Plant Trans-Golgi Network/Early Endosome pH regulation requires Cation Chloride Cotransporter (CCC1)

McKay, Daniel; McFarlane, Heather E.; Qu, Yanghua; Situmorang, Apriadi; Gilliham, Matthew; Wege, Stefanie

doi:10.7554/elife.70701

Cited by 11 publications

(10 citation statements)

References 69 publications

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“…Expanded signaling and transport, possibly related to filamentous growth, include calcium signaling (OG 56), zinc-induced facilitators (OG 258), cysteine-rich fibroblast growth factor receptors found in the Golgi apparatus (OG 518), and cation/H+ antiporters (OG 809). Cation/H+ antiporters are closely related to A. thaliana nhx5/nhx6 that act on pH and ion homeostasis in the endosome and are key for membrane trafficking in the trans-Golgi network (Bassil et al, 2011; McKay et al, 2022), and diverse developmental processes (Dragwidge et al, 2018). A dynein homolog (OG 72) was significantly contracted in Zygnematophyceae ( Table S3B ), which might be associated with cytokinesis of cilia and flagella and thus in line with the loss of motile gametes in Zygnematophyceae and Embryophyta (OG 72 was also identified as contracted in that ancestor).…”

Section: Resultsmentioning

confidence: 99%

Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Feng

Zheng

Irisarri

et al. 2023

Preprint

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The filamentous and unicellular algae of the class Zygnematophyceae are the closest algal relatives of land plants. Inferring the properties of the last common ancestor shared by these algae and land plants allows us to identify decisive traits that enabled the conquest of land by plants. We sequenced four genomes of filamentous Zygnematophyceae (three strains of Zygnema circumcarinatum and one strain of Z. cylindricum) and generated chromosome-scale assemblies for all strains of the emerging model system Z. circumcarinatum. Comparative genomic analyses reveal expanded genes for signaling cascades, environmental response, and intracellular trafficking that we associate with multicellularity. Gene family analyses suggest that Zygnematophyceae share all the major enzymes with land plants for cell wall polysaccharide synthesis, degradation, and modifications; most of the enzymes for cell wall innovations, especially for polysaccharide backbone synthesis, were gained more than 700 million years ago. In Zygnematophyceae, these enzyme families expanded, forming co-expressed modules. Transcriptomic profiling of over 19 growth conditions combined with co-expression network analyses uncover cohorts of genes that unite environmental signaling with multicellular developmental programs. Our data shed light on a molecular chassis that balances environmental response and growth modulation across more than 600 million years of streptophyte evolution.

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Section: Resultsmentioning

confidence: 99%

Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Feng

Zheng

Irisarri

et al. 2023

Preprint

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“…Nevertheless, the respective importance of their combined functions (PPi hydrolysis coupled to proton pumping) still awaits demonstration of their impact on biological functions. As deletion of these transporters has no overall impact on PPi homeostasis, it will be important to characterize the impact of vhp2 mutations on Golgi pH maintenance, likely in combination with mutations of other known membrane-bound pH regulators present in the endomembrane network (McKay et al, 2022). Overall, a careful analysis of these mutants, particularly under stress conditions where PPi could be limiting, and where pH maintenance within the Golgi might be affected, is necessary to understand under which conditions the dual activity of these proteins (pyrophosphatase/proton pump) could become limiting.…”

Section: Discussionmentioning

confidence: 99%

Roles of type II H+-PPases and PPsPase1/PECP2 in early developmental stages and PPi homeostasis of Arabidopsis thaliana

et al. 2023

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The regulation of intracellular pyrophosphate (PPi) level is crucial for proper morphogenesis across all taxonomic kingdoms. PPi is released as a byproduct from ~200 metabolic reactions, then hydrolyzed by either membrane-bound (H+-PPase) or soluble pyrophosphatases (PPases). In Arabidopsis, the loss of the vacuolar H+-PPase/FUGU5, a key enzyme in PPi homeostasis, results in delayed growth and a number of developmental defects, pointing to the importance of PPi homeostasis in plant morphogenesis. The Arabidopsis genome encodes several PPases in addition to FUGU5, such as PPsPase1/PECP2, VHP2;1 and VHP2;2, although their significance regarding PPi homeostasis remains elusive. Here, to assess their contribution, phenotypic analyses of cotyledon aspect ratio, palisade tissue cellular phenotypes, adaxial side pavement cell complexity, stomatal distribution, and etiolated seedling length were performed, provided that they were altered due to excess PPi in a fugu5 mutant background. Overall, our analyses revealed that the above five traits were unaffected in ppspase1/pecp2, vhp2;1 and vhp2;2 loss-of-function mutants, as well as in fugu5 mutant lines constitutively overexpressing PPsPase1/PECP2. Furthermore, metabolomics revealed that ppspase1/pecp2, vhp2;1 and vhp2;2 etiolated seedlings exhibited metabolic profiles comparable to the wild type. Together, these results indicate that the contribution of PPsPase1/PECP2, VHP2;1 and VHP2;2 to PPi levels is negligible in comparison to FUGU5 in the early stages of seedling development.

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“…pH regulation in a cell is dependent on the proton pump and antiporter activities, but other mechanisms are also needed. Recent findings suggest that CCC1, a cation-chloride cotransporter in Arabidopsis , is necessary for the regulation of pH in the Golgi-network early endosome [ 299 ]. If this regulation does not function, the plant cannot develop normally, it will obtain reduced size, chlorophyll defects, and stem necrosis and cannot respond to abiotic stress [ 42 ].…”

Section: Ph Changes and Signaling Under Salinitymentioning

confidence: 99%

Ion Changes and Signaling under Salt Stress in Wheat and Other Important Crops

Lindberg,

Premkumar

2023

Plants

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High concentrations of sodium (Na+), chloride (Cl−), calcium (Ca2+), and sulphate (SO42−) are frequently found in saline soils. Crop plants cannot successfully develop and produce because salt stress impairs the uptake of Ca2+, potassium (K+), and water into plant cells. Different intracellular and extracellular ionic concentrations change with salinity, including those of Ca2+, K+, and protons. These cations serve as stress signaling molecules in addition to being essential for ionic homeostasis and nutrition. Maintaining an appropriate K+:Na+ ratio is one crucial plant mechanism for salt tolerance, which is a complicated trait. Another important mechanism is the ability for fast extrusion of Na+ from the cytosol. Ca2+ is established as a ubiquitous secondary messenger, which transmits various stress signals into metabolic alterations that cause adaptive responses. When plants are under stress, the cytosolic-free Ca2+ concentration can rise to 10 times or more from its resting level of 50–100 nanomolar. Reactive oxygen species (ROS) are linked to the Ca2+ alterations and are produced by stress. Depending on the type, frequency, and intensity of the stress, the cytosolic Ca2+ signals oscillate, are transient, or persist for a longer period and exhibit specific “signatures”. Both the influx and efflux of Ca2+ affect the length and amplitude of the signal. According to several reports, under stress Ca2+ alterations can occur not only in the cytoplasm of the cell but also in the cell walls, nucleus, and other cell organelles and the Ca2+ waves propagate through the whole plant. Here, we will focus on how wheat and other important crops absorb Na+, K+, and Cl− when plants are under salt stress, as well as how Ca2+, K+, and pH cause intracellular signaling and homeostasis. Similar mechanisms in the model plant Arabidopsis will also be considered. Knowledge of these processes is important for understanding how plants react to salinity stress and for the development of tolerant crops.

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Plant Trans-Golgi Network/Early Endosome pH regulation requires Cation Chloride Cotransporter (CCC1)

Cited by 11 publications

References 69 publications

Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Chromosome-level genomes of multicellular algal sisters to land plants illuminate signaling network evolution

Roles of type II H+-PPases and PPsPase1/PECP2 in early developmental stages and PPi homeostasis of Arabidopsis thaliana

Ion Changes and Signaling under Salt Stress in Wheat and Other Important Crops

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