Fuller Alexandra W, Young Phoebe, Pierce B Daniel, Kitson-Finuff Jamie, Jain Purvi, Schneider Karl, Lazar Stephen, Taran Olga, Palmer Andrew G, Lynn David G
Departments of Biology and Chemistry, Emory University, Atlanta, GA, United States of America.
Gottwald Science Center, University of Richmond, Richmond, VA, United States of America.
PLoS One. 2017 Sep 13;12(9):e0182655. doi: 10.1371/journal.pone.0182655. eCollection 2017.
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.
根际是植物根系周围狭窄的土壤区域，是植物、细菌和各种其他生物体之间相互作用的复杂网络。专性寄生植物对宿主衍生信号（即异源识别素）的绝对依赖，以调节宿主定殖的关键发育检查点，这为了解根际的化学动态提供了一个窗口。这些固着的入侵者在一个称为半生成的过程中利用过氧化氢对近端宿主植物的成熟根表面进行化学修饰，并生成对苯醌（BQs）。由此产生的氧化还原活性信号网络调节宿主附着所需的空间和时间定殖。包括拟南芥在内的非寄生植物的最新证据表明，活性氧（ROS）的产生调节与根识别相关的类似氧化还原回路，这拓宽了异源识别素在寄生虫之外的作用。在这里，我们比较了寄生植物亚洲独脚金和非寄生拟南芥对异源识别素二甲氧基苯醌（DMBQ）的反应。暴露于DMBQ模拟了成熟根表面的接近程度，刺激了两种植物细胞质Ca2+浓度的增加，但在寄生虫和非寄生虫中导致了显著不同的表型反应。在亚洲独脚金中，DMBQ诱导宿主附着器官吸器的发育，并降低根尖处的ROS产生，而在拟南芥中，ROS产生增加且根尖的进一步生长受到抑制。Ca2+通道的阻断和抗氧化剂的添加均导致寄生和非寄生植物中DMBQ反应的降低。这些结果与Ca2+调节NADPH氧化酶的活性一致，而NADPH氧化酶又通过外部醌/氢醌氧化还原循环维持ROS的自催化产生。从机制上讲，这种化学过程类似于黑白摄影，新出现的动态反应扩散网络为根际结构精确的时空控制奠定了基础。
