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A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis

Saiko Yoshida, Alja van der Schuren, Maritza van Dop, Luc van Galen, Shunsuke Saiga, Milad Adibi, Barbara Moller, Peter Marhavy, Richard Smith, Jiri Friml, Dolf Weijers

Preprint posted on November 27, 2018 https://www.biorxiv.org/content/early/2018/11/27/479113

Subcellular signposts – or more? SOSEKI proteins are local outputs of the plant’s global coordinate system

Selected by Martin Balcerowicz

Background: Polarity is an essential component of plant development

The establishment of a three-dimensional body of a multicellular organism relies on directional growth, which is also reflected at the cellular level. Cell polarity in its broadest sense is defined as asymmetry along one axis or in one direction and can manifest itself in cell shape, function or distribution of cellular components. It can also determine the plane of cell division and thereby control division asymmetry1, 2. The two major axes of a plant, apical-basal (tip-to-base) and radial (inner-outer) are determined by asymmetric cell divisions during embryogenesis – in fact, the zygote itself already displays polarity and its first division is asymmetric3.

Our understanding of how polarity in plants is generated is still limited. A long-standing factor in controlling plant polarity is the plant hormone auxin, which is directionally transported due to polar distributions of its transport proteins. The auxin signal is then transduced into the regulation of gene expression through a set of receptors and transcription factors. MONOPTEROS (MP) is one of these AUXIN RESPONSE FACTORS and local inhibition of MP is known to alter asymmetric divisions2.  In their preprint, Yoshida et al. analysed the previously uncharacterised MP target SOSEKI1 (SOK1) – Japanese for “cornerstone” – and its paralogues for potential roles in cell polarity.

Key findings: A novel group of proteins translates global axes into polar localisation independent of tissue context

The authors identify SOK1-5 as novel polarly localised proteins in Arabidopsis. Accumulation of SOK-YFP fusion proteins was detected in embryos and roots, and all of them exhibited polar localisation within the cell (Figure 1). For instance, SOK1-YFP was observed at the outer apical corners of vascular cells in the root and the developing embryo, while SOK2-YFP localised to the inner basal edge of endodermal cells.

Ectopic expression of SOK1/2-YFP did not alter their apical-basal polarity in any cell type, suggesting that it is an intrinsic property of these proteins. SOK1-YFP did however change its inner/outer polarity in such a way that it was always oriented towards the cortex-endodermis junction. Thus, SOK proteins are able to integrate positional information on both the apical-basal and radial axes. Intriguingly, the fact that they can do so in any cell implies that a universal coordinate system exists throughout the plant that these proteins rely on.

Figure 1: Localisation of SOK-YFP fusion proteins in longitudinal cross sections of primary roots counterstained with propidium iodide (A-E) and in globular stage embryos (F-J) (reproduced with altered numbering from Yoshida et al., Fig. 1 C-G and Fig. 2 A-E, under a CC-BY 4.0 license).

 

What do SOK proteins do with the spatial information they integrate? Ectopic expression of SOK1 caused alterations in the orientation of cell divisions in all cell types. This effect depended on two domains of the protein: a central domain that promotes membrane association, and an N-terminal domain that is required for focused polar localisation. This N-terminal domain resembles a DIX (Dishevelled and Axin) domain, an oligomerisation domain described in several animal proteins such as the polarity regulator Dishevelled4. Indeed, the DIX-like domain was found to promote homodimerisation of SOK1 detected by BiFC and FRET assays. Thus, the DIX domain represents a commonality between animal and plant polarity mechanisms.

What I like about this preprint

This preprint catches a very exciting moment in research: it is not every day that you get to investigate a completely uncharacterised group of proteins, let alone proteins with quite intriguing molecular behaviour. Understanding the molecular function of the SOKs and the mechanism by which they integrate positional information could lead to a massive leap in our understanding of plant polarity as a whole.

Open questions/future directions

  • The preprint focuses on embryo and root phenotypes as these are the structures SOKs are expressed in – but how do SOK proteins behave when expressed e.g. in leaves? Does ectopic SOK expression cause aberrant divisions in above-ground organs as well?
  • SOK1 was originally identified as a downstream target of the auxin response factor MP. Does auxin have any effect on the remaining SOK proteins besides SOK1, and is there any evidence that a link between auxin and SOKs is relevant in a developmental context?
  • Knock-out mutants will be an invaluable resource to understand the SOKs’ function. Multiple mutants might be required though to find a clearly altered phenotype – in fact, if a single mutation was sufficient to visibly alter development, it might already have been included in this preprint.

References/Further reading

  1. Qi J, Greb T (2017). Cell polarity in plants: the Yin and Yang of cellular functions. Curr Opinion Plant Biol. 35: 105-110.
  2. Shao W, Dong J (2016). Polarity in plant asymmetric cell division: Division orientation and cell fate differentiation. Dev. Bio. 419(1): 121-131.
  3. Souter M, Lindsey K (2000). Polarity and signalling in plant embryogenesis. Exp. Bot. 51(347):971-983.
  4. Bienz M (2014). Signalosome assembly by domains undergoing dynamic head-to-tail polymerization. Trends Biochem. Sci. 39(10): 487-95.

Tags: arabidopsis, asymmetry, cell division, polarity

Posted on: 20th December 2018 , updated on: 21st December 2018

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  • Author's response

    Dolf Weijers and Saiko Yoshida shared

    Thank you for selecting our preprint for writing this pre-light, and for the clear summary. The questions raised are all very interesting, and subject of our ongoing research…perhaps not surprisingly. We will below respond to the questions formulated in the pre-light.

    Q:How do SOK proteins behave when expressed e.g. in leaves? Does ectopic SOK expression cause aberrant divisions in above-ground organs as well?

    A: Excellent question: is the ability to induce oblique division dependent upon the context SOK1 is misexpressed in? To be frank, we have not explored this aspect much, since our primary focus has been on the early embryo and its direct descendant organ: the root tip. The promoter we used for misimpression (RPS5A) is not very active outside of the meristems, and therefore addressing this question will require modifying the misimpression promoter for one that is active in the leaf. What we can tell is that polar SOK localisation is certainly not limited to the organs we described in the preprint…(more to come later).

    Q: Does auxin have any effect on the remaining SOK proteins besides SOK1, and is there any evidence that a link between auxin and SOKs is relevant in a developmental context?

    A: Yes, not only SOK1 but also SOK5 was identified as a gene down regulated upon inhibiting auxin response in embryos. We have no evidence that SOK2,3 or 4 respond to auxin.
    With regards to the relevance of the auxin-regulation, we can unfortunately not yet answer this question…see next point…

    Q: Knock-out mutants will be an invaluable resource to understand the SOKs’ function. Multiple mutants might be required though to find a clearly altered phenotype – in fact, if a single mutation was sufficient to visibly alter development, it might already have been included in this preprint.

    A: Indeed, and this has been a complete nightmare! We have spent a lot of effort on identifying or generating loss-of-function lines for SOK1, which has been very (!) difficult and disappointing. As anyone will understand, this is a top priority and a necessary step to understand what the molecular, cellular and developmental function of this intriguing protein family is.

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