Patterned proliferation orients tissue-wide stress to control root vascular symmetry in Arabidopsis

Fujiwara, Motohiro; Imamura, Miyu; Matsushita, Katsuyoshi; Roszak, Pawel; Yamashino, Takafumi; Hosokawa, Yoichiroh; Nakajima, Keiji; Fujimoto, Koichi; Miyashima, Shunsuke

doi:10.1016/j.cub.2023.01.036

Cited by 10 publications

(3 citation statements)

References 100 publications

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“…Thus, we proposed that increased stele area in irk-4 was a secondary defect resulting from increased endodermal cell numbers in the radial axis due to excess LADs (Campos et al, 2020). Consistent with this, root vascular patterning and symmetry was recently connected to compressive stress on vascular cell types, likely from the surrounding cell layers (endodermis and pericycle) (Fujiwara et al, 2023). However, our data suggest there may be more complexity in the relationship between endodermal LADs and stele area increases and the roles of IRK and PXC2 in repressing them.…”

Section: Discussionmentioning

confidence: 62%

PXC2, a polarized receptor kinase, functions to repress ground tissue cell divisions and restrict stele size

Goff¹,

Jm²

2021

Preprint

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In plants, coordination of cell division and differentiation is critical for tissue patterning and organ development. Directional cell signaling and cell polarity have been proposed to participate in coordination of these developmental processes. For instance, a leucine-rich repeat receptor-like kinase (LRR-RLK) named INFLORESCENCE AND ROOT APICES KINASE (IRK) functions to restrict stele area and inhibit longitudinal anticlinal divisions (LADs) in the endodermis where it is polarly localized. The LRR-RLK most closely related to IRK is PXY/TDR CORRELATED 2 (PXC2) and we find that PXC2 shows similar polarized accumulation as IRK in root cell types. To further understand how these proteins operate in directional cell-cell signaling and root development we explored PXC2 function. pxc2 roots have an increase in stele area, indicating that PXC2 also functions to restrict stele size. Additionally, compared to either single mutant, irk pxc2 roots have an enhanced phenotype with further increases in endodermal LADs and stele area indicating redundant activities of these receptors. The double mutant also exhibits abnormal root growth, suggesting broader functions of PXC2 and IRK in the root. However, PXC2 is not functionally equivalent to IRK, as endodermal misexpression of PXC2 did not fully rescue irk. We propose that PXC2 is at least partially redundant to IRK with a more predominant role for IRK in repression of endodermal LADs. Our results are consistent with the hypothesis that repression of specific endodermal cell divisions and stele area through a PXC2/IRK-mediated directional signaling pathway is required for coordinated root growth and development.

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Section: Discussionmentioning

confidence: 62%

PXC2, a polarized receptor kinase, functions to repress ground tissue cell divisions and restrict stele size

Goff¹,

Jm²

2021

Preprint

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“…The initial radial pattern in the stele (Fig. 3a) is determined by mutual interactions between auxin and cytokinin signaling (Bishopp et al ., 2011; De Rybel et al ., 2014) and possibly reinforced by mechanical constrains emerging from formative cell divisions (Fujiwara et al ., 2023). Moreover, the pattern is likely stabilized by PEAR genes because they are cytokinin‐inducible, since the auxin‐cytokinin interactions set up high cytokinin signaling in the early protophloem lineage (Fukuda & Ohashi‐Ito, 2019; Miyashima et al ., 2019).…”

Section: Protophloem Development In the Arabidopsis Root Tipmentioning

confidence: 99%

Phloem development

Hardtke

2023

New Phytologist

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The evolution of the plant vascular system is a key process in Earth history because it enabled plants to conquer land and transform the terrestrial surface. Among the vascular tissues, the phloem is particularly intriguing because of its complex functionality. In angiosperms, its principal components are the sieve elements, which transport phloem sap, and their neighboring companion cells. Together, they form a functional unit that sustains sap loading, transport, and unloading. The developmental trajectory of sieve elements is unique among plant cell types because it entails selective organelle degradation including enucleation. Meticulous analyses of primary, so-called protophloem in the Arabidopsis thaliana root meristem have revealed key steps in protophloem sieve element formation at single-cell resolution. A transcription factor cascade connects specification with differentiation and also orchestrates phloem pole patterning via noncell-autonomous action of sieve element-derived effectors. Reminiscent of vascular tissue patterning in secondary growth, these involve receptor kinase pathways, whose antagonists guide the progression of sieve element differentiation. Receptor kinase pathways may also safeguard phloem formation by maintaining the developmental plasticity of neighboring cell files. Our current understanding of protophloem development in the A. thaliana root has reached sufficient detail to instruct molecular-level investigation of phloem formation in other organs.

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“…In addition, the cytokinin-induced GATA-type transcription factor HANABA TARANU (HAN) was shown to finetune the proliferation position and frequency in the vascular bundle together with B-type ARRs. It is suggested that this activity shapes the mechanical stresses in the vascular bundle and help to control tissue boundaries (Fujiwara et al, 2023).…”

Section: An Auxin/cytokinin Interplay Controls Vascular Cell Prolifer...mentioning

confidence: 99%

Hormonal control of the molecular networks guiding vascular tissue development in the primary root meristem of Arabidopsis

Sun

Yang

Rybel

2023

Journal of Experimental Botany

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Vascular tissues serve a dual function in plants, both providing physical support and controlling the transport of nutrients, water, hormones, and other small signaling molecules. Xylem tissues transport water from root to shoot; phloem tissues transfer photosynthates from shoot to root; while divisions of the (pro)cambium increase the number of xylem and phloem cells. Although vascular development constitutes a continuous process from primary growth in the early embryo and meristem regions to secondary growth in the mature plant organs, it can be artificially separated into distinct processes including cell type specification, proliferation, patterning, and differentiation. In this review, we focus on how hormonal signals orchestrate the molecular regulation of vascular development in the Arabidopsis primary root meristem. Although auxin and cytokinin have taken center stage in this aspect since their discovery, other hormones including brassinosteroids, abscisic acid, and jasmonic acid also take leading roles during vascular development. All these hormonal cues synergistically or antagonistically participate in the development of vascular tissues, forming a complex hormonal control network.

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Patterned proliferation orients tissue-wide stress to control root vascular symmetry in Arabidopsis

Cited by 10 publications

References 100 publications

PXC2, a polarized receptor kinase, functions to repress ground tissue cell divisions and restrict stele size

PXC2, a polarized receptor kinase, functions to repress ground tissue cell divisions and restrict stele size

Phloem development

Hormonal control of the molecular networks guiding vascular tissue development in the primary root meristem of Arabidopsis

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