Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis

Abstract

In plants, multistep component systems play important roles in signal transduction in response to environmental stimuli and plant growth regulators. Arabidopsis contains six nonethylene receptor histidine kinases, and, among them, AHK1/ATHK1, AHK2, AHK3, and CRE1 were shown to be stress-responsive, suggesting their roles in the regulation of plant response to abiotic stress. Gain-and loss-of-function studies in Arabidopsis indicated that AHK1 is a positive regulator of drought and salt stress responses and abscisic acid (ABA) signaling. Microarray analysis of the ahk1 mutant revealed a down-regulation of many stress-and/or ABA-inducible genes, including AREB1, ANAC, and DREB2A transcription factors and their downstream genes. These data suggest that AHK1 functions upstream of AREB1, ANAC, and DREB2A and positively controls stress responses through both ABA-dependent and ABAindependent signaling pathways. In addition, AHK1 plays important roles in plant growth because the ahk1 ahk2 ahk3 triple mutant showed further reduced growth. Unlike AHK1, loss-offunction analysis of ahk2, ahk3, and cre1 implied that the stressresponsive AHK2, AHK3, and CRE1 act as negative regulators in ABA signaling. AHK2 and AHK3 also negatively control osmotic stress responses in Arabidopsis because ahk2, ahk3, and ahk2 ahk3 mutants were strongly tolerant to drought and salt stress due to up-regulation of many stress-and/or ABA-inducible genes. Last, cytokinin clearly mediates stress responses because it was required for CRE1 to function as a negative regulator of osmotic stress.cross-talk ͉ microarray ͉ osmotic stress ͉ plant growth P lants are constantly exposed to environmental stresses that frequently impose constraints on their growth and productivity. Cells have developed elaborate and sensitive protection systems that enable them to rapidly signal, respond, and properly adapt to various stresses, including drought and high salinity (1-5). Phosphorylation, which is catalyzed by protein kinases, is a key mechanism for intracellular signal transduction in both eukaryotic and prokaryotic cells. Exposure of Saccharomyces cerevisiae to a high-osmolarity environment leads to rapid phosphorylation and activation of the MAPK kinase Hog1 through either the SLN1 or SHO1 branch of the HOG pathway (6). Overexpression of Arabidopsis histidine kinase AHK1/ATHK1 in S. cerevisiae sln1 and sho1 deletion mutants enables the yeast mutant to grow normally under high-salinity conditions, suggesting that the histidine kinase (HK) AHK1 can sense and transduce a signal of external osmolarity to downstream targets (7). Moreover, the AHK1 transcript accumulated in Arabidopsis in response to changes in external osmolarity, suggesting the functional importance of AHK1 for the efficient sensing of environmental signals. However, it is still not known whether AHK1 functions as an osmosensor in plants.Beside the nonethylene receptor AHK1, the Arabidopsis genome encodes 10 other putative HKs: the ethylene receptor (ER) HKs ETR1, ETR2, EIN4, ERS1, and ERS2 and the ...

Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response

“…The CK receptors AHK2 and AHK3 were previously reported to act as negative regulators in drought response (10,12). However, the physiological and molecular mechanisms by which the CK signaling acts, the stress-related specific functions of other TCS components, and the identification of downstream components of CK phosphorelay involved in the regulation of drought response were not completely understood and required further in-depth characterization (7).…”

“…We previously published that the ahk2,3 double mutant, which has a distinguishable shoot growth retardation phenotype in comparison with other single and double combinations of ahk2, ahk3, and ahk4 genes, possessed the strongest drought-tolerant phenotype (10). To further characterize the functional role of the five Arabidopsis AHPencoding genes in drought stress response, we collected various combinations of ahp mutants from available public resources (13).…”

“…Within the CK signaling cascade, all three CK receptor Arabidopsis HKs-AHK2, AHK3, and AHK4/cytokinin response 1 (CRE1)-are known to be involved in the response to cold, drought, and salt stresses (10,11). Analyses of ahk2, ahk3, and ahk4 single, double, and triple mutants suggest that AHK2, AHK3, and AHK4 function as negative regulators in abscisic acid (ABA), salt, and drought signaling pathways (10,12). However, the specific functions of the downstream At HPts (AHPs) and most Arabidopsis response regulators (ARRs) within CK signaling during abiotic stress responses remain to be elucidated.…”

ArabidopsisHistidine Kinase CKI1 Acts Upstream of HISTIDINE PHOSPHOTRANSFER PROTEINS to Regulate Female Gametophyte Development and Vegetative Growth

“…For example, AHK1, another homolog of the cytokinin receptors, has been shown to be involved in both the stress response and seed maturation (Urao et al, 1999;Tran et al, 2007;Wohlbach et al, 2008). Interestingly, several type-A ARR genes are coexpressed with AHK1, and different combinations of multiple arr mutants show altered responses to osmotic stress (Wohlbach et al, 2008).…”

ATHK1 acts downstream of hydrogen peroxide to mediate ABA signaling through regulation of calcium channel activity in Arabidopsis guard cells

“…Researchers have shown that ATHK1 mRNA is highly expressed in root tissue, compared with other tissues, and rapidly accumulates in response to changes in soil salinity or osmotic variation, thus making it a highly efficient sensor to environmental fluctuations [8,12,13]. Recent research revealed that ATHK1 plays a unique role in the regulation of processes controlling desiccation, which occur during seed formation.…”