Arabidopsis Annexin1 Mediates the Radical-Activated Plasma Membrane Ca2+- and K+-Permeable Conductance in Root Cells

Laohavisit, Anuphon; Shang, Zhonglin; Rubio, Lourdes; Cuin, Tracey Ann; Véry, Anne‐Aliénor; Wang, Aihua; Mortimer, Jenny C.; Macpherson, Neil; Coxon, Katy M.; Battey, Nicholas H.; Brownlee, Colin; Park, Ohkmae K.; Sentenac, Hervé; Shabala, Sergey; Webb, Alex A. R.; Davies, Julia M.

doi:10.1105/tpc.112.097881

Cited by 170 publications

(213 citation statements)

References 53 publications

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“…These results were exciting for the plant ion transport community, since in addition to the fact that they raised questions of structural evolution within the HKT family, at least for the former of these studies, they identified OsHKT2;4 as a potential actor of plant cell Ca 2+ signaling, in which very few proteins playing a role as Ca 2+ transporters or channels have been clearly identified at the molecular level so far (White et al, 2002;Ali et al, 2007;Cho et al, 2009;Laohavisit et al, 2010Laohavisit et al, , 2012.…”

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The Rice Monovalent Cation Transporter OsHKT2;4: Revisited Ionic Selectivity

et al. 2012

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The family of plant membrane transporters named HKT (for high-affinity K+ transporters) can be subdivided into subfamilies 1 and 2, which, respectively, comprise Na+-selective transporters and transporters able to function as Na+-K+ symporters, at least when expressed in yeast (Saccharomyces cerevisiae) or Xenopus oocytes. Surprisingly, a subfamily 2 member from rice (Oryza sativa), OsHKT2;4, has been proposed to form cation/K+ channels or transporters permeable to Ca2+ when expressed in Xenopus oocytes. Here, OsHKT2;4 functional properties were reassessed in Xenopus oocytes. A Ca2+ permeability through OsHKT2;4 was not detected, even at very low external K+ concentration, as shown by highly negative OsHKT2;4 zero-current potential in high Ca2+ conditions and lack of sensitivity of OsHKT2;4 zero-current potential and conductance to external Ca2+. The Ca2+ permeability previously attributed to OsHKT2;4 probably resulted from activation of an endogenous oocyte conductance. OsHKT2;4 displayed a high permeability to K+ compared with that to Na+ (permeability sequence: K+ > Rb+ ≈ Cs+ > Na+ ≈ Li+ ≈ NH4 +). Examination of OsHKT2;4 current sensitivity to external pH suggested that H+ is not significantly permeant through OsHKT2;4 in most physiological ionic conditions. Further analyses in media containing both Na+ and K+ indicated that OsHKT2;4 functions as K+-selective transporter at low external Na+, but transports also Na+ at high (>10 mm) Na+ concentrations. These data identify OsHKT2;4 as a new functional type in the K+ and Na+-permeable HKT transporter subfamily. Furthermore, the high permeability to K+ in OsHKT2;4 supports the hypothesis that this system is dedicated to K+ transport in the plant.

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The Rice Monovalent Cation Transporter OsHKT2;4: Revisited Ionic Selectivity

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“…7 To deal with Fe-or Cu-induced toxicity, plants need to enhance antioxidant defenses; this phenomenon has been reported for a wide range of species such as radicals-activated K + channels are involved in programmed cell death in plant cells. 33 Recently, Lahoavist et al 36 showed that the hydroxyl-radical activated Ca 2+ and K + conductance in Arabidopsis is mediated by annexin1 at the mature and elongation zone levels. In all these studies, the hydroxyl radical generation occurred at the external side of the plasma membrane, and under non-physiological (1mM of the hydroxyl-radical generation mixture Cu/Asc) conditions.…”

Section: Transition Metalsmentioning

confidence: 99%

“…4 The latter may interact with TM in the cell walls in the presence of ascorbic acid, to produce substantial quantities of OH • in apoplast. 5 This apoplastic OH • could activate Ann1-mediated Ca 2+ and K + conductances 6 at both mature and elongation zones 36 resulting in further increase in cytosolic Ca 2+ (hence, a positive feedback loop) and decline in cytosolic K + pool. Apoplastic peroxide produced as a result of nADP(H) oxidase stimulation will be also transported in the cytosol via aquaporins, further increasing cytosolic OH • levels by interacting with TM.…”

Section: Figurementioning

confidence: 99%

“…The activation of plasma membrane calcium influx by ROS in plant cells has been a hot topic during the last decade resulting in multiple publications. [30][31][32][33][34][35][36][37] This activation shows high spatial-and dose-dependence, and varies with the type of ROS. [33][34][35][36][37] Of specific interest is ROS-induced K + efflux.…”

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confidence: 99%

“…[30][31][32][33][34][35][36][37] This activation shows high spatial-and dose-dependence, and varies with the type of ROS. [33][34][35][36][37] Of specific interest is ROS-induced K + efflux. The latter has been reported in most of the abiotic stresses that imply ROS generation, such as copper 37,38,41 or Al toxicity, 39,40 salinity, 33,42 and waterlogging.…”

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Transition metals: A double edge sward in ROS generation and signaling

Rodrigo-Moreno¹,

Poschenrieder²,

Shabala³

2013

Plant Signaling & Behavior

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Recently, reactive oxygen species (ROS) have emerged as important signaling molecules mediating a broad range of plant adaptive and developmental responses. In plant cells, both photosynthetic and respiratory electron-transport chains, as well as the NADPH oxidases and peroxidases are involved in ROS generation. 1 ROS have been shown to regulate gene expression and signaling transduction pathways and, as such, can control numerous processes, like root gravitropism, hypersensitive response to pathogens, stomatal closure and cell expansion and development. 1-5 During pathogen attack, programmed cell death (PCD) is induced in order to isolate cells and therefore avoiding pathogen spread. ROS play a crucial role in this signaling network. 6 In many cases, ROS production is genetically programmed and is induced during development. Generation of singlet oxygen induces controlled PCD in aleurone cells, leaf senescence, tracheary elements maturation or trichome development. 4 While ROS control over numerous adaptive and developmental responses is absolutely essential, a controlled balance of ROSproducing and ROS-scavenging systems must be kept to ensure an accurate execution of signaling without provoking toxicity. Several types of ROS may be formed in plant cells. These forms can be poorly reactive (non-radicals, such as H 2 O 2 or O 3 ) or can Transition metals such as iron (Fe) and Copper (Cu) are essential for plant cell development. At the same time, due their capability to generate hydroxyl radicals they can be potentially toxic to plant metabolism. Recent works on hydroxyl-radical activation of ion transporters suggest that hydroxyl radicals generated by transition metals could play an important role in plant growth and adaptation to imbalanced environments. in this mini-review, the relation between transition metals uptake and utilization and oxidative stress-activated ion transport in plant cells is analyzed, and a new model depicting both apoplastic and cytosolic mode of ROS signaling to plasma membrane transporters is suggested.

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Tip Growth

Gilroy

Swanson

2017

Encyclopedia of Life Sciences

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Pollen tubes and root hairs grow by a highly focused deposition of new wall and membrane materials at their growing apex. Comparison of the machinery that localises such growth between these cell types has revealed common components, providing important insight into how plant cells control cell expansion. Such elements include the small GTPases (e.g. ROPs and RABs), gradients and intricate spatial patterning in the fluxes of ions (e.g. Ca 2+ and H + ) and partitioning of membrane lipids (such as the phosphoinositides). These regulators are coupled to focused action of the secretory machinery (e.g. the exocyst) and cytoskeletal dynamics, with integral roles emerging for actin, tubulin and their associated motor proteins. These components form an integrated regulatory network that imposes robust spatial localisation of the growth machinery and so supports the production of an elongating tube‐like growth form where cell expansion is limited to the very apex, that is, tip growth. Key Concepts Tip growth represents the focused expansion of plant cells, such as root hairs and pollen tubes, localised to the apex of an elongating, tube‐like growth form. Expansion is limited to where the tip cell wall yields to internal turgor pressure. Maintained growth requires the focused delivery of cell wall and membrane materials to the growing apex, while strengthening the sides of the tube to resist further expansion. A network of cellular regulators combine to focus the activity of the growth machinery to the growing tip. Localised action of components such as small GTPases, gradients of ions, the cytoskeleton and maintenance of specialised regions of membrane composition interact to provide the spatial information that limits the activity of the secretory machinery to the very tip of the cell.

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Arabidopsis Annexin1 Mediates the Radical-Activated Plasma Membrane Ca²⁺- and K⁺-Permeable Conductance in Root Cells

Cited by 170 publications

References 53 publications

The Rice Monovalent Cation Transporter OsHKT2;4: Revisited Ionic Selectivity

The Rice Monovalent Cation Transporter OsHKT2;4: Revisited Ionic Selectivity

Transition metals: A double edge sward in ROS generation and signaling

Tip Growth

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