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2017 ; 12
(9
): e0182655
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Redox-mediated quorum sensing in plants
#MMPMID28902851
Fuller AW
; Young P
; Pierce BD
; Kitson-Finuff J
; Jain P
; Schneider K
; Lazar S
; Taran O
; Palmer AG
; Lynn DG
PLoS One
2017[]; 12
(9
): e0182655
PMID28902851
show ga
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.
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