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Aberrant protein phosphatase 2C leads to abscisic acid insensitivity and high transpiration in parasitic Striga

Abstract

Striga parasitizes major crops in arid regions, depriving the host crop of nutrients through the transpiration stream and causing vast agricultural damage. Here, we report on the mechanism underlying how Striga maintains high transpiration under drought conditions. We found that Striga did not respond to abscisic acid, the phytohormone responsible for controlling stomatal closure. Protein phosphatase 2C of Striga (ShPP2C1) is not regulated by abscisic acid receptors, and this feature is attributable to specific mutations in its amino acid sequence. Moreover, Arabidopsis transformed with ShPP2C1 showed an abscisic acid-insensitive phenotype, indicating that ShPP2C1 functions as a dominant negative regulator of abscisic acid signal transduction. These findings suggest that ShPP2C1 interrupts abscisic acid signalling in Striga, resulting in high transpiration and subsequent efficient absorption of host nutrients under drought conditions.

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Data availability

The RNA sequencing data have been deposited at the DNA Databank of Japan under accession codes DRX142184, DRX142185. Complementary DNAs were registered at the DNA Databank of Japan with accession numbers as follows: ShPYL1, LC377366; ShPYL2, LC377367; ShPYL3, LC377368; ShPYL4, LC377369; ShPYL5, LC377370; ShPYL6, LC377371; ShPYL7, LC377372; ShPYL8, LC377373; ShPP2C1, LC377362; ShPP2C2, LC377363; ShPP2C3, LC377364; ShPP2C4, LC377365. Other data that support the findings of this study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank A.G.T. Babiker for providing Striga seeds. We also thank T. Hosouchi and S. Shinpo for technical support in Illumina sequencing; N. Arimoto, M. Negishi and Y. Yamakawa for supporting transgenic Arabidopsis experiments; Y. Tsuchiya and K. Hanada for advising on identification of the ABA receptor and PP2C from Striga; and T. Hirayama for providing the Columbia accession background Arabidopsis abi1c mutant. This work was supported by grants from MEXT/JSPS KAKENHI (No. 17H05009 to M.O., No. 15H05248 to Y.S.), MEXT/JSPS Bilateral Programs (to Y.S.), the Joint Research Program of Arid Land Research Center, Tottori University (No. 28C2004 to Y.S.) and Japan Science and Technology Agency (PRESTO, No. JPMJPR15Q5 to M.O.); and the SATREPS Striga project to Y.S.

Author information

Y.S. and M.O. conceived and designed the project. H.F. and H.S. contributed to physiological research on S. hermonthica. H.F. performed gene expression analysis, protein expression, purification and biochemical assays. H.S. and M.M. performed next generation sequencing and data analysis. M.O. carried out molecular cloning, transgenic plant generation and physiological analysis of transformants. H.F., M.O. and Y.S. wrote the manuscript.

Competing interests

The authors declare no competing interests.

Correspondence to Masanori Okamoto or Yukihiro Sugimoto.

Supplementary information

Supplementary Information

Supplementary Figures 1–8, Supplementary Table 1, Supplementary Methods and Supplementary References.

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Further reading

Fig. 1: Physiological analysis of ABA sensitivity in Striga.
Fig. 2: Molecular characterization of ShPYLs and ShPP2Cs.
Fig. 3: Functional analysis of ShPP2C1 and like-mutagenized AtABI1 in Arabidopsis.