Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells

Higaki, Takumi; Kutsuna, Natsumaro; Sano, Takeshi; Kondo, Noriaki; Hasezawa, Seiichiro

doi:10.1111/j.1365-313x.2009.04032.x

Cited by 229 publications

(325 citation statements)

References 34 publications

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“…A 30‐min dark treatment induced reorganisation of guard‐cell actin filaments into an irregular, mesh‐like arrangement in WT, whilst most actin filaments in opal5 guard cells remained bundled during the same treatment. To quantify the extent of actin filament bundling in guard cells, skewness was measured before and after dark treatments (Higaki et al ., 2010). The dark treatment caused a significant decrease in skewness in WT guard cells (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Serial images were projected, and the skewness of the distribution of GFP‐fABD2 fluorescence intensity in the overlaid images was used as an indicator of the extent of filament bundling. Skewness was quantified using the I mage J software (http://rsb.info.nih.gov/ij/) as previously described (Higaki et al ., 2010). Images of 100 guard cells (50 stomata) per genotype or treatment were collected and analysed.…”

Section: Methodsmentioning

confidence: 99%

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Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Isner

Costa

et al. 2017

New Phytologist

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Summary Stomata respond to darkness by closing to prevent excessive water loss during the night. Although the reorganisation of actin filaments during stomatal closure is documented, the underlying mechanisms responsible for dark‐induced cytoskeletal arrangement remain largely unknown.We used genetic, physiological and cell biological approaches to show that reorganisation of the actin cytoskeleton is required for dark‐induced stomatal closure.The opal5 mutant does not close in response to darkness but exhibits wild‐type (WT) behaviour when exposed to abscisic acid (ABA) or CaCl2. The mutation was mapped to At5g18410, encoding the PIR/SRA1/KLK subunit of the Arabidopsis SCAR/WAVE complex. Stomata of an independent allele of the PIR gene (Atpir‐1) showed reduced sensitivity to darkness and F1 progenies of the cross between opal5 and Atpir‐1 displayed distorted leaf trichomes, suggesting that the two mutants are allelic. Darkness induced changes in the extent of actin filament bundling in WT. These were abolished in opal5. Disruption of filamentous actin using latrunculin B or cytochalasin D restored wild‐type stomatal sensitivity to darkness in opal5.Our findings suggest that the stomatal response to darkness is mediated by reorganisation of guard cell actin filaments, a process that is finely tuned by the conserved SCAR/WAVE–Arp2/3 actin regulatory module.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Isner

Costa

et al. 2017

New Phytologist

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“…To do this, we focused on cell segments for which we had images of periclinal microtubules for at least seven time points prior to lobe initiation. The mean cortical occupancies (Higaki et al, 2010) of periclinal microtubules over time were calculated within opposing regions of interest (ROIs) in the two adjacent cells at the lobing interface. The ROIs were termed V, to denote the microtubule signals in the cell that would adopt a convex shape, and C, to denote the microtubule signals in the adjacent cell that would adopt a concave shape (Fig.…”

Section: Anticlinal Microtubules Are Not Stable Structures That Predimentioning

confidence: 99%

Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

et al. 2017

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The leaf epidermis is a biomechanical shell that influences the size and shape of the organ. Its morphogenesis is a multiscale process in which nanometer-scale cytoskeletal protein complexes, individual cells, and groups of cells pattern growth and define macroscopic leaf traits. Interdigitated growth of neighboring cells is an evolutionarily conserved developmental strategy. Understanding how signaling pathways and cytoskeletal proteins pattern cell walls during this form of tissue morphogenesis is an important research challenge. The cellular and molecular control of a lobed cell morphology is currently thought to involve PIN-FORMED (PIN)-type plasma membrane efflux carriers that generate subcellular auxin gradients. Auxin gradients were proposed to function across cell boundaries to encode stable offset patterns of cortical microtubules and actin filaments between adjacent cells. Many models suggest that long-lived microtubules along the anticlinal cell wall generate local cell wall heterogeneities that restrict local growth and specify the timing and location of lobe formation. Here, we used Arabidopsis (Arabidopsis thaliana) reverse genetics and multivariate long-term time-lapse imaging to test current cell shape control models. We found that neither PIN proteins nor long-lived microtubules along the anticlinal wall predict the patterns of lobe formation. In fields of lobing cells, anticlinal microtubules are not correlated with cell shape and are unstable at the time scales of cell expansion. Our analyses indicate that anticlinal microtubules have multiple functions in pavement cells and that lobe initiation is likely controlled by complex interactions among cell geometry, cell wall stress patterns, and transient microtubule networks that span the anticlinal and periclinal walls.Plant leaves are thin, mechanically durable organs. Their size and shape influence the efficiency of photosynthetic light capture and strongly influence crop yield (Zhu et al., 2010). The growth properties of the leaf epidermis can influence the morphology of the organ (Savaldi-Goldstein et al., 2007); therefore, there is a strong desire to understand how the division and growth of epidermal cells contribute to polarized growth at the level of tissues and organs. In the plant kingdom, an undulating cell shape is commonly generated in the leaf epidermis as polyhedral cells exit the cell division cycle and undergo an extended phase of polarized expansion (Panteris et al., 1993;Panteris and Galatis, 2005;Andriankaja et al., 2012). Interdigitated growth may give the leaf mechanical stability (Onoda et al., 2015;Sahaf and Sharon, 2016) and/or influence polarized growth at spatial scales that extend beyond that of individual cells (Elsner et al., 2012;Remmler and Rolland-Lagan, 2012).The biomechanics of the lobing process is complex. As in all other plant cell types, turgor pressure provides the driving force for pavement cell morphogenesis, and the physical connectivity of adjacent cells strongly influences the resulting mechanical stre...

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“…Together with its high and stable expression in epidermal cells of mature rosette leaves, we chose GFP-hTalin to study the organization of AFs in adf4 and ADF1-4Ri plants. We performed microscopic image analysis for the quantitative evaluation of AF bundling and density (Higaki et al, 2010b) in both uninfected (Supplemental Fig. S12) and G. orontii-infected (Fig.…”

Section: Af Organization Was Affected Only At Very Early Infection Timentioning

confidence: 99%

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

2016

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Actin-depolymerizing factors (ADFs) are conserved proteins that function in regulating the structure and dynamics of actin microfilaments in eukaryotes. In this study, we present evidence that Arabidopsis (Arabidopsis thaliana) subclass I ADFs, particularly ADF4, functions as a susceptibility factor for an adapted powdery mildew fungus. The null mutant of ADF4 significantly increased resistance against the adapted powdery mildew fungus Golovinomyces orontii. The degree of resistance was further enhanced in transgenic plants in which the expression of all subclass I ADFs (i.e. ADF1-ADF4) was suppressed. Microscopic observations revealed that the enhanced resistance of adf4 and ADF1-4 knockdown plants (ADF1-4Ri) was associated with the accumulation of hydrogen peroxide and cell death specific to G. orontii-infected cells. The increased resistance and accumulation of hydrogen peroxide in ADF1-4Ri were suppressed by the introduction of mutations in the salicylic acid-and jasmonic acid-signaling pathways but not by a mutation in the ethylene-signaling pathway. Quantification by microscopic images detected an increase in the level of actin microfilament bundling in ADF1-4Ri but not in adf4 at early G. orontii infection time points. Interestingly, complementation analysis revealed that nuclear localization of ADF4 was crucial for susceptibility to G. orontii. Based on its G. orontii-infected-cell-specific phenotype, we suggest that subclass I ADFs are susceptibility factors that function in a direct interaction between the host plant and the powdery mildew fungus.Powdery mildew is an obligate biotrophic fungal pathogen that infects approximately 10,000 plant species, including crops, vegetables, and ornamental plants, thus causing extensive economic losses worldwide (Takamatsu, 2004). In an effort to understand the plant response to powdery mildew fungal infection and the mechanism of plant-powdery mildew fungus interactions, many mutants of host plants, particularly the model plant Arabidopsis (Arabidopsis thaliana), have been identified and analyzed.Genes for which loss causes increased resistance to a pathogen could encode factors involved in the suppression of plant immunity or susceptibility factors that function in support of the pathogenic infection. Previously identified Arabidopsis genes, the loss of whose expression causes enhanced resistance against adapted powdery mildew fungi, include POWDERY MILDEW RESISTANT1 (PMR1)

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Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells

Cited by 229 publications

References 34 publications

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Actin filament reorganisation controlled by the SCAR/WAVE complex mediates stomatal response to darkness

Reassessing the Roles of PIN Proteins and Anticlinal Microtubules during Pavement Cell Morphogenesis

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

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