Salt-dependent regulation of a CNG channel subfamily in Arabidopsis

Kugler, Annette; Köhler, Barbara; Palme, Klaus; Wolff, Patricia; Dietrich, Petra

doi:10.1186/1471-2229-9-140

Cited by 94 publications

(71 citation statements)

References 41 publications

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“…CNGC20 expression increased during development and was maximal in mature and senescent leaves. With respect to function, both genes appeared to respond to changes in salt concentration in the shoot, but in different cell types and at different times after treatment (Kugler et al, 2009). Therefore, the divergence in connectivity in our analysis seems to agree with observed divergence in expression in the seedling during early development as well as some potential divergence in function between these two duplicated genes.…”

Section: Network Connectivity and Divergence Is Greater In Wgd Pairssupporting

confidence: 80%

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Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis thaliana

et al. 2015

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(J.P.); 0000-0002-7220-7305 (S.W.).Plant genomes contain large numbers of duplicated genes that contribute to the evolution of new functions. Following duplication, genes can exhibit divergence in their coding sequence and their expression patterns. Changes in the cis-regulatory element landscape can result in changes in gene expression patterns. High-throughput methods developed recently can identify potential cis-regulatory elements on a genome-wide scale. Here, we use a recent comprehensive data set of DNase I sequencingidentified cis-regulatory binding sites (footprints) at single-base-pair resolution to compare binding sites and network connectivity in duplicated gene pairs in Arabidopsis (Arabidopsis thaliana). We found that duplicated gene pairs vary greatly in their cis-regulatory element architecture, resulting in changes in regulatory network connectivity. Whole-genome duplicates (WGDs) have approximately twice as many footprints in their promoters left by potential regulatory proteins than do tandem duplicates (TDs). The WGDs have a greater average number of footprint differences between paralogs than TDs. The footprints, in turn, result in more regulatory network connections between WGDs and other genes, forming denser, more complex regulatory networks than shown by TDs. When comparing regulatory connections between duplicates, WGDs had more pairs in which the two genes are either partially or fully diverged in their network connections, but fewer genes with no network connections than the TDs. There is evidence of younger TDs and WGDs having fewer unique connections compared with older duplicates. This study provides insights into cis-regulatory element evolution and network divergence in duplicated genes.

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Section: Network Connectivity and Divergence Is Greater In Wgd Pairssupporting

confidence: 80%

“…2B). Reporter assays used to study the expression of CNGC19 and CNGC20 showed the two genes were differentially expressed in roots and shoots (Kugler et al, 2009). The CNGC19 gene was predominantly active in roots already at early growth stages.…”

Section: Network Connectivity and Divergence Is Greater In Wgd Pairsmentioning

confidence: 99%

Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis thaliana

et al. 2015

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“…However, only a few studies have shown the disappearance of a defined plasma membrane Ca 2+ channel activity in plants upon mutation of candidate Ca 2+ channel genes Michard et al, 2011;Laohavisit et al, 2012;Vincill et al, 2012). Some CNGCs have been found to be involved in cation nutrient intake, including monovalent cation intake (Guo et al, 2010;Caballero et al, 2012), salt tolerance (Guo et al, 2008;Kugler et al, 2009), programmed cell death and pathogen responses (Clough et al, 2000;Balagué et al, 2003;Urquhart et al, 2007;Abdel-Hamid et al, 2013), thermal sensing (Finka et al, 2012;Gao et al, 2012), and pollen tube growth (Chang et al, 2007;Frietsch et al, 2007;Tunc-Ozdemir et al, 2013a, 2013b. Direct in vivo disappearance of Ca 2+ channel activity in cngc disruption mutants has been demonstrated in only a few cases thus far Gao et al, 2012).…”

Section: +mentioning

confidence: 99%

Identification of Cyclic GMP-Activated Nonselective Ca2+-Permeable Cation Channels and Associated CNGC5 and CNGC6 Genes in Arabidopsis Guard Cells

et al. 2013

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Cytosolic Ca2+ in guard cells plays an important role in stomatal movement responses to environmental stimuli. These cytosolic Ca 2+ increases result from Ca 2+ influx through Ca 2+ -permeable channels in the plasma membrane and Ca 2+ release from intracellular organelles in guard cells. However, the genes encoding defined plasma membrane Ca 2+ -permeable channel activity remain unknown in guard cells and, with some exceptions, largely unknown in higher plant cells. Here, we report the identification of two Arabidopsis (Arabidopsis thaliana) cation channel genes, CNGC5 and CNGC6, that are highly expressed in guard cells. Cytosolic application of cyclic GMP (cGMP) and extracellularly applied membrane-permeable 8-Bromoguanosine 39,59-cyclic monophosphate-cGMP both activated hyperpolarization-induced inward-conducting currents in wild-type guard cells using Mg 2+ as the main charge carrier. The cGMP-activated currents were strongly blocked by lanthanum and gadolinium and also conducted Ba 2+ , Ca 2+, and Na + ions. cngc5 cngc6 double mutant guard cells exhibited dramatically impaired cGMP-activated currents. In contrast, mutations in CNGC1, CNGC2, and CNGC20 did not disrupt these cGMP-activated currents. The yellow fluorescent protein-CNGC5 and yellow fluorescent protein-CNGC6 proteins localize in the cell periphery. Cyclic AMP activated modest inward currents in both wild-type and cngc5cngc6 mutant guard cells. Moreover, cngc5 cngc6 double mutant guard cells exhibited functional abscisic acid (ABA)-activated hyperpolarization-dependent Ca 2+ -permeable cation channel currents, intact ABA-induced stomatal closing responses, and whole-plant stomatal conductance responses to darkness and changes in CO 2 concentration. Furthermore, cGMPactivated currents remained intact in the growth controlled by abscisic acid2 and abscisic acid insensitive1 mutants. This research demonstrates that the CNGC5 and CNGC6 genes encode unique cGMP-activated nonselective Ca 2+ -permeable cation channels in the plasma membrane of Arabidopsis guard cells.Plants lose water via transpiration and take in CO 2 for photosynthesis through stomatal pores. Each stomatal pore is surrounded by two guard cells, and stomatal movements are driven by the change of turgor pressure in guard cells. The intracellular second messenger Ca 2+ functions in guard cell signal transduction (Schroeder and

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“…The CNGC3, CNGC10, CNGC19 and CNGC20 have been reported to be associated with the response to, and tolerance of salt in A. thaliana plants (Guo et al 2008;Kugler et al 2009). Both CNGC19 and CNGC20 were upregulated by salt treatment within hours; however, the loss of either channel did not lead to a salt-related growth phenotype or change in the Na + (K + ) content change compared with the wild type (Kugler et al 2009).…”

Section: Introductionmentioning

confidence: 98%

Cyclic nucleotide gated channel 10 negatively regulates salt tolerance by mediating Na+ transport in Arabidopsis

et al. 2014

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A number of cyclic nucleotide gated channel (CNGC) genes have been identified in plant genomes, but their functions are mainly undefined. In this study, we identified the role of CNGC10 in the response of Arabidopsis thaliana to salt stress. The cngc10 T-DNA insertion mutant showed greater tolerance to salt than wild-type A. thaliana during seed germination and seedling growth. The cngc10 mutant accumulated less Na(+) and K(+), but not less Ca(2+), in shoots in response to salt stress. By contrast, overexpression of CNGC10 resulted in greater sensitivity to salt stress, and complementation of this gene recovered salt sensitivity. In response to salt stress, heterologous expression of CNGC10 in the Na(+) sensitive yeast mutant strain B31 inhibited growth due to accumulation of Na(+) at a rate greater than that of yeast transformed with an empty vector. Quantitative RT-PCR analysis demonstrated that CNGC10 was expressed mainly in roots and flowers. GUS analysis of a root cross section indicated that CNGC10 was expressed mainly in the endodermis and epidermis. Furthermore, the expression of CNGC10 in roots was dramatically inhibited by exposure to 200 mM NaCl for 6 h. These data suggest that CNGC10 negatively regulates salt tolerance in A. thaliana and may be involved in mediating Na(+) transport.

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Salt-dependent regulation of a CNG channel subfamily in Arabidopsis

Cited by 94 publications

References 41 publications

Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis thaliana

Evolution of cis-regulatory elements and regulatory networks in duplicated genes of Arabidopsis thaliana

Identification of Cyclic GMP-Activated Nonselective Ca2+-Permeable Cation Channels and Associated CNGC5 and CNGC6 Genes in Arabidopsis Guard Cells

Cyclic nucleotide gated channel 10 negatively regulates salt tolerance by mediating Na+ transport in Arabidopsis

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