Transcriptome dynamics of Arabidopsis during sequential biotic and abiotic stresses

Silvia Coolen, Silvia Proietti, Richard Hickman, Nelson H. Davila Olivas, Pingping Huang, Marcel C. van Verk, Johan A. van Pelt, Alexander H.J. Wittenberg, Martin de Vos, Marcel Prins, Joop J.A. van Loon, Mark G.M. Aarts, Marcel Dicke, Corné M.J. Pieterse, Saskia C.M. van Wees

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59 Citations (Scopus)

Abstract

In nature, plants have to cope with a wide range of stress conditions that often occur simultaneously or in sequence. To investigate how plants cope with multi-stress conditions, we analyzed the dynamics of whole-transcriptome profiles of Arabidopsis thaliana exposed to six sequential double stresses inflicted by combinations of: (i) infection by the necrotrophic fungus Botrytis cinerea, (ii) herbivory by chewing larvae of Pieris rapae, and (iii) drought stress. Each of these stresses induced specific expression profiles over time, in which one-third of all differentially expressed genes was shared by at least two single stresses. Of these, 394 genes were differentially expressed during all three stress conditions, albeit often in opposite directions. When two stresses were applied in sequence, plants displayed transcriptome profiles that were very similar to the second stress, irrespective of the nature of the first stress. Nevertheless, significant first-stress signatures could be identified in the sequential stress profiles. Bioinformatic analysis of the dynamics of co-expressed gene clusters highlighted specific clusters and biological processes of which the timing of activation or repression was altered by a prior stress. The first-stress signatures in second stress transcriptional profiles were remarkably often related to responses to phytohormones, strengthening the notion that hormones are global modulators of interactions between different types of stress. Because prior stresses can affect the level of tolerance against a subsequent stress (e.g. prior herbivory strongly affected resistance to B. cinerea), the first-stress signatures can provide important leads for the identification of molecular players that are decisive in the interactions between stress response pathways.

Original languageEnglish
Pages (from-to)249-267
JournalThe Plant Journal
Volume86
Issue number3
DOIs
Publication statusPublished - 2016

Keywords

  • Arabidopsis thaliana
  • Botrytis cinerea
  • combinatorial plant stress
  • drought stress
  • gene regulatory network
  • Pieris rapae
  • plant hormones
  • RNA-Seq
  • transcript profiling
  • 016-3950

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    Coolen, S., Proietti, S., Hickman, R., Davila Olivas, N. H., Huang, P., van Verk, M. C., ... van Wees, S. C. M. (2016). Transcriptome dynamics of Arabidopsis during sequential biotic and abiotic stresses. The Plant Journal, 86(3), 249-267. https://doi.org/10.1111/tpj.13167