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
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
Combined use of Trichoderma and beneficial bacteria (mainly Bacillus and Pseudomonas): development of microbial synergistic bio-inoculants in sustainable agriculture
(Elsevier, 2022) Poveda Arias, Jorge; Eugui Arrizabalaga, Daniel; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura
Agriculture nowadays is facing many challenges, with among the most important to be able to feed the increasing human population through more sustainable and environmentally friendly production. In this context, the use of microorganisms has been extensively studied, both with fungi such as Trichoderma spp. and with bacteria, such as Bacillus spp. or Pseudomonas spp. While inoculation with these microorganisms has a positive effect on crops, their combination offers even greater potential as plant growth promoters and as biocontrol agents, with diverse mechanisms that are thoroughly considered in this review. Synergies between Trichoderma and bacteria cause more benefits than the sum of their parts, and this makes them a promising alternative for managing crops and controlling diseases or pests in modern agriculture. However, more studies are needed to determine the specific mechanisms of this synergistic effect in certain lines of research, since there is extensive data about their use as plant growth promoters or biocontrol agents against diseases and certain pests, but little or no information is available about their use against diseases caused by viruses or the effect on plant tolerance to abiotic stresses.
Open Access
Deciphering plant health status: the link between secondary metabolites, fungal community and disease incidence in olive tree
(Frontiers Media, 2023) Gomes, Teresa; Pereira, José Alberto; Moya-Laraño, Jordi; Poveda Arias, Jorge; Lino-Neto, Teresa; Baptista, Paula; Institute for Multidisciplinary Research in Applied Biology - IMAB; Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa
Plant-associated microorganisms are increasingly recognized to play key roles in host health. Among several strategies, associated microorganisms can promote the production of specific metabolites by their hosts. However, there is still a huge gap in the understanding of such mechanisms in plant-microorganism interaction. Here, we want to determine whether different levels of olive leaf spot (OLS) disease incidence were related to differences in the composition of fungal and secondary metabolites (i.e. phenolic and volatile compounds) in leaves from olive tree cultivars with contrasting OLS susceptibilities (ranging from tolerant to highly susceptible). Accordingly, leaves with three levels of OLS incidence from both cultivars were used to assess epiphytic and endophytic fungal communities, by barcoding of cultivable isolates, as well as to evaluate leaf phenolic and volatile composition. Fungal and metabolite compositions variations were detected according to the level of disease incidence. Changes were particularly noticed for OLS-tolerant cultivars, opposing to OLS-susceptible cultivars, suggesting that disease development is linked, not only to leaf fungal and metabolite composition, but also to host genotype. A set of metabolites/fungi that can act as predictive biomarkers of plant tolerance/susceptibility to OLS disease were identified. The metabolites ¿-farnesene and p-cymene, and the fungi Fusarium sp. and Alternaria sp. were more related to disease incidence, while Pyronema domesticum was related to the absence of disease symptoms. Cultivar susceptibility to OLS disease is then suggested to be driven by fungi, volatile and phenolic host leaves composition, and above all to plant-fungus interaction. A deeper understanding of these complex interactions may unravel plant defensive responses.
Open Access
Mechanisms involved in drought stress tolerance triggered by rhizobia strains in wheat
(Frontiers Media, 2022) Barquero, Marcia; Poveda Arias, Jorge; Laureano Marín, Ana M.; Ortiz Liébana, Noemí; Brañas, Javier; González Andrés, Fernando; Institute for Multidisciplinary Research in Applied Biology - IMAB
Rhizobium spp. is a well-known microbial plant biostimulant in non-legume crops, but little is known about the mechanisms by which rhizobia enhance crop productivity under drought stress. This work analyzed the mechanisms involved in drought stress alleviation exerted by Rhizobium leguminosarum strains in wheat plants under water shortage conditions. Two (LBM1210 and LET4910) of the four R. leguminosarum strains significantly improved the growth parameters (fresh and dry aerial weight, FW and DW, respectively), chlorophyll content, and relative water content (RWC) compared to a non-inoculated control under water stress, providing values similar to or even higher for FW (+4%) and RWC (+2.3%) than the non-inoculated and non-stressed control. Some other biochemical parameters and gene expression explain the observed drought stress alleviation, namely the reduction of MDA, H2O2 (stronger when inoculating with LET4910), and ABA content (stronger when inoculating with LBM1210). In agreement with these results, inoculation with LET4910 downregulated DREB2 and CAT1 genes in plants under water deficiency and upregulated the CYP707A1 gene, while inoculation with LBM1210 strongly upregulated the CYP707A1 gene, which encodes an ABA catabolic enzyme. Conversely, from our results, ethylene metabolism did not seem to be involved in the alleviation of drought stress exerted by the two strains, as the expression of the CTR1 gene was very similar in all treatments and controls. The obtained results regarding the effect of the analyzed strains in alleviating drought stress are very relevant in the present situation of climate change, which negatively influences agricultural production.
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
Filamentous fungi as biocontrol agents in olive (Olea europaea L.) diseases: mycorrhizal and endophytic fungi
(Elsevier, 2021) Poveda Arias, Jorge; Baptista, Paula; Institute for Multidisciplinary Research in Applied Biology - IMAB
Olive (Olea europaea) is a crop of great agronomic, economic and cultural interest for the Mediterranean Basin, although the increase in world demand for olive oil is expanding its cultivation by other countries in the southern hemisphere. The main olive pathogens include bacteria (Pseudomonas savastanoi pv. savastanoi, Xylella fastidiosa), fungi (Colletotrichum spp., Verticillium dahliae, Fusarium spp. Rhizoctonia solani), oomycetes (Phytophthora spp.) and nematodes (Meloidogyne spp.). To combat these pathogens, different biocontrol strategies have been developed with bacteria and yeasts, although its capacity for establishment in the field entails several difficulties. In this sense, filamentous fungi represent an efficient and effective alternative in the control of the different pathogens of the olive tree. The present review compiles all the studies existing so far in the biocontrol of these pathogens through the use of mycorrhizal and endophytic filamentous fungi, making a separate section for the genus Trichoderma due to the special interest that their use has generated. The mechanisms used by these fungi include competition for space and nutrients, parasitism, antibiosis or activation of the plant's defensive responses, among others.
Open Access
Microorganisms as biocontrol agents against bacterial citrus diseases
(Elsevier, 2021) Poveda Arias, Jorge; Roeschlin, Roxana Andrea; Marano, María Rosa; Favaro, María Alejandra; Institute for Multidisciplinary Research in Applied Biology - IMAB
Citrus represents one of the most widely grown crops on the planet, extensively cultivated for both the fresh fruit and juice markets. The productivity of citrus orchards can be seriously affected by highly aggressive pathogenic bacteria, such as Xanthomonas citri subsp. citri, Xylella fastidiosa subsp. pauca and currently Candidatus Liberibacter asiaticus. Different microbiological biocontrol agents have been described against these pathogens, such as antagonistic bacteria (mainly species from Pseudomonas and Bacillus genus) and bacteriophages. This review summarizes all the microbiological control strategies reported so far against bacterial diseases that affect citrus, highlighting those fields of study where there is great potential yet to be discovered.
Open Access
Broccoli (Brassica oleracea var. italica) biomass as a resource for obtaining glucosinolate extracts to control postharvest fungal diseases
(Springer, 2025-05-27) Eugui Arrizabalaga, Daniel; Fernández San Millán, Alicia; Velasco, Pablo; Veramendi Charola, Jon; Rodríguez, Víctor Manuel; Poveda Arias, Jorge; Agronomía, Biotecnología y Alimentación; Agronomia, Bioteknologia eta Elikadura; Institute for Multidisciplinary Research in Applied Biology - IMAB
Broccoli (Brassica oleracea var. italica) is a crop of great agronomic and economic importance worldwide. Because its edible parts are the inflorescences, large quantities of non-commercial biomass are produced each year in the field and in the food industry. In order to develop a circular economy around the broccoli crop, the present work develops glucosinolates (GSL) extracts with antimicrobial capacity for postharvest use in tomato, apple and table white grape against fungal diseases produced by the pathogens Botrytis cinerea, Alternaria alternata and Penicillium expansum. GSL extracts from organic crop management reported a higher content of GSLs than conventional management. These extracts are not effective in the control of A. alternata and P. expansum, possibly due to the absence of sinigrin. Furthermore, the extracts were ineffective in the control of B. cinerea on table white grapes, possibly due to the non-climacteric fruit condition and an absence in the induction of ethylene-mediated plant defenses. However, intact GSL extracts were effective in controlling B. cinerea on apple, while the addition of myrosinase enzyme caused effectiveness also on tomato and apple. Therefore, obtaining GSL extracts with biopesticidal capacity against B. cinerea in postharvest could be a circular economy strategy for broccoli agriculture and industry.
Open Access
Activation of sweet pepper defense responses by novel and known biocontrol agents of the genus Bacillus against Botrytis cinerea and Verticillium dahliae
(Springer, 2022) Poveda Arias, Jorge; Calvo, Javier; Barquero, Marcia; González Andrés, Fernando; Institute for Multidisciplinary Research in Applied Biology - IMAB; Universidad Pública de Navarra / Nafarroako Unibertsitate Publikoa
The Fresno-Benavente Pepper (F-BP) Protected Geographical Indication (PGI) is a horticultural crop characterized by its great agronomic, economic and cultural importance in the region of Castilla y León (Spain). Field production is threatened by verticillium wilt caused by Verticillium dahliae and postharvest losses due to grey mould caused by Botrytis cinerea. Eight Bacillus spp. strains endophytically isolated from F-BP roots were used in the study. By conducting an in vitro antagonism study, we found that all Bacillus strains were effective against B. cinerea and five of them showed high antagonism against V. dahliae, with B. siamensis and B. proteolyticus strains being the most effective against both pathogens. Eight Bacillus strains were used for an infection test in F-BP fruits and plants to test their activity against both fungal pathogens. We report that Bacillus thuringiensis, B. siamensis and B. pumilus (SCFC 1–2) could control B. cinerea in pepper fruits through direct action and local activation of plant defences. In the case of V. dahliae root infection, plant roots inoculated with B. siamensis and B. proteolyticus were able to significantly decrease the occurrence of disease through direct action and local activation of jasmonic acid as a defence response. Therefore, we propose that B. siamensis could be used to control B. cinerea and V. dahliae in F-BP fruits and plants, respectively, through direct antagonism as well as the induction of local plant defence responses.