The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling

Shi, Chun Lin; Wangenheim, Daniel von; Herrmann, Ullrich; Wildhagen, Mari; Kulik, Ivan; Köpf, Andreas; Ishida, Takashi; Olsson, Vilde; Anker, Mari Kristine; Albert, Markus; Butenko, Melinka A.; Felix, Georg; Sawa, Shinichiro; Claassen, Manfred; Friml, Jiřı́; Aalen, Reidunn B.

doi:10.1038/s41477-018-0212-z

Cited by 70 publications

(76 citation statements)

References 33 publications

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“…It has frequently been observed that some of the released cells are dead or die a few hours after their release. For instance, in Arabidopsis thaliana , lateral root cap border‐like cells seem to undergo programmed cell death during their release unlike columella‐derived border‐like cells (Fendrych et al , ; Shi et al , ). The same observation was also made for flax Linum usitatissimum root border cells (Plancot et al , ).…”

Section: Rets and Nets Form From Pre‐existing Tissue And Organ Cellsmentioning

confidence: 99%

Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence?

et al. 2019

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The root cap releases cells that produce massive amounts of mucilage containing polysaccharides, proteoglycans, extracellular DNA (exDNA) and a variety of antimicrobial compounds. The released cells – known as border cells or border‐like cells – and mucilage secretions form networks that are defined as root extracellular traps (RETs). RETs are important players in root immunity. In animals, phagocytes are some of the most abundant white blood cells in circulation and are very important for immunity. These cells combat pathogens through multiple defence mechanisms, including the release of exDNA‐containing extracellular traps (ETs). Traps of neutrophil origin are abbreviated herein as NETs. Similar to phagocytes, plant root cap‐originating cells actively contribute to frontline defence against pathogens. RETs and NETs are thus components of the plant and animal immune systems, respectively, that exhibit similar compositional and functional properties. Herein, we describe and discuss the formation, molecular composition and functional similarities of these similar but different extracellular traps.

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Section: Rets and Nets Form From Pre‐existing Tissue And Organ Cellsmentioning

confidence: 99%

Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence?

et al. 2019

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“…IDA and the IDL peptides control cell separation processes during plant development and in response to abiotic and biotic stress 7,14,19,24 . The regulation of IDA expression is under developmental control but can also be activated by abiotic and biotic stimuli.…”

Section: Fig 7: Ida Regulates Cell Separation and Modulates Immunitymentioning

confidence: 99%

“…IDA signaling through HAE and HSL2 regulates 3 cell wall remodeling genes in the endodermal, cortical and epidermal tissues overlaying the LR primordia during LR emergence 8 . In addition, IDA-LIKE 1 (IDL1), one of the eight members in the IDL peptide family 11 that shares a conserved C-terminal domain which in IDA is processed to a functional 14 amino acid hydroxylated peptide 12,13 , signals through HSL2 to regulate cell separation during root cap sloughing 14 .…”

Section: Introductionmentioning

confidence: 99%

A dual function of the IDA peptide in regulating cell separation and modulating plant immunity at the molecular level

Olsson

Smakowska-Luzan

Breiden

et al. 2019

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The abscission of floral organs and emergence of lateral roots in Arabidopsis is regulated by the peptide ligand INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) and the receptor protein kinases HAESA (HAE), HAESA-LIKE 2 (HSL2) and members of the SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) family. These cell separation processes lead to induction of defense-associated genes to protect against pathogen invasion. However, the molecular coordination between abscission and immunity has not been thoroughly explored. Here we show that IDA induces a receptor-dependent release of cytosolic calcium and an extracellular release of reactive oxygen species which are signatures of defense responses. IDA promotes heteromerization between HSL2 and RECEPTOR LIKE KINASE 7 (RLK7), a receptor that enhances immunity and pathogen responses, and utilizes this novel signaling module to regulate the expression of defense-associated genes. We propose a molecular mechanism by which IDA drives specific immune response in cells destined for separation to guard them from pathogen attack.

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“…As described for IDA-like families in other species [12], the different members of the N. benthamiana family are also expressed in multiple plant tissues (Figure 4). This is not a surprise since the IDA-like signaling peptides, as cell-to-cell communication elements, function in several cell separation events, including lateral root emergence and root cap sloughing [10,11]. Interestingly, in plants of N. benthamiana actively growing, the highest expression level of most members of the IDA-like family was found in nodes and internodes.…”

Section: Expression Patterns Of Ida-like Genes In Nicotiana Benthamiamentioning

confidence: 99%

“…The function of IDA peptides, as cell-to-cell communication elements, does not appear to be solely 4 restricted to their roles in abscission. The activity of these peptides has also recently been involved in other developmental processes in Arabidopsis all of them settled on cell separation events such as the emergence of lateral roots and the root cap sloughing [10,11]. In addition, IDA peptides have recently been involved in the response to abiotic stresses.…”

Section: Introductionmentioning

confidence: 99%

Differential expression of IDA (INFLORESCENCE DEFICIENT IN ABSCISSION)-like genes in Nicotiana benthamiana during corolla abscission, stem growth and water stress

Ventimilla

Domingo

Talón

et al. 2019

Preprint

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Background IDA (INFLORESCENCE DEFICIENT IN ABSCISSION)-like signaling peptides and the associated HAE (HAESA)-like family of receptor kinases were originally reported in the model plant Arabidopsis thaliana (Arabidopsis) to be involved in the regulation of abscission. IDA peptides, as cell-to-cell communication elements, appear to be implicated in many developmental processes that rely on cell separation events, and even in the responses to abiotic stresses. However, the knowledge related to the molecular machinery regulating abscission and other cell separation processes in economically important crops is scarce. In this work, we determined the conservation and phylogeny of the IDA-like and HAE-like gene families in relevant species of the Solanaceae family and analyzed the expression of these genes in Nicotiana benthamiana to identify members involved in abscission, stem growth and response to drought conditions. Results The phylogenetic relationships among the IDA-like members of the species of Solanaceae studied, grouped the NbenIDA1 (A and B) and NbenIDA2 (A and B) pairs of genes with the Arabidopsis prepropeptides related to abscission. In silico analyses of the regulatory elements of the promoter region of IDA-like members showed that these two pairs of genes, NbenIDA1 and NbenIDA2, contained drought and hormonal response elements, although NbenIDA2A lacked the hormonal regulatory elements. Expression analyses showed that both NbenIDA1 genes were upregulated during corolla abscission. NbenIDA1 and NbenIDA2 genes showed tissue differential expression under water stress conditions, since NbenIDA1 genes were highly expressed in stressed leaves while NbenIDA2 genes, especially NbenIDA2B, were highly expressed in stressed roots. In non-stressed active growing plants, nodes and internodes were the tissues with the highest expression levels of all members of the IDA-like family and their putative HAE-like receptors. Conclusion The results suggest that NbenIDA1A and NbenIDA1B are both involved in the natural process of corolla abscission while the NbenIDA1 and NbenIDA2 pair of genes are implicated in the response to water stress. The data also suggest that IDA peptides may be important during stem growth and development. These results add new evidence that the functional module formed by IDA peptides and its receptor kinases, as defined in Arabidopsis, may also be conserved in Solanaceae.

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The dynamics of root cap sloughing in Arabidopsis is regulated by peptide signalling

Cited by 70 publications

References 33 publications

Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence?

Root extracellular traps versus neutrophil extracellular traps in host defence, a case of functional convergence?

A dual function of the IDA peptide in regulating cell separation and modulating plant immunity at the molecular level

Differential expression of IDA (INFLORESCENCE DEFICIENT IN ABSCISSION)-like genes in Nicotiana benthamiana during corolla abscission, stem growth and water stress

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