TypiCal but DeliCate Ca++re: Dissecting the Essence of Calcium Signaling Network as a Robust Response Coordinator of Versatile Abiotic and Biotic Stimuli in Plants

Plant growth, development, and ultimately crop productivity are largely impacted by the interaction of plants with different abiotic and biotic factors throughout their life cycle. Perception of different abiotic stresses, such as salt, cold, drought, heat, and heavy metals, and interaction with beneficial and harmful biotic agents by plants lead to transient, sustained, or oscillatory changes of [calcium ion, Ca2+]cyt within the cell. Significant progress has been made in the decoding of Ca2+ signatures into downstream responses to modulate differential developmental and physiological responses in the whole plant. Ca2+ sensor proteins, mainly calmodulins (CaMs), calmodulin-like proteins (CMLs), and others, such as Ca2+-dependent protein kinases (CDPKs), calcineurin B-like proteins (CBLs), and calmodulin-binding transcription activators (CAMTAs) have played critical roles in coupling the specific stress stimulus with an appropriate response. This review summarizes the current understanding of the Ca2+ influx and efflux system in plant cells and various Ca2+ binding protein-mediated signal transduction pathways that are delicately orchestrated to mitigate abiotic and biotic stresses. The probable interactions of different components of Ca2+ sensor relays and Ca2+ sensor responders in response to various external stimuli have been described diagrammatically focusing on established pathways and latest developments. Present comprehensive insight into key components of the Ca2+ signaling toolkit in plants can provide an innovative framework for biotechnological manipulations toward crop improvability in near future.

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Genome-wide identification and biochemical characterization of calcineurin B-like calcium sensor proteins in Chlamydomonas reinhardtii

Biochemical Journal ◽

10.1042/bcj20190960 ◽

2020 ◽

Vol 477 (10) ◽

pp. 1879-1892

Author(s):

Manoj Kumar ◽

Komal Sharma ◽

Akhilesh K. Yadav ◽

Kajal Kanchan ◽

Madhu Baghel ◽

...

Keyword(s):

Chlamydomonas Reinhardtii ◽

Biochemical Characterization ◽

Abiotic And Biotic Stresses ◽

Biotic Stresses ◽

Physiological Processes ◽

Calcineurin B ◽

Genome Wide ◽

Dependent Protein ◽

Sensor Proteins

Calcium (Ca2+) signaling is involved in the regulation of diverse biological functions through association with several proteins that enable them to respond to abiotic and biotic stresses. Though Ca2+-dependent signaling has been implicated in the regulation of several physiological processes in Chlamydomonas reinhardtii, Ca2+ sensor proteins are not characterized completely. C. reinhardtii has diverged from land plants lineage, but shares many common genes with animals, particularly those encoding proteins of the eukaryotic flagellum (or cilium) along with the basal body. Calcineurin, a Ca2+/calmodulin-dependent protein phosphatase, is an important effector of Ca2+ signaling in animals, while calcineurin B-like proteins (CBLs) play an important role in Ca2+ sensing and signaling in plants. The present study led to the identification of 13 novel CBL-like Ca2+ sensors in C. reinhardtii genome. One of the archetypical genes of the newly identified candidate, CrCBL-like1 was characterized. The ability of CrCBL-like1 protein to sense as well as bind Ca2+ were validated using two-step Ca2+-binding kinetics. The CrCBL-like1 protein localized around the plasma membrane, basal bodies and in flagella, and interacted with voltage-gated Ca2+ channel protein present abundantly in the flagella, indicating its involvement in the regulation of the Ca2+ concentration for flagellar movement. The CrCBL-like1 transcript and protein expression were also found to respond to abiotic stresses, suggesting its involvement in diverse physiological processes. Thus, the present study identifies novel Ca2+ sensors and sheds light on key players involved in Ca2+signaling in C. reinhardtii, which could further be extrapolated to understand the evolution of Ca2+ mediated signaling in other eukaryotes.

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Faculty Opinions recommendation of Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.13864964.15302066 ◽

2012 ◽

Author(s):

Giles Oldroyd

Keyword(s):

Protein Kinase ◽

Lotus Japonicus ◽

Dependent Protein Kinase ◽

Calmodulin Binding ◽

Calcium Calmodulin Dependent ◽

Dependent Protein

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Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1511182112 ◽

2015 ◽

Vol 112 (30) ◽

pp. 9166-9173 ◽

Cited By ~ 94

Author(s):

Xiao-yu Zheng ◽

Mian Zhou ◽

Heejin Yoo ◽

Jose L. Pruneda-Paz ◽

Natalie Weaver Spivey ◽

...

Keyword(s):

Salicylic Acid ◽

Systemic Acquired Resistance ◽

Acquired Resistance ◽

Signal Transduction Pathway ◽

Temporal Regulation ◽

Calmodulin Binding ◽

Regulation Of Biosynthesis ◽

Pathogen Entry ◽

Transcription Activators ◽

Transcriptional Induction

The plant hormone salicylic acid (SA) is essential for local defense and systemic acquired resistance (SAR). When plants, such as Arabidopsis, are challenged by different pathogens, an increase in SA biosynthesis generally occurs through transcriptional induction of the key synthetic enzyme isochorismate synthase 1 (ICS1). However, the regulatory mechanism for this induction is poorly understood. Using a yeast one-hybrid screen, we identified two transcription factors (TFs), NTM1-LIKE 9 (NTL9) and CCA1 HIKING EXPEDITION (CHE), as activators of ICS1 during specific immune responses. NTL9 is essential for inducing ICS1 and two other SA synthesis-related genes, PHYTOALEXIN-DEFICIENT 4 (PAD4) and ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1), in guard cells that form stomata. Stomata can quickly close upon challenge to block pathogen entry. This stomatal immunity requires ICS1 and the SA signaling pathway. In the ntl9 mutant, this response is defective and can be rescued by exogenous application of SA, indicating that NTL9-mediated SA synthesis is essential for stomatal immunity. CHE, the second identified TF, is a central circadian clock oscillator and is required not only for the daily oscillation in SA levels but also for the pathogen-induced SA synthesis in systemic tissues during SAR. CHE may also regulate ICS1 through the known transcription activators CALMODULIN BINDING PROTEIN 60g (CBP60g) and SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) because induction of these TF genes is compromised in the che-2 mutant. Our study shows that SA biosynthesis is regulated by multiple TFs in a spatial and temporal manner and therefore fills a gap in the signal transduction pathway between pathogen recognition and SA production.

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Calmodulin-binding transcription activators and perspectives for applications in biotechnology

Applied Microbiology and Biotechnology ◽

10.1007/s00253-015-6966-6 ◽

2015 ◽

Vol 99 (24) ◽

pp. 10379-10385 ◽

Cited By ~ 9

Author(s):

Chenjia Shen ◽

Yanjun Yang ◽

Liqun Du ◽

Huizhong Wang

Keyword(s):

Calmodulin Binding ◽

Transcription Activators

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Isolation of the native form of chicken gizzard myosin light-chain kinase

Biochemical Journal ◽

10.1042/bj2180863 ◽

1984 ◽

Vol 218 (3) ◽

pp. 863-870 ◽

Cited By ~ 87

Author(s):

P K Ngai ◽

C A Carruthers ◽

M P Walsh

Keyword(s):

Light Chain ◽

Myosin Light Chain Kinase ◽

Myosin Light Chain ◽

Binding Protein ◽

Cross Reactivity ◽

Native Form ◽

Chicken Gizzard ◽

Calmodulin Binding ◽

Chymotryptic Peptide ◽

Dependent Protein

A simple and rapid procedure for the purification of the native form of chicken gizzard myosin light-chain kinase (Mr 136000) is described which eliminates problems of proteolysis previously encountered. During this procedure, a calmodulin-binding protein of Mr 141000, which previously co-purified with the myosin light-chain kinase, is removed and shown to be a distinct protein on the basis of lack of kinase activity, different chymotryptic peptide maps, lack of cross-reactivity with a monoclonal antibody to turkey gizzard myosin light-chain kinase, and lack of phosphorylation by the purified catalytic subunit of cyclic AMP-dependent protein kinase. This Mr-141000 calmodulin-binding protein is identified as caldesmon on the basis of Ca2+-dependent interaction with calmodulin, subunit Mr, Ca2+-independent interaction with skeletal-muscle F-actin, Ca2+-dependent competition between calmodulin and F-actin for caldesmon, and tissue content.

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High molecular weight calmodulin-binding protein is phosphorylated by calmodulin-dependent protein kinase VI from bovine cardiac muscle

Signal Transduction Mechanisms ◽

10.1007/978-1-4615-2015-3_3 ◽

1995 ◽

pp. 29-34

Author(s):

Shigeo Taketa ◽

Junor A. Barnes ◽

Mandeep Ubhi ◽

Rajendra K. Sharma

Keyword(s):

Molecular Weight ◽

Protein Kinase ◽

Cardiac Muscle ◽

High Molecular Weight ◽

Binding Protein ◽

Dependent Protein Kinase ◽

Calmodulin Binding ◽

Dependent Protein

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Grapevines under drought do not express esca leaf symptoms

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2112825118 ◽

2021 ◽

Vol 118 (43) ◽

pp. e2112825118

Author(s):

Giovanni Bortolami ◽

Gregory A. Gambetta ◽

Cédric Cassan ◽

Silvina Dayer ◽

Elena Farolfi ◽

...

Keyword(s):

Stomatal Conductance ◽

Water Potential ◽

Stress Responses ◽

Carbon Balance ◽

Nonstructural Carbohydrates ◽

Complex Interactions ◽

Whole Plant ◽

Underlying Causes ◽

Abiotic And Biotic Factors ◽

Leaf Symptoms

In the context of climate change, plant mortality is increasing worldwide in both natural and agroecosystems. However, our understanding of the underlying causes is limited by the complex interactions between abiotic and biotic factors and the technical challenges that limit investigations of these interactions. Here, we studied the interaction between two main drivers of mortality, drought and vascular disease (esca), in one of the world’s most economically valuable fruit crops, grapevine. We found that drought totally inhibited esca leaf symptom expression. We disentangled the plant physiological response to the two stresses by quantifying whole-plant water relations (i.e., water potential and stomatal conductance) and carbon balance (i.e., CO2 assimilation, chlorophyll, and nonstructural carbohydrates). Our results highlight the distinct physiology behind these two stress responses, indicating that esca (and subsequent stomatal conductance decline) does not result from decreases in water potential and generates different gas exchange and nonstructural carbohydrate seasonal dynamics compared to drought.

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