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ROS production by localized SCHENGEN receptor module drives lignification at subcellular precision

Satoshi Fujita, Damien De Bellis, Kai H. Edel, Phillipp Köster, Tonni Grube Andersen, Emanuel Schmid-Siegert, Valérie Dénervaud Tendon, Alexandre Pfister, Peter Marhavý, Robertas Ursache, Verónica G. Doblas, Jean Daraspe, Audrey Creff, Gwyneth Ingram, Jörg Kudla, Niko Geldner

Preprint posted on October 25, 2019 https://www.biorxiv.org/content/10.1101/818997v1

It’s all about localization, localization, localization! Unraveling the SCHENGEN signaling pathway guiding localized lignification of the Casparian strip.

Selected by Marc Somssich

Background

Plant roots are designed to take up water and nutrients from the soil to support plant growth1. Once taken up by the cells of the outermost root tissue, the epidermis, water and nutrients travel towards the central cylinder of the roots, the vascular tissue1. The vasculature serves as transport tissue to actively send water and nutrients towards the aerial parts of the plant. For most of the distance from epidermis to vasculature, water and nutrients can be transported apoplastically – that is not entering the cells, but travelling in the small space between cells1. Only when they reach the final layer of cells before the vascular tissue, the endodermis, are they forced by the Casparian strip (CS) to travel through the cells, instead of between them1,2. The CS is a diffusion barrier, tightly sealing the space between the cells of the endodermis, thereby protecting the vascular tissue from any potential threats, such as toxic substances and pathogens1. In order to cross the endodermis into the vasculature, anything needs to be actively transported in, and then out of the endodermal cells, providing the plant with a chance to be selective and keeping everything out that could harm the plant1. It is therefore vital for the plant’s life that the CS develops normally, as any aberration to its structure or localization could be fatal1.

Key findings

Fujita and colleagues have now unraveled a full signaling pathway directing localized lignification of the CS, thereby sealing it3. This includes a peptide signal (CIFs in Fig. 1) with corresponding receptor/co-receptor pair (SGN1/3 in Fig. 1), a downstream phospho-relay (black arrows in Fig. 1) towards reactive oxygen species (ROS)-producing oxidases (RBOHF in Fig. 1), localized ROS-release (black dots in Fig. 1) and eventual ROS-triggered lignification of the CS (marked by CASPs in Fig. 1). This pathway stands out by the delicate positioning of each protein to specific regions of individual endodermal cells, which directs the localization of the CS to the exact center of the cell, and at the same time provides an internal feedback-loop, enabling the cell to sense when lignification is complete (Fig. 1).

Fig. 1 Specific localizations of the Casparian strip and the different components of the SCHENGEN-pathway in an endodermal cell (taken from the preprint3).

The CASPARIAN STRIP INTEGRITY FACTOR (CIF) peptides are produced in the vasculature, from where they diffuse towards the endodermis (from ‘inner’ to ‘outer’ in Fig. 1, with ‘inner’ signifying the side facing the vasculature, and ‘outer’ signifying the side facing the epidermis). Before the CS is formed, its position is already determined by the localization of CASPARIAN STRIP DOMAIN PROTEINS (CASPs) proteins. The CIF-peptide receptor SCHENGEN3 (SGN3) is furthermore localized very specifically on both sides of this CASP protein cluster. Before the CS is fully formed, CIF can still diffuse past this region, and is therefore bound by SGN3 on both, the inner and outer side of the CS. On the outer side, SGN3 can interact with its co-receptor SGN1, which is specifically localized only to this outer-facing membrane of the cell. This binding of CIF to the SGN1/3 pair in the specific location on the outer side of the CS, then triggers a phosphor-relay from SGN3 to SGN1 to the oxidase RBOHF, which localized specifically to the region of the future CS, as marked by the CASPs. RBOHF then releases ROS specifically into the apoplast at the region of the CS, thereby leading to its lignification and closure. At this stage, the CIF molecules can no longer diffuse past the CS, and will therefore only bind to the SGN3 receptor on the inner side, but not the SGN1/3 receptor pair on the outer side, thereby automatically shutting down this pathway once its job (the closure of the CS) is complete.

Finally, the authors also find that the phosphor-relay can divert at SGN1 to also phosphorylate a MAPkinase cascade, leading to a transcriptional response to CIF-peptide signal perception.

Future directions

The most remarkable thing about this work is the delicate positioning of the different proteins and actions. In this regards, some the function of some localizations has not been fully described yet. For example, if SGN3 only functions on the outer side of the CS, where it can dimerize with SGN1, then why is SGN3 also localized to the inner side of the CS, where it can also bin CIF?

And what is the role of RBOHD, another oxidase that populates the plasma membrane everywhere except for the CS-region, where RBOHF localizes, and that can also be phosphorylated by SGN1? At least on the outer-facing side of the endodermal cell, RBOHD and SGN1 are co-localizing, so it must be assumed that they have a function here.

But overall this is such a nice and complete story, that it is hard to find questions that remain open.

References

1. Barbosa ICR, Rojas-Murcia N, Geldner N. The Casparian strip—one ring to bring cell biology to lignification? Curr Opin Biotechnol. 2019;56: 121–129. Available at doi:10.1016/j.copbio.2018.10.004

2. Caspary R. Bemerkungen über die Schutzscheide und die Bildung des Stammes und der Wurzel. Jahrbücher für wissenschaftliche Botanik. 1866.

3. Fujita S, Bellis D de, Edel KH, Köster P, Andersen TG, Schmid-Siegert E, et al. ROS production by localized SCHENGEN receptor module drives lignification at subcellular precision. bioRxiv. 2019;: 1–28. Available at doi:10.1101/818997

Tags: arabidopsis, casparian strip, endodermis, plant development, root development

Posted on: 22nd November 2019 , updated on: 25th November 2019

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