Dataset Information

Arabidopsis KASH Proteins SINE1 and SINE2 Are Involved in Microtubule Reorganization During ABA-Induced Stomatal Closure.

ABSTRACT: Abscisic acid (ABA) induces stomatal closure by utilizing complex signaling mechanisms, allowing for sessile plants to respond rapidly to ever-changing environmental conditions. ABA regulates the activity of plasma membrane ion channels and calcium-dependent protein kinases, Ca²⁺ oscillations, and reactive oxygen species (ROS) concentrations. Throughout ABA-induced stomatal closure, the cytoskeleton undergoes dramatic changes that appear important for efficient closure. However, the precise role of this cytoskeletal reorganization in stomatal closure and the nature of its regulation are unknown. We have recently shown that the plant KASH proteins SINE1 and SINE2 are connected to actin organization during ABA-induced stomatal closure but their role in microtubule (MT) organization remains to be investigated. We show here that depolymerizing MTs using oryzalin can restore ABA-induced stomatal closure deficits in sine1-1 and sine2-1 mutants. GFP-MAP4-visualized MT organization is compromised in sine1-1 and sine2-1 mutants during ABA-induced stomatal closure. Loss of SINE1 or SINE2 results in loss of radially organized MT patterning in open guard cells, aberrant MT organization during stomatal closure, and an overall decrease in the number of MT filaments or bundles. Thus, SINE1 and SINE2 are necessary for establishing MT patterning and mediating changes in MT rearrangement, which is required for ABA-induced stomatal closure.

SUBMITTER: Biel A

PROVIDER: S-EPMC7722481 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Publications

Arabidopsis KASH Proteins SINE1 and SINE2 Are Involved in Microtubule Reorganization During ABA-Induced Stomatal Closure.

Biel Alecia A Moser Morgan M Meier Iris I

Frontiers in plant science 20201120

Abscisic acid (ABA) induces stomatal closure by utilizing complex signaling mechanisms, allowing for sessile plants to respond rapidly to ever-changing environmental conditions. ABA regulates the activity of plasma membrane ion channels and calcium-dependent protein kinases, Ca<sup>2+</sup> oscillations, and reactive oxygen species (ROS) concentrations. Throughout ABA-induced stomatal closure, the cytoskeleton undergoes dramatic changes that appear important for efficient closure. However, the p ...[more]

PMID: 33324432

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Project description:Stomata, microscopic pores in leaf surfaces through which water loss and carbon dioxide uptake occur, are closed in response to drought by the phytohormone abscisic acid (ABA). This process is vital for drought tolerance and has been the topic of extensive experimental investigation in the last decades. Although a core signaling chain has been elucidated consisting of ABA binding to receptors, which alleviates negative regulation by protein phosphatases 2C (PP2Cs) of the protein kinase OPEN STOMATA 1 (OST1) and ultimately results in activation of anion channels, osmotic water loss, and stomatal closure, over 70 additional components have been identified, yet their relationships with each other and the core components are poorly elucidated. We integrated and processed hundreds of disparate observations regarding ABA signal transduction responses underlying stomatal closure into a network of 84 nodes and 156 edges and, as a result, established those relationships, including identification of a 36-node, strongly connected (feedback-rich) component as well as its in- and out-components. The network's domination by a feedback-rich component may reflect a general feature of rapid signaling events. We developed a discrete dynamic model of this network and elucidated the effects of ABA plus knockout or constitutive activity of 79 nodes on both the outcome of the system (closure) and the status of all internal nodes. The model, with more than 1024 system states, is far from fully determined by the available data, yet model results agree with existing experiments in 82 cases and disagree in only 17 cases, a validation rate of 75%. Our results reveal nodes that could be engineered to impact stomatal closure in a controlled fashion and also provide over 140 novel predictions for which experimental data are currently lacking. Noting the paucity of wet-bench data regarding combinatorial effects of ABA and internal node activation, we experimentally confirmed several predictions of the model with regard to reactive oxygen species, cytosolic Ca2+ (Ca2+c), and heterotrimeric G-protein signaling. We analyzed dynamics-determining positive and negative feedback loops, thereby elucidating the attractor (dynamic behavior) repertoire of the system and the groups of nodes that determine each attractor. Based on this analysis, we predict the likely presence of a previously unrecognized feedback mechanism dependent on Ca2+c. This mechanism would provide model agreement with 10 additional experimental observations, for a validation rate of 85%. Our research underscores the importance of feedback regulation in generating robust and adaptable biological responses. The high validation rate of our model illustrates the advantages of discrete dynamic modeling for complex, nonlinear systems common in biology.

Dataset Information

Arabidopsis KASH Proteins SINE1 and SINE2 Are Involved in Microtubule Reorganization During ABA-Induced Stomatal Closure.

Publications

Arabidopsis KASH Proteins SINE1 and SINE2 Are Involved in Microtubule Reorganization During ABA-Induced Stomatal Closure.

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