scholarly journals An Evolutionarily Conserved Receptor-like Kinases Signaling Module Controls Cell Wall Integrity During Tip-Growth

2019 ◽  
Author(s):  
Jens Westermann ◽  
Susanna Streubel ◽  
Christina Maria Franck ◽  
Roswitha Lentz ◽  
Liam Dolan ◽  
...  
Keyword(s):  
Cell Wall ◽  
Tip Growth ◽  
Root Hairs ◽  
Pollen Tubes ◽  
Cell Wall Integrity ◽  
Marchantia Polymorpha ◽  
Evolutionarily Conserved ◽  
Receptor Kinases ◽  
The Common ◽  
Encoding Genes

AbstractRooting cells and pollen tubes – key adaptative innovations that evolved during the colonization and subsequent radiation of plants on land – expand by tip-growth. Tip-growth relies on a tight coordination between the protoplast growth and the synthesis/remodeling of the external cell wall. In root hairs and pollen tubes of the seed plant Arabidopsis thaliana, cell wall integrity (CWI) mechanisms monitor this coordination through the Malectin-like receptor kinases (MLRs) such as AtANXUR1 and AtFERONIA that act upstream of the AtMARIS PTI1-like kinase. Here, we show that rhizoid growth in the early diverging plant, Marchantia polymorpha, is also controlled by an MLR and PTI1-like signaling module. Rhizoids, root hairs and pollen tubes respond similarly to disruption of MLR and PTI1-like encoding genes. Thus, the MLR/PTI1-like signaling module that controls CWI during tip-growth is conserved between M. polymorpha and A. thaliana suggesting it was active in the common ancestor of land plants.

scholarly journals An Evolutionarily Conserved Receptor-like Kinases Signaling Module Controls Cell Wall Integrity During Tip Growth

2019 ◽  
Vol 29 (23) ◽  
pp. 4153 ◽  
Author(s):  
Jens Westermann ◽  
Susanna Streubel ◽  
Christina Maria Franck ◽  
Roswitha Lentz ◽  
Liam Dolan ◽  
...  
Keyword(s):  
Cell Wall ◽  
Tip Growth ◽  
Cell Wall Integrity ◽  
Evolutionarily Conserved

scholarly journals An Evolutionarily Conserved Receptor-like Kinases Signaling Module Controls Cell Wall Integrity During Tip Growth

2019 ◽  
Vol 29 (22) ◽  
pp. 3899-3908.e3 ◽  
Author(s):  
Jens Westermann ◽  
Susanna Streubel ◽  
Christina Maria Franck ◽  
Roswitha Lentz ◽  
Liam Dolan ◽  
...  
Keyword(s):  
Cell Wall ◽  
Tip Growth ◽  
Cell Wall Integrity ◽  
Evolutionarily Conserved

scholarly journals PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during Arabidopsis anther development

2018 ◽  
Author(s):  
Joseph R. Jacobowitz ◽  
Jing-Ke Weng
Keyword(s):  
Cell Wall ◽  
Pollen Development ◽  
Tapetal Cell ◽  
Pollen Grains ◽  
Anther Development ◽  
Cell Wall Integrity ◽  
Class Iii ◽  
Male Sterile ◽  
Male Gametes ◽  
Encoding Genes

AbstractPollen and microspore development is an essential step in the life cycle of all land plants that generate male gametes. Within flowering plants, pollen development occurs inside of the anther. Here, we report the identification of two class III peroxidase-encoding genes, PRX9 and PRX40, that are genetically redundant and essential for proper anther and pollen development in Arabidopsis thaliana. Arabidopsis double mutants devoid of functional PRX9 and PRX40 are male-sterile. The mutant anthers display swollen, hypertrophic tapetal cells and pollen grains, suggesting disrupted cell wall integrity. These phenotypes ultimately lead to nearly 100%-penetrant pollen degeneration upon anther maturation. Using immunochemical and biochemical approaches, we show that PRX9 and PRX40 are likely extensin peroxidases that contribute to the establishment of tapetal cell wall integrity during anther development. This work identifies PRX9 and PRX40 as the first extensin peroxidases to be described in Arabidopsis and highlights the importance of extensin cross-linking during plant development.

scholarly journals Microtubule associated protein WAVE DAMPENED2-LIKE (WDL) controls microtubule bundling and the stability of the site of tip-growth in Marchantia polymorpha rhizoids

PLoS Genetics ◽  
2021 ◽  
Vol 17 (6) ◽  
pp. e1009533
Author(s):  
Clement Champion ◽  
Jasper Lamers ◽  
Victor Arnold Shivas Jones ◽  
Giulia Morieri ◽  
Suvi Honkanen ◽  
...  
Keyword(s):  
Cell Surface ◽  
Tip Growth ◽  
Root Hairs ◽  
The Body ◽  
Marchantia Polymorpha ◽  
Linkage Groups ◽  
Spatial Stability ◽  
Apical Dome ◽  
Genes Encoding ◽  
Microtubule Networks

Tip-growth is a mode of polarized cell expansion where incorporation of new membrane and wall is stably restricted to a single, small domain of the cell surface resulting in the formation of a tubular projection that extends away from the body of the cell. The organization of the microtubule cytoskeleton is conserved among tip-growing cells of land plants: bundles of microtubules run longitudinally along the non-growing shank and a network of fine microtubules grow into the apical dome where growth occurs. Together, these microtubule networks control the stable positioning of the growth site at the cell surface. This conserved dynamic organization is required for the spatial stability of tip-growth, as demonstrated by the formation of sinuous tip-growing cells upon treatment with microtubule-stabilizing or microtubule-destabilizing drugs. Microtubule associated proteins (MAPs) that either stabilize or destabilize microtubule networks are required for the maintenance of stable tip-growth in root hairs of flowering plants. NIMA RELATED KINASE (NEK) is a MAP that destabilizes microtubule growing ends in the apical dome of tip-growing rhizoid cells in the liverwort Marchantia polymorpha. We hypothesized that both microtubule stabilizing and destabilizing MAPs are required for the maintenance of the stable tip-growth in liverworts. To identify genes encoding microtubule-stabilizing and microtubule-destabilizing activities we generated 120,000 UV-B mutagenized and 336,000 T-DNA transformed Marchantia polymorpha plants and screened for defective rhizoid phenotypes. We identified 119 mutants and retained 30 mutants in which the sinuous rhizoid phenotype was inherited. The 30 mutants were classified into at least 4 linkage groups. Characterisation of two of the linkage groups showed that MAP genes–WAVE DAMPENED2-LIKE (WDL) and NIMA-RELATED KINASE (NEK)–are required to stabilize the site of tip growth in elongating rhizoids. Furthermore, we show that MpWDL is required for the formation of a bundled array of parallel and longitudinally orientated microtubules in the non-growing shank of rhizoids where MpWDL-YFP localizes to microtubule bundles. We propose a model where the opposite functions of MpWDL and MpNEK on microtubule bundling are spatially separated and promote tip-growth spatial stability.

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to Immunity and Beyond

2018 ◽  
Vol 69 (1) ◽  
pp. 301-328 ◽  
Author(s):  
Christina Maria Franck ◽  
Jens Westermann ◽  
Aurélien Boisson-Dernier
Keyword(s):  
Cell Wall ◽  
Cell Wall Integrity ◽  
Receptor Kinases

scholarly journals LRR-extensins of vegetative tissues are a functionally conserved family of RALF1 receptors interacting with the receptor kinase FERONIA

2019 ◽  
Author(s):  
Aline Herger ◽  
Shibu Gupta ◽  
Gabor Kadler ◽  
Christina Maria Franck ◽  
Aurélien Boisson-Dernier ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Cell Wall ◽  
Plasma Membrane ◽  
Cell Growth ◽  
Mechanical Stability ◽  
Root Hairs ◽  
Cell Wall Integrity ◽  
Receptor Kinase ◽  
Growth Processes ◽  
Evolutionary Diversification

AbstractPlant cell growth requires the coordinated expansion of the protoplast and the cell wall that confers mechanical stability to the cell. An elaborate system of cell wall integrity sensors monitors cell wall structures and conveys information on cell wall composition and growth factors to the cell. LRR-extensins (LRXs) are cell wall-attached extracellular regulators of cell wall formation and high-affinity binding sites for RALF (rapid alkalinization factor) peptide hormones that trigger diverse physiological processes related to cell growth. RALF peptides are also perceived by receptors at the plasma membrane and LRX4 of Arabidopsis thaliana has been shown to also interact with one of these receptors, FERONIA (FER). Here, we demonstrate that several LRXs, including the main LRX protein of root hairs, LRX1, interact with FER and RALF1 to coordinate growth processes. Membrane association of LRXs correlate with binding to FER, indicating that LRXs represent a physical link between intra- and extracellular compartments via interaction with membrane-localized proteins. Finally, despite evolutionary diversification of the LRR domains of various LRX proteins, many of them are functionally still overlapping, indicative of LRX proteins being central players in regulatory processes that are conserved in very different cell types.Author SummaryCell growth in plants requires the coordinated enlargement of the cell and the surrounding cell wall, which is ascertained by an elaborate system of cell wall integrity sensors, proteins involved in the exchange of information between the cell and the cell wall. In Arabidopsis thaliana, LRR-extensins (LRXs) are localized in the cell wall and are binding RALF peptides, hormones that regulate cell growth-related processes. LRX4 also binds the plasma membrane-localized receptor kinase FERONIA (FER), establishing a link between the cell and the cell wall. It is not clear, however, whether the different LRXs of Arabidopsis have similar functions and how they interact with their binding partners. Here, we demonstrate that interaction with FER and RALFs requires the LRR domain of LRXs and several but not all LRXs can bind these proteins. This explains the observation that mutations in several of the LRXs induce phenotypes comparable to a fer mutant, establishing that LRX-FER interaction is important for proper cell growth. Some LRXs, however, appear to influence cell growth processes in different ways, which remain to be identified.

Microtubules are at the tips of root hairs and form helical patterns corresponding to inner wall fibrils

1985 ◽  
Vol 75 (1) ◽  
pp. 225-238 ◽  
Author(s):  
C.W. Lloyd ◽  
B. Wells
Keyword(s):  
Cell Wall ◽  
Phosphate Buffer ◽  
Tip Growth ◽  
Root Hairs ◽  
Onion Root ◽  
Apical Dome ◽  
Radish Root ◽  
Contradictory Evidence ◽  
Shadow Cast ◽  
Optimized Conditions

Root hairs have sometimes provided contradictory evidence for microtubule/microfibril parallelism. This tissue was re-examined using optimized conditions for the fixation, before immunofluorescence, of root hairs. In phosphate buffer, microtubules did not enter the apical tip of radish root hairs and were clearly fragmented. However, in an osmotically adjusted microtubule-stabilizing buffer, microtubules were observed within the apical dome and appeared unfragmented. Microtubules are not, therefore, absent from the region where new cell wall is presumed to be generated during tip growth. A spiralling of microtubules was seen at the apices of onion root hairs. Using shadow-cast preparations of macerated radish root hairs, it was confirmed that steeply helical microtubules matched the texture of the inner wall. In onion, the 45 degrees microtubular helices are accompanied by similarly wound inner wall fibrils. Results do not support the view that microtubules are not involved in the oriented deposition of fibrils in root hairs. Instead, they are interpreted in terms of a flexible helical cytoskeleton, which is capable of changing its pitch but is sensitive to fixation conditions.

scholarly journals An evolutionarily conserved NIMA-related kinase directs rhizoid tip growth in the basal land plant Marchantia polymorpha

Development ◽  
2018 ◽  
Vol 145 (5) ◽  
pp. dev154617 ◽  
Author(s):  
Kento Otani ◽  
Kimitsune Ishizaki ◽  
Ryuichi Nishihama ◽  
Shogo Takatani ◽  
Takayuki Kohchi ◽  
...  
Keyword(s):  
Tip Growth ◽  
Land Plant ◽  
Marchantia Polymorpha ◽  
Evolutionarily Conserved

Defective control of growth rate and cell diameter in tip-growing root hairs of the rhd4 mutant of Arabidopsis thaliana

1999 ◽  
Vol 77 (4) ◽  
pp. 494-507 ◽  
Author(s):  
M E Galway ◽  
D C Lane ◽  
J W Schiefelbein
Keyword(s):  
Growth Rate ◽  
Arabidopsis Thaliana ◽  
Cell Wall ◽  
Osmotic Stress ◽  
Tip Growth ◽  
Turgor Pressure ◽  
Root Hairs ◽  
Recessive Mutation ◽  
Cell Diameter ◽  
Hair Diameter

A recessive mutation in the RHD4 gene of Arabidopsis thaliana L. affects the control of tip growth in seedling root hairs. Fully grown rhd4 root hairs are half the length of wild-type (WT) hairs. The hairs are wider, and they vary in diameter during tip growth. Light microscopy and motion analysis revealed that rhd4 hairs grow more slowly and that hair growth rate varies more than in WT hairs. Hair diameter increases at the rhd4 hair tips when tip growth slows. Ultrastructural analysis revealed cell wall thickenings in some mutant hairs. WT hairs were grown in a hyperosmotic medium in an attempt to mimic the rhd4 hairs and investigate the control of root hair morphology. Osmotic stress increased WT hair diameter and induced hair bulging and also increased the diameters of rhd4 hairs. Osmotic stress could disrupt tip growth through reduced turgor pressure and (or) reduced concentrations of cytosolic calcium. Together these results indicate that RHD4 is required to maintain a uniform rate of tip growth in root hairs.Key words: Arabidopsis thaliana, cell wall, cryofixation, mutant, root hairs, tip growth.

scholarly journals Exocytosis and endocytosis: coordinating and fine-tuning the polar tip growth domain in pollen tubes

2020 ◽  
Vol 71 (8) ◽  
pp. 2428-2438 ◽  
Author(s):  
Jingzhe Guo ◽  
Zhenbiao Yang
Keyword(s):  
Cell Wall ◽  
Rho Gtpases ◽  
Intracellular Signaling ◽  
Tip Growth ◽  
Apical Cell ◽  
Turgor Pressure ◽  
Pollen Tubes ◽  
Fine Tuning ◽  
Rop Gtpase ◽  
Specialized Form

Abstract Pollen tubes rapidly elongate, penetrate, and navigate through multiple female tissues to reach ovules for sperm delivery by utilizing a specialized form of polar growth known as tip growth. This process requires a battery of cellular activities differentially occurring at the apical growing region of the plasma membrane (PM), such as the differential cellular signaling involving calcium (Ca2+), phospholipids, and ROP-type Rho GTPases, fluctuation of ions and pH, exocytosis and endocytosis, and cell wall construction and remodeling. There is an emerging understanding of how at least some of these activities are coordinated and/or interconnected. The apical active ROP modulates exocytosis to the cell apex for PM and cell wall expansion differentially occurring at the tip. The differentiation of the cell wall involves at least the preferential distribution of deformable pectin polymers to the apex and non-deformable pectin polymers to the shank of pollen tubes, facilitating the apical cell expansion driven by high internal turgor pressure. Recent studies have generated inroads into how the ROP GTPase-based intracellular signaling is coordinated spatiotemporally with the external wall mechanics to maintain the tubular cell shape and how the apical cell wall mechanics are regulated to allow rapid tip growth while maintaining the cell wall integrity under the turgor pressure. Evidence suggests that exocytosis and endocytosis play crucial but distinct roles in this spatiotemporal coordination. In this review, we summarize recent advances in the regulation and coordination of the differential pectin distribution and the apical domain of active ROP by exocytosis and endocytosis in pollen tubes.

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