Priming of Plant Defenses against Ophiostoma novo-ulmi by Elm (Ulmus minor Mill.) Fungal Endophytes

Abstract

Some fungal endophytes of forest trees are recognized as beneficial symbionts against stresses. In previous works, two elm endophytes from the classes Cystobasidiomycetes and Eurotiomycetes promoted host resistance to abiotic stress, and another elm endophyte from Dothideomycetes enhanced host resistance to Dutch elm disease (DED). Here, we hypothesize that the combined effect of these endophytes activate the plant immune and/or antioxidant system, leading to a defense priming and/or increased oxidative protection when exposed to the DED pathogen Ophiostoma novo-ulmi. To test this hypothesis, the short-term defense gene activation and antioxidant response were evaluated in DED-susceptible (MDV1) and DED-resistant (VAD2 and MDV2.3) Ulmus minor genotypes inoculated with O. novo-ulmi, as well as two weeks earlier with a mixture of the above-mentioned endophytes. Endophyte inoculation induced a generalized transient defense activation mediated primarily by salicylic acid (SA). Subsequent pathogen inoculation resulted in a primed defense response of variable intensity among genotypes. Genotypes MDV1 and VAD2 displayed a defense priming driven by SA, jasmonic acid (JA), and ethylene (ET), causing a reduced pathogen spread in MDV1. Meanwhile, the genotype MDV2.3 showed lower defense priming but a stronger and earlier antioxidant response. The defense priming stimulated by elm fungal endophytes broadens our current knowledge of the ecological functions of endophytic fungi in forest trees and opens new prospects for their use in the biocontrol of plant diseases.

Deciphering the Genome-Wide Transcriptomic Changes during Interactions of Resistant and Susceptible Genotypes of American Elm with Ophiostoma novo-ulmi

“…PLDβ1 expression is repressed by salicylic acid (SA), and the mutation of PLDβ1 enhanced SA production and signaling pathways upon pathogen infection [49,50]. On the other hand, PR4 and PR5 (thaumatin 1) genes were significantly upregulated in the resistant genotype, suggesting that resistance to DED in U. americana could be attributed to the simultaneous activation of SA and JA signaling, which agrees with previous findings [9,17]. Hence, it may be inferred that in the American elm-Onu pathosystem, the RPM1-mediated activation of ETI and repression of the PLDβ1 might be crucial for the resistance, and that the Onu pathogen might induce the PLDβ1 in the susceptible, leading to the disease development.…”

“…The induction of defense-related genes and plant hormone jasmonic acid (JA) during the necrotrophic phase of DED has also been characterized as a resistance mechanism by comparing resistant and susceptible U. americana genotypes. Furthermore, at the early stage of DED, the application of salicylic acid (SA) enhanced elm resistance in the field and indicated that the coordinated action of SA and JA might be crucial in DED, as reported for resistance to diseases caused by other hemibiotrophic pathogens [9,17,18]. Despite these efforts toward dissecting the defense mechanisms against DED, the molecular responses of resistant and susceptible American elm genotypes to DED at the whole-transcriptmic level are still unknown.…”

No priming, just fighting—endophytic yeast attenuates the defense response and the stress induced by Dutch elm disease inUlmus minorMill.

“…The reduced pathogen proliferation in this genotype may be indicative of and partly explain its high DED-resistance level. This result supports a recent work where higher O. novo-ulmi dispersal was observed in M-DV1 than in M-DV2.3 plants (Martínez-Arias et al 2021a), indicating a consistent behavior of M-DV2.3 in limiting O. novo-ulmi spread when compared to other genotypes, possibly because this genotype develops vessels of smaller diameter (Pita et al 2018) and length (authors, unpublished results). In turn, colonization of plants by P5 was rather similar in all elm genotypes, with the exception of the susceptible M-DV1, whose roots showed higher presence of P5.…”

Fungal Endophytes and Their Role in Agricultural Plant Protection against Pests and Pathogens

“…Endophytes possess mechanisms such as exoenzymes to allow them access to these strengthened cells, but the deposits may prevent pathogens from doing the same [ 71 ]. Endophytes can also act as priming stimuli that induce plant defence responses through transcriptional reprogramming; for example, by modulating the expression of downstream defence-related genes such as those involved in salicylic acid, jasmonic acid and ethylene signaling pathways [ 70 , 73 , 74 , 75 , 76 ]. Colonization by endophytes (and pathogens) and subsequent metabolite secretion have also been associated with increasing the rate of photosynthesis ( Sclerotinia sclerotiorum ), chlorophyll content of plant cells, density of trichomes and stomata on plant tissues ( Beauveria bassiana ), antioxidant enzyme activity, callose deposition, cell lignification and phytoalexin accumulation ( Diaporthe liquidambaris ) [ 70 , 73 , 77 ].…”