Small-Molecule Screens Reveal Novel Haustorium Inhibitors in the Root Parasitic Plant <i>Triphysaria versicolor</i>

Wang, Yaxin; Steele, Daniel; Murdock, Maylin; Lai, Seigmund Wai Tsuen; Yoder, John I.

doi:10.1094/phyto-04-19-0115-r

Cited by 12 publications

(10 citation statements)

References 43 publications

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“…The process of haustorium development was reported to be more sensitive to cellular redox states than root growth [38], but in broomrape we found that the reduction in radicle growth was induced at lower benzoquinone concentrations than those concentrations active for haustorium induction. It has been debated whether the growth cessation is necessary for haustorium functioning, or if it is the consequence of a reduction in resources required for root growth [31].…”

Section: Induction Of Haustoriummentioning

confidence: 51%

Effects of Benzoquinones on Radicles of Orobanche and Phelipanche Species

Fernández‐Aparicio

Masi

Cimmino

2021

Plants

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The holoparasitic broomrape weeds (Orobanche and Phelipanche species) cause severe yield losses throughout North Africa, the Middle East, and Southern and Eastern Europe. These parasitic weeds form an haustorium at the tip of their radicles to infect the crop upon detection of the host-derived haustorium-inducing factors. Until now, the haustorial induction in the broomrapes remains less studied than in other parasitic plant species. Known haustorium-inducing factors active in hemiparasites, such as Striga and Triphysaria species, were reported to be inefficient for the induction of haustoria in broomrape radicles. In this work, the haustorium-inducing activity of p-benzoquinone and 2,6-dimethoxy-p-benzoquinone (BQ and DMBQ) on radicles of three different broomrapes, namely Orobanche cumana, Orobanche minor and Phelipanche ramosa, is reported. Additional allelopathic effects of benzoquinones on radicle growth and radicle necrosis were studied. The results of this work suggest that benzoquinones play a role in the induction of haustorium in broomrapes. Although dependent on the broomrape species assayed and the concentration of quinones used in the test, the activity of BQ appeared to be stronger than that of DMBQ. The redox property represented by p-benzoquinone, which operates in several physiological processes of plants, insects and animals, is invoked to explain this different activity. This work confirms the usefulness of benzoquinones as haustorium-inducing factors for holoparasitic plant research. The findings of this work could facilitate future studies in the infection process, such as host-plant recognition and haustorial formation.

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Section: Induction Of Haustoriummentioning

confidence: 51%

Effects of Benzoquinones on Radicles of Orobanche and Phelipanche Species

Fernández‐Aparicio

Masi

Cimmino

2021

Plants

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“…DMBQ did not induce visible signs of toxicity in P. ramosa as has been observed in other parasitic weeds which have been described as turning brown and die at concentrations higher than 50 µM [52,61]. Unlike more hydrophobic quinones, DMBQ is sufficiently soluble in water to make fresh working stocks at 1 mM directly in water, without the solvent DMSO usually used in labs to make stock solutions for haustorial induction assays of Phelipanche, Striga, and Triphysaria [49,65,66]. The effect of quercetin was evaluated at concentration range of 100 µM and 5 µM (Figure 4B,G).…”

Section: Resultsmentioning

confidence: 66%

Allelopathic Effect of Quercetin, a Flavonoid from Fagopyrum esculentum Roots in the Radicle Growth of Phelipanche ramosa: Quercetin Natural and Semisynthetic Analogues Were Used for a Structure-Activity Relationship Investigation

Fernández‐Aparicio

Masi

Cimmino

et al. 2021

Plants

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Allelopathic potential of buckwheat roots on the radicle growth of the broomrape weed species Orobanche cumana and Phelipanche ramosa was studied. Buckwheat root exudates induced a significant growth inhibition in P. ramosa radicles but radicles of O. cumana were not affected. Among the metabolites present in the root organic extract we identified the flavonol quercetin and the stilbene p-coumaric acid methyl ester with only quercetin showing inhibitory effect on P. ramosa. The activity of quercetin was compared with other two similar flavanoids, the flavone apigenin and the dihydroflavanol 3-O-acetylpadmatin extracted respectively from Lavandula stoechas and Dittrichia viscosa plants. In this comparative assay only 3-O-acetylpadmatin besides quercetin, showed inhibition activity of radicle growth while apigenin was inactive. These results indicated that the presence of two ortho-free hydroxy groups of C ring, like catechol, could be an important feature to impart activity while the carbon skeleton of B ring and substituents of both A and B rings are not essential. Besides reduction of radicle growth, haustorium induction was observed at the tip of P. ramosa radicles treated with quercetin which swelled and a layer of papillae was formed. Activity of quercetin on haustorium induction in P. ramosa was assayed in comparison with the known haustorium-inducing factor 2,6-dimethoxy-p-benzoquinone (DMBQ) and a three partial methyl ether derivatives semisynthetized from quercetin. Results indicated that P. ramosa haustorium was induced by DMBQ at concentrations of 1–0.5 mM and quercetin and its derivatives at concentration range 0.1–0.05 mM.

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“…Also, chemically inhibiting peroxidase activity, and thus altering the redox homeostasis, reduces haustorium formation in Striga spp. and Triphysaria (Wada et al ., 2019; Wang et al ., 2019). The expression of a superoxide dismutase in P. japonicum intrusive cells further supports a role for redox regulating enzymes in haustorium development.…”

Section: Discussionmentioning

confidence: 99%

Subtilase activity in the intrusive cells mediates haustorium maturation in parasitic plants

Ogawa

Wakatake

Spallek

et al. 2020

Preprint

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Parasitic plants that infect crops are devastating to agriculture throughout the world. They develop a unique inducible organ called the haustorium, which connects the vascular systems of the parasite and host to establish a flow of water and nutrients. Upon contact with the host, the haustorial epidermal cells at the interface with the host differentiate into specific cells called intrusive cells that grow endophytically towards the host vasculature. Then, some of the intrusive cells re-differentiate to form a xylem bridge that connects the vasculatures of the parasite and host. Despite the prominent role of intrusive cells in host infection, the molecular mechanisms mediating parasitism in the intrusive cells are unknown. In this study, we investigated differential gene expression in the intrusive cells of the facultative parasite Phtheirospermum japonicum in the family Orobanchaceae by RNA-Sequencing of laser-microdissected haustoria. We then used promoter analyses to identify genes that are specifically induced in intrusive cells, and used promoter fusions with genes encoding fluorescent proteins to develop intrusive cell-specific markers. Four of the intrusive cell-specific genes encode subtilisin-like serine proteases (SBTs), whose biological functions in parasitic plants are unknown. Expression of an SBT inhibitor in the intrusive cells inhibited their development, inhibited the development of the xylem bridge, and reduced auxin response levels near the site where the xylem bridge normally develops. Therefore, we propose that subtilase activity plays an important role in haustorium development in this parasitic plant.One sentence summaryTissue-specific analysis showed that the subtilases specifically expressed in intrusive cells regulate auxin-mediated host-parasite connections in the parasitic plant Phtheirospermum japonicum.

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Small-Molecule Screens Reveal Novel Haustorium Inhibitors in the Root Parasitic Plant Triphysaria versicolor

Cited by 12 publications

References 43 publications

Effects of Benzoquinones on Radicles of Orobanche and Phelipanche Species

Effects of Benzoquinones on Radicles of Orobanche and Phelipanche Species

Allelopathic Effect of Quercetin, a Flavonoid from Fagopyrum esculentum Roots in the Radicle Growth of Phelipanche ramosa: Quercetin Natural and Semisynthetic Analogues Were Used for a Structure-Activity Relationship Investigation

Subtilase activity in the intrusive cells mediates haustorium maturation in parasitic plants

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