedidia et al. [16] suggest that this effect of greater root growth in plants inoculated with Trichoderma is due to the colonization of the fungus in the rhizosphere, providing a positive effect on the mycorrhizal interaction with plants. More highly developed roots allow plants to explore a greater volume of soil and consequently absorb a higher amount of available nutrients. Among all the cultivars evaluated, only BRS Mediterrânea showed a significant increase in fresh mass of the aerial part compared to the control. This positive effect of Trichoderma species is very important for increasing lettuce yield, as the final commercialized product is its leaves. The better the appearance of the harvested product, the greater the profits for producers. Pereira et al. [14] obtained an increase in fresh mass with T. harzianum and T. asperellum strains, where the gain of fresh mass of the aerial part was approximately 40% higher than the control. Steffen et al. [21] evaluated the potential of two non-commercial strains of Trichoderma asperelloides and T. virens for their ability to increase cabbage yield under field conditions and verified an increase of 36.65% and 47.97% in leaf fresh mass commercialized in the first harvest, demonstrating the potential of this fungus in other vegetables. Several studies have been conducted with species of Trichoderma to verify the relationship of its inoculation with increased vegetative growth and productivity. It was shown that growth promotion by Trichoderma species was dependent on their ability to colonize plant roots [27]. When T. brevicrassum TC967 colonized the surface of the cucumber roots, cucumber growth was promoted [28]. Ousley et al. [29] observed that some Trichoderma strains inhibited lettuce seed germination but also promoted plant growth, which may also depend on the strain, method of preparation and application of the inoculum. The potential of Trichoderma spp. in plant growth promotion, as in the case studied in this work, may be related to the increase in the synthesis of plant hormones such as auxins and ethylene [30]. Auxins are important in plant development and are associated with vital plant functions such as cell division, multiplication and elongation. Ethylene, on the other hand, can reorganize the cell wall microfibrils. This reorganization reduces height growth and provides greater radial growth of plant tissues, making them more vigorous [31]. The best plant height performance obtained with the BRS Mediterrânea cultivar is close to the values verified with the Regina cultivar in the study conducted by Silva et al. [22], in which they reached an increase of 34% in relation to the control without inoculation of Trichoderma. The ability of Trichoderma to promote plant height gains has been attributed to the production of phytohormones and greater efficiency in the use of nutrients [10]. The use of these fungi in crop production is an interesting biotechnological tool to increase productivity. Recent discoveries reinforce the idea that some biological control agents can have several positive effects on plants, in addition to disease control. This effect includes the stimulation of plant growth, increased yield, greater bioavailability and nutrient absorption, as well as improving the quality of the commercialized products as a result of sustainable production [7,23,24,25]. Many products containing Trichoderma have been commercially available since the rise of biological control in modern agriculture. Their availability provided an opportunity for farmers become familiar with the benefits of applying these fungi on their crops. Plant growth promotion microorganisms for agriculture, biotechnology and nanotechnology exploit actinomycetes, bacteria, fungi and cyanobacteria, and their usage makes it possible to produce vegetables without chemical fertilizers and phytosanitary products. Combining all their natural multidimensional attributions in microbiology, based on the ability of Trichoderma inoculation to increase plant growth and stimulate plant defense mechanisms, researchers are continuing to explore these 11 Lima et al.; JSRR, 28(2): 7-14, 2022; Article no.JSRR.84852 species` effectiveness in controlling transmitted fungal and bacterial diseases. soil3. The results achieved in this study demonstrated the diversity of Trichoderma benefits and showed a positive contribution to the growth of BRS Leila, BRS Lélia and BRS Mediterrânea cultivars. Lettuce growth promotion under greenhouse conditions 30 days after inoculating the strains was significant. The growth promotion resulting from application of the strains tested here needs further investigation for application in seedling growth promotion as well. These results should further contribute to knowledge about plant nutrition and biological control of plant diseases, through the direct and indirect mechanisms of Trichoderma. 4. 5. 6. 4. CONCLUSION 1. Trichoderma virens was the species that most contributed to an increment in the analyzed variables. 2. Among the cultivars tested, BRS Mediterrânea was the one that best responded to the inoculation of Trichoderma spp. 3. Among the tested cultivars, BRS Lélia was the least responsive to Trichoderma spp. inoculation, but showed increases in all analyzed variables. 7. 8. DISCLAIMER The products used for this research are commonly and predominantly used products in our area of research and country. There is absolutely no conflict of interest between the authors and producers of the products because we do not intend to use these products as an avenue for any litigation but for the advancement of knowledge. The research was not funded by the producing company; instead, it was funded by personal efforts of the authors. 9. COMPETING INTERESTS Authors have interests exist. declared that 10. no competing REFERENCES 1. 2. Ryder EJ. Lettuce, Endive and Chicory: th crop production science in Horticulture. 1 ed. US Department of Agriculture, Agricultural Research Service, New York: CABI Publishing;1999. Sala FC, Costa CP. Melhoramento de alface, In: Nick C, Bórem A, editors. 11. 12 Melhoramento de Hortaliças, Viçosa: UFV;2016. Azevedo Filho JA. A cultura da alface, In: Collariccio A, Chaves ALR, editors. Aspectos fitossanitários da cultura da th alface, São Paulo: Instituto Biológico, 29 ed; 2017. Paula Júnior TJ, Venzon M. 101 Culturas: th Manual de tecnologia agrícola. 3 ed. 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Plant Physiology. 5th ed. ol.2019.104151 Sinauer: Sunderland. 2013;952. _______________________________________________________________________________ © 2022 Lima et al.; This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Peer-review history: The peer review history for this paper can be accessed here: https://www.sdiarticle5.com/review-history/84852 14