International Journal of Molecular Sciences

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17 pages, 3822 KiB

Open AccessArticle

The Hydrophobin HYTLO1 Secreted by the Biocontrol Fungus Trichoderma longibrachiatum Triggers a NAADP-Mediated Calcium Signalling Pathway in Lotus japonicus

by Roberto Moscatiello, Simone Sello, Michelina Ruocco, Ani Barbulova, Enrico Cortese, Sebastiano Nigris, Barbara Baldan, Maurizio Chiurazzi, Paola Mariani, Matteo Lorito and Lorella Navazio

Int. J. Mol. Sci. 2018, 19(9), 2596; https://doi.org/10.3390/ijms19092596 - 1 Sep 2018

Cited by 31 | Viewed by 4981

Abstract

Trichoderma filamentous fungi are increasingly used as biocontrol agents and plant biostimulants. Growing evidence indicates that part of the beneficial effects is mediated by the activity of fungal metabolites on the plant host. We have investigated the mechanism of plant perception of HYTLO1, [...] Read more.

Trichoderma filamentous fungi are increasingly used as biocontrol agents and plant biostimulants. Growing evidence indicates that part of the beneficial effects is mediated by the activity of fungal metabolites on the plant host. We have investigated the mechanism of plant perception of HYTLO1, a hydrophobin abundantly secreted by Trichoderma longibrachiatum, which may play an important role in the early stages of the plant-fungus interaction. Aequorin-expressing Lotus japonicus suspension cell cultures responded to HYTLO1 with a rapid cytosolic Ca²⁺ increase that dissipated within 30 min, followed by the activation of the defence-related genes MPK3, WRK33, and CP450. The Ca²⁺-dependence of these gene expression was demonstrated by using the extracellular Ca²⁺ chelator EGTA and Ned-19, a potent inhibitor of the nicotinic acid adenine dinucleotide phosphate (NAADP) receptor in animal cells, which effectively blocked the HYTLO1-induced Ca²⁺ elevation. Immunocytochemical analyses showed the localization of the fungal hydrophobin at the plant cell surface, where it forms a protein film covering the plant cell wall. Our data demonstrate the Ca²⁺-mediated perception by plant cells of a key metabolite secreted by a biocontrol fungus, and provide the first evidence of the involvement of NAADP-gated Ca²⁺ release in a signalling pathway triggered by a biotic stimulus. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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7 pages, 31605 KiB

Open AccessCommunication

Plasma Membrane-Localized Calcium Pumps and Copines Coordinately Regulate Pollen Germination and Fertility in Arabidopsis

by Yun Li, Jinping Guo, Ziyuan Yang and Dong-Lei Yang

Int. J. Mol. Sci. 2018, 19(6), 1774; https://doi.org/10.3390/ijms19061774 - 15 Jun 2018

Cited by 20 | Viewed by 5329

Abstract

Calcium plays an important role in plant growth, development, and response to environmental stimuli. Copines are conserved plasma membrane-localized calcium-binding proteins which regulate plant immune responses and development. In this study, we found that copine proteins BON2 and BON3, the paralogs of BON1, [...] Read more.

Calcium plays an important role in plant growth, development, and response to environmental stimuli. Copines are conserved plasma membrane-localized calcium-binding proteins which regulate plant immune responses and development. In this study, we found that copine proteins BON2 and BON3, the paralogs of BON1, physically interact with calcium pumps ACA8 and ACA10 in Arabidopsis. Notably, ACA9, the closest homologue of ACA8 and ACA10 functioning in pollen tube growth, interacts with all three copines. This is consistent with the protein–protein interactions between the two protein families, the aca8, aca10, aca8/aca10, bon1/2/3 mutants as well as aca9 mutant exhibited defects on pollen germination and seed production. Taken together, plasma membrane-localized interacting calcium pumps and copines coordinately control pollen tube growth, likely through manipulating calcium efflux. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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18 pages, 3654 KiB

Open AccessArticle

Ca²⁺/Calmodulin-Dependent AtSR1/CAMTA3 Plays Critical Roles in Balancing Plant Growth and Immunity

by Peiguo Yuan, Liqun Du and B. W. Poovaiah

Int. J. Mol. Sci. 2018, 19(6), 1764; https://doi.org/10.3390/ijms19061764 - 14 Jun 2018

Cited by 39 | Viewed by 5869

Abstract

During plant-pathogen interactions, plants have to relocate their resources including energy to defend invading organisms; as a result, plant growth and development are usually reduced. Arabidopsis signal responsive1 (AtSR1) has been documented as a negative regulator of plant immune responses and could serve [...] Read more.

During plant-pathogen interactions, plants have to relocate their resources including energy to defend invading organisms; as a result, plant growth and development are usually reduced. Arabidopsis signal responsive1 (AtSR1) has been documented as a negative regulator of plant immune responses and could serve as a positive regulator of plant growth and development. However, the mechanism by which AtSR1 balances plant growth and immunity is poorly understood. Here, we performed a global gene expression profiling using Affymetrix microarrays to study how AtSR1 regulates defense- and growth-related genes in plants with and without bacterial pathogen infection. Results revealed that AtSR1 negatively regulates most of the immune-related genes involved in molecular pattern-triggered immunity (PTI), effector-triggered immunity (ETI), and in salicylic acid (SA)- and jasmonate (JA)-mediated signaling pathways. AtSR1 may rigidly regulate several steps of the SA-mediated pathway, from the activation of SA synthesis to the perception of SA signal. Furthermore, AtSR1 may also regulate plant growth through its involvement in regulating auxin- and BRs-related pathways. Although microarray data revealed that expression levels of defense-related genes induced by pathogens are higher in wild-type (WT) plants than that in atsr1 mutant plants, WT plants are more susceptible to the infection of virulent pathogen as compared to atsr1 mutant plants. These observations indicate that the AtSR1 functions in suppressing the expression of genes induced by pathogen attack and contributes to the rapid establishment of resistance in WT background. Results of electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation (ChIP)-PCR assays suggest that AtSR1 acts as transcription factor in balancing plant growth and immunity, through interaction with the “CGCG” containing CG-box in the promotors of its target genes. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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Review

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21 pages, 6837 KiB

Open AccessReview

What Drives Symbiotic Calcium Signalling in Legumes? Insights and Challenges of Imaging

by Teresa Vaz Martins and Valerie N. Livina

Int. J. Mol. Sci. 2019, 20(9), 2245; https://doi.org/10.3390/ijms20092245 - 7 May 2019

Cited by 4 | Viewed by 4146

Abstract

We review the contribution of bioimaging in building a coherent understanding of Ca

^{2 +}

signalling during legume-bacteria symbiosis. Currently, two different calcium signals are believed to control key steps of the symbiosis: a Ca

^{2 +}

gradient at the tip of the [...] Read more.

We review the contribution of bioimaging in building a coherent understanding of Ca

^{2 +}

signalling during legume-bacteria symbiosis. Currently, two different calcium signals are believed to control key steps of the symbiosis: a Ca

^{2 +}

gradient at the tip of the legume root hair is involved in the development of an infection thread, while nuclear Ca

^{2 +}

oscillations, the hallmark signal of this symbiosis, control the formation of the root nodule, where bacteria fix nitrogen. Additionally, different Ca

^{2 +}

spiking signatures have been associated with specific infection stages. Bioimaging is intrinsically a cross-disciplinary area that requires integration of image recording, processing and analysis. We used experimental examples to critically evaluate previously-established conclusions and draw attention to challenges caused by the varying nature of the signal-to-noise ratio in live imaging. We hypothesise that nuclear Ca

^{2 +}

spiking is a wide-range signal involving the entire root hair and that the Ca

^{2 +}

signature may be related to cytoplasmic streaming. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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16 pages, 676 KiB

Open AccessReview

Actin Cytoskeleton as Actor in Upstream and Downstream of Calcium Signaling in Plant Cells

by Dong Qian and Yun Xiang

Int. J. Mol. Sci. 2019, 20(6), 1403; https://doi.org/10.3390/ijms20061403 - 20 Mar 2019

Cited by 42 | Viewed by 7109

Abstract

In plant cells, calcium (Ca²⁺) serves as a versatile intracellular messenger, participating in several fundamental and important biological processes. Recent studies have shown that the actin cytoskeleton is not only an upstream regulator of Ca²⁺ signaling, but also a downstream [...] Read more.

In plant cells, calcium (Ca²⁺) serves as a versatile intracellular messenger, participating in several fundamental and important biological processes. Recent studies have shown that the actin cytoskeleton is not only an upstream regulator of Ca²⁺ signaling, but also a downstream regulator. Ca²⁺ has been shown to regulates actin dynamics and rearrangements via different mechanisms in plants, and on this basis, the upstream signaling encoded within the Ca²⁺ transient can be decoded. Moreover, actin dynamics have also been proposed to act as an upstream of Ca²⁺, adjust Ca²⁺ oscillations, and establish cytosolic Ca²⁺ ([Ca²⁺]_cyt) gradients in plant cells. In the current review, we focus on the advances in uncovering the relationship between the actin cytoskeleton and calcium in plant cells and summarize our current understanding of this relationship. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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14 pages, 646 KiB

Open AccessReview

The Significance of Calcium in Photosynthesis

by Quan Wang, Sha Yang, Shubo Wan and Xinguo Li

Int. J. Mol. Sci. 2019, 20(6), 1353; https://doi.org/10.3390/ijms20061353 - 18 Mar 2019

Cited by 91 | Viewed by 8898

Abstract

As a secondary messenger, calcium participates in various physiological and biochemical reactions in plants. Photosynthesis is the most extensive biosynthesis process on Earth. To date, researchers have found that some chloroplast proteins have Ca²⁺-binding sites, and the structure and function of [...] Read more.

As a secondary messenger, calcium participates in various physiological and biochemical reactions in plants. Photosynthesis is the most extensive biosynthesis process on Earth. To date, researchers have found that some chloroplast proteins have Ca²⁺-binding sites, and the structure and function of some of these proteins have been discussed in detail. Although the roles of Ca²⁺ signal transduction related to photosynthesis have been discussed, the relationship between calcium and photosynthesis is seldom systematically summarized. In this review, we provide an overview of current knowledge of calcium’s role in photosynthesis. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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12 pages, 684 KiB

Open AccessReview

Calcium: A Critical Factor in Pollen Germination and Tube Elongation

by Ren Hua Zheng, Shun De Su, Hui Xiao and Hui Qiao Tian

Int. J. Mol. Sci. 2019, 20(2), 420; https://doi.org/10.3390/ijms20020420 - 19 Jan 2019

Cited by 62 | Viewed by 12575

Abstract

Pollen is the male gametophyte of higher plants. Its major function is to deliver sperm cells to the ovule to ensure successful fertilization. During this process, many interactions occur among pollen tubes and pistil cells and tissues, and calcium ion (Ca²⁺) [...] Read more.

Pollen is the male gametophyte of higher plants. Its major function is to deliver sperm cells to the ovule to ensure successful fertilization. During this process, many interactions occur among pollen tubes and pistil cells and tissues, and calcium ion (Ca²⁺) dynamics mediate these interactions among cells to ensure that pollen reaches the embryo sac. Although the precise functions of Ca²⁺ dynamics in the cells are unknown, we can speculate about its roles on the basis of its spatial and temporal characteristics during these interactions. The results of many studies indicate that calcium is a critical element that is strongly related to pollen germination and pollen tube growth. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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16 pages, 733 KiB

Open AccessReview

Role of Ca²⁺ in Mediating Plant Responses to Extracellular ATP and ADP

by Greg Clark and Stanley J. Roux

Int. J. Mol. Sci. 2018, 19(11), 3590; https://doi.org/10.3390/ijms19113590 - 14 Nov 2018

Cited by 22 | Viewed by 5462

Abstract

Among the most recently discovered chemical regulators of plant growth and development are extracellular nucleotides, especially extracellular ATP (eATP) and extracellular ADP (eADP). Plant cells release ATP into their extracellular matrix under a variety of different circumstances, and this eATP can then function [...] Read more.

Among the most recently discovered chemical regulators of plant growth and development are extracellular nucleotides, especially extracellular ATP (eATP) and extracellular ADP (eADP). Plant cells release ATP into their extracellular matrix under a variety of different circumstances, and this eATP can then function as an agonist that binds to a specific receptor and induces signaling changes, the earliest of which is an increase in the concentration of cytosolic calcium ([Ca²⁺]_cyt). This initial change is then amplified into downstream-signaling changes that include increased levels of reactive oxygen species and nitric oxide, which ultimately lead to major changes in the growth rate, defense responses, and leaf stomatal apertures of plants. This review presents and discusses the evidence that links receptor activation to increased [Ca²⁺]_cyt and, ultimately, to growth and diverse adaptive changes in plant development. It also discusses the evidence that increased [Ca²⁺]_cyt also enhances the activity of apyrase (nucleoside triphosphate diphosphohydrolase) enzymes that function in multiple subcellular locales to hydrolyze ATP and ADP, and thus limit or terminate the effects of these potent regulators. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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16 pages, 1277 KiB

Open AccessReview

Plant Calcium Signaling in Response to Potassium Deficiency

by Xiaoping Wang, Ling Hao, Biping Zhu and Zhonghao Jiang

Int. J. Mol. Sci. 2018, 19(11), 3456; https://doi.org/10.3390/ijms19113456 - 3 Nov 2018

Cited by 42 | Viewed by 8919

Abstract

Potassium (K⁺) is an essential macronutrient of living cells and is the most abundant cation in the cytosol. K⁺ plays a role in several physiological processes that support plant growth and development. However, soil K⁺ availability is very low [...] Read more.

Potassium (K⁺) is an essential macronutrient of living cells and is the most abundant cation in the cytosol. K⁺ plays a role in several physiological processes that support plant growth and development. However, soil K⁺ availability is very low and variable, which leads to severe reductions in plant growth and yield. Various K⁺ shortage-activated signaling cascades exist. Among these, calcium signaling is the most important signaling system within plant cells. This review is focused on the possible roles of calcium signaling in plant responses to low-K⁺ stress. In plants, intracellular calcium levels are first altered in response to K⁺ deficiency, resulting in calcium signatures that exhibit temporal and spatial features. In addition, calcium channels located within the root epidermis and root hair zone can then be activated by hyperpolarization of plasma membrane (PM) in response to low-K⁺ stress. Afterward, calcium sensors, including calmodulin (CaM), CaM-like protein (CML), calcium-dependent protein kinase (CDPK), and calcineurin B-like protein (CBL), can act in the sensing of K⁺ deprivation. In particular, the important components regarding CBL/CBL-interacting protein kinase (CBL/CIPK) complexes-involved in plant responses to K⁺ deficiency are also discussed. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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19 pages, 2395 KiB

Open AccessReview

The Arabidopsis Calcium-Dependent Protein Kinases (CDPKs) and Their Roles in Plant Growth Regulation and Abiotic Stress Responses

by Sujuan Shi, Shugui Li, Muhammad Asim, Jingjing Mao, Dizhi Xu, Zia Ullah, Guanshan Liu, Qian Wang and Haobao Liu

Int. J. Mol. Sci. 2018, 19(7), 1900; https://doi.org/10.3390/ijms19071900 - 28 Jun 2018

Cited by 147 | Viewed by 12833

Abstract

As a ubiquitous secondary messenger in plant signaling systems, calcium ions (Ca²⁺) play essential roles in plant growth and development. Within the cellular signaling network, the accurate decoding of diverse Ca²⁺ signal is a fundamental molecular event. Calcium-dependent protein kinases [...] Read more.

As a ubiquitous secondary messenger in plant signaling systems, calcium ions (Ca²⁺) play essential roles in plant growth and development. Within the cellular signaling network, the accurate decoding of diverse Ca²⁺ signal is a fundamental molecular event. Calcium-dependent protein kinases (CDPKs), identified commonly in plants, are a kind of vital regulatory protein deciphering calcium signals triggered by various developmental and environmental stimuli. This review chiefly introduces Ca²⁺ distribution in plant cells, the classification of Arabidopsis thaliana CDPKs (AtCDPKs), the identification of the Ca²⁺-AtCDPK signal transduction mechanism and AtCDPKs’ functions involved in plant growth regulation and abiotic stress responses. The review presents a comprehensive overview of AtCDPKs and may contribute to the research of CDPKs in other plants. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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26 pages, 341 KiB

Open AccessReview

Pharmacological Strategies for Manipulating Plant Ca²⁺ Signalling

by Kjell De Vriese, Alex Costa, Tom Beeckman and Steffen Vanneste

Int. J. Mol. Sci. 2018, 19(5), 1506; https://doi.org/10.3390/ijms19051506 - 18 May 2018

Cited by 28 | Viewed by 6029

Abstract

Calcium is one of the most pleiotropic second messengers in all living organisms. However, signalling specificity is encoded via spatio-temporally regulated signatures that act with surgical precision to elicit highly specific cellular responses. How this is brought about remains a big challenge in [...] Read more.

Calcium is one of the most pleiotropic second messengers in all living organisms. However, signalling specificity is encoded via spatio-temporally regulated signatures that act with surgical precision to elicit highly specific cellular responses. How this is brought about remains a big challenge in the plant field, in part due to a lack of specific tools to manipulate/interrogate the plant Ca²⁺ toolkit. In many cases, researchers resort to tools that were optimized in animal cells. However, the obviously large evolutionary distance between plants and animals implies that there is a good chance observed effects may not be specific to the intended plant target. Here, we provide an overview of pharmacological strategies that are commonly used to activate or inhibit plant Ca²⁺ signalling. We focus on highlighting modes of action where possible, and warn for potential pitfalls. Together, this review aims at guiding plant researchers through the Ca²⁺ pharmacology swamp. Full article

(This article belongs to the Special Issue Calcium Signals in Plant Cells)

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