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Microtubule-based perception of mechanical conflicts controls plant organ morphogenesis

Dorothee Stöckle, Blanca Jazmin Reyes-Hernández, Amaya Vilches Barro, Milica Nenadic, Zsófia Winter, Sophie Marc-Martin, Lotte Bald, Robertas Ursache, Satoshi Fujita, Alexis Maizel, Joop EM Vermeer

Preprint posted on September 10, 2021 https://www.biorxiv.org/content/10.1101/2021.09.09.459674v1

Integrating hormone- and mechanosignaling pathways: A breakthrough in how lateral roots break through

Selected by Marc Somssich

The development of plant shape and form, morphogenesis, is dependent on directed growth. The primary plant root grows down, with new cells being continuously produced in the tip, powering this growth and producing a regular, radial pattern of clearly defined tissues. Lateral root outgrowth, however, breaks this regular pattern, as lateral roots grow out of the side of the primary root, thus changing growth direction within a tissue (1,2). Lateral root initiation and outgrowth, is therefore an interesting developmental process to study the control of growth direction and postembryonic organogenesis (1,2). Plant hormones are known signals involved in growth coordination between cell populations within and across tissues, and auxin-signaling has been identified as the main inductive cue for lateral root development (1,2). Mechanosignaling is a second pathway involved in this process (1,2). A lateral root is initiated as a primordium (LRP) in cells of the pericycle, and then needs to break through the overlying endodermis cells to grow out. The endodermis responds to the expanding underlying LRP by thinning out, eventually allowing the lateral root to break through. This endodermal response is likely to be initiated in part through the mechanical stress put on the endodermis by the expanding LRP (1,2). 

In the new preprint discussed here (3), Dorothee Stöckle and colleagues from the lab of Joop Vermeer, as well as colleagues from the Alexis Maizel and Niko Geldner lab, integrate these two signaling pathways. By doing so, the authors continue to take the study of lateral root development from the hormone/auxin field, which was all the hype 20 years ago (There you go auxin-fans – I said it! Rather, wrote it), to the currently booming field of plant mechanobiology. 

With the emergence of plant mechanobiology, cortical microtubules (CMTs) were assigned a new role as putative tensile stress sensors in plant cells (4). Based on this hypothesis, as well as a previous study from the Maizel/Vermeer labs showing that cytoskeleton dynamics are involved in lateral root initiation (5), Dorothee Stöckle and colleagues decided to look at the organization of CMTs around the lateral root initiation site. Despite the significant challenge of imaging the CMT network in the inner root tissue, the authors not only managed to image the CMTs in the endodermis, but even showed that the CMTs are differentially organized within individual endodermis cells (Fig. 1A). At the inner side of the cell, facing the neighboring pericycle cells, the CMTs are organized in anisotropic arrays along the root-to-shoot axis. On the outer cell side, facing the cortex, the CMTs show an isotropic organization, without a clear orientation. Following lateral root initiation, the CMTs on the inner side lose this highly organized pattern and become isotropic, now resembling the cortex-facing side of the cell (Fig.1B). 


Fig. 1: CMT organization in endodermis cells neighboring a lateral root initiation site. A) CMT organization on the inner- and outer-facing side of the endodermis cell before LRP initiation. B) CMT organization after LRP initiation. Figure adapted from ref. 3. 

This reorganization is required for proper outgrowth of the lateral root and seems to function downstream of the auxin signal, which primes the endodermis for lateral root emergence. In order to test if the observed CMT response is directly connected to the priming auxin signal, the authors mine their previously published transcriptome dataset of auxin-treated endodermis cells for potential candidate proteins that could be involved in this signal-response integration (6). They find a MICROTUBULE-ASSOCIATED PROTEIN, MAP70-5 (7), to be differentially regulated following auxin-treatment. Under the microscope, MAP70-5 shows a highly distinct, punctate localization in metaxylem cells, but upon lateral root initiation additionally appears in endodermal cells overlying the initiated lateral root primordium (Fig. 2). Since the MAP70-5 regulatory sequences contain a putative auxin response element, this upregulation may represent a link to the priming auxin-signal, and indeed, the upregulation is lost in plants mutated for this priming signal (dominant negative forms of shy2 (1)). At later stages of lateral root development, MAP70-5 is enriched along the CMT arrays on the side of the endodermis cell facing the outgrowing lateral root, indicating a role for MAP70-5 in controlling the observed changes in CMT-organization on this side. map70-5 mutants, on the other hand, show defects in lateral root outgrowth. Interestingly, the mutants have several, sometimes contradictory effects. While the distinct CMT-organization on the LRP-facing side of the endodermis cells is lost in the mutant, and endodermis-thinning and lateral root outgrowth are impaired – all as it would be expected – there is also an increase in LRP initiation. Furthermore, primary root length is reduced in the mutant, and the lateral root development zone is shorter. Therefore, MAP70-5 seems to be a negative regulator of lateral root initiation, but a positive regulator (or rather facilitator) of lateral root outgrowth, and, furthermore, may play a role in primary root development. 


Fig. 2:
Localization of mCitrine-MAP70-5 during lateral root emergence at Stages I-III (A-C). MAP70-5::mCitrine-MAP70-5 in green, plasma membrane markers LBD16pro::3xmCherry:SYP122 (A, B) or UBQ10pro::tdTomato:RCI2a (C) in magenta. * indicates the endodermis. Figure adapted from ref. 3. 

The identification of MAP70-5 as a facilitator of lateral root emergence neatly links the priming auxin-signal to the CMT-mediated mechanoperception of increased tensile stress coming from the expanding LRP. But it also opens several new lines of research, as MAP70-5 appears to be involved in more than just this response. It will be interesting to find out how MAP70-5 influences LRP-initiation and to investigate its role in primary root development. Next to the beautiful single-cell microscopy and cell biology presented in this work, the linking of a hormone signaling-pathway to a mechanoperception pathway is a great feat, as it represents another linkage between a ‘traditional’ (hormone-signaling) and an emerging (mechano-devo (8)) field of plant developmental biology. 

A couple of questions that arise from this preprint include how the initial CMT organization on the inner side of the endodermis is initiated and maintained by MAP70-5. MAP70-5 is only expressed in the endodermis in response to LRP initiation, before which it is restricted to the metaxylem. So how are the anisotropic CMT arrays initially formed and maintained on the inner side of the endodermis? Also, how is MAP70-5 localization and function restricted to the one side of the cell? And, since cell wall synthesis and architecture are tightly linked to CMT organization, it would be interesting to find out if the inner and outer cell walls are structurally different. Is the inner wall initially more rigid? And if so, how does it become loose later, when later root emergence needs to be facilitated? Finally, the authors write about one auxin responsive element in the MAP70-5 regulatory sequences. However, as these elements are presumed to only be active in tandem arrangement (9), it would be interesting to confirm if MAP70-5 is expression is indeed directly induced by auxin. 

At last, I would also like to point out that writing this summary was made easy for me by a very nice Twitter-thread summary by Joop Vermeer: https://twitter.com/Vermeer_Lab/status/1436621700792205312 

References: 

  1. Vermeer, J. E. M. et al. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science (80-. ). 343, 178–83 (2014). doi:10.1126/science.1245871
  2. Vilches-Barro, A. & Maizel, A. Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr. Opin. Plant Biol. 23, 31–8 (2015). doi:10.1016/j.pbi.2014.10.005
  3. Stöckle, D. et al. Microtubule-based perception of mechanical conflicts controls plant organ morphogenesis. bioRxiv 459674 (2021) doi:10.1101/2021.09.09.459674.
  4. Hamant, O., Inoue, D., Bouchez, D., Dumais, J. & Mjolsness, E. Are microtubules tension sensors? Nat. Commun. 10, 2360 (2019). doi:10.1038/s41467-019-10207-y
  5. Vilches Barro, A. et al. Cytoskeleton Dynamics Are Necessary for Early Events of Lateral Root Initiation in Arabidopsis. Curr. Biol. 1–12 (2019) doi:10.1016/j.cub.2019.06.039.
  6. Ursache, R. et al. GDSL-domain proteins have key roles in suberin polymerization and degradation. Nat. Plants (2021) doi:10.1038/s41477-021-00862-9.
  7. Korolev, A. V., Chan, J., Naldrett, M. J., Doonan, J. H. & Lloyd, C. W. Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells. Plant J. 42, 547–555 (2005). doi:10.1111/j.1365-313X.2005.02393.x
  8. Hamant, O. Mechano-devo. Mech. Dev. (2017) doi:10.1016/j.mod.2017.02.004.
  9. Freire-Rios, A. et al. Architecture of DNA elements mediating ARF transcription factor binding and auxin-responsive gene expression in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 117, 24557–24566 (2020). doi:10.1073/pnas.2009554117

Tags: cytoskeleton, lateral roots, microscopy, microtubules, plant biology, plant mechanobiology, root development

Posted on: 23rd September 2021

doi: https://doi.org/10.1242/prelights.30710

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