Decomposer animals induce differential expression of defence and auxin-responsive genes in plants

Effects of decomposers on plant growth are generally ascribed to nutrient mobilization. However, Collembola, which are ubiquitous and abundant decomposers in soil, are known to alter root morphology with, in some cases, the nutrient content of plants remaining unaffected. We studied the interaction of Collembola (Protaphorura fimata) with the model plant Arabidopsis thaliana in order to link phenotypic responses of A. thaliana to decomposers using changes in gene expression. Collembola reduced the growth of A. thaliana during early growth stages, but this decrease was compensated later. Expression analyses revealed striking differences in the response of plant roots and shoots three and six days after exposure of Arabidopsis to Collembola. Among the specifically affected transcripts in roots, the induction of auxin-responsive genes was significantly increased after six days, suggesting that P. fimata provoked auxin-related signalling in roots. In shoots, transcriptional changes were more diverse and functional categories involved in defence and metabolic re-arrangements were significantly affected. These responses might have been related to the transitory reduction in growth which presumably was caused by Collembola feeding on and/or damaging roots. The results suggest that Collembola may improve plant resistance against the attack by herbivores by stimulating the production of secondary compounds while concomitantly compensating the costs of producing them by fostering root growth and nutrient exploitation.

► Decomposer animals change auxin signalling in plant roots. ► Concurrently, they induce systemic defence responses in plant shoots. ► Both plant primary and plant secondary metabolism are affected. ► The results have major implications for the view how terrestrial systems function.