A Rho-based reaction-diffusion system governs cell wall patterning in metaxylem vessels

Nagashima, Yoshiki; Tsugawa, Satoru; Mochizuki, Atsushi; Sasaki, Takema; Fukuda, Hiroo; Oda, Y.

doi:10.1038/s41598-018-29543-y

Cited by 56 publications

(59 citation statements)

References 40 publications

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“…Recent destined to become pits (Oda & Fukuda, 2013;Oda, Iida, Kondo, & Fukuda, 2010;Sasaki, Fukuda, & Oda, 2017 formation has features consistent with a classical Turing reactiondiffusion mechanism (Nagashima et al, 2018).…”

Section: How Is Pit Formati On Altered To Miti G Ate C Avitati On Vmentioning

confidence: 86%

“…Protein complexes containing MICROTUBULE DEPLETION DOMAIN1 (MIDD1) and RHO‐RELATED PROTEIN FROM PLANTS11 (ROP11) actively promote the disassembly of cortical microtubules and thus exclude cellulose synthase complexes and secondary cell wall formation in regions destined to become pits (Oda & Fukuda, ; Oda, Iida, Kondo, & Fukuda, ; Sasaki, Fukuda, & Oda, ). Interestingly, mutation or changes in expression of these and MIDD1/ROP11 interacting proteins can dramatically change the spacing and size of pits (Nagashima et al, ). Mathematical modeling shows that pit formation has features consistent with a classical Turing reaction‐diffusion mechanism (Nagashima et al, ).…”

Section: How Is Pit Formation Altered To Mitigate Cavitation Vulnerabmentioning

confidence: 99%

“…Interestingly, mutation or changes in expression of these and MIDD1/ROP11 interacting proteins can dramatically change the spacing and size of pits (Nagashima et al, ). Mathematical modeling shows that pit formation has features consistent with a classical Turing reaction‐diffusion mechanism (Nagashima et al, ).…”

Section: How Is Pit Formation Altered To Mitigate Cavitation Vulnerabmentioning

confidence: 99%

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Wood and water: How trees modify wood development to cope with drought

Rodriguez‐Zaccaro

Groover

2019

Plants People Planet

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Societal Impact Statement Drought plays a conspicuous role in forest mortality, and is expected to become more severe in future climate scenarios. Recent surges in drought‐associated forest tree mortality have been documented worldwide. For example, recent droughts in California and Texas killed approximately 129 million and 300 million trees, respectively. Drought has also induced acute pine tree mortality across east‐central China, and across extensive areas in southwest China. Understanding the biological processes that enable trees to modify wood development to mitigate the adverse effects of drought will be crucial for the development of successful strategies for future forest management and conservation. Summary Drought is a recurrent stress to forests, causing periodic forest mortality with enormous economic and environmental costs. Wood is the water‐conducting tissue of tree stems, and trees modify wood development to create anatomical features and hydraulic properties that can mitigate drought stress. This modification of wood development can be seen in tree rings where not only the amount of wood but also the morphology of the water‐conducting cells are modified in response to environmental conditions. In this review, we provide an overview of how trees conduct water, and how trees modify wood development to affect water conduction properties in response to drought. We discuss key needs for new research, and how new knowledge of wood formation can play a role in the conservation of forests under threat by climate change.

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Section: How Is Pit Formati On Altered To Miti G Ate C Avitati On Vmentioning

confidence: 86%

Section: How Is Pit Formation Altered To Mitigate Cavitation Vulnerabmentioning

confidence: 99%

Section: How Is Pit Formation Altered To Mitigate Cavitation Vulnerabmentioning

confidence: 99%

See 1 more Smart Citation

Wood and water: How trees modify wood development to cope with drought

Rodriguez‐Zaccaro

Groover

2019

Plants People Planet

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“…For instance, a ROP11-based reaction-diffusion mechanism drives localized secondary wall thickenings during differentiation of meta-xylem cells, which produce pitted wall patterns. This mechanism involves local activation of ROP11 at the plasma membrane and recruitment of microtubule depolymerizers, such as MICROTUBULE DEPLETION DOMAIN (MIDD)1 and KINESIN (KIN)13A (Oda and Fukuda 2012a; Oda and Fukuda 2013; Nagashima et al 2018). The microtubule-associated proteins IQ-DOMAIN (IQD)13 and IQD14 control the shape of the active ROP11 domains whereas BOUNDARY OF ROP DOMAIN (BDR)1 and WALLIN (WAL) direct actin filaments to the border of the active ROP11 domain (Sugiyama et al 2017; Sugiyama et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Long-term single-cell imaging and simulations of microtubules reveal driving forces for wall pattering during proto-xylem development

Schneider

Klooster

Picard

et al. 2020

Preprint

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42Plants are the tallest organisms on Earth; a feature sustained by solute-transporting 43 xylem vessels in the plant vasculature. The xylem vessels are supported by strong 44 cell walls that are assembled in intricate patterns. Cortical microtubules direct wall 45 deposition and need to rapidly re-organize during xylem cell development. We 46 established long-term live-cell imaging of single Arabidopsis cells undergoing proto-47 xylem trans-differentiation, resulting in spiral wall patterns, to investigate the 48 microtubule re-organization. The initial disperse microtubule array rapidly readjusted 49 into well-defined microtubule bands, which required local de-stabilization of individual 50 microtubules in band-interspersing gap regions. Using extensive microtubule 51 simulations, we could recapitulate the process in silico and found that local 52 recruitment of microtubule-bound nucleation is critical for pattern formation, which we 53 confirmed in vivo. Our simulations further indicated that the initial microtubule 54 alignment impact microtubule band patterning. We confirmed this prediction using 55 katanin mutants, which have microtubule organization defects, and uncovered active 56 KATANIN recruitment to the forming microtubule bands. Our combination of 57 quantitative microscopy and modelling outlines a framework towards a 58 comprehensive understanding of microtubule re-organization during wall pattern 59 formation. 60 61 62The plant vasculature contains xylem cells that are organised in interconnected 63 tubular networks to enable efficient water distribution to plant organs, and that 64 support plant stature (Myburg et al. 2001). All plant cells are surrounded by primary 65 cell walls, which dictate growth direction. Xylem cells are reinforced by an additional 66 wall layer, referred to as a secondary wall, that is deposited in local thickenings that 67 form highly ordered spatial patterns (Turner et al. 2007). Xylem cells subsequently 68 undergo programmed cell death, which leads to the clearing of their cytoplasmic 69 content and the resulting formation of a hollow tube that provides the water-70 conducting capacity of vascular plants (Meents et al. 2018).71 The major load-bearing component of plant cell walls is cellulose; a β-1,4-72 linked glucan. Cellulose is synthesised by cellulose synthase (CESA) complexes 73 (CSCs) that span the plasma membrane (Schneider et al. 2016). Nascent cellulose 74 chains coalesce via hydrogen bonds, get entangled in the cell wall and further 75 synthesis thus forces the CSCs to move in the membrane (Diotallevi and Mulder 76 4 2007). The CSC delivery to, and locomotion within, the plasma membrane is guided 77 by cortical microtubules that presumably are associated with the plasma membrane 78 (Paradez et al. 2006; Crowell et al. 2009; Gutierrez et al. 2009; Watanabe et al. 79 2015). Cortical microtubules thus directionally and spatially template the cellulose 80 synthesis machinery during cell wall deposition. 81Microtubules undergo dynamic re-organizati...

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“…In addition, we show that different ROP-based Turing mechanisms have a very similar response to a directional reduction in activator diffusion. Therefore, the proposed orientation mechanism seems sufficiently general to apply to different reaction-diffusion systems able to generate coexisting spots, stripes, and gaps, of which many variants exist [6,30,29]. However, it is important that diffusion restriction applies predominantly to the active form, because diffusion restriction of all components in the same way will not 395 yield banded patterns with controlled orientation.…”

Section: Directional Diffusion Restriction Can Orient Rop Patterns Inmentioning

confidence: 99%

Robust banded protoxylem pattern formation through microtubule-based directional ROP diffusion restriction

Jacobs¹,

Molenaar²,

Deinum³

2019

Preprint

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In plant vascular tissue development, different cell wall patterns are formed, offering different mechanical properties optimised for different growth stages. Critical in these patterning processes are Rho of Plants (ROP) proteins, a class of evolutionarily conserved small GTPase proteins responsible for local membrane domain formation in many organisms. While the spotted metaxylem pattern can easily be understood as a result of a Turing-style reaction-diffusion mechanism, it remains an open question how the consistent orientation of evenly spaced bands and spirals as found in protoxylem is achieved. We hypothesise that this orientation results from an interaction between ROPs and an array of transversely oriented cortical microtubules that acts as a directional diffusion barrier. Here, we explore this hypothesis using partial differential equation models with anisotropic ROP diffusion and show that a horizontal microtubule array acting as a vertical diffusion barrier to active ROP can yield a horizontally banded ROP pattern. We then study the underlying mechanism in more detail, finding that it can only orient curved pattern features but not straight lines. This implies that, once formed, banded and spiral patterns cannot be reoriented by this mechanism. Finally, we observe that ROPs and microtubules together only form ultimately static patterns if the interaction is implemented with sufficient biological realism.

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A Rho-based reaction-diffusion system governs cell wall patterning in metaxylem vessels

Cited by 56 publications

References 40 publications

Wood and water: How trees modify wood development to cope with drought

Wood and water: How trees modify wood development to cope with drought

Long-term single-cell imaging and simulations of microtubules reveal driving forces for wall pattering during proto-xylem development

Robust banded protoxylem pattern formation through microtubule-based directional ROP diffusion restriction

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