Comparative metabolomic profiling reveals molecular mechanisms underlying growth promotion and disease resistance in wheat conferred by <i>Piriformospora indica</i> in the field

<i>Piriformospora indica</i>, a plant root-colonizing basidiomycete fungus, exhibits strong growth-promoting activity in symbiosis with a broad range of plants. Here, we report the potential of <i>P.</i><i>indica</i> to improve growth, yield, and disease resistance in wheat in the field. In the present study, <i>P.</i> <i>indica</i> successfully colonized wheat through chlamydospores and formed dense mycelial networks that covered roots. Plants subjected to the seed soaking (SS) treatment with <i>P.</i> <i>indica</i> chlamydospore suspensions enhanced tillering 2.28-fold compared to the non-inoculated wheat in the tillering stage. In addition, <i>P.</i> <i>indica</i> colonization promoted vegetative growth significantly during the three-leaf, tillering, and jointing stages. Moreover, the <i>P.</i> <i>indica</i>-SS-treatment enhanced wheat yield by 16.37 ± 1.63%, by increasing grains per ear and panicle weight and decreased damage to wheat shoot and root architecture markedly, with high field control effects against <i>Fusarium pseudograminearum</i> (81.59 ± 1.32%), <i>Bipolaris sorokiniana</i> (82.19 ± 1.59%), and <i>Rhizoctonia cerealis</i> (75.98 ± 1.36%). Most of the primary metabolites, such as amino acids, nucleotides, and lipids, involved in vegetative reproduction were increased in <i>P.</i> <i>indica</i>-SS-treatment plants, whereas secondary metabolites, such as terpenoids, polyketides, and alkaloids, decreased following <i>P.</i> <i>indica</i> inoculation. The up-regulated processes of protein, carbohydrate, and lipid metabolism indicated that <i>P.</i> <i>indica</i> colonization increased growth, yield, and disease resistance via the acceleration of plant primary metabolism. In conclusion, <i>P.</i> <i>indica</i> improved morphological, physiological, and metabolic substance levels, and further promoted its growth, yield, and disease resistance in wheat.