Redox-mediated quorum sensing in plants.
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 obl...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2017-01-01
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| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC5597120?pdf=render |
| _version_ | 1818435255933075456 |
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| author | Alexandra W Fuller Phoebe Young B Daniel Pierce Jamie Kitson-Finuff Purvi Jain Karl Schneider Stephen Lazar Olga Taran Andrew G Palmer David G Lynn |
| author_facet | Alexandra W Fuller Phoebe Young B Daniel Pierce Jamie Kitson-Finuff Purvi Jain Karl Schneider Stephen Lazar Olga Taran Andrew G Palmer David G Lynn |
| author_sort | Alexandra W Fuller |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-14T16:49:59Z |
| format | Article |
| id | doaj.art-38207289cc1442b2b9fb763d1d874848 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-14T16:49:59Z |
| publishDate | 2017-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-38207289cc1442b2b9fb763d1d8748482022-12-21T22:54:05ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01129e018265510.1371/journal.pone.0182655Redox-mediated quorum sensing in plants.Alexandra W FullerPhoebe YoungB Daniel PierceJamie Kitson-FinuffPurvi JainKarl SchneiderStephen LazarOlga TaranAndrew G PalmerDavid G LynnThe 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.http://europepmc.org/articles/PMC5597120?pdf=render |
| spellingShingle | Alexandra W Fuller Phoebe Young B Daniel Pierce Jamie Kitson-Finuff Purvi Jain Karl Schneider Stephen Lazar Olga Taran Andrew G Palmer David G Lynn Redox-mediated quorum sensing in plants. PLoS ONE |
| title | Redox-mediated quorum sensing in plants. |
| title_full | Redox-mediated quorum sensing in plants. |
| title_fullStr | Redox-mediated quorum sensing in plants. |
| title_full_unstemmed | Redox-mediated quorum sensing in plants. |
| title_short | Redox-mediated quorum sensing in plants. |
| title_sort | redox mediated quorum sensing in plants |
| url | http://europepmc.org/articles/PMC5597120?pdf=render |
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