Redox-mediated quorum sensing in plants

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.

Reactive Oxygen Species (ROS) Generation Is Indispensable for Haustorium Formation of the Root Parasitic Plant Striga hermonthica

“…Therefore, it is possible that the observed H 2 O 2 accumulated at later stages of haustorium formation may represent its developmental function on cell growth, that involves cell wall modification and expansion. Previous studies in Striga asiatica reported that H 2 O 2 strongly accumulated at the radicle tip and disappeared about 2 h after HIF treatment (Keyes et al, 2007; Fuller et al, 2017). In contrast to this, we observed almost no H 2 O 2 fluorescence at the radicle tip before the haustorium induction treatment, with major H 2 O 2 accumulation appearing after 10–15 h of haustorium induction (Figure 3).…”

Mapping Reaction-Diffusion Networks at the Plant Wound Site With Pathogens

“…Here the production of H 2 O 2 at the parasite root tip is proposed to create a mild wound response via peroxidase oxidation of wall phenols in the host in order to generate the haustorial inducing benzoquinone at the host/parasite interface ( Chang and Lynn, 1986 ; Keyes et al., 2007 ). The parasite has been shown to have low phenol content in its own cell wall to avoid self-response, and this concept has been generalized to root meristematic tissue of other dicots including tobacco ( Fuller et al., 2017 ). In contrast to mature tobacco tissue, two-week-old tobacco seedlings failed to induce AB650 wt or YHL301 ss (data not shown).…”

“…The plant root provides reduced carbon and dioxygen to the rhizosphere ( Walker et al., 2003 ), setting up both ends of life’s universal redox network. Indeed, redox-active phenols, quinones, flavins, and phenazines ( Bais et al., 2006 ; Tomilov et al., 2006 ; Uteau et al., 2015 ; Rasmann and Turlings, 2016 ) are prevalent in the rhizosphere where redox active processes have been highlighted in biofilm biogeography ( Stacy et al., 2014 ), allelopathy ( Tomilov et al., 2006 ), quorum sensing ( Fuller et al., 2017 ), and most notably, in the critical spatiotemporal dynamics of semagenesis ensuring success of the parasitic plants ( Keyes et al., 2007 ; Liang et al., 2016 ; Fuller et al., 2017 ). The initial discoveries of the reaction diffusion dynamics of semagenesis ( Chang et al., 1986 ; Fate et al., 1990 ; Smith et al., 1990 ) motivated further explorations of model reaction-diffusion systems in the rhizosphere ( Taran et al., 2019 ).…”

Quorum Sensing Behavior in the Model Unicellular Eukaryote Chlamydomonas reinhardtii

“…Article formation, and many other phenotypes with significance to host-microbial associations, microbial ecology, and more (Miller and Bassler, 2001). QS has emerged as a convergent strategy among various microorganisms as a way to couple phenotypic switching to cell density (Fuller et al, 2017). However, while prevalent in fungi, there are no examples of this phenomenon among other eukaryotes.…”