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Article ; Online: CIPK‐B is essential for salt stress signalling in Marchantia polymorpha

Tansley, Connor / Houghton, James / Rose, Althea M. E. / Witek, Bartosz / Payet, Rocky D. / Wu, Taoyang / Miller, J. Benjamin

New Phytologist. 2023 Mar., v. 237, no. 6 p.2210-2223

2023

Abstract: Calcium signalling is central to many plant processes, with families of calcium decoder proteins having expanded across the green lineage and redundancy existing between decoders. The liverwort Marchantia polymorpha has fast become a new model plant, but ...

Abstract	Calcium signalling is central to many plant processes, with families of calcium decoder proteins having expanded across the green lineage and redundancy existing between decoders. The liverwort Marchantia polymorpha has fast become a new model plant, but the calcium decoders that exist in this species remain unclear. We performed phylogenetic analyses to identify the calcineurin B‐like (CBL) and CBL‐interacting protein kinase (CIPK) network of M. polymorpha. We analysed CBL‐CIPK expression during salt stress, and determined protein–protein interactions using yeast two‐hybrid and bimolecular fluorescence complementation. We also created genetic knockouts using CRISPR/Cas9. We confirm that M. polymorpha has two CIPKs and three CBLs. Both CIPKs and one CBL show pronounced salt‐responsive transcriptional changes. All M. polymorpha CBL‐CIPKs interact with each other in planta. Knocking out CIPK‐B causes increased sensitivity to salt, suggesting that this CIPK is involved in salt signalling. We have identified CBL‐CIPKs that form part of a salt tolerance pathway in M. polymorpha. Phylogeny and interaction studies imply that these CBL‐CIPKs form an evolutionarily conserved salt overly sensitive pathway. Hence, salt responses may be some of the early functions of CBL‐CIPK networks and increased abiotic stress tolerance required for land plant emergence.
Keywords	CRISPR-Cas systems ; Marchantia polymorpha ; calcium ; fluorescence ; mosses and liverworts ; phylogeny ; protein kinases ; salt stress ; salt tolerance ; stress tolerance ; transcription (genetics) ; two hybrid system techniques
Language	English
Dates of publication	2023-03
Size	p. 2210-2223.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18633
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: CIPK-B is essential for salt stress signalling in Marchantia polymorpha.

Tansley, Connor / Houghton, James / Rose, Althea M E / Witek, Bartosz / Payet, Rocky D / Wu, Taoyang / Miller, J Benjamin

The New phytologist

2023 Volume 237, Issue 6, Page(s) 2210–2223

Abstract	Calcium signalling is central to many plant processes, with families of calcium decoder proteins having expanded across the green lineage and redundancy existing between decoders. The liverwort Marchantia polymorpha has fast become a new model plant, but the calcium decoders that exist in this species remain unclear. We performed phylogenetic analyses to identify the calcineurin B-like (CBL) and CBL-interacting protein kinase (CIPK) network of M. polymorpha. We analysed CBL-CIPK expression during salt stress, and determined protein-protein interactions using yeast two-hybrid and bimolecular fluorescence complementation. We also created genetic knockouts using CRISPR/Cas9. We confirm that M. polymorpha has two CIPKs and three CBLs. Both CIPKs and one CBL show pronounced salt-responsive transcriptional changes. All M. polymorpha CBL-CIPKs interact with each other in planta. Knocking out CIPK-B causes increased sensitivity to salt, suggesting that this CIPK is involved in salt signalling. We have identified CBL-CIPKs that form part of a salt tolerance pathway in M. polymorpha. Phylogeny and interaction studies imply that these CBL-CIPKs form an evolutionarily conserved salt overly sensitive pathway. Hence, salt responses may be some of the early functions of CBL-CIPK networks and increased abiotic stress tolerance required for land plant emergence.
MeSH term(s)	Marchantia/genetics ; Marchantia/metabolism ; Plant Proteins/genetics ; Plant Proteins/metabolism ; Phylogeny ; Calcium/metabolism ; Salt Tolerance/genetics ; Stress, Physiological/genetics ; Calcium-Binding Proteins/metabolism
Chemical Substances	Plant Proteins ; Calcium (SY7Q814VUP) ; Calcium-Binding Proteins
Language	English
Publishing date	2023-01-20
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18633
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Book ; Online: Non-Adaptive Matroid Prophet Inequalities

Chawla, Shuchi / Goldner, Kira / Karlin, Anna R. / Miller, J. Benjamin

2020

Abstract: We investigate non-adaptive algorithms for matroid prophet inequalities. Matroid prophet inequalities have been considered resolved since 2012 when [KW12] introduced thresholds that guarantee a tight 2-approximation to the prophet; however, this ... ...

Abstract	We investigate non-adaptive algorithms for matroid prophet inequalities. Matroid prophet inequalities have been considered resolved since 2012 when [KW12] introduced thresholds that guarantee a tight 2-approximation to the prophet; however, this algorithm is adaptive. Other approaches of [CHMS10] and [FSZ16] have used non-adaptive thresholds with a feasibility restriction; however, this translates to adaptively changing an item's threshold to infinity when it cannot be taken with respect to the additional feasibility constraint, hence the algorithm is not truly non-adaptive. A major application of prophet inequalities is in auction design, where non-adaptive prices possess a significant advantage: they convert to order-oblivious posted pricings, and are essential for translating a prophet inequality into a truthful mechanism for multi-dimensional buyers. The existing matroid prophet inequalities do not suffice for this application. We present the first non-adaptive constant-factor prophet inequality for graphic matroids.
Keywords	Computer Science - Data Structures and Algorithms ; Computer Science - Computer Science and Game Theory
Subject code	000
Publishing date	2020-11-18
Publishing country	us
Document type	Book ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Insights into methionine S-methylation in diverse organisms.

Peng, Ming / Li, Chun-Yang / Chen, Xiu-Lan / Williams, Beth T / Li, Kang / Gao, Ya-Nan / Wang, Peng / Wang, Ning / Gao, Chao / Zhang, Shan / Schoelmerich, Marie C / Banfield, Jillian F / Miller, J Benjamin / Le Brun, Nick E / Todd, Jonathan D / Zhang, Yu-Zhong

Nature communications

2022 Volume 13, Issue 1, Page(s) 2947

Abstract: Dimethylsulfoniopropionate (DMSP) is an important marine anti-stress compound, with key roles in global nutrient cycling, chemotaxis and, potentially, climate regulation. Recently, diverse marine Actinobacteria, α- and γ-proteobacteria were shown to ... ...

Abstract	Dimethylsulfoniopropionate (DMSP) is an important marine anti-stress compound, with key roles in global nutrient cycling, chemotaxis and, potentially, climate regulation. Recently, diverse marine Actinobacteria, α- and γ-proteobacteria were shown to initiate DMSP synthesis via the methionine (Met) S-methyltransferase enzyme (MmtN), generating S-methyl-Met (SMM). Here we characterize a roseobacterial MmtN, providing structural and mechanistic insights into this DMSP synthesis enzyme. We propose that MmtN uses the proximity and desolvation mechanism for Met S-methylation with two adjacent MmtN monomers comprising the Met binding site. We also identify diverse functional MmtN enzymes in potentially symbiotic archaeal Candidatus Woesearchaeota and Candidate Phyla Radiation (CPR) bacteria, and the animalcule Adineta steineri, not anticipated to produce SMM and/or DMSP. These diverse MmtN enzymes, alongside the larger plant MMT enzyme with an N-terminus homologous to MmtN, likely utilize the same proximity and desolvation mechanism. This study provides important insights into the catalytic mechanism of SMM and/or DMSP production, and proposes roles for these compounds in secondary metabolite production, and SMM cycling in diverse organisms and environments.
MeSH term(s)	Bacteria/metabolism ; Methionine/metabolism ; Methylation ; Methyltransferases/genetics ; Methyltransferases/metabolism
Chemical Substances	Methionine (AE28F7PNPL) ; Methyltransferases (EC 2.1.1.-)
Language	English
Publishing date	2022-05-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-30491-5
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Article ; Online: Optogenetic control of gene expression in plants in the presence of ambient white light.

Ochoa-Fernandez, Rocio / Abel, Nikolaj B / Wieland, Franz-Georg / Schlegel, Jenia / Koch, Leonie-Alexa / Miller, J Benjamin / Engesser, Raphael / Giuriani, Giovanni / Brandl, Simon M / Timmer, Jens / Weber, Wilfried / Ott, Thomas / Simon, Rüdiger / Zurbriggen, Matias D

Nature methods

2020 Volume 17, Issue 7, Page(s) 717–725

Abstract: Optogenetics is the genetic approach for controlling cellular processes with light. It provides spatiotemporal, quantitative and reversible control over biological signaling and metabolic processes, overcoming limitations of chemically inducible systems. ...

Abstract	Optogenetics is the genetic approach for controlling cellular processes with light. It provides spatiotemporal, quantitative and reversible control over biological signaling and metabolic processes, overcoming limitations of chemically inducible systems. However, optogenetics lags in plant research because ambient light required for growth leads to undesired system activation. We solved this issue by developing plant usable light-switch elements (PULSE), an optogenetic tool for reversibly controlling gene expression in plants under ambient light. PULSE combines a blue-light-regulated repressor with a red-light-inducible switch. Gene expression is only activated under red light and remains inactive under white light or in darkness. Supported by a quantitative mathematical model, we characterized PULSE in protoplasts and achieved high induction rates, and we combined it with CRISPR-Cas9-based technologies to target synthetic signaling and developmental pathways. We applied PULSE to control immune responses in plant leaves and generated Arabidopsis transgenic plants. PULSE opens broad experimental avenues in plant research and biotechnology.
MeSH term(s)	Arabidopsis/genetics ; Arabidopsis/immunology ; CRISPR-Cas Systems/genetics ; Gene Expression Regulation, Plant ; Light ; Models, Theoretical ; Optogenetics ; Plants, Genetically Modified
Language	English
Publishing date	2020-06-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2169522-2
ISSN	1548-7105 ; 1548-7091
ISSN (online)	1548-7105
ISSN	1548-7091
DOI	10.1038/s41592-020-0868-y
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Article ; Online: Characterizing standard genetic parts and establishing common principles for engineering legume and cereal roots.

Feike, Doreen / Korolev, Andrey V / Soumpourou, Eleni / Murakami, Eiichi / Reid, Dugald / Breakspear, Andrew / Rogers, Christian / Radutoiu, Simona / Stougaard, Jens / Harwood, Wendy A / Oldroyd, Giles E D / Miller, J Benjamin

Plant biotechnology journal

2019 Volume 17, Issue 12, Page(s) 2234–2245

Abstract: Plant synthetic biology and cereal engineering depend on the controlled expression of transgenes of interest. Most engineering in plant species to date has relied heavily on the use of a few, well-established constitutive promoters to achieve high levels ...

Abstract	Plant synthetic biology and cereal engineering depend on the controlled expression of transgenes of interest. Most engineering in plant species to date has relied heavily on the use of a few, well-established constitutive promoters to achieve high levels of expression; however, the levels of transgene expression can also be influenced by the use of codon optimization, intron-mediated enhancement and varying terminator sequences. Most of these alternative approaches for regulating transgene expression have only been tested in small-scale experiments, typically testing a single gene of interest. It is therefore difficult to interpret the relative importance of these approaches and to design engineering strategies that are likely to succeed in different plant species, particularly if engineering multigenic traits where the expression of each transgene needs to be precisely regulated. Here, we present data on the characterization of 46 promoters and 10 terminators in Medicago truncatula, Lotus japonicus, Nicotiana benthamiana and Hordeum vulgare, as well as the effects of codon optimization and intron-mediated enhancement on the expression of two transgenes in H. vulgare. We have identified a core set of promoters and terminators of relevance to researchers engineering novel traits in plant roots. In addition, we have shown that combining codon optimization and intron-mediated enhancement increases transgene expression and protein levels in barley. Based on our study, we recommend a core set of promoters and terminators for broad use and also propose a general set of principles and guidelines for those engineering cereal species.
MeSH term(s)	Edible Grain/genetics ; Fabaceae/genetics ; Gene Expression Regulation, Plant ; Genetic Engineering ; Plant Roots/genetics ; Plants, Genetically Modified ; Promoter Regions, Genetic ; Transgenes
Language	English
Publishing date	2019-05-23
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2136367-5
ISSN	1467-7652 ; 1467-7644
ISSN (online)	1467-7652
ISSN	1467-7644
DOI	10.1111/pbi.13135
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Characterizing standard genetic parts and establishing common principles for engineering legume and cereal roots

Plant biotechnology journal. 2019 Dec., v. 17, no. 12

2019

Abstract: Plant synthetic biology and cereal engineering depend on the controlled expression of transgenes of interest. Most engineering in plant species to date has relied heavily on the use of a few, well‐established constitutive promoters to achieve high levels ...

Abstract	Plant synthetic biology and cereal engineering depend on the controlled expression of transgenes of interest. Most engineering in plant species to date has relied heavily on the use of a few, well‐established constitutive promoters to achieve high levels of expression; however, the levels of transgene expression can also be influenced by the use of codon optimization, intron‐mediated enhancement and varying terminator sequences. Most of these alternative approaches for regulating transgene expression have only been tested in small‐scale experiments, typically testing a single gene of interest. It is therefore difficult to interpret the relative importance of these approaches and to design engineering strategies that are likely to succeed in different plant species, particularly if engineering multigenic traits where the expression of each transgene needs to be precisely regulated. Here, we present data on the characterization of 46 promoters and 10 terminators in Medicago truncatula, Lotus japonicus, Nicotiana benthamiana and Hordeum vulgare, as well as the effects of codon optimization and intron‐mediated enhancement on the expression of two transgenes in H. vulgare. We have identified a core set of promoters and terminators of relevance to researchers engineering novel traits in plant roots. In addition, we have shown that combining codon optimization and intron‐mediated enhancement increases transgene expression and protein levels in barley. Based on our study, we recommend a core set of promoters and terminators for broad use and also propose a general set of principles and guidelines for those engineering cereal species.
Keywords	Hordeum vulgare ; Lotus corniculatus var. japonicus ; Medicago truncatula ; Nicotiana benthamiana ; barley ; biotechnology ; gene expression ; legumes ; synthetic biology ; transgenes
Language	English
Dates of publication	2019-12
Size	p. 2234-2245.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	2136367-5
ISSN	1467-7652 ; 1467-7644
ISSN (online)	1467-7652
ISSN	1467-7644
DOI	10.1111/pbi.13135
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Phosphorylation of S344 in the calmodulin-binding domain negatively affects CCaMK function during bacterial and fungal symbioses.

Routray, Pratyush / Miller, J Benjamin / Du, Liqun / Oldroyd, Giles / Poovaiah, B W

The Plant journal : for cell and molecular biology

2013 Volume 76, Issue 2, Page(s) 287–296

Abstract: Calcium and Ca(2+)/calmodulin-dependent protein kinase (CCaMK) plays a critical role in the signaling pathway that establishes root nodule symbiosis and arbuscular mycorrhizal symbiosis. Calcium-dependent autophosphorylation is central to the regulation ... ...

Abstract	Calcium and Ca(2+)/calmodulin-dependent protein kinase (CCaMK) plays a critical role in the signaling pathway that establishes root nodule symbiosis and arbuscular mycorrhizal symbiosis. Calcium-dependent autophosphorylation is central to the regulation of CCaMK, and this has been shown to promote calmodulin binding. Here, we report a regulatory mechanism of Medicago truncatula CCaMK (MtCCaMK) through autophosphorylation of S344 in the calmodulin-binding/autoinhibitory domain. The phospho-ablative mutation S344A did not have significant effect on its kinase activities, and supports root nodule symbiosis and arbuscular mycorrhizal symbiosis, indicating that phosphorylation at this position is not required for establishment of symbioses. The phospho-mimic mutation S344D show drastically reduced calmodulin-stimulated substrate phosphorylation, and this coincides with a compromised interaction with calmodulin and its interacting partner, IPD3. Functional complementation tests revealed that the S344D mutation blocked root nodule symbiosis and reduced the mycorrhizal association. Furthermore, S344D was shown to suppress the spontaneous nodulation associated with a gain-of-function mutant of MtCCaMK (T271A), revealing that phosphorylation at S344 of MtCCaMK is adequate for shutting down its activity, and is epistatic over previously identified T271 autophosphorylation. These results reveal a mechanism that enables CCaMK to 'turn off' its function through autophosphorylation.
MeSH term(s)	Binding Sites ; Calcium/physiology ; Calcium-Calmodulin-Dependent Protein Kinases/genetics ; Calcium-Calmodulin-Dependent Protein Kinases/physiology ; Calmodulin/physiology ; Genetic Complementation Test ; Medicago truncatula/genetics ; Medicago truncatula/microbiology ; Medicago truncatula/physiology ; Mutagenesis, Site-Directed ; Mycorrhizae/physiology ; Phosphorylation ; Plant Proteins/genetics ; Plant Proteins/physiology ; Plant Root Nodulation/physiology ; Rhizobium/physiology ; Signal Transduction ; Symbiosis
Chemical Substances	Calmodulin ; Plant Proteins ; Calcium-Calmodulin-Dependent Protein Kinases (EC 2.7.11.17) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2013-10
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1088037-9
ISSN	1365-313X ; 0960-7412
ISSN (online)	1365-313X
ISSN	0960-7412
DOI	10.1111/tpj.12288
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Calcium/Calmodulin-Dependent Protein Kinase Is Negatively and Positively Regulated by Calcium, Providing a Mechanism for Decoding Calcium Responses during Symbiosis Signaling

Miller, J. Benjamin / Akira Miyahara / Amitesh Pratap / Giles E.D. Oldroyd / Liang Zhou / Richard J. Morris / Stephen Bornemann

plant cell. 2013 Dec., v. 25, no. 12

2013

Abstract: This study dissects the regulation of a calcium/calmodulin-dependent protein kinase (CCaMK) during symbiotic signaling and reveals that CCaMK is both negatively and positively regulated by calcium to create a robust molecular switch that is responsive to ...

Abstract	This study dissects the regulation of a calcium/calmodulin-dependent protein kinase (CCaMK) during symbiotic signaling and reveals that CCaMK is both negatively and positively regulated by calcium to create a robust molecular switch that is responsive to calcium concentrations associated with both the basal state and with oscillations.
Keywords	calcium ; calcium-calmodulin-dependent protein kinase ; symbiosis
Language	English
Dates of publication	2013-12
Size	p. 5053-5066.
Publishing place	American Society of Plant Biologists
Document type	Article
ZDB-ID	623171-8
ISSN	1532-298X ; 1040-4651
ISSN (online)	1532-298X
ISSN	1040-4651
DOI	10.1105/tpc.113.116921
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Article ; Online: Calcium/Calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling.

Miller, J Benjamin / Pratap, Amitesh / Miyahara, Akira / Zhou, Liang / Bornemann, Stephen / Morris, Richard J / Oldroyd, Giles E D

The Plant cell

2013 Volume 25, Issue 12, Page(s) 5053–5066

Abstract: The establishment of symbiotic associations in plants requires calcium oscillations that must be decoded to invoke downstream developmental programs. In animal systems, comparable calcium oscillations are decoded by calmodulin (CaM)-dependent protein ... ...

Abstract	The establishment of symbiotic associations in plants requires calcium oscillations that must be decoded to invoke downstream developmental programs. In animal systems, comparable calcium oscillations are decoded by calmodulin (CaM)-dependent protein kinases, but symbiotic signaling involves a calcium/CaM-dependent protein kinase (CCaMK) that is unique to plants. CCaMK differs from the animal CaM kinases by its dual ability to bind free calcium, via calcium binding EF-hand domains on the protein, or to bind calcium complexed with CaM, via a CaM binding domain. In this study, we dissect this dual regulation of CCaMK by calcium. We find that calcium binding to the EF-hand domains promotes autophosphorylation, which negatively regulates CCaMK by stabilizing the inactive state of the protein. By contrast, calcium-dependent CaM binding overrides the effects of autophosphorylation and activates the protein. The differential calcium binding affinities of the EF-hand domains compared with those of CaM suggest that CCaMK is maintained in the inactive state at basal calcium concentrations and is activated via CaM binding during calcium oscillations. This work provides a model for decoding calcium oscillations that uses differential calcium binding affinities to create a robust molecular switch that is responsive to calcium concentrations associated with both the basal state and with oscillations.
MeSH term(s)	Calcium/metabolism ; Calcium Signaling ; Calcium-Calmodulin-Dependent Protein Kinases/genetics ; Calcium-Calmodulin-Dependent Protein Kinases/metabolism ; Medicago truncatula/metabolism ; Medicago truncatula/microbiology ; Models, Biological ; Models, Molecular ; Molecular Sequence Data ; Phosphorylation ; Protein Structure, Tertiary ; Sinorhizobium meliloti/metabolism ; Symbiosis
Chemical Substances	Calcium-Calmodulin-Dependent Protein Kinases (EC 2.7.11.17) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2013-12-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	623171-8
ISSN	1532-298X ; 1040-4651
ISSN (online)	1532-298X
ISSN	1040-4651
DOI	10.1105/tpc.113.116921
Database	MEDical Literature Analysis and Retrieval System OnLINE

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