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

Fujioka, Hijiri; Samejima, Hiroaki; Suzuki, Hideyuki; Mizutani, Masaharu; Okamoto, Masanori; Sugimoto, Yukihiro

doi:10.1038/s41477-019-0362-7

Cited by 36 publications

(39 citation statements)

References 23 publications

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“…While receptors displaying high basal activity might obscure ABA-mediated fine-tuning processes, Arabidopsis, Striga, Solanum, Oryza and Triticum still maintain both receptors P with a narrower response range alongside receptors that allow a broader range of response (23)(24)(25)(26)(27). Arabidopsis PYL10 stands out as an example of a receptor with high basal activity, as its regulation by ABA affects less than 50% of the response magnitude ( Fig.…”

Section: Resultsmentioning

confidence: 99%

A ligand-independent origin of abscisic acid perception

Sun

Harpazi

Wijerathna-Yapa

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

103

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Land plants are considered monophyletic, descending from a single successful colonization of land by an aquatic algal ancestor. The ability to survive dehydration to the point of desiccation is a key adaptive trait enabling terrestrialization. In extant land plants, desiccation tolerance depends on the action of the hormone abscisic acid (ABA) that acts through a receptor-signal transduction pathway comprising a PYRABACTIN RESISTANCE 1-like (PYL)–PROTEIN PHOSPHATASE 2C (PP2C)–SNF1-RELATED PROTEIN KINASE 2 (SnRK2) module. Early-diverging aeroterrestrial algae mount a dehydration response that is similar to that of land plants, but that does not depend on ABA: Although ABA synthesis is widespread among algal species, ABA-dependent responses are not detected, and algae lack an ABA-binding PYL homolog. This raises the key question of how ABA signaling arose in the earliest land plants. Here, we systematically characterized ABA receptor-like proteins from major land plant lineages, including a protein found in the algal sister lineage of land plants. We found that the algal PYL-homolog encoded by Zygnema circumcarinatum has basal, ligand-independent activity of PP2C repression, suggesting this to be an ancestral function. Similarly, a liverwort receptor possesses basal activity, but it is further activated by ABA. We propose that co-option of ABA to control a preexisting PP2C-SnRK2-dependent desiccation-tolerance pathway enabled transition from an all-or-nothing survival strategy to a hormone-modulated, competitive strategy by enabling continued growth of anatomically diversifying vascular plants in dehydrative conditions, enabling them to exploit their new environment more efficiently.

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Section: Resultsmentioning

confidence: 99%

A ligand-independent origin of abscisic acid perception

Sun

Harpazi

Wijerathna-Yapa

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

103

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“…Interestingly, some PYL–PP2C interactions may not be dependent on ABA, and the physiological significance of these interactions, as well as whether some Clade A PP2Cs can escape PYL repression and remain active during stress, is a matter of continued debate (Bhaskara et al, ; Hao et al, ; Tischer et al, ). Another interesting recent study showed that the ShPP2C1 of parasite Striga contained mutations around the tryptophan residue crucial for PYL‐ABA‐PP2C complex formation and thus had minimal ABA receptor interaction leading to ABA insensitivity and high transpiration (Fujioka et al, ).…”

Section: Posttranslational Mechanisms Regulating Phosphatase Activitymentioning

confidence: 99%

The flip side of phospho‐signalling: Regulation of protein dephosphorylation and the protein phosphatase 2Cs

Bhaskara

Wong

Verslues

2019

Plant Cell & Environment

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Protein phosphorylation is a key signalling mechanism and has myriad effects on protein function. Phosphorylation by protein kinases can be reversed by protein phosphatases, thus allowing dynamic control of protein phosphorylation. Although this may suggest a straightforward kinase-phosphatase relationship, plant genomes contain five times more kinases than phosphatases. Here, we examine phospho-signalling from a protein phosphatase centred perspective and ask how relatively few phosphatases regulate many phosphorylation sites. The most abundant class of plant phosphatases, the protein phosphatase 2Cs (PP2Cs), is surrounded by a web of regulation including inhibitor and activator proteins as well as posttranslational modifications that regulate phosphatase activity, control phosphatase stability, or determine the subcellular locations where the phosphatase is present and active. These mechanisms are best established for the Clade A PP2Cs, which are key components of stress and abscisic acid signalling.We also describe other PP2C clades and illustrate how these phosphatases are highly regulated and involved in a wide range of physiological functions. Together, these examples of multiple layers of phosphatase regulation help explain the unbalanced kinase-phosphatase ratio. Continued use of phosphoproteomics to examine phosphatase targets and phosphatase-kinase relationships will be important for deeper understanding of phosphoproteome regulation.

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“…Although this could suggest a correlation between the degree of parasitism and ABA sensitivity in seeds, this seems not to be true because both obligate parasites and Arabidopsis are hypersensitive to exogenous ABA compared with seeds of T. versicolor (Figure a; Okazaki et al, ). It is noteworthy that we describe S. hermonthica as hypersensitive to ABA, although this parasitic plant has been recently reported as hyposensitive due to mutation of one of the protein phosphatase 2C (PP2C) involved in ABA signal transduction (Fujioka et al, ). Due to enormous genetic variations between and within Striga populations (Bozkurt, Muth, Parzies, & Haussmann, ; Unachukwu et al, ), one explanation is arguably that S. hermonthica seeds used in this present study are genetically different from seeds used in Fujioka et al () and may not possess the PP2C gain‐of‐function mutation.…”

Section: Discussionmentioning

confidence: 97%

“…It is noteworthy that we describe S. hermonthica as hypersensitive to ABA, although this parasitic plant has been recently reported as hyposensitive due to mutation of one of the protein phosphatase 2C (PP2C) involved in ABA signal transduction (Fujioka et al, ). Due to enormous genetic variations between and within Striga populations (Bozkurt, Muth, Parzies, & Haussmann, ; Unachukwu et al, ), one explanation is arguably that S. hermonthica seeds used in this present study are genetically different from seeds used in Fujioka et al () and may not possess the PP2C gain‐of‐function mutation. We also argue that other PP2C could impose ABA‐mediated dormancy.…”

Section: Discussionmentioning

confidence: 97%

CYP707As are effectors of karrikin and strigolactone signalling pathways in Arabidopsis thaliana and parasitic plants

Brun

Thoiron

Braem

et al. 2019

Plant Cell & Environment

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Karrikins stimulate Arabidopsis thaliana germination, whereas parasitic weeds of the Orobanchaceae family have evolved to respond to host-exuded compounds such as strigolactones, dehydrocostus lactone, and 2-phenylethyl isothiocyanate. In Phelipanche ramosa, strigolactone-induced germination was shown to require one of the CYP707A proteins involved in abscisic acid catabolism. Here, germination and gene expression were analysed to investigate the role of CYP707As in germination of both parasitic plants and Arabidopsis upon perception of germination stimulants, after using pharmacological inhibitors and Arabidopsis mutants disrupting germination signals. CYP707A genes were up-regulated upon treatment with effective germination stimulants in both parasitic plants and Arabidopsis. Obligate parasitic plants exhibited both intensified up-regulation of CYP707A genes and increased sensitivity to the CYP707A inhibitor abscinazole-E2B, whereas Arabidopsis cyp707a mutants still positively responded to germination stimulation. In Arabidopsis, CYP707A regulation required the canonical karrikin signalling pathway KAI2/MAX2/SMAX1 and the transcription factor WRKY33. Finally, CYP707As and WRKY33 also modulatedArabidopsis root architecture in response to the synthetic strigolactone rac-GR24, and wrky33-1 exhibited a shoot hyperbranched phenotype. This study suggests that the lack of host-independent germination in obligate parasites is associated with an exacerbated CYP707A induction and that CYP707As and WRKY33 are new players involved in a variety of strigolactone/karrikin responses.

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

Cited by 36 publications

References 23 publications

A ligand-independent origin of abscisic acid perception

A ligand-independent origin of abscisic acid perception

The flip side of phospho‐signalling: Regulation of protein dephosphorylation and the protein phosphatase 2Cs

CYP707As are effectors of karrikin and strigolactone signalling pathways in Arabidopsis thaliana and parasitic plants

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