How does Striga hermonthica Bewitch its hosts?

ABSTRACT

The common name witchweed synonymous with the Latin name Striga befits the bewitching effects, viz wilting and chlorosis, the parasite inflicts on its hosts long before it emerges and becomes visible above the ground. However, interactions in the rhizosphere between host roots and Striga seedlings are concealed and inscrutable. In vitro experiments revealed that abscisic acid was produced by S. hermonthica seedlings and a considerable portion of the phytohormone was exuded. The phytohormone in the rhizosphere could, at least in part, contribute to the bewitching effects, disrupt host immunity and promote commencement of parasitism.

KEYWORDS:

• Striga
• witchweed
• abscisic acid

Text

The root parasitic weed Striga hermonthica represents the greatest biological constraint for food production across northern sub-tropical Africa.¹ Although S. hermonthica has functional chlorophyll, its photosynthetic ability is insufficient for autotrophic growth² and it is therefore imperative for Striga to assimilate nutrients from its host for survival and growth. To this end, Striga life cycle is strongly cued to that of its host. Germination only occurs in the presence of a suitable host, which Striga locates using germination signals, strigolactones released from host roots.³ Following germination, the Striga radicle elongates and in close proximity to the host roots differentiates into a specialized organ the haustorium, which develops in response to host-derived chemical cues.⁴ Finally, the haustorium penetrates the host root, comes in contact with the endodermis, where haustorial cells elongate and divide to establish vascular connections with the host.⁵ Once the vascular continuity is established translocation of host materials to the parasite begins. Striga inflicts its bewitching effects, viz wilting and chlorosis, on its host long before it emerges and becomes visible above the ground.

The ability of the parasite to draw water and nutrients from the host almost certainly depends on the flux of sap across the xylem bridge.⁵ The transpiration gap between Striga and the host plant is presumed to accelerate diversion of water and nutrients to the parasite. In general, drought stress induces stomatal closure in terrestrial plants, suppresses transpiration and thereby reduces water consumption. In contrast, Striga maintains opened stomata and high transpiration even under water deficit.⁶ Recently, we revealed that the abnormal stomatal behavior resides on an aberrant protein phosphatase designated as ShPP2C1 which induces loss of sensitivity to abscisic acid (ABA) in Striga. During the course of the study, we found that ABA level in Striga seeds was negligible before germination, whereas high concentrations of ABA were detected in the seedlings,⁷ indicating that Striga is able to synthesize ABA independently. Further analysis revealed that ABA production and exudation by Striga seedlings increased drastically within twelve hours subsequent to germination induced with the synthetic strigolactone analog GR24 (Figure 1a,b). Further, sorghum growth was suppressed by treatment with ABA at 1 µM in aquaculture solution (Figure 2a,b).

Figure 1. (a) ABA contents in extracts and exudates of Striga seeds and seedlings after GR24 treatment. Data are means ± S.D. (n = 3 biologically independent). Striga seeds (ca. 100 mg per φ90 mm glass fiber filter paper), conditioned for 7 days in the dark at 30°C, were treated with GR24 at 1 µM. ABA in the seeds/seedlings and paper were analyzed separately as described previously.⁷ (b) Time series of photograph of Striga seed and seedling on the glass fiber filter paper after GR24 treatment. Representative images from 10 independent seeds/seedlings with similar results are shown. White triangles represent emerging radicles.

Figure 2. (a) Shoot length of sorghum plants grown in different concentrations of ABA. Two-day-old sorghum seedlings were transferred into aquaculture solutions containing 0–10⁻⁶ M (+)-ABA with 0.1% EtOH. Data are means ± S.D. (n= 5 biologically independent plants). (b) Photograph of sorghum plants at 8 days after the commencement of ABA treatment.

The fact that Striga germinates in close proximity of its host roots taken in conjunction with the finding that a considerable proportion of the ABA produced by the parasite seedlings is exuded in the host rhizosphere and the notable susceptibility of sorghum to ABA (Figure 2) suggest that ABA exuded from Striga seedlings could, at least in part, reduce growth and contribute to the bewitching effects the parasite inflicts on its host at the early stages of their interactions. Further, the results pinpoint the plausibility that ABA produced and exuded by Striga seedlings in the rhizosphere may play a crucial role in disruption of host immunity and commencement of parasitism. ABA produced by several phytopathogens acts as a specific effector and/or virulence factor that represses host immune responses and allows for pathogen establishment and disease development.^8–10

Acknowledgments

The authors are grateful to Professor Abdel Gabar Babiker, National Center for Research, Sudan, for critical reading of the manuscript.

Additional information

Funding

This work was supported, in part, by JST/JICA SATREPS (JPMJSA1607) and JSPS KAKENHI (15H05248).