Publications by authors named "Hillel Fromm"

41 Publications

GABA signaling in plants: targeting the missing pieces of the puzzle.

Authors:
Hillel Fromm

J Exp Bot 2020 10;71(20):6238-6245

School of Plant Sciences and Food Security, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.

The adaptation of plants to unstable environments relies on their ability to sense their surroundings and to generate and transmit corresponding signals to different parts of the plant to evoke changes necessary for optimizing growth and defense. Plants, like animals, contain a huge repertoire of intra- and intercellular signals, including organic and inorganic molecules. The occurrence of neurotransmitter-like signaling molecules in plants has been an intriguing field of research. Among these, γ-aminobutyric acid (GABA) was discovered in plants over half a century ago, and studies of its roles as a primary metabolite have been well documented, particularly in the context of stress responses. In contrast, evidence of the potential mechanism by which GABA acts as a signaling molecule in plants has only recently been reported. In spite of this breakthrough, the roles of GABA as a signaling molecule in plants have yet to be established and several aspects of the complexity of the GABA signaling system remain obscure. This review summarizes the uncertainties in GABA signaling in plants and suggests research directions and technologies that would help in answering unsolved questions.
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http://dx.doi.org/10.1093/jxb/eraa358DOI Listing
October 2020

A Ca/CaM-regulated transcriptional switch modulates stomatal development in response to water deficit.

Sci Rep 2019 08 22;9(1):12282. Epub 2019 Aug 22.

Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, 47907, USA.

Calcium (Ca) signals are decoded by the Ca-sensor protein calmodulin (CaM) and are transduced to Ca/CaM-binding transcription factors to directly regulate gene expression necessary for acclimation responses in plants. The molecular mechanisms of Ca/CaM signal transduction processes and their functional significance remains enigmatic. Here we report a novel Ca/CaM signal transduction mechanism that allosterically regulates DNA-binding activity of GT2-LIKE 1 (GTL1), a transrepressor of STOMATAL DENSITY AND DISTRIBUTION 1 (SDD1), to repress stomatal development in response to water stress. We demonstrated that Ca/CaM interaction with the 2 helix of the GTL1 N-terminal trihelix DNA-binding domain (GTL1N) destabilizes a hydrophobic core of GTL1N and allosterically inhibits 3 helix docking to the SDD1 promoter, leading to osmotic stress-induced Ca/CaM-dependent activation (de-repression) of SDD1 expression. This resulted in GTL1-dependent repression of stomatal development in response to water-deficit stress. Together, our results demonstrate that a Ca/CaM-regulated transcriptional switch on a trihelix transrepressor directly transduces osmotic stress to repress stomatal development to improve plant water-use efficiency as an acclimation response.
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http://dx.doi.org/10.1038/s41598-019-47529-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6706580PMC
August 2019

Root Plasticity in the Pursuit of Water.

Authors:
Hillel Fromm

Plants (Basel) 2019 Jul 22;8(7). Epub 2019 Jul 22.

School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

One of the greatest challenges of terrestrial vegetation is to acquire water through soil-grown roots. Owing to the scarcity of high-quality water in the soil and the environment's spatial heterogeneity and temporal variability, ranging from extreme flooding to drought, roots have evolutionarily acquired tremendous plasticity regarding their geometric arrangement of individual roots and their three-dimensional organization within the soil. Water deficiency has also become an increasing threat to agriculture and dryland ecosystems due to climate change. As a result, roots have become important targets for genetic selection and modification in an effort to improve crop resilience under water-limiting conditions. This review addresses root plasticity from different angles: Their structures and geometry in response to the environment, potential genetic control of root traits suitable for water-limiting conditions, and contemporary and future studies of the principles underlying root plasticity post-Darwin's 'root-brain' hypothesis. Our increasing knowledge of different disciplines of plant sciences and agriculture should contribute to a sustainable management of natural and agricultural ecosystems for the future of mankind.
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http://dx.doi.org/10.3390/plants8070236DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6681320PMC
July 2019

CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 6: A Key Regulator of Na Homeostasis during Germination.

Plant Physiol 2019 06 20;180(2):1101-1118. Epub 2019 Mar 20.

School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

Salinity impairs seed germination and seedling establishment. We investigated the role of Arabidopsis () CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 6 (CAMTA6) in salinity stress responses during early germination. Compared with the wild type, the and mutants were more tolerant to NaCl and abscisic acid (ABA) and accumulated less Na In contrast, 4- to 11-d-old seedlings were more sensitive to NaCl. In , expression of (), encoding an Na/K transporter, was restricted to the radicles and was not enhanced by NaCl or ABA. During germination, the double mutant was as sensitive as the wild type and to NaCl, suggesting that HKT1;1 is crucial for the salt tolerance of An ABA response element in the promoter was found to be indispensable for the enhanced expression of the gene in response to NaCl and to ABA. Transcriptome analysis of the wild type and with and without salt treatment revealed 1,020 up-regulated and 1,467 down-regulated salt-responsive genes in the wild type. Among these, 638 up-regulated and 1,242 down-regulated genes were classified as CAMTA6-dependent. Expression of several known salt stress-associated genes, including and , was impaired in mutants. Bioinformatics analysis of the 5' upstream sequences of the salt-responsive CAMTA6-dependent up-regulated genes revealed the CACGTGTC motif as the most prominent element, representing an ABA response element and a potential CAMTA-binding site. We suggest that CAMTA6 regulates, directly or indirectly, the expression of most of the salt-responsive genes in germinating seeds, including genes that are crucial for Na homeostasis and salt stress tolerance.
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http://dx.doi.org/10.1104/pp.19.00119DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6548231PMC
June 2019

A transportome-scale amiRNA-based screen identifies redundant roles of Arabidopsis ABCB6 and ABCB20 in auxin transport.

Nat Commun 2018 10 11;9(1):4204. Epub 2018 Oct 11.

School of Plant Sciences and Food Security, Tel Aviv University, Tel Aviv, 69978, Israel.

Transport of signaling molecules is of major importance for regulating plant growth, development, and responses to the environment. A prime example is the spatial-distribution of auxin, which is regulated via transporters to govern developmental patterning. A critical limitation in our ability to identify transporters by forward genetic screens is their potential functional redundancy. Here, we overcome part of this functional redundancy via a transportome, multi-targeted forward-genetic screen using artificial-microRNAs (amiRNAs). We generate a library of 3000 plant lines expressing 1777 amiRNAs, designed to target closely homologous genes within subclades of transporter families and identify, genotype and quantitatively phenotype, 80 lines showing reproducible shoot growth phenotypes. Within this population, we discover and characterize a strong redundant role for the unstudied ABCB6 and ABCB20 genes in auxin transport and response. The unique multi-targeted lines generated in this study could serve as a genetic resource that is expected to reveal additional transporters.
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http://dx.doi.org/10.1038/s41467-018-06410-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6182007PMC
October 2018

MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted Ca signal essential for root water tracking in .

Proc Natl Acad Sci U S A 2018 07 16;115(31):8031-8036. Epub 2018 Jul 16.

School of Plant Sciences and Food Security, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel;

Ever since Darwin postulated that the tip of the root is sensitive to moisture differences and that it "transmits an influence to the upper adjoining part, which bends towards the source of moisture" [Darwin C, Darwin F (1880) , pp 572-574], the signal underlying this tropic response has remained elusive. Using the FRET-based Cameleon Ca sensor , we show that a water potential gradient applied across the root tip generates a slow, long-distance asymmetric cytosolic Ca signal in the phloem, which peaks at the elongation zone, where it is dispersed laterally and asymmetrically to peripheral cells, where cell elongation occurs. In addition, the MIZ1 protein, whose biochemical function is unknown but is required for root curvature toward water, is indispensable for generating the slow, long-distance Ca signal. Furthermore, biochemical and genetic manipulations that elevate cytosolic Ca levels, including mutants of the endoplasmic reticulum (ER) Ca-ATPase isoform ECA1, enhance root curvature toward water. Finally, coimmunoprecipitation of plant proteins and functional complementation assays in yeast cells revealed that MIZ1 directly binds to ECA1 and inhibits its activity. We suggest that the inhibition of ECA1 by MIZ1 changes the balance between cytosolic Ca influx and efflux and generates the cytosolic Ca signal required for water tracking.
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http://dx.doi.org/10.1073/pnas.1804130115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6077737PMC
July 2018

SELENOPROTEIN O is a chloroplast protein involved in ROS scavenging and its absence increases dehydration tolerance in Arabidopsis thaliana.

Plant Sci 2018 May 3;270:278-291. Epub 2018 Mar 3.

School of Plant Sciences and Food Security, Tel Aviv University, P.O. Box 39040, Tel Aviv 6997801, Israel. Electronic address:

The evolutionary conserved family of Selenoproteins performs redox-regulatory functions in bacteria, archaea and eukaryotes. Among them, members of the SELENOPROTEIN O (SELO) subfamily are located in mammalian and yeast mitochondria, but their functions are thus far enigmatic. Screening of T-DNA knockout mutants for resistance to the proline analogue thioproline (T4C), identified mutant alleles of the plant SELO homologue in Arabidopsis thaliana. Absence of SELO resulted in a stress-induced transcriptional activation instead of silencing of mitochondrial proline dehydrogenase, and also high elevation of Δ(1)-pyrroline-5-carboxylate dehydrogenase involved in degradation of proline, thereby alleviating T4C inhibition and lessening drought-induced proline accumulation. Unlike its animal homologues, SELO was localized to chloroplasts of plants ectopically expressing SELO-GFP. The protein was co-fractionated with thylakoid membrane complexes, and co-immunoprecipitated with FNR, PGRL1 and STN7, all involved in regulating PSI and downstream electron flow. The selo mutants displayed extended survival under dehydration, accompanied by longer photosynthetic activity, compared with wild-type plants. Enhanced expression of genes encoding ROS scavenging enzymes in the unstressed selo mutant correlated with higher oxidant scavenging capacity and reduced methyl viologen damage. The study elucidates SELO as a PSI-related component involved in regulating ROS levels and stress responses.
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http://dx.doi.org/10.1016/j.plantsci.2018.02.023DOI Listing
May 2018

The Cholodny-Went theory does not explain hydrotropism.

Plant Sci 2016 Nov 12;252:400-403. Epub 2016 Sep 12.

Department of Molecular Biology & Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978 Israel. Electronic address:

Optimization of water foraging by plants is partially achieved by the ability of roots to direct growth towards high water potential, a phenomenon termed hydrotropism. In contrast to gravitropism and phototropism, which require auxin redistribution, as suggested by the Cholodny-Went theory, hydrotropism is not mediated by the phytohormone auxin, which raises questions about the mechanism underlying this tropic response. Here we specify the open questions in this field of research and discuss the possible interactions of abscisic acid, calcium and reactive oxygen species as part of a dynamic system of sensing water potential in the root tip, transmission of the signal to the root elongation zone and promoting root curvature towards water. We conclude that root hydrotropism is mediated by inter-cellular signals that are not explained by the Cholodny-Went theory.
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http://dx.doi.org/10.1016/j.plantsci.2016.09.004DOI Listing
November 2016

Reactive Oxygen Species Tune Root Tropic Responses.

Plant Physiol 2016 10 17;172(2):1209-1220. Epub 2016 Aug 17.

Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel (G.K., D.S., H.F.); andMina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 5290002, Israel (G.M.)

The default growth pattern of primary roots of land plants is directed by gravity. However, roots possess the ability to sense and respond directionally to other chemical and physical stimuli, separately and in combination. Therefore, these root tropic responses must be antagonistic to gravitropism. The role of reactive oxygen species (ROS) in gravitropism of maize and Arabidopsis (Arabidopsis thaliana) roots has been previously described. However, which cellular signals underlie the integration of the different environmental stimuli, which lead to an appropriate root tropic response, is currently unknown. In gravity-responding roots, we observed, by applying the ROS-sensitive fluorescent dye dihydrorhodamine-123 and confocal microscopy, a transient asymmetric ROS distribution, higher at the concave side of the root. The asymmetry, detected at the distal elongation zone, was built in the first 2 h of the gravitropic response and dissipated after another 2 h. In contrast, hydrotropically responding roots show no transient asymmetric distribution of ROS Decreasing ROS levels by applying the antioxidant ascorbate, or the ROS-generation inhibitor diphenylene iodonium attenuated gravitropism while enhancing hydrotropism. Arabidopsis mutants deficient in Ascorbate Peroxidase 1 showed attenuated hydrotropic root bending. Mutants of the root-expressed NADPH oxidase RBOH C, but not rbohD, showed enhanced hydrotropism and less ROS in their roots apices (tested in tissue extracts with Amplex Red). Finally, hydrostimulation prior to gravistimulation attenuated the gravistimulated asymmetric ROS and auxin signals that are required for gravity-directed curvature. We suggest that ROS, presumably HO, function in tuning root tropic responses by promoting gravitropism and negatively regulating hydrotropism.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5047083PMC
http://dx.doi.org/10.1104/pp.16.00660DOI Listing
October 2016

Hydrotropism: Root Bending Does Not Require Auxin Redistribution.

Mol Plant 2016 05 19;9(5):757-759. Epub 2016 Feb 19.

Department of Molecular Biology & Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel. Electronic address:

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http://dx.doi.org/10.1016/j.molp.2016.02.001DOI Listing
May 2016

Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined?

Front Plant Sci 2015 9;6:419. Epub 2015 Jun 9.

Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel Aviv University , Tel Aviv, Israel.

γ-Aminobutyric acid (GABA) is a non-proteinogenic amino acid that is found in uni- and multi-cellular organisms and is involved in many aspects of plant life cycle. GABA metabolism occurs by the action of evolutionary conserved enzymes that constitute the GABA shunt, bypassing two steps of the TCA cycle. The central position of GABA in the interface between plant carbon and nitrogen metabolism is well established. In parallel, there is evidence to support a role for GABA as a signaling molecule in plants. Here we cover some of the recent findings on GABA metabolism and signaling in plants and further suggest that the metabolic and signaling aspects of GABA may actually be inseparable.
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http://dx.doi.org/10.3389/fpls.2015.00419DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4460296PMC
June 2015

Repression and De-repression of Gene Expression in the Plant Immune Response: The Complexity of Modulation by Ca²⁺ and Calmodulin.

Mol Plant 2015 May 26;8(5):671-3. Epub 2015 Jan 26.

Department of Molecular Biology & Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

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http://dx.doi.org/10.1016/j.molp.2015.01.019DOI Listing
May 2015

Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress.

BMC Genomics 2014 Jun 10;15:456. Epub 2014 Jun 10.

Durham Centre for Crop Improvement Technology, School of Biological and Biomedical Sciences, Durham University, South Road, DH1 3LE Durham, UK.

Background: Abiotic stresses which include drought and heat are amongst the main limiting factors for plant growth and crop productivity. In the field, these stress types are rarely presented individually and plants are often subjected to a combination of stress types. Sorghum bicolor is a cereal crop which is grown in arid and semi-arid regions and is particularly well adapted to the hot and dry conditions in which it originates and is now grown as a crop. In order to better understand the mechanisms underlying combined stress tolerance in this important crop, we have used microarrays to investigate the transcriptional response of Sorghum subjected to heat and drought stresses imposed both individually and in combination.

Results: Microarrays consisting of 28585 gene probes identified gene expression changes equating to ~4% and 18% of genes on the chip following drought and heat stresses respectively. In response to combined stress ~20% of probes were differentially expressed. Whilst many of these transcript changes were in common with those changed in response to heat or drought alone, the levels of 2043 specific transcripts (representing 7% of all gene probes) were found to only be changed following the combined stress treatment. Ontological analysis of these 'unique' transcripts identified a potential role for specific transcription factors including MYB78 and ATAF1, chaperones including unique heat shock proteins (HSPs) and metabolic pathways including polyamine biosynthesis in the Sorghum combined stress response.

Conclusions: These results show evidence for both cross-talk and specificity in the Sorghum response to combined heat and drought stress. It is clear that some aspects of the combined stress response are unique compared to those of individual stresses. A functional characterization of the genes and pathways identified here could lead to new targets for the enhancement of plant stress tolerance, which will be particularly important in the face of climate change and the increasing prevalence of these abiotic stress types.
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http://dx.doi.org/10.1186/1471-2164-15-456DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4070570PMC
June 2014

Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic.

Mol Plant 2014 Jun 19;7(6):1065-1068. Epub 2014 Feb 19.

The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev Sede Boqer Campus 84990, Israel. Electronic address:

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http://dx.doi.org/10.1093/mp/ssu017DOI Listing
June 2014

Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling.

Genome Biol 2013 Feb 1;14(2):R11. Epub 2013 Feb 1.

Background: The Amoebozoa constitute one of the primary divisions of eukaryotes, encompassing taxa of both biomedical and evolutionary importance, yet its genomic diversity remains largely unsampled. Here we present an analysis of a whole genome assembly of Acanthamoeba castellanii (Ac) the first representative from a solitary free-living amoebozoan.

Results: Ac encodes 15,455 compact intron-rich genes, a significant number of which are predicted to have arisen through inter-kingdom lateral gene transfer (LGT). A majority of the LGT candidates have undergone a substantial degree of intronization and Ac appears to have incorporated them into established transcriptional programs. Ac manifests a complex signaling and cell communication repertoire, including a complete tyrosine kinase signaling toolkit and a comparable diversity of predicted extracellular receptors to that found in the facultatively multicellular dictyostelids. An important environmental host of a diverse range of bacteria and viruses, Ac utilizes a diverse repertoire of predicted pattern recognition receptors, many with predicted orthologous functions in the innate immune systems of higher organisms.

Conclusions: Our analysis highlights the important role of LGT in the biology of Ac and in the diversification of microbial eukaryotes. The early evolution of a key signaling facility implicated in the evolution of metazoan multicellularity strongly argues for its emergence early in the Unikont lineage. Overall, the availability of an Ac genome should aid in deciphering the biology of the Amoebozoa and facilitate functional genomic studies in this important model organism and environmental host.
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http://dx.doi.org/10.1186/gb-2013-14-2-r11DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4053784PMC
February 2013

Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems.

Plant Cell 2012 Jan 17;24(1):66-79. Epub 2012 Jan 17.

Department of Molecular Biology and Ecology of Plants, Tel Aviv University, Tel Aviv 69978, Israel.

The gibberellins (GAs) are a group of endogenous compounds that promote the growth of most plant organs, including stem internodes. We show that in tobacco (Nicotiana tabacum) the presence of leaves is essential for the accumulation of bioactive GAs and their immediate precursors in the stem and consequently for normal stem elongation, cambial proliferation, and xylem fiber differentiation. These processes do not occur in the absence of maturing leaves but can be restored by application of C(19)-GAs, identifying the presence of leaves as a requirement for GA signaling in stems and revealing the fundamental role of GAs in secondary growth regulation. The use of reporter genes for GA activity and GA-directed DELLA protein degradation in Arabidopsis thaliana confirms the presence of a mobile signal from leaves to the stem that induces GA signaling.
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http://dx.doi.org/10.1105/tpc.111.093096DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3289570PMC
January 2012

A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism.

Plant J 2011 Aug 31;67(3):485-98. Epub 2011 May 31.

Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel.

In plants, γ-aminobutyric acid (GABA) accumulates in the cytosol in response to a variety of stresses. GABA is transported into mitochondria, where it is catabolized into TCA cycle or other intermediates. Although there is circumstantial evidence for mitochondrial GABA transporters in eukaryotes, none have yet been identified. Described here is an Arabidopsis protein similar in sequence and topology to unicellular GABA transporters. The expression of this protein complements a GABA-transport-deficient yeast mutant. Thus the protein was termed AtGABP to indicate GABA-permease activity. In vivo localization of GABP fused to GFP and immunobloting of subcellular fractions demonstrate its mitochondrial localization. Direct [(3) H]GABA uptake measurements into isolated mitochondria revealed impaired uptake into mitochondria of a gabp mutant compared with wild-type (WT) mitochondria, implicating AtGABP as a major mitochondrial GABA carrier. Measurements of CO(2) release, derived from radiolabeled substrates in whole seedlings and in isolated mitochondria, demonstrate impaired GABA-derived input into the TCA cycle, and a compensatory increase in TCA cycle activity in gabp mutants. Finally, growth abnormalities of gabp mutants under limited carbon availability on artificial media, and in soil under low light intensity, combined with their metabolite profiles, suggest an important role for AtGABP in primary carbon metabolism and plant growth. Thus, AtGABP-mediated transport of GABA from the cytosol into mitochondria is important to ensure proper GABA-mediated respiration and carbon metabolism. This function is particularly essential for plant growth under conditions of limited carbon.
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http://dx.doi.org/10.1111/j.1365-313X.2011.04612.xDOI Listing
August 2011

How calmodulin binding transcription activators (CAMTAs) mediate auxin responses.

Plant Signal Behav 2010 Oct 1;5(10):1311-4. Epub 2010 Oct 1.

Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel Aviv University, Israel.

Phenotypic plasticity is an adaptive feature of all organisms, which, in land plants, entails changes in orientation of growth (tropism), patterns of development, organ architecture, timing of developmental processes, and resource allocation. However, little is known about the molecular components that integrate exogenous environmental cues with internal hormonal signaling pathways. This addendum describes a role for calcium-regulated calmodulin-binding transcription 1 (CAMTA1) in auxin signaling and stress responses. We discuss possible mechanisms that may underlie this role of CAMTA1, and speculate on the more general roles of CAMTAs in auxin responses and phenotypic plasticity.
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http://dx.doi.org/10.4161/psb.5.10.13158DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3115376PMC
October 2010

Calcium-regulated transcription in plants.

Mol Plant 2010 Jul 9;3(4):653-69. Epub 2010 May 9.

Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel-Aviv University 69978, Tel-Aviv, Israel.

The past two decades revealed a plethora of Ca2+-responsive proteins and downstream targets in plants, of which several are unique to plants. More recent high-throughput 'omics' approaches and bioinformatics are exposing Ca2+-responsive cis-elements and the corresponding Ca2+-responsive genes. Here, we review the current knowledge on Ca2+-signaling pathways that regulate gene expression in plants, and we link these to mechanisms by which plants respond to biotic and abiotic stresses.
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http://dx.doi.org/10.1093/mp/ssq019DOI Listing
July 2010

Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis.

Planta 2010 Jun 10;232(1):165-78. Epub 2010 Apr 10.

Department of Plant Sciences, Faculty of Life Sciences, Tel Aviv University, Tel Aviv, Israel.

Auxin is a key plant hormone that regulates various aspects of plant development. However, the mechanisms integrating auxin growth effects with stress responses are not fully understood. In this study, we investigated the possible role of calmodulin-binding transcription activator 1 (CAMTA1), an Arabidopsis thaliana calcium/calmodulin-binding transcription activator, in auxin signaling and its responses to different stresses. Plants harboring the AtCAMTA1 promoter fused to the GUS reporter gene revealed cell-specific expression patterns reminiscent of auxin responses. The responsiveness of CAMTA1 to auxin was further assessed by chemical disturbances in polar auxin transport, and by RT-PCR analysis of gene expression of dissected leaf sections from plants exposed to the auxin transport inhibitor NPA. Furthermore, the intensity and cell-specific expression patterns of CAMTA1 changed significantly and differentially on exposure to increasing salt concentrations and heat. Transcriptome analysis of a camta1 T-DNA insertion mutant revealed 63 up-regulated genes, of which 17 are associated with auxin signaling. Finally, analysis of hypocotyl elongation in the presence and absence of auxin revealed that camta1 T-DNA insertion mutants and CAMTA1-repressor lines are hyper-responsive to auxin compared to wild-type seedlings. Thus, CAMTA1 participates in auxin signaling and responds to abiotic stresses.
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http://dx.doi.org/10.1007/s00425-010-1153-6DOI Listing
June 2010

Environmental conditions affect the color, taste, and antioxidant capacity of 11 pomegranate accessions' fruits.

J Agric Food Chem 2009 Oct;57(19):9197-209

Migal Galilee Technology Center, Kiryat Shmona, Israel.

The well-established health beneficial value of pomegranate juice is leading to increased demand for pomegranate products and to the expansion of pomegranate orchards worldwide. The current study describes differences in the chemical composition of major ingredients of the arils and peels of 11 accessions grown in Mediterranean and desert climates in Israel. In most of the accessions, the levels of antioxidant activity and content of total phenolics, total anthocyanins, total soluble solids, glucose, fructose, and acidity were higher in the aril juice of fruit grown in the Mediterranean climate compared to those grown in the desert climate. However, the peels of fruit grown in the desert climate exhibited higher antioxidant activity, and the levels of total phenolics, including the two hydrolyzable tannins, punicalagin and punicalin, were higher compared to those in the peels of fruit grown in the Mediterranean climate. The results indicate that environmental conditions significantly affect pomegranate fruit quality and health beneficial compounds.
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http://dx.doi.org/10.1021/jf901466cDOI Listing
October 2009

Mutants of GABA transaminase (POP2) suppress the severe phenotype of succinic semialdehyde dehydrogenase (ssadh) mutants in Arabidopsis.

PLoS One 2008 10;3(10):e3383. Epub 2008 Oct 10.

Botanical Institute, University of Cologne, Cologne, Germany.

Background: The gamma-aminubutyrate (GABA) shunt bypasses two steps of the tricarboxylic acid cycle, and is present in both prokaryotes and eukaryotes. In plants, the pathway is composed of the calcium/calmodulin-regulated cytosolic enzyme glutamate decarboxylase (GAD), the mitochondrial enzymes GABA transaminase (GABA-T; POP2) and succinic semialdehyde dehydrogenase (SSADH). We have previously shown that compromising the function of the GABA-shunt, by disrupting the SSADH gene of Arabidopsis, causes enhanced accumulation of reactive oxygen intermediates (ROIs) and cell death in response to light and heat stress. However, to date, genetic investigations of the relationships between enzymes of the GABA shunt have not been reported.

Principal Findings: To elucidate the role of succinic semialdehyde (SSA), gamma-hydroxybutyrate (GHB) and GABA in the accumulation of ROIs, we combined two genetic approaches to suppress the severe phenotype of ssadh mutants. Analysis of double pop2 ssadh mutants revealed that pop2 is epistatic to ssadh. Moreover, we isolated EMS-generated mutants suppressing the phenotype of ssadh revealing two new pop2 alleles. By measuring thermoluminescence at high temperature, the peroxide contents of ssadh and pop2 mutants were evaluated, showing that only ssadh plants accumulate peroxides. In addition, pop2 ssadh seedlings are more sensitive to exogenous SSA or GHB relative to wild type, because GHB and/or SSA accumulate in these plants.

Significance: We conclude that the lack of supply of succinate and NADH to the TCA cycle is not responsible for the oxidative stress and growth retardations of ssadh mutants. Rather, we suggest that the accumulation of SSA, GHB, or both, produced downstream of the GABA-T transamination step, is toxic to the plants, resulting in high ROI levels and impaired development.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0003383PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2557145PMC
November 2008

Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis.

FEBS Lett 2008 Mar 25;582(6):943-8. Epub 2008 Feb 25.

Department of Plant Sciences, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

Calmodulin-binding transcription activator (CAMTA) 3 (also called SR1) is a calmodulin-binding transcription factor in Arabidopsis. Two homozygous T-DNA insertion mutants (camta3-1, camta3-2) showed enhanced spontaneous lesions. Transcriptome analysis of both mutants revealed 6 genes with attenuated expression and 99 genes with elevated expression. Of the latter, 32 genes are related to defense against pathogens (e.g. WRKY33, PR1 and chitinase). Propagation of a virulent strain of the bacterial pathogen Pseudomonas syringae and the fungal pathogen Botrytis cinerea were attenuated in both mutants. Moreover, both mutants accumulated high levels of H2O2. We suggest that CAMTA3 regulates the expression of a set of genes involved in biotic defense responses.
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http://dx.doi.org/10.1016/j.febslet.2008.02.037DOI Listing
March 2008

Highway or byway: the metabolic role of the GABA shunt in plants.

Trends Plant Sci 2008 Jan 21;13(1):14-9. Epub 2007 Dec 21.

Department Willmitzer, Max Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 Potsdam-Golm, Germany.

Much of the recent work on the gamma-aminobutyrate (GABA) shunt in plants has concentrated on stress/pest-associated and signalling roles. However, fifty years after the structural elucidation of the pathway, aspects of its regulation and even of its biological significance remain largely obscure. Here, we assess the importance of GABA metabolism in plants, reviewing relevant biological circumstances and taking advantage of high-throughput data accessibility and computational approaches. We discuss the premise that GABA metabolism plays a major role in carbon and nitrogen primary metabolism. We further evaluate technological developments that will likely allow us to address the quantitative importance of this shunt within the biological processes to which it contributes.
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http://dx.doi.org/10.1016/j.tplants.2007.10.005DOI Listing
January 2008

Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.

Plant J 2007 Dec 19;52(5):850-64. Epub 2007 Sep 19.

Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Gent, Belgium.

The Arabidopsis thaliana genome expresses five evolutionarily conserved prohibitin (PHB) genes that are divided into type-I (AtPHB3 and AtPHB4) and type-II (AtPHB1, AtPHB2 and AtPHB6) classes, based on their phylogenetic relationships with yeast PHB1 and PHB2, respectively. Yeast and animal PHBs are reported to have diverse roles in the cell cycle, mitochondrial electron transport, aging and apoptosis. All transcribed Arabidopsis PHB genes are primarily expressed in both shoot and root proliferative tissues, where they are present in mitochondrial multimeric complexes. Loss of function of the type-I AtPHB4 had no phenotypic effects, while loss of function of the homologous AtPHB3 caused mitochondrial swelling, decreased meristematic cell production, increased cell division time and reduced cell expansion rates, leading to severe growth retardation. Double knockout atphb3 atphb4 plants were not viable, but transgenic lines overexpressing AtPHB3 or AtPHB4 showed leaf shape aberrations and an increased shoot branching phenotype. Genome-wide microarray analysis revealed that both knockout and overexpression perturbations of AtPHB3 and AtPHB4 provoked an altered abundance of mitochondrial and stress-related transcripts. We propose that plant type-I PHBs take part in protein complexes that are necessary for proficient mitochondrial function or biogenesis, thereby supporting cell division and differentiation in apical tissues.
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http://dx.doi.org/10.1111/j.1365-313X.2007.03276.xDOI Listing
December 2007

CAMTAs: calmodulin-binding transcription activators from plants to human.

FEBS Lett 2007 Aug 1;581(21):3893-8. Epub 2007 Aug 1.

Department of Plant Sciences, Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel.

Recently, a novel family of calmodulin-binding transcription activators (CAMTAs) was reported in various eukaryotes. All CAMTAs share a similar domain organization, with a novel type of sequence-specific DNA-binding domain (designated CG-1). This domain could bind DNA directly and activate transcription, or interact with other transcription factors, not through DNA binding, thus acting as a co-activator of transcription. Investigations of CAMTAs in various organisms imply a broad range of functions from sensory mechanisms to embryo development and growth control, highlighted by the apparent involvement of mammalian CAMTA2 in cardiac growth, and of CAMTA1 in tumor suppression and memory performance.
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http://dx.doi.org/10.1016/j.febslet.2007.07.051DOI Listing
August 2007

Cyclic nucleotide-gated channels in plants.

FEBS Lett 2007 May 16;581(12):2237-46. Epub 2007 Feb 16.

Nirit Seeds Ltd., Moshav Hadar-Ham 42935, Israel.

Until recently the role of cyclic nucleotide monophosphates (cNMPs) in plants had been controversial, with equivocal data about their concentrations, biosynthetic and degrading enzymes, and cellular targets. This review discusses the current knowledge in this field, with focus on the largest class of cNMP targets in plant cells, the cyclic nucleotide-gated channels (CNGCs). Aspects of structure and function are addressed, with reference to studies in heterologous systems and in planta. The picture emerging, albeit still fragmented, is of proteins with diverse functions in the control of ion homeostasis, development, and defense against biotic and abiotic threats.
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http://dx.doi.org/10.1016/j.febslet.2007.02.017DOI Listing
May 2007

Ca-Responsive cis-Elements in Plants.

Plant Signal Behav 2007 Jan;2(1):17-9

Department of Plant Sciences; Faculty of Life Sciences; Tel Aviv University; Tel Aviv, Israel.

External physical and chemical stimuli are transduced via second messengers, following primary interaction with specific membrane or soluble receptors. Ca(2+) is an important second messenger in plants as in other eukaryotes, mediating responses to numerous environmental stimuli and affecting a multitude of cellular processes including gene expression. However, there is yet very little information concerning the cis-elements that mediate Ca(2+)-responsive gene expression. In this article we discuss a recent investigation combining bioinformatics with experimental data, revealing DNA regulatory elements that convey specific cytosolic Ca(2+) transients to the transcription machinery.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2633890PMC
http://dx.doi.org/10.4161/psb.2.1.3611DOI Listing
January 2007

Rapid transcriptome changes induced by cytosolic Ca2+ transients reveal ABRE-related sequences as Ca2+-responsive cis elements in Arabidopsis.

Plant Cell 2006 Oct 15;18(10):2733-48. Epub 2006 Sep 15.

Department of Plant Sciences, Weizman Institute of Science, Rehovot 76100, Israel.

The regulation of gene expression by cellular calcium is crucial for plant defense against biotic and abiotic stresses. However, the number of genes known to respond to specific transient calcium signals is limited, and as yet there is no definition of a calcium-responsive cis element in plants. Here, we generated specific cytosolic calcium transients in intact Arabidopsis thaliana seedlings and linked them to early transcriptome changes, followed by bioinformatic analysis of the responsive genes. A cytosolic calcium transient induced by calmodulin antagonists and blocked by lanthanides was characterized using aequorin-based luminometry and photon imaging. Analysis of transcriptome changes revealed 230 calcium-responsive genes, of which 162 were upregulated and 68 were downregulated. These include known early stress-responsive genes as well as genes of unknown function. Analysis of their upstream regions revealed, exclusively in the upregulated genes, a highly significant occurrence of a consensus sequence (P < 10(-13)) comprising two abscisic acid-specific cis elements: the abscisic acid-responsive element (ABRE; CACGTG[T/C/G]) and its coupling element ([C/A]ACGCG[T/C/G]) [corrected] Finally, we show that a tetramer of the ABRE cis element is sufficient to confer transcriptional activation in response to cytosolic Ca(2+) transients. Thus, at least for some specific Ca(2+) transients and motif combinations, ABREs function as Ca(2+)-responsive cis elements.
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http://dx.doi.org/10.1105/tpc.106.042713DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1626612PMC
October 2006

C-terminal residues of plant glutamate decarboxylase are required for oligomerization of a high-molecular weight complex and for activation by calcium/calmodulin.

Biochim Biophys Acta 2006 May 20;1764(5):872-6. Epub 2006 Mar 20.

Department of Life Sciences, Ben-Gurion University, POB 653, Beer-Sheva 84105, Israel.

Bacterial glutamate decarboxylase (GAD) is a homohexameric enzyme of about 330 kDa. Plant GAD differs from the bacterial enzyme in having a C-terminal extension of 33 amino acids within which resides a calmodulin (CaM)-binding domain. In order to assess the role of the C-terminal extension in the formation of GAD complexes and in activation by Ca2+/CaM, we examined complexes formed with the purified full-length recombinant petunia GAD expressed in E. coli, and with a 9 amino acid C-terminal deletion mutant (GADDeltaC9). Size exclusion chromatography revealed that the full-length GAD formed complexes of about 580 kDa and 300 kDa in the absence of Ca2+/CaM, whereas in the presence of Ca2+/CaM all complexes shifted to approximately 680 kDa. With deletion of 9 amino acids from the C-terminus (KKKKTNRVC(500)), the ability to bind CaM in the presence of Ca2+, and to purify it by CaM-affinity chromatography was retained, but the formation of GAD complexes larger than 340 kDa and enzyme activation by Ca2+/CaM were completely abolished. Hence, responsiveness to Ca2+/CaM is associated with the formation of protein complexes of 680 kDa, and requires some or all of the nine C-terminal amino acid residues. We suggest that evolution of plant GAD from a bacterial ancestral enzyme involved the formation of higher molecular weight complexes required for activation by Ca2+/CaM.
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http://dx.doi.org/10.1016/j.bbapap.2006.02.007DOI Listing
May 2006
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