Interactive Effects of Mycorrhizae, Soil Phosphorus, and Light on Growth and Induction and Priming of Defense in Plantago lanceolata

Abstract

Increasing demands to reduce fertilizer and pesticide input in agriculture has triggered interest in arbuscular mycorrhizal fungi (AMF) that can enhance plant growth and confer mycorrhiza-induced resistance (MIR). MIR can be based on a variety of mechanisms, including induction of defense compounds, and sensitization of the plant’s immune system (priming) for enhanced defense against later arriving pests or pathogens signaled through jasmonic acid (JA). However, growth and resistance benefits of AMF highly depend on environmental conditions. Low soil P and non-limiting light conditions are expected to enhance MIR, as these conditions favor AMF colonization and because of observed positive cross-talk between the plant’s phosphate starvation response (PSR) and JA-dependent immunity. We therefore tested growth and resistance benefits of the AMF Funneliformis mosseae in Plantago lanceolata plants grown under different levels of soil P and light intensity. Resistance benefits were assessed in bioassays with the leaf chewing herbivore Mamestra brassicae. Half of the plants were induced by jasmonic acid prior to the bioassays to specifically test whether AMF primed plants for JA-signaled defense under different abiotic conditions. AMF reduced biomass production but contrary to prediction, this reduction was not strongest under conditions considered least optimal for carbon-for-nutrient trade (low light, high soil P). JA application induced resistance to M. brassicae, but its extent was independent of soil P and light conditions. Strikingly, in younger plants, JA-induced resistance was annulled by AMF under high resource conditions (high soil P, ample light), indicating that AMF did not prime but repressed JA-induced defense responses. In older plants, low soil P and light enhanced susceptibility to M. brassicae due to enhanced leaf nitrogen levels and reduced leaf levels of the defense metabolite catalpol. By contrast, in younger plants, low soil P enhanced resistance. Our results highlight that defense priming by AMF is not ubiquitous and calls for studies revealing the causes of the increasingly observed repression of JA-mediated defense by AMF. Our study further shows that in our system abiotic factors are significant modulators of defense responses, but more strongly so by directly modulating leaf quality than by modulating the effects of beneficial microbes on resistance.

Mycorrhiza-Induced Resistance against Foliar Pathogens Is Uncoupled of Nutritional Effects under Different Light Intensities

“…Our results indicate that under our experimental conditions, the costs of the high colonization rates and vesicle formation seem to override the photosynthetic and nutritional benefits of the symbiosis. While growth promotion is a common feature of mycorrhizal symbiosis, growth depression has also been reported even within the same plant–AMF combination, and these contrasting mycorrhizal growth responses commonly depend on environmental conditions [ 33 , 34 , 35 ]. In agreement with this, our results support that the effects of mycorrhizal inoculation on plant growth and nutrient acquisition depend on light availability.…”

“…The fungi deliver to the root cells P acquired by their network of extraradical mycelia from soil areas hardly accessible to roots, and other nutritional benefits have been reported, including improved iron, zinc, copper, sulfur, and nitrogen acquisition [ 15 , 29 ]. In return, it has been estimated that up to 20% of plant-fixed carbon compounds can be transferred to the AMF [ 30 ] constituting the “symbiotic costs.” A delicate balance between the symbiosis costs and benefits rules the interaction, and although growth promotion is common in mycorrhizal plants, negative mycorrhizal growth responses (MGR) have also been observed in certain plant–AMF combinations or environmental conditions [ 31 , 32 , 33 , 34 , 35 ]. It is accepted that plants control the extent of fungal colonization according to the environmental conditions and their needs [ 16 ].…”

“…It has been reported that in plants colonized by multiple AMF, plant preferential allocation of resources towards the most beneficial mutualist depends upon above-ground resources [ 36 ]. Thus, understanding the regulation of AM symbiosis and its benefits under different conditions is required to understand its context-dependency [ 16 , 33 , 35 , 37 ].…”

Pseudomonas Inoculation Stimulates Endophytic Azospira Population and Induces Systemic Resistance to Bacterial Wilt

“…Soil is closely associated with the fitness, growth, and immunity of plants (Mendes et al, 2011;Qu et al, 2021). The balance of the soil ecosystem is key to the healthy growth of plants, whereas the outbreak of soil-borne disease is the most intuitive manifestation of an imbalance in the soil ecosystem (Berendsen et al, 2012;Rout and Southworth, 2013;Kwak et al, 2018).…”

Arbuscular mycorrhizal fungi influence host infection during epidemics in a wild plant pathosystem

“…Ecological costs can occur when combinations of host and mutualist species or genotypes are mismatched (Klironomos, 2003; Hoeksema et al ., 2010), resulting in inefficient mutualisms that fail to convert host resources in to necessary benefits (Johnson et al ., 1997; Jones & Smith, 2004; Grman, 2012). Furthermore, unfavorable abiotic conditions could reduce or negate potential mutualist benefits (Hoeksema et al ., 2010; Qu et al ., 2021). In addition, defensive benefits from mutualists may not be effective against all antagonist species (e.g., depending on the lifestyle and infection strategy of the pathogen) (Pozo & Azcón-Aguilar, 2007), or be durable to changes in pathogen traits or composition in the environment.…”