Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis

Kim, Woe‐Yeon; Ali, Zahir; Park, Hyojin; Park, Su Jung; Cha, Joon‐Yung; Perez‐Hormaeche, Javier; Quintero, Francisco J.; Shin, Gilok; Kim, Mi Ri; Zhang, Qiang; Li, Ning; Park, Hyeong Cheol; Lee, Sang Yeol; Bressan, Ray A.; Pardo, José M.; Bohnert, Hans J.; Yun, Dae‐Jin

doi:10.1038/ncomms2357

Cited by 249 publications

(298 citation statements)

References 56 publications

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“…2 D and E and 4 C and D). It was previously shown that RD29A had a gated induction by salt, and that this likely is connected to GI, a core circadian protein involved in flowering time (32). Future studies will help determine whether there is a direct connection between PRR7 and GI activities regarding circadian compensation of salt and drought responses.…”

Section: Discussionmentioning

confidence: 99%

HsfB2b-mediated repression ofPRR7directs abiotic stress responses of the circadian clock

Kolmos

Chow

Pruneda‐Paz

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The circadian clock perceives environmental signals to reset to local time, but the underlying molecular mechanisms are not well understood. Here we present data revealing that a member of the heat shock factor (Hsf) family is involved in the input pathway to the plant circadian clock. Using the yeast one-hybrid approach, we isolated several Hsfs, including HEAT SHOCK FACTOR B2b (HsfB2b), a transcriptional repressor that binds the promoter of PSEUDO RESPONSE REGULATOR 7 (PRR7) at a conserved binding site. The constitutive expression of HsfB2b leads to severely reduced levels of the PRR7 transcript and late flowering and elongated hypocotyls. HsfB2b function is important during heat and salt stress because HsfB2b overexpression sustains circadian rhythms, and the hsfB2b mutant has a short circadian period under these conditions. HsfB2b is also involved in the regulation of hypocotyl growth under warm, short days. Our findings highlight the role of the circadian clock as an integrator of ambient abiotic stress signals important for the growth and fitness of plants.circadian clock | Hsf | heat compensation | salt tolerance T he circadian clock is an endogenous timing mechanism that ensures that daily rhythmic processes are synchronized with the environment. The circadian oscillator runs with a period of ∼24 h. It entrains to environmental signals, such as light and temperature, and in this way is able to anticipate daily environmental changes (1). Molecular genetics and modeling have revealed that the circadian system comprises several interconnected feedback loops involving multiple phase-specific gene products (2).In the model plant Arabidopsis, the morning feedback loops are composed of the major oscillator proteins CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), which peak in abundance at dawn and activate the expression of early-late morning genes PSEUDO RESPONSE REGULATOR 9 (PRR9) and PRR7 (3). Pseudoresponse regulator (PRR) proteins are transcriptional repressors, and PRR9 and PRR7 close the morning loops by binding to the CCA1 and LHY promoters (4). The transcription of PRR9 is acutely activated by light, a feature that is not shared by PRR7 (3, 5). Disruption of either locus results in a mild clock phenotype, including an increased clock period of ∼1 h and an elongated hypocotyl (6-8). The double loss-of-function mutant exhibits a strong synergistic phenotype with free-running period lengths of up to 35 h and loss of temperature entrainment and compensation, indicating overlapping roles for PRR9 and PRR7 (3, 9, 10).The ambient environment influences the circadian clock in a number of different ways. Although the most well-studied input cue is light, temperature is a major zeitgeber as well (11). Brief pulses (from minutes to hours, depending on the intensity) result in acute responses from the clock. Importantly, the severity of such responses is time-dependent and gated by the oscillator (12-14). Longer durations of zeitgeber change can function as an entrainment signal and general...

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Section: Discussionmentioning

confidence: 99%

HsfB2b-mediated repression ofPRR7directs abiotic stress responses of the circadian clock

Kolmos

Chow

Pruneda‐Paz

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…The least well understood of these interactions is that of salinity and the control of reproduction. This problem is now beginning to be addressed at the molecular level with studies such as that by Kim et al (2013). These authors reported that in A. thaliana the flowering time regulator, GIGANTEA (GI), physically interacts with the SNF1-related protein kinase, SOS2 under non-saline conditions.…”

Section: Major Aspects Of Plant Function and Their Relationships To Smentioning

confidence: 99%

The integration of activity in saline environments: problems and perspectives

Cheeseman

2013

Functional Plant Biol.

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Abstract. The successful integration of activity in saline environments requires flexibility of responses at all levels, from genes to life cycles. Because plants are complex systems, there is no 'best' or 'optimal' solution and with respect to salt, glycophytes and halophytes are only the ends of a continuum of responses and possibilities. In this review, I briefly examine seven major aspects of plant function and their responses to salinity including transporters, secondary stresses, carbon acquisition and allocation, water and transpiration, growth and development, reproduction, and cytosolic function and 'integrity'. I conclude that new approaches are needed to move towards understanding either organismal integration or 'salt tolerance', especially cessation of protocols dependent on sudden, often lethal, shock treatments and the embracing of systems level resources. Some of the tools needed to understand the integration of activity and even 'salt stress' are already in hand, such as those for whole-transcriptome analysis. Others, ranging from discovery studies of the nature of the cytosol to expanded tool kits for proteomic, metabolomic and epigenomic studies, still need to be further developed. After resurrecting the distinction between applied stress and the resultant strain and noting that with respect to salinity, the strain is manifest in changes at all -omic levels, I conclude that it should be possible to model and quantify stress responses.

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“…Among these stresses, the role of GI in salt tolerance is best understood. In Arabidopsis, GI sequesters SALT OVERLY SENSITIVE2 (SOS2), a protein kinase that serves as a positive regulator of salt tolerance (28). Release of SOS2 from GI in response to elevated salt permits formation of the SOS2/SOS3 protein kinase complex that associates with and phosphorylates SOS1, activating its Na + /H + antiport activity and enhancing salt tolerance (45).…”

Section: Gi Was First Identified As a Supervital Mutant Of Arabidopsismentioning

confidence: 99%

“…In Arabidopsis, GI has been shown to function as a negative regulator of resistance to salt stress, and gi loss-of-function mutants show increased salt resistance (28). Accordingly, we tested our panel of Arabidopsis gi-201 mutants carrying the B. rapa GI alleles for salt tolerance as measured by fresh weight of aerial tissues following growth in the presence or absence of NaCl.…”

Section: Significancementioning

confidence: 99%

“…More recently, GI has emerged as a key player in a number of stress responses, notably to drought, cold, and salinity (25,27,28). Loss of GI function in Arabidopsis results in increased tolerance to both freezing and salt stress in Arabidopsis, and our analysis of B. rapa GI loss-of-function mutants shows a similar enhancement of freezing and salt resistance in B. rapa, suggesting that the roles of GI in resistance to these two stresses is conserved between species.…”

Section: Gi Was First Identified As a Supervital Mutant Of Arabidopsismentioning

confidence: 99%

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Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

Xie

Lou

Hermand

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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GIGANTEA (GI) was originally identified by a late-flowering mutant in Arabidopsis, but subsequently has been shown to act in circadian period determination, light inhibition of hypocotyl elongation, and responses to multiple abiotic stresses, including tolerance to high salt and cold (freezing) temperature. Genetic mapping and analysis of families of heterogeneous inbred lines showed that natural variation in GI is responsible for a major quantitative trait locus in circadian period in Brassica rapa. We confirmed this conclusion by transgenic rescue of an Arabidopsis gi-201 loss of function mutant. The two B. rapa GI alleles each fully rescued the delayed flowering of Arabidopsis gi-201 but showed differential rescue of perturbations in red light inhibition of hypocotyl elongation and altered cold and salt tolerance. The B. rapa R500 GI allele, which failed to rescue the hypocotyl and abiotic stress phenotypes, disrupted circadian period determination in Arabidopsis. Analysis of chimeric B. rapa GI alleles identified the causal nucleotide polymorphism, which results in an amino acid substitution (S264A) between the two GI proteins. This polymorphism underlies variation in circadian period, cold and salt tolerance, and red light inhibition of hypocotyl elongation. Loss-of-function mutations of B. rapa GI confer delayed flowering, perturbed circadian rhythms in leaf movement, and increased freezing and increased salt tolerance, consistent with effects of similar mutations in Arabidopsis. Collectively, these data suggest that allelic variation of GI-and possibly of clock genes in general-offers an attractive target for molecular breeding for enhanced stress tolerance and potentially for improved crop yield.abiotic stress tolerance | circadian clock | hypocotyl elongation | flowering time | natural variation T he last half-century has seen dramatic increases in agricultural productivity. Despite the approximate doubling in world population since 1964, the proportion with insufficient food has dropped by ∼75%, although ∼1 billion remain underfed, and twice that many suffer from micronutrient deficiencies (1). Predicted growth in population and in per capita consumption will require an estimated doubling of crop production by 2050 (2). However, yield trends for maize, rice, wheat, and soybean-four major crops that currently produce nearly two-thirds of global agricultural calories-are insufficient to achieve this doubling (3). Therefore, there is a pressing need not simply to sustain, but actually to accelerate yield improvement.One strategy to increase yield is to identify genetic variation in plant regulatory networks that limit yield to define targets for programs of marker-assisted (molecular) breeding. The circadian clock has been implicated as a target for increasing yield (4-6). Plant circadian clocks comprise multiple interlocked feedback loops (7-9). There is natural variation in clock function in both weedy and cultivated species (10-15), although few of the genes responsible for these quantitative trait loc...

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Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis

Cited by 249 publications

References 56 publications

HsfB2b-mediated repression ofPRR7directs abiotic stress responses of the circadian clock

HsfB2b-mediated repression ofPRR7directs abiotic stress responses of the circadian clock

The integration of activity in saline environments: problems and perspectives

Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

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