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      Dynamic calcium signals mediate the feeding response of the carnivorous sundew plant

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          Abstract

          Some of the most spectacular examples of botanical carnivory—in which predator plants catch and digest animals presumably to supplement the nutrient-poor soils in which they grow—occur within the Droseraceae family. For example, sundews of the genus Drosera have evolved leaf movements and enzyme secretion to facilitate prey digestion. The molecular underpinnings of this behavior remain largely unknown; however, evidence suggests that prey-induced electrical impulses are correlated with movement and production of the defense hormone jasmonic acid (JA), which may alter gene expression. In noncarnivorous plants, JA is linked to electrical activity via changes in cytoplasmic Ca 2+. Here, we find that dynamic Ca 2+ changes also occur in sundew ( Drosera spatulata) leaves responding to prey-associated mechanical and chemical stimuli. Furthermore, inhibition of these Ca 2+ changes reduced expression of JA target genes and leaf movements following chemical feeding. Our results are consistent with the presence of a conserved Ca 2+-dependent JA signaling pathway in the sundew feeding response and provide further credence to the defensive origin of plant carnivory.

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          Most cited references17

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          How the Venus flytrap snaps.

          The rapid closure of the Venus flytrap (Dionaea muscipula) leaf in about 100 ms is one of the fastest movements in the plant kingdom. This led Darwin to describe the plant as "one of the most wonderful in the world". The trap closure is initiated by the mechanical stimulation of trigger hairs. Previous studies have focused on the biochemical response of the trigger hairs to stimuli and quantified the propagation of action potentials in the leaves. Here we complement these studies by considering the post-stimulation mechanical aspects of Venus flytrap closure. Using high-speed video imaging, non-invasive microscopy techniques and a simple theoretical model, we show that the fast closure of the trap results from a snap-buckling instability, the onset of which is controlled actively by the plant. Our study identifies an ingenious solution to scaling up movements in non-muscular engines and provides a general framework for understanding nastic motion in plants.
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            Glutamate triggers long-distance, calcium-based plant defense signaling

            Animals require rapid, long-range molecular signaling networks to integrate sensing and response throughout their bodies. The amino acid glutamate acts as an excitatory neurotransmitter in the vertebrate central nervous system, facilitating long-range information exchange via activation of glutamate receptor channels. Similarly, plants sense local signals, such as herbivore attack, and transmit this information throughout the plant body to rapidly activate defense responses in undamaged parts. Here we show that glutamate is a wound signal in plants. Ion channels of the GLUTAMATE RECEPTOR–LIKE family act as sensors that convert this signal into an increase in intracellular calcium ion concentration that propagates to distant organs, where defense responses are then induced.
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              Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators

              Genetically encoded calcium indicators (GECIs) can be used to image activity in defined neuronal populations. However, current GECIs produce inferior signals compared to synthetic indicators and recording electrodes, precluding detection of low firing rates. We developed a single-wavelength GECI based on GCaMP2 (GCaMP3), with increased baseline fluorescence (3x), dynamic range (3x), and higher affinity for calcium (1.3x). GCaMP3 fluorescence changes triggered by single action potentials were detected in pyramidal cell dendrites, with signal-to-noise ratio and photostability significantly better than GCaMP2, D3cpVenus, and TN-XXL. In Caenorhabditis elegans chemosensory neurons and the Drosophila melanogaster antennal lobe, sensory stimulation-evoked fluorescence responses were significantly enhanced with the new indicator (4–6x). In somatosensory and motor cortical neurons in the intact mouse, GCaMP3 detected calcium transients with amplitudes linearly dependent on action potential number. Long-term imaging in the motor cortex of behaving mice revealed large fluorescence changes in imaged neurons over months.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                12 July 2022
                26 July 2022
                12 July 2022
                : 119
                : 30
                : e2206433119
                Affiliations
                [1] aPlant Biology Laboratory, Salk Institute for Biological Studies , La Jolla, CA 92037;
                [2] bDepartment of Biology, Washington University in St. Louis , St. Louis, MO 63130;
                [3] cNSF Center for Engineering MechanoBiology , St. Louis, MO 63105;
                [4] dHHMI, Salk Institute for Biological Studies , La Jolla, CA 92037
                Author notes
                2To whom correspondence may be addressed. Email: procko@ 123456salk.edu .

                Edited by Natasha Raikhel, Center for Plant Cell Biology, Riverside, CA; received April 12, 2022; accepted May 24, 2022

                Author contributions: C.P., I.R., E.S.H., and J.C. designed research; C.P., I.R., C.H., and R.A.R. performed research; C.P. and I.R. analyzed data; and C.P. and I.R. wrote the paper.

                1C.P. and I.R. contributed equally to this work.

                Author information
                https://orcid.org/0000-0002-4374-4283
                https://orcid.org/0000-0001-5711-2861
                https://orcid.org/0000-0002-7877-6947
                https://orcid.org/0000-0002-4246-065X
                Article
                202206433
                10.1073/pnas.2206433119
                9335315
                35858457
                8ad2a990-c555-4535-8339-1c1d7df5755e
                Copyright © 2022 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

                History
                : 24 May 2022
                Page count
                Pages: 3
                Funding
                Funded by: HHS | National Institutes of Health (NIH) 100000002
                Award ID: 5R35GM122604
                Award Recipient : Joanne Chory
                Funded by: Howard Hughes Medical Institute (HHMI) 100000011
                Award ID: 55108530
                Award Recipient : Elizabeth S Haswell
                Categories
                428
                524
                Biological Sciences
                Plant Biology
                Brief Report

                carnivorous plants,calcium signaling,mechanosensation,sundew

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