An adenylyl cyclase with a phosphodiesterase domain in basal plants with a motile sperm system

Kasahara, Masahiro; Suetsugu, Noriyuki; Urano, Yuki; Yamamoto, Chiaki; Ohmori, Mikiya; Takada, Yuki; Okuda, Shujiro; Nishiyama, Tomoaki; Sakayama, Hidetoshi; Kohchi, Takayuki; Takahashi, Fumio

doi:10.1038/srep39232

Cited by 46 publications

(38 citation statements)

References 61 publications

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“…Again, much like in the case of the cyclases, a BLAST search with an annotated C. reinhardtii PDE (A8HNW2_CHLRE) does not return any plausible candidate with reasonable similarity. However, recently a liverwort ( Marchantia polymorpha ) protein has been reported that has both AC and PDE domain and both activities ( Kasahara et al, 2016 ). Incidentally, the molecule does contain an AC catalytic center motif ([RKS]X[CTGH]X{8,12}[KR]X{1,3}[DE]) but has no ortholog in Arabidopsis or other higher plants for that matter.…”

Section: Out-lookmentioning

confidence: 99%

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

Gehring

Turek

2017

Front. Plant Sci.

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The cyclic nucleotide monophosphates (cNMPs), and notably 3′,5′-cyclic guanosine monophosphate (cGMP) and 3′,5′-cyclic adenosine monophosphate (cAMP) are now accepted as key signaling molecules in many processes in plants including growth and differentiation, photosynthesis, and biotic and abiotic defense. At the single molecule level, we are now beginning to understand how cNMPs modify specific target molecules such as cyclic nucleotide-gated channels, while at the systems level, a recent study of the Arabidopsis cNMP interactome has identified novel target molecules with specific cNMP-binding domains. A major advance came with the discovery and characterization of a steadily increasing number of guanylate cyclases (GCs) and adenylate cyclases (ACs). Several of the GCs are receptor kinases and include the brassinosteroid receptor, the phytosulfokine receptor, the Pep receptor, the plant natriuretic peptide receptor as well as a nitric oxide sensor. We foresee that in the near future many more molecular mechanisms and biological roles of GCs and ACs and their catalytic products will be discovered and further establish cNMPs as a key component of plant responses to the environment.

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Section: Out-lookmentioning

confidence: 99%

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

Gehring

Turek

2017

Front. Plant Sci.

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“…Additionally, components of cAMP signaling pathways, as well as cAMP interacting proteins (i.e., ACs, phosphodiesterases (PDEs) and protein kinase A (PKA)) have been reported ( Assmann, 1995 ; Gehring, 2010 ; Donaldson et al, 2016 ). To date, however, no gene encoding a PDE has been identified in higher angiosperms, although a recent study has identified a class III AC in the liverwort Marchantia polymorpha which also harbors a functional N-terminal PDE domain ( Kasahara et al, 2016 ). This protein has orthologs only in basal land plants and charophytes, thus a bona fide PDE-AC in higher plants remains elusive.…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis thaliana K+-Uptake Permease 5 (AtKUP5) Contains a Functional Cytosolic Adenylate Cyclase Essential for K+ Transport

et al. 2018

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Potassium (K+) is the most abundant cation in plants, and its uptake and transport are key to growth, development and responses to the environment. Here, we report that Arabidopsis thaliana K+ uptake permease 5 (AtKUP5) contains an adenylate cyclase (AC) catalytic center embedded in its N-terminal cytosolic domain. The purified recombinant AC domain generates cAMP in vitro; and when expressed in Escherichia coli, increases cAMP levels in vivo. Both the AC domain and full length AtKUP5 rescue an AC-deficient E. coli mutant, cyaA, and together these data provide evidence that AtKUP5 functions as an AC. Furthermore, full length AtKUP5 complements the Saccharomyces cerevisiae K+ transport impaired mutant, trk1 trk2, demonstrating its function as a K+ transporter. Surprisingly, a point mutation in the AC center that impairs AC activity, also abolishes complementation of trk1 trk2, suggesting that a functional catalytic AC domain is essential for K+ uptake. AtKUP5-mediated K+ uptake is not affected by cAMP, the catalytic product of the AC, but, interestingly, causes cytosolic cAMP accumulation. These findings are consistent with a role for AtKUP5 as K+ flux sensor, where the flux-dependent cAMP increases modulate downstream components essential for K+ homeostasis, such as cyclic nucleotide gated channels.

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“…This GC-derived AC motif has further identified a functional AC center in a pentatricopeptide repeat-containing protein (AtPPR) [ 92 ] and predicted several candidate ACs in Arabidopsis thaliana [ 15 , 17 ] some of which are currently under experimental evaluation. Recently, a functional AC domain that contains the AC catalytic center motif has been reported in liverwort Marchantia polymorpha and interestingly, this protein also harbors a phosphodiesterase (PDE) domain that is capable of degrading cyclic nucleotide monophosphates [ 93 ] thus representing an example of a complex multi-domain plant protein capable of regulating cellular cyclic nucleotide monophosphates levels. However, this protein has orthologues only in basal land plants and charophytes that use motile sperms as the male gamete [ 93 ] and thus a bona fide PDE-AC in higher plants remains elusive.…”

Section: Nucleotide Cyclase Functional Centers In Plantsmentioning

confidence: 99%

Discovery of Novel Functional Centers With Rationally Designed Amino Acid Motifs

Wong

Tian

Gehring

et al. 2018

Computational and Structural Biotechnology Journal

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Plants are constantly exposed to environmental stresses and in part due to their sessile nature, they have evolved signal perception and adaptive strategies that are distinct from those of other eukaryotes. This is reflected at the cellular level where receptors and signalling molecules cannot be identified using standard homology-based searches querying with proteins from prokaryotes and other eukaryotes. One of the reasons for this is the complex domain architecture of receptor molecules. In order to discover hidden plant signalling molecules, we have developed a motif-based approach designed specifically for the identification of functional centers in plant molecules. This has made possible the discovery of novel components involved in signalling and stimulus-response pathways; the molecules include cyclic nucleotide cyclases, a nitric oxide sensor and a novel target for the hormone abscisic acid. Here, we describe the major steps of the method and illustrate it with recent and experimentally confirmed molecules as examples. We foresee that carefully curated search motifs supported by structural and bioinformatic assessments will uncover many more structural and functional aspects, particularly of signalling molecules.

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An adenylyl cyclase with a phosphodiesterase domain in basal plants with a motile sperm system

Cited by 46 publications

References 61 publications

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

The Arabidopsis thaliana K+-Uptake Permease 5 (AtKUP5) Contains a Functional Cytosolic Adenylate Cyclase Essential for K+ Transport

Discovery of Novel Functional Centers With Rationally Designed Amino Acid Motifs

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