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.
Highlights
The plant rhizosphere is so richly populated by mutualistic associations that it has been dubbed the second plant genome [1]
The activity of EF-hand containing NADPH oxidases has been positively correlated with Ca2+ concentrations in A. thaliana, supporting a link between BQ-mediated reactive oxygen species (ROS) production and calcium regulation [36,37,38]
Given the morphological signatures of haustorial growth, swelling of the root tip and development of the haustorial hairs [39,40], the general role of calcium dynamics on ROS production [36,41,42,43], as well as polar growth of root hairs [34,41], we reasoned that Ca+2 signaling may integrate BQ exposures to internal biochemical events in plants
Summary
The plant rhizosphere is so richly populated by mutualistic associations that it has been dubbed the second plant genome [1]. Bacterial colonization depends on a rich and diverse chemical language where the rates of exudation, the inherent physical and biological stability of the agents, and the differential responses of members of the rhizosphere all contribute to this information rich and biologically dynamic signaling landscape [4,5,6,7,8] Beyond their role in regulating plant-microbial associations, insights into the plant’s contribution to this signaling landscape has emerged from studies on: (i) host recognition by parasitic plants [9,10,11,12], (ii) kin recognition/selection [13,14,15,16], and (iii) allelopathy [17,18]. Persistent exposure of the parasite root meristem to BQs is necessary and sufficient to induce organogenesis of the parasite’s attachment organ, the haustorium [9,22,23], and serves as a signature for viable host roots
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