A Poly(A) Ribonuclease Controls the Cellotriose-Based Interaction between <i>Piriformospora indica</i> and Its Host Arabidopsis

Abstract

<i>Piriformospora indica</i>, an endophytic root-colonizing fungus, efficiently promotes plant growth and induces resistance to abiotic stress and biotic diseases. <i>P. indica</i> fungal cell wall extract induces cytoplasmic calcium elevation in host plant roots. Here, we show that cellotriose (CT) is an elicitor-active cell wall moiety released by <i>P. indica</i> into the medium. CT induces a mild defense-like response, including the production of reactive oxygen species, changes in membrane potential, and the expression of genes involved in growth regulation and root development. CT-based cytoplasmic calcium elevation in Arabidopsis (<i>Arabidopsis thaliana</i>) roots does not require the BAK1 coreceptor or the putative Ca²⁺ channels TPC1, GLR3.3, GLR2.4, and GLR2.5 and operates synergistically with the elicitor chitin. We identified an ethyl methanesulfonate-induced mutant (<i>cytoplasmic</i><i>calcium elevation mutant</i>) impaired in the response to CT and various other cellooligomers (<i>n</i> = 2-7), but not to chitooligomers (<i>n</i> = 4-8), in roots. The mutant contains a single nucleotide exchange in the gene encoding a poly(A) ribonuclease (AtPARN; At1g55870) that degrades the poly(A) tails of specific mRNAs. The wild-type <i>PARN</i> cDNA, expressed under the control of a 35S promoter, complements the mutant phenotype. Our identification of cellotriose as a novel chemical mediator casts light on the complex <i>P. indica</i>-plant mutualistic relationship.