Barley Leaf Transcriptome and Metabolite Analysis Reveals New Aspects of Compatibility and Piriformospora indica–Mediated Systemic Induced Resistance to Powdery Mildew

Abstract

Colonization of barley roots with the basidiomycete fungus Piriformospora indica (Sebacinales) induces systemic resistance against the biotrophic leaf pathogen Blumeria graminis f. sp. hordei (B. graminis). To identify genes involved in this mycorrhiza-induced systemic resistance, we compared the leaf transcriptome of P. indica-colonized and noncolonized barley plants 12, 24, and 96 h after challenge with a virulent race of B. graminis. The leaf pathogen induced specific gene sets (e.g., LRR receptor kinases and WRKY transcription factors) at 12 h postinoculation (hpi) (prepenetration phase) and vesicle-localized gene products 24 hpi (haustorium establishment). Metabolic analysis revealed a progressing shift of steady state contents of the intermediates glucose-1-phosphate, uridinediphosphate-glucose, and phosphoenolpyruvate 24 and 96 hpi, indicating that B. graminis shifts central carbohydrate metabolism in favor of sucrose biosynthesis. Both B. graminis and P. indica increased glutamine and alanine contents, whereas substrates for starch and nitrogen assimilation (adenosinediphosphate- glucose and oxoglutarate) decreased. In plants that were more B. graminis resistant due to P. indica root colonization, 22 transcripts, including those of pathogenesis-related genes and genes encoding heat-shock proteins, were differentially expressed ?twofold in leaves after B. graminis inoculation compared with non-mycorrhized plants. Detailed expression analysis revealed a faster induction after B. graminis inoculation between 8 and 16 hpi, suggesting that priming of these genes is an important mechanism of P. indica-induced systemic disease resistance.

Bacteria-Triggered Systemic Immunity in Barley Is Associated with WRKY and ETHYLENE RESPONSIVE FACTORs But Not with Salicylic Acid

“…Moreover, systemic leaves of plants pretreated with the root-colonizing and plant growth-promoting fungus Piriformospora indica display enhanced resistance to Bgh (Waller et al, 2005). Similar to our leaf-to-leaf response, this root-to-leaf ISR response does not appear to be correlated with SA or JA signaling but with relatively few gene expression changes in the aboveground, systemic tissue (Waller et al, 2005(Waller et al, , 2008) that might prime the leaves for both apoplast alkalinization and expression changes of a specific set of genes, including three PR genes, upon Bgh infection (Felle et al, 2009;Molitor et al, 2011). Alternatively, leaf-to-leaf and root-to-leaf systemic immune responses might be primed independently of the (limited) gene expression changes observed in the putatively primed tissue but instead might be regulated by, for example, posttranslational protein modifications (Beckers et al, 2009).…”

Effect of several rhizobacteria strains on barley resistance againstPyrenophora gramineaunder field conditions

“…Cordova-Campos et al (2012) found that basal resistance to Pseudomonas syringae pathovars was signifi cantly greater in wild accessions of bean Phaseolus vulgaris than in modern cultivars. In a recent work on barley, Molitor et al (2011) demonstrated that following inoculation of powdery mildew infected plant with Piriformospora indica, there was a priming of powdery mildew defuse-associated genes at an early stage of the infection.…”

Antioxidant activity and gene expression associated with cadmium toxicity in wheat affected by mycorrhizal fungus

“…In particular, the main effects of this fungus were not remarkable, resulting in no significant induction in transcription of the studied antioxidant genes. Therefore, influence of mix-colonization treatment, particularly in Molitor et al (2011) indicated that P. indica could induce transcription of a wide range of pathogenesis-related genes and they concluded that P. indica likely induced disease resistance through genes encoding heat-shock proteins.…”