Redox-mediated quorum sensing in plants

PLoS One. 2017 Sep 13;12(9):e0182655. doi: 10.1371/journal.pone.0182655. eCollection 2017.

Abstract

The rhizosphere, the narrow zone of soil around plant roots, is a complex network of interactions between plants, bacteria, and a variety of other organisms. The absolute dependence on host-derived signals, or xenognosins, to regulate critical developmental checkpoints for host commitment in the obligate parasitic plants provides a window into the rhizosphere's chemical dynamics. These sessile intruders use H2O2 in a process known as semagenesis to chemically modify the mature root surfaces of proximal host plants and generate p-benzoquinones (BQs). The resulting redox-active signaling network regulates the spatial and temporal commitments necessary for host attachment. Recent evidence from non-parasites, including Arabidopsis thaliana, establishes that reactive oxygen species (ROS) production regulates similar redox circuits related to root recognition, broadening xenognosins' role beyond the parasites. Here we compare responses to the xenognosin dimethoxybenzoquinone (DMBQ) between the parasitic plant Striga asiatica and the non-parasitic A. thaliana. Exposure to DMBQ simulates the proximity of a mature root surface, stimulating an increase in cytoplasmic Ca2+ concentration in both plants, but leads to remarkably different phenotypic responses in the parasite and non-parasite. In S. asiatica, DMBQ induces development of the host attachment organ, the haustorium, and decreases ROS production at the root tip, while in A. thaliana, ROS production increases and further growth of the root tip is arrested. Obstruction of Ca2+ channels and the addition of antioxidants both lead to a decrease in the DMBQ response in both parasitic and non-parasitic plants. These results are consistent with Ca2+ regulating the activity of NADPH oxidases, which in turn sustain the autocatalytic production of ROS via an external quinone/hydroquinone redox cycle. Mechanistically, this chemistry is similar to black and white photography with the emerging dynamic reaction-diffusion network laying the foundation for the precise temporal and spatial control underlying rhizosphere architecture.

MeSH terms

  • Arabidopsis* / drug effects
  • Arabidopsis* / growth & development
  • Arabidopsis* / metabolism
  • Arabidopsis* / parasitology
  • Benzoquinones / pharmacology
  • Calcium Signaling / drug effects
  • Host-Parasite Interactions* / drug effects
  • Hydrogen Peroxide / metabolism
  • Hydrogen Peroxide / pharmacology
  • Meristem / drug effects
  • Meristem / growth & development
  • Meristem / metabolism
  • Meristem / parasitology
  • Oxidation-Reduction
  • Plant Physiological Phenomena*
  • Plant Roots / drug effects
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Plant Roots / parasitology
  • Quorum Sensing / physiology*
  • Reactive Oxygen Species / metabolism
  • Striga / drug effects
  • Striga / growth & development
  • Striga / physiology

Substances

  • Benzoquinones
  • Reactive Oxygen Species
  • Hydrogen Peroxide

Grants and funding

We thank Emory University for undergraduate student research fellowships to AWF and PY, the Florida Institute of Technology for graduate fellowship support of SL, the NIH FIRST Fellowship to BDP, and Emory University’s Department of Neurology for fellowship support to OT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.