Open Access
Endophytic fungi as direct plant growth promoters for sustainable agricultural production
(Springer, 2021) Poveda Arias, Jorge; Eugui Arrizabalaga, Daniel; Abril Urías, Patricia; Velasco, Pablo; Institute for Multidisciplinary Research in Applied Biology - IMAB
Current rates of population growth require the development of new agricultural strategies to feed the world human and livestock. The massive use of agricultural chemicals causes serious damage to the environment, and to human and animal health. For this reason, the use of endophytic fungi represents a biological alternative in increasing agricultural productivity in a sustainable way. This group of microorganisms, which inhabit plant tissues and organs without causing symptoms of damage, includes a great diversity of filamentous fungi and yeasts that are capable of increasing agricultural productivity. Some of the mechanisms involved in promoting plant growth by means of endophytic fungi include the increasing access to nutrients (nitrogen, phosphorus, potassium, zinc, iron, etc.), production of plant hormones, the ethylene amount reduction, or increase in water acquisition rate. This review tries to compile all the works carried out in the last decades on endophytic fungi use as plant growth promoters with great potential in agriculture.
Open Access
Editorial: Beneficial effects of fungal endophytes in major agricultural crops
(Frontiers Media, 2022) Poveda Arias, Jorge; Baptista, Paula; Sacristán, Soledad; Velasco, Pablo; Institute for Multidisciplinary Research in Applied Biology - IMAB
Endophytic microorganisms are those that can dwell within plant tissues without any external sign of infection or other harmful effects on the host plants (Burragoni and Jeon, 2021). In recent decades, the important role that both bacterial and fungal endophytes play in plant growth and development, as well as in their ability to survive in their environment, has been identified (Burragoni and Jeon, 2021). Endophytic fungi can be found colonizing any plant organ, presenting a very different distribution and diversity among plants of different species, among plants of the same species, and even among organs of the same plant (Aamir et al., 2020). In crops, endophytic fungi act through different beneficial pathways, as biofertilizers promoting plant growth, as biological control agents of pathogens and pests or as inducers of tolerance under abiotic stresses, having great importance in the development of new strategies for sustainable agriculture (Aamir et al., 2020). These benefits for crops have been studied in the papers published in this Research Topic: promotion of plant growth in tomato (Paradza et al.), cotton (Silva et al.) and wheat (Asim et al.), increased tolerance under salt stress in tritordeum and perennial ryegrass (Toghueo et al.), as biological control agents against pathogenic fungi through antibiosis and mycoparasitism (Silva et al.), or as insecticidal agents through activation of systemic plant defenses (Paradza et al.; Agbessenou et al.), among others.
Open Access
Fungal endophytes of Brassicaceae: molecular interactions and crop benefits
(Carnegie Institution por Science, 2022) Poveda Arias, Jorge; Díaz González, Sandra; Díaz Urbano, María; Velasco, Pablo; Sacristán, Soledad; Institute for Multidisciplinary Research in Applied Biology - IMAB
Brassicaceae family includes an important group of plants of great scientific interest, e.g., the model plant Arabidopsis thaliana, and of economic interest, such as crops of the genus Brassica (Brassica oleracea, Brassica napus, Brassica rapa, etc.). This group of plants is characterized by the synthesis and accumulation in their tissues of secondary metabolites called glucosinolates (GSLs), sulfur-containing compounds mainly involved in plant defense against pathogens and pests. Brassicaceae plants are among the 30% of plant species that cannot establish optimal associations with mycorrhizal hosts (together with other plant families such as Proteaceae, Chenopodiaceae, and Caryophyllaceae), and GSLs could be involved in this evolutionary process of non-interaction. However, this group of plants can establish beneficial interactions with endophytic fungi, which requires a reduction of defensive responses by the host plant and/or an evasion, tolerance, or suppression of plant defenses by the fungus. Although much remains to be known about the mechanisms involved in the Brassicaceae-endophyte fungal interaction, several cases have been described, in which the fungi need to interfere with the GSL synthesis and hydrolysis in the host plant, or even directly degrade GSLs before they are hydrolyzed to antifungal isothiocyanates. Once the Brassicaceae-endophyte fungus symbiosis is formed, the host plant can obtain important benefits from an agricultural point of view, such as plant growth promotion and increase in yield and quality, increased tolerance to abiotic stresses, and direct and indirect control of plant pests and diseases. This review compiles the studies on the interaction between endophytic fungi and Brassicaceae plants, discussing the mechanisms involved in the success of the symbiosis, together with the benefits obtained by these plants. Due to their unique characteristics, the family Brassicaceae can be seen as a fruitful source of novel beneficial endophytes with applications to crops, as well as to generate new models of study that allow us to better understand the interactions of these amazing fungi with plants.
Open Access
Agronomic and metabolomic side-effects of a divergent selection for indol-3-ylmethylglucosinolate content in kale (Brassica oleracea var. acephala)
(MDPI, 2021) Poveda Arias, Jorge; Velasco, Pablo; Haro, Antonio de; Johansen, Tor J.; McAlvay, Alex C.; Möllers, Christian; Mølmann, Jorgen A.B.; Ordiales, Elena; Rodríguez, Víctor Manuel; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura
Brassica oleracea var. acephala (kale) is a cruciferous vegetable widely cultivated for its leaves and flower buds in Europe and a food of global interest as a 'superfood'. Brassica crops accumulate phytochemicals called glucosinolates (GSLs) which play an important role in plant defense against biotic stresses. Studies carried out to date suggest that GSLs may have a role in the adaptation of plants to different environments, but direct evidence is lacking. We grew two kale populations divergently selected for high and low indol-3-ylmethylGSL (IM) content (H-IM and L-IM, respectively) in different environments and analyzed agronomic parameters, GSL profiles and metabolomic profile. We found a significant increase in fresh and dry foliar weight in H-IM kale populations compared to L-IM in addition to a greater accumulation of total GSLs, indole GSLs and, specifically, IM and 1-methoxyindol-3-ylmethylGSL (1MeOIM). Metabolomic analysis revealed a significant different concentration of 44 metabolites in H-IM kale populations compared to L-IM. According to tentative peak identification from MS interpretation, 80% were phenolics, including flavonoids (kaempferol, quercetin and anthocyanin derivates, including acyl flavonoids), chlorogenic acids (esters of hydroxycinnamic acids and quinic acid), hydroxycinnamic acids (ferulic acid and p-coumaric acid) and coumarins. H-IM kale populations could be more tolerant to diverse environmental conditions, possibly due to GSLs and the associated metabolites with predicted antioxidant potential.
Open Access
Glucosinolates as an effective tool in plant-parasitic nematodes control: exploiting natural plant defenses
(Elsevier, 2022) Eugui Arrizabalaga, Daniel; Escobar, Carolina; Velasco, Pablo; Poveda Arias, Jorge; Agronomia, Bioteknologia eta Elikadura; Institute for Multidisciplinary Research in Applied Biology - IMAB; Agronomía, Biotecnología y Alimentación
Plant-parasitic nematodes (PPNs) are an important damaging biotic agent for numerous crops around the world, causing serious losses directly and indirectly. Cultural and chemical control strategies were mainly used to PPNs management. However, the choice of chemical nematicides is strictly limited in the agrosystems due to their toxicity, their impact to the environment and, therefore, banning policies. The main lines of action of biological control strategies for nematode control, are based on the development of antagonist microorganism formulations and the use of plant extracts with nematicidal potential. There are many plant secondary metabolites with effective nematicidal potential. In this sense, glucosinolates (GSLs) and, especially, glucosinolate hydrolysis products (GHPs) show relevant nematicidal activity. The effects through which these compounds control nematodes, both direct and indirect are diverse, such as toxicity, anti-hatching effect or promotion of competing saprophytic nematodes or nematophagous bacteria populations. The present work compiles many of the studies that describe the use of GSLs and GHPs as nematicides in agriculture, through very diverse strategies that range from crop rotation with Brassicales to the direct application of GSLs and GHPs to the soil. The authors present GSLs and GHPs as a more sustainable and suitable alternative in nematode control, remarking the need to further research in the modes of action and the impact on environment.
Open Access
Glucosinolate-extracts from residues of conventional and organic cultivated broccoli leaves (brassica oleracea var. italica) as potential industrially-scalable efficient biopesticides against fungi, oomycetes and plant parasitic nematodes
(Elsevier, 2023) Eugui Arrizabalaga, Daniel; Velasco, Pablo; Abril Urías, Patricia; Escobar, Carolina; Gómez-Torres, Óscar; Caballero, Sara; Poveda Arias, Jorge; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura
This study aimed to standarize a protocol for obtaining a bioactive extract from broccoli (Brassica oleracea var. italica) crop residues, that is suitable for application on an industrial scale and effective in reducing plant disease incidence. For this purpose, the influence of several extraction factors in the glucosinolate (GSL) content was studied with leaves collected from two conventional broccoli fields and two organic broccoli fields. The analysis showed that lyophilization had no influence on the GSL content. Storage of plant material under two different temperatures (− 20ºC and − 80ºC) had no influence on the GSLs content of the extracts. Phytotoxicity of the extracts was studied with six different plant seeds, and also cytotoxicity was determined with human liver cells in vitro. The extracts were phytotoxic at dilutions above 10%, while cell toxicity was low. Extracts concentrations of 0.1%, 1% and 2% were tested in vitro against eight plant pathogenic fungi and two oomycetes in solid and in liquid media. The extracts reduced the growth of several plant pathogenic fungi at 2% dilution by up to 38.37% against Alternaria alternata and up to 46.55% against Sclerotinia sclerotiorum. When combined with myrosinase enzyme the effect of the extracts was enhanced, reaching inhibition values of 67.06% against A. alternata in solid medium and 68.52% against Rhizoctonia solani in liquid medium. In contrast, the same extracts increased the growth of the plant pathogenic oomycetes Pythium ultimum and Phytophthora cactorum. The effect of the same extracts in the free leaving larvae, J2s, of the plant-parasitic nematode (PPN) Meloidogyne javanica was not obvious. Minor significant differences were obtained but with no clear dose-response in nematode mortality, and no inhibition of eggs hatching was observed. These results show the industrial potential of using broccoli residues to obtain extracts with biopesticide activity against plant pathogenic fungi.
Open Access
Endophytic fungi from kale (Brassica oleracea var. acephala) modify roots-glucosinolate profile and promote plant growth in cultivated Brassica species. First description of Pyrenophora gallaeciana
(Frontiers Media, 2022) Poveda Arias, Jorge; Rodríguez, Víctor Manuel; Díaz Urbano, María; Sklenář, František; Saati-Santamaría, Zaki; Menéndez, Esther; Velasco, Pablo; Institute for Multidisciplinary Research in Applied Biology - IMAB
Endophytic fungi of crops can promote plant growth through various mechanisms of action (i.e., improve nutrient uptake and nutrient use efficiency, and produce and modulate plant hormones). The genus Brassica includes important horticultural crops, which have been little studied in their interaction with endophytic fungi. Previously, four endophytic fungi were isolated from kale roots (Brassica oleracea var. acephala), with different benefits for their host, including plant growth promotion, cold tolerance, and induction of resistance to pathogens (Xanthomonas campestris) and pests (Mamestra brassicae). In the present work, the molecular and morphological identification of the four different isolates were carried out, describing them as the species Acrocalymma vagum, Setophoma terrestris, Fusarium oxysporum, and the new species Pyrenophora gallaeciana. In addition, using a representative crop of each Brassica U’s triangle species and various in vitro biochemical tests, the ability of these fungi to promote plant growth was described. In this sense, the four fungi used promoted the growth of B. rapa, B. napus, B. nigra, B. juncea, and B. carinata, possibly due to the production of auxins, siderophores, P solubilization or cellulase, xylanase or amylase activity. Finally, the differences in root colonization between the four endophytic fungi and two pathogens (Leptosphaeria maculans and Sclerotinia sclerotiorum) and the root glucosinolate profile were studied, at different times. In this way, how the presence of progoitrin in the roots reduces their colonization by endophytic and pathogenic fungi was determined, while the possible hydrolysis of sinigrin to fungicidal products controls the colonization of endophytic fungi, but not of pathogens.
Open Access
First study on the root endophytic fungus Trichoderma hamatum as an entomopathogen: development of a fungal bioinsecticide against cotton leafworm (Spodoptera littoralis)
(Elsevier, 2023) Lana, Maite; Simón de Goñi, Oihane; Velasco, Pablo; Rodríguez, Víctor Manuel; Caballero Murillo, Primitivo; Poveda Arias, Jorge; Institute for Multidisciplinary Research in Applied Biology - IMAB; Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa
Cotton leaf worm (Spodoptera littoralis) is a pest that produces important losses in horticultural and ornamental crops in greenhouse, being classified as quarantine pest A2 by EPPO. One of the strategies proposed to control agricultural pests in a health and environmentally friendly way is biological control with entomopathogenic fungi. The genus of filamentous fungi Trichoderma includes different species with direct (infection, antibiosis, anti-feeding, etc.) and indirect (systemic activation of plant defenses) insecticidal capacity, however, the species T. hamatum has never been described previously as entomopathogenic. In this work, the entomopathogenic capacity of T. hamatum on S. littoralis L3 larvae was analyzed by applying spores and fungal filtrates (topically and orally). Infection by spores was compared with the commercial entomopathogenic fungus Beauveria bassiana, obtaining similar results with respect to the production of larval mortality. Oral application of spores reported high mortality and fungal colonization of larvae, however, T. hamatum did not show chitinase activity when grown in the presence of S. littoralis tissues. Therefore, infection of S. littoralis larvae by T. hamatum is through natural openings such as mouth, anus or spiracles. With respect to the application of filtrates, only those obtained from the liquid culture of T. hamatum in contact with S. littoralis tissues reported a significant reduction in larval growth. Metabolomic analysis of the filtrates determined that the filtrate with insecticidal capacity presented the siderophore rhizoferrin in large quantities, which could be responsible for this activity. However, the production of this siderophore had never been previously described in Trichoderma and its insecticidal capacity was unknown. In conclusion, T. hamatum presents entomopathogenic capacity against S. littoralis larvae through the application of spores and filtrates, and both ways could be the basis for the development of efficient bioinsecticides against the pest.
Open Access
Trichoderma hamatum increases productivity, glucosinolate content and antioxidant potential of different leafy Brassica vegetables
(MDPI, 2021) Velasco, Pablo; Rodríguez, Víctor Manuel; Soengas, Pilar; Poveda Arias, Jorge; Institute for Multidisciplinary Research in Applied Biology - IMAB
Brassica crops include important vegetables known as 'superfoods' due to the content of phytochemicals of great interest to human health, such as glucosinolates (GSLs) and antioxidant compounds. On the other hand, Trichoderma is a genus of filamentous fungi that includes several species described as biostimulants and/or biological control agents in agriculture. In a previous work, an endophytic strain of Trichoderma hamatum was isolated from kale roots (Brassica oleracea var. acephala), describing its ability to induce systemic resistance in its host plant. In the present work, some of the main leafy Brassica crops (kale, cabbage, leaf rape and turnip greens) have been root‐inoculated with T. hamatum, having the aim to verify the possible capacity of the fungus as a biostimulant in productivity as well as the foliar content of GSLs and its antioxidant potential, in order to improve these 'superfoods'. The results reported, for the first time, an increase in the productivity of kale (55%), cabbage (36%) and turnip greens (46%) by T. hamatum root inoculation. Furthermore, fungal inoculation reported a significant increase in the content of total GSLs in cabbage and turnip greens, mainly of the GSLs sinigrin and gluconapin, respectively, along with an increase in their antioxidant capacity. Therefore, T. hamatum could be a good agricultural biostimulant in leafy Brassica crops, increasing the content of GSLs and antioxidant potential of great food and health interest.