A Dof-CLE circuit controls phloem organization

Qian, Pingping; Song, Wen; Zaizen-Iida, Miki; Kume, Sawa; Wang, Guodong; Zhang, Ye; Kinoshita-Tsujimura, Kaori; Chai, Jijie; Kakimoto, Tatsuo

doi:10.1038/s41477-022-01176-0

Cited by 24 publications

(32 citation statements)

References 52 publications

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“…Thereby, phloem poles* suppressed phloem pole* formation in their vicinity, expected to result in a patchy pattern of phloem poles as observed in planta [38]. The inhibition of phloem poles in their immediate environment is reminiscent to the CLE45/RECEPTOR LIKE PROTEIN KINASE 2 (RPK2) signaling cascade restricting protophloem sieve element identity to its usual position [39, 40]. It is worth noting that in our model, CLE41* was still produced in both phloem poles* and phloem parenchyma* but with a higher rate in phloem poles*.…”

Section: Resultsmentioning

confidence: 99%

Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

Lebovka

Mele

Zakieva

et al. 2020

Preprint

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Precise organization of growing structures is a fundamental problem in developmental biology. In plants, radial growth is mediated by the cambium, a stem cell niche continuously producing wood (xylem) and bast (phloem) in a strictly bidirectional manner. While this process contributes large parts to terrestrial biomass, cambium dynamics eludes direct experimental access due to obstacles in live cell imaging. Here, we present a cell-based computational model visualizing cambium activity and integrating the function of central cambium regulators. Performing iterative comparisons of plant and model anatomies, we conclude that an intercellular signaling module consisting of the receptor-like kinase PXY and its ligand CLE41 constitutes a minimal framework sufficient for instructing tissue organization. Employing genetically encoded markers for different cambium domains in backgrounds with altered PXY/CLE41 activity, we furthermore propose that the module is part of a larger regulatory circuit using the phloem as a morphogenetic center. Our model highlights the importance of intercellular communication along the radial sequence of tissues within the cambium area and shows that a limited number of factors is sufficient to create a stable bidirectional tissue production.

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Section: Resultsmentioning

confidence: 99%

Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

Lebovka

Mele

Zakieva

et al. 2020

Preprint

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“…Here we identified a new molecular player in root protophloem formation, a small signaling peptide gene CLE33. In the Arabidopsis root, phloem-specific DOF transcription factors induce a set of positive regulators of phloem development, and CLEs which downregulate DOF expression in a feedback loop (2,3). With DOF binding-sites in its upstream regulatory sequence, CLE33 is likely involved in this genetic circuit.…”

Section: Discussionmentioning

confidence: 99%

“…The process of PSE formation requires radical cellular modifications, including cell wall reinforcement, enucleation and sieve plate formation (14,15). The genetic control of protophloem development in Arabidopsis has been studied intensively in the last decade (2,4,5,12,14,16), including precise transcriptomics analysis of the whole phloem pole (12) and developing SEs (14). Protophloem differentiation is controlled by multiple regulators such as hormone gradients, DOF transcription factors and SMXL transcriptional repressors (2,3).…”

Section: Mainmentioning

confidence: 99%

“…The genetic control of protophloem development in Arabidopsis has been studied intensively in the last decade (2,4,5,12,14,16), including precise transcriptomics analysis of the whole phloem pole (12) and developing SEs (14). Protophloem differentiation is controlled by multiple regulators such as hormone gradients, DOF transcription factors and SMXL transcriptional repressors (2,3). In addition, two membrane-localized proteins, BREVIS RADIX (BRX) and OCTOPUS (OPS) act as positive regulators of protophloem development (4,5).…”

Section: Mainmentioning

confidence: 99%

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A novel Arabidopsis peptide represses phloem differentiation via autocrine and paracrine signaling

Hazak

Carbonnel

Cornelis

2023

Preprint

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Plant meristems require a constant supply of photoassimilates and hormones to the dividing meristematic cells. In the growing root, such supply is delivered by protophloem sieve elements (1). Due to its preeminent function for the root apical meristem, protophloem is the first tissue to differentiate. This process is regulated by a genetic circuit involving in one-side the positive regulators DOF transcription factors (2, 3), OCTOPUS (OPS)(4) and BREVIX RADIX (BRX)(5), and in the other-side the negative regulators CLAVATA3/EMBRYO SURROUNDING REGION RELATED (CLE) peptides and their cognate receptors BARELY ANY MERISTEM (BAM) receptor-like kinases and co-receptors CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIKs)(2, 6-8). brx and ops mutants harbor a discontinuous protophloem (4, 5) that can be fully rescued by mutation in BAM3 (5) but only partially rescued by multiple mutations in all three known phloem-specific CLE genes, CLE25/26/45 (2, 6). These observations suggest that one or more additional CLE peptides play a role in protophloem formation. By reanalyzing Arabidopsis genome, we have identified a novel CLE gene closely related to CLE45, named CLE33, that is expressed in developing protophloem and is perceived by BAM3. Mutations in CLE33 and CLE45 are together sufficient to fully suppress brx and ops discontinuous protophloem phenotype. Furthermore, in these mutants we observed ectopic protophloem differentiation in neighboring cells, supporting the current model where phloem-specific CLE peptides act as paracrine signals to maintain a single functional protophloem cell file (2). CLE33 orthologs are found in basal angiosperms, monocots and eudicots, and the gene duplication giving rise to CLE45 in Arabidopsis and other Brassicaceae appears to be a recent event. We, thus, have discovered a novel peptide gene that is an ancient angiosperms’ CLE gene, and an essential player in the genetic circuit controlling protophloem formation.

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“…CLAVATA3/ESR-like ( CLE25 ), CLE26, and CLE45 genes for the secretory peptides repress PSE formation [ 26 , 27 , 28 , 29 ]. Phloem-enriched Dof transcription factors (PEARs) help the phloem formation by activating the precursors of phloem and surrounding cell division [ 25 , 30 , 31 , 32 ]. In the mature inflorescence stem of Arabidopsis thaliana , fluorescence-activated nuclear sorting (FACS) and laser capture microdissection approaches with next-generation RNA sequencing have provided genome-wide gene expression maps, covering more than 15,000 genes as being differentially expressed among vascular bundles, the proximal and distal cambium, phloem and other stem tissues at different development stages [ 31 ].…”

Section: Introductionmentioning

confidence: 99%

Biomolecular Strategies for Vascular Bundle Development to Improve Crop Yield

et al. 2022

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The need to produce crops with higher yields is critical due to a growing global population, depletion of agricultural land, and severe climate change. Compared with the “source” and “sink” transport systems that have been studied a lot, the development and utilization of vascular bundles (conducting vessels in plants) are increasingly important. Due to the complexity of the vascular system, its structure, and its delicate and deep position in the plant body, the current research on model plants remains basic knowledge and has not been repeated for crops and applied to field production. In this review, we aim to summarize the current knowledge regarding biomolecular strategies of vascular bundles in transport systems (source-flow-sink), allocation, helping crop architecture establishment, and influence of the external environment. It is expected to help understand how to use sophisticated and advancing genetic engineering technology to improve the vascular system of crops to increase yield.

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A Dof-CLE circuit controls phloem organization

Cited by 24 publications

References 52 publications

Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

Computational modelling of cambium activity provides a regulatory framework for simulating radial plant growth

A novel Arabidopsis peptide represses phloem differentiation via autocrine and paracrine signaling

Biomolecular Strategies for Vascular Bundle Development to Improve Crop Yield

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