Fungal endophytes of Brassicaceae: Molecular interactions and crop benefits

Abstract

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.

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

“…Endophytic fungi have received increasing interest in recent years. However, the numbers of isolates and newly described fungi are still low, especially within Brassica crops ( Poveda et al, 2022 ). The ability of different endophytic fungi to promote plant growth in crops, thanks to various mechanisms, has been widely reviewed in recent years ( Rana et al, 2019 ; Rigobelo and Baron, 2021 ).…”

“…S. sclerotiorum acts directly on these toxic hydrolysis products through an isothiocyanate hydrolase ( Chen et al, 2020 ). In the specific case of endophytic fungi, GSLs’ tolerance that supports them to colonize their hosts’ tissues is not fully understood ( Poveda et al, 2022 ). In the case of Trichoderma , the production of myrosinase-binding proteins modifies the hydrolysis of GSLs to allow/contribute to Brassicaceae root colonization ( Poveda et al, 2019 ), with the indole GSLs involved in controling the level of colonization ( Poveda, 2021 ).…”

“…Endophytic fungi could induce the expression of synthesis genes, the activation of plant enzymes that hydrolyze them, or act directly against them ( Poveda et al, 2022 ). In this sense, differences in tolerance and/or degradation of GSLs by endophytic and pathogenic fungi may be explained by specific genomic comparisons.…”

“…Conversely, few studies have focused on the diversity of endophytic fungi and their role as plant stimulators in Brassica crops ( Card et al, 2015 ; Poveda et al, 2022 ). A previous study described, for the first time, the diversity of root endophytic fungi in kale roots, and how some isolates could promote plant growth and resilience ( Poveda et al, 2020c ).…”

Key insights into secondary metabolites from various Chaetomium species

“…These metabolites are well known for their antioxidant, antibiotic, antiviral, anti-diabetic, immunosuppressive, anticancer, and insecticidal properties (Dwibedi and Saxena 2019 ; Torres-Mendoza et al 2020 ). Recently, several novel bioactive compounds have been isolated from fungal endophytes, including xylarosides, penicidones, xylariol, and benzoquinone derivatives (Poveda et al 2022 ).…”