The alternative oxidase pathway is involved in optimizing photosynthesis inMedicago truncatulainfected byFusarium oxysporumandRhizoctonia solani

Abstract

Phytopathogen infection alters primary metabolism status and plant development. The alternative oxidase (AOX) has been hypothesized to increase under pathogen attack preventing reductions, thus optimizing photosynthesis and growth. In this study, two genotypes of Medicago truncatula, one relatively resistant (Jemalong A17) and one susceptible (TN1.11), were infected with Fusarium oxysporum and Rhizoctonia solani. The in vivo foliar respiratory activities of the cytochrome oxidase pathway (COP) and the alternative oxidase pathway (AOP) were measured using the oxygen isotope fractionation. Gas exchange and photosynthesis‐related parameters were measured and calculated together with antioxidant enzymes activities and organic acids contents. Our results show that the in vivo activity of AOX (valt) plays a role under fungal infection. When infected with R. solani, the increase of valt in A17 was concomitant to an increase in net assimilation, in mesophyll conductance, to an improvement in the maximum velocity of Rubisco carboxylation and to unchanged malate content. However, under F. oxysporum infection, the induced valt was accompanied by an enhancement in the antioxidant enzymes, superoxide dismutase (SOD; EC1.15.1.1), catalase (CAT; EC1.11.1.6) and guaiacol peroxidase (GPX; EC1.11.1.7), activities and to an unchanged tricarboxylic acid cycle intermediates. These results provide new insight into the role of the in vivo activity of AOX in coordinating primary metabolism interactions that, partly, modulate the relative resistance of M. truncatula to diseases caused by soil‐borne pathogenic fungi.

Co-infection by Soil-Borne Fungal Pathogens Alters Disease Responses Among Diverse Alfalfa Varieties

“…locations within root tissues after penetrating through the root epidermis. Fo enters through the root cortex to xylem vessels where proliferation, growth, and spread occur without damaging cortex tissues Fang and Barbetti, 2014;Gordon, 2017) while Rs damages the intracellular cement of root cortex tissues where cells dissolve without affecting xylem vessels (Ajayi-Oyetunde and Bradley, 2018;Batnini et al, 2020). It is likely that the two root pathogens work cooperatively with Fo acting in xylem vessels and Rs acting in cortex tissues, which result in enhanced negative effects on plant growth when plants were coinfected.…”

“…Fom is the host-specific pathogen of alfalfa and other Medicago spp. (Rispail and Rubiales, 2014;Gill et al, 2018;Batnini et al, 2020). Rs, mainly associated with root rot disease, has been classified into 14 anastomosis groups based on hyphal anastomosis reactions (Ajayi-Oyetunde and Bradley, 2018;Li et al, 2019).…”

“…Rs, mainly associated with root rot disease, has been classified into 14 anastomosis groups based on hyphal anastomosis reactions (Ajayi-Oyetunde and Bradley, 2018;Li et al, 2019). Extensive studies have been performed on Fo and Rs in many crops, and studies are often limited to a single pathogen with its host (Gordon, 2017;Ajayi-Oyetunde and Bradley, 2018;Fang et al, 2019;Oladzad et al, 2019;Batnini et al, 2020). However, the combined effects of both pathogens on plants and how plants respond to the co-infection remain unknown.…”

In Vivo Metabolic Regulation of Alternative Oxidase under Nutrient Deficiency—Interaction with Arbuscular Mycorrhizal Fungi and Rhizobium Bacteria

“…In fact, measurements of in vivo AOX activity have been performed in leaves of six legumes species: common bean ( Phaseolus vulgaris ), garden pea ( Pisum sativum ), barrel medic ( Medicago truncatula ), soybean ( Glycine max ), mung bean ( Vigna radiata ) and faba bean ( Vicia faba ). These experiments have been important to evaluate the regulation of the AOX activity under P limitation, high light, salinity, pathogen infection and variable temperatures [ 25 , 26 , 27 , 51 , 106 , 125 , 126 ]. Furthermore, legumes are suitable for the study of the regulation of AOX activity by N availability in roots because of their ability to establish symbiosis with a group of soil bacteria collectively designated as rhizobia.…”

“…In other words, rates of photosynthesis are incremented (due to the decrease of photosynthetic limitations) because microsymbiont leads plants to produce large amounts of carbon compounds required for its metabolism [19]. This phenomenon, called positive-feedback of photosynthesis [24], could be accompanied by adjustments in the energy efficiency of respiration, considering the tight relationship between photosynthesis and AOX activity [25][26][27][28]. Thus, adjustments in the energy efficiency of respiration can be conditioned by the metabolic costs of microsymbiont maintenance or by the metabolic benefits of improved nutrition, which in turn may depend on the microbial symbiont's energy efficiency of respiration.…”